Surfing the wave, cycle, life history, and genes/proteins expressed by testicular germ cells. Part 2: Changes in spermatid organelles associated with development of spermatozoa

Microscopy Research and Technique

Volumn 73, Issue 4, 2010, Pages 279-319

  Hermo, Louis ^a   Pelletier, R Marc ^b   Cyr, Daniel G ^c   Smith, Charles E ^d  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF MONTREAL   (Canada)

^c UNIVERSITÉ LAVAL   (Canada)

^d UNIVERSITÉ DE MONTRÉAL   (Canada)

Author keywords

Acrosome; Chromatoid body; ER; Golgi; Manchette; Nucleus; Sperm head and chromatin

Indexed keywords

BACTERIA; CELL MEMBRANES; CYTOLOGY; GENES;

ACROSOME; CHROMATOID BODIES; CYCLE LIVES; ER; GERM CELLS; GOLGI; MANCHETTE; NUCLEUS; SPERM HEAD AND CHROMATIN; STRUCTURAL MODIFICATIONS;

RATS;

RATTUS;

EID: 77950953915     PISSN: 1059910X     EISSN: 10970029     Source Type: Journal    
DOI: 10.1002/jemt.20787     Document Type: Article

References (441)

1. Abhyankar MM, Urekar C, Reddi PP. 2007. A novel CpG-free vertebrate insulator silences the testis-specific SP-10 gene in somatic tissues: Role for TDP-43 in insulator function. J Biol Chem 282: 36143-36154.
2. Acharya KK, Govind CK, Shore AN, Stoler MH, Reddi PP. 2006. cisrequirement for the maintenance of round spermatid-specific transcription. Dev Biol 295: 781-790.
3. Adham IM, Nayernia K, Engel W. 1997. Spermatozoa lacking acrosin protein show delayed fertilization. Mol Reprod Dev 46: 370-376. (Pubitemid 27098591)
4. Adham IM, Nayernia K, Burkhardt-Gottges E, Topaloglu O, Dixkens C, Holstein AF, Engel W. 2001. Teratozoospermia in mice lacking the transition protein 2 (Tnp2). Mol Hum Reprod 7: 513-520. (Pubitemid 32536871)
5. Akama TO, Nakagawa H, Sugihara K, Narisawa S, Ohyama C, Nishi-mura S, O'Brien DA, Moremen KW, Millan JL, Fukuda MN. 2002. Germ cell survival through carbohydrate-mediated interaction with Sertoli cells. Science 295: 124-127. (Pubitemid 34052360)
6. Akhmanova A, Mausset-Bonnefont AL, van Cappellen W, Keijzer N, Hoogenraad CC, Stepanova T, Drabek K, van der Wees J, Mommaas M, Onderwater J, van der Meulen H, Tanenbaum ME, Medema RH, Hoogerbrugge J, Vreeburg J, Uringa EJ, Grootegoed JA, Grosveld F, Galjart N. 2005. The microtubule plus-end-tracking protein CLIP-170 associates with the spermatid manchette and is essential for spermatogenesis. Genes Dev 19: 2501-2515. (Pubitemid 41483697)
7. Alekseev OM, Widgren EE, Richardson RT, O'Rand MG. 2005. Association of NASP with HSP90 in mouse spermatogenic cells: Stimulation of ATPase activity and transport of linker histones into nuclei. J Biol Chem 280: 2904-2911.
8. Alsheimer M, Drewes T, Schutz W, Benavente R. 2005. The cancer/testis antigen CAGE-1 is a component of the acrosome of spermatids and spermatozoa. Eur J Cell Biol 84: 445-452. (Pubitemid 40353081)
9. Anahara R, Toyama Y, Maekawa M, Kai M, Ishino F, Toshimori K, Mori C. 2006. Flutamide depresses expression of cortactin in the ectoplasmic specialization between the Sertoli cells and spermatids in the mouse testis. Food Chem Toxicol 44: 1050-1056. (Pubitemid 43850073)
10. Anakwe OO, Gerton GL. 1990. Acrosome biogenesis begins during meiosis: Evidence from the synthesis and distribution of an acrosomal glycoprotein, acrogranin, during guinea pig spermatogenesis. Biol Reprod 42: 317-328.
11. Ashman JB, Hall ES, Eveleth J, Boekelheide K. 1992. Tau, the neuronal heat-stable microtubule-associated protein, is also present in the cross-linked microtubule network of the testicular spermatid manchette. Biol Reprod 46: 120-129.
12. Baalasubramanian S, Harris CL, Donev RM, Mizuno M, Omidvar N, Song WC, Morgan BP. 2004. CD59a is the primary regulator of membrane attack complex assembly in the mouse. J Immunol 173: 3684-3692. (Pubitemid 39280729)
13. Baba T, Kashiwabara S, Watanabe K, Itoh H, Michikawa Y, Kimura K, Takada M, Fukamizu A, Arai Y. 1989. Activation and maturation mechanisms of boar acrosin zymogen based on the deduced primary structure. J Biol Chem 264: 11920-11927. (Pubitemid 19185363)
14. Baba T, Azuma S, Kashiwabara S, Toyoda Y. 1994a. Sperm from mice carrying a targeted mutation of the acrosin gene can penetrate the oocyte zona pellucida and effect fertilization. J Biol Chem 269: 31845-31849. (Pubitemid 24379557)
15. Baba T, Niida Y, Michikawa Y, Kashiwabara S, Kodaira K, Takenaka M, Kohno N, Gerton GL, Arai Y. 1994b. An acrosomal protein, sp32, in mammalian sperm is a binding protein specific for two proacrosins and an acrosin intermediate. J Biol Chem 269: 10133-10140. (Pubitemid 24196633)
16. Balhorn R, Weston S, Thomas C, Wyrobek AJ. 1984. DNA packaging in mouse spermatids. Synthesis of protamine variants and four transition proteins. Exp Cell Res 150: 298-308. (Pubitemid 14192470)
17. Banu Y, Matsuda M, Yoshihara M, Kondo M, Sutou S, Matsukuma S. 2002. Golgi matrix protein gene. Golga3/Mea2, rearranged and reexpressed in pachytene spermatocytes restores spermatogenesis in the mouse. Mol Reprod Dev 61: 288-301. (Pubitemid 34117046)
18. Baskaran R, Rao MR. 1991. Mammalian spermatid specific protein. TP2, is a zinc metalloprotein with two finger motifs. Biochem Biophys Res Commun 179: 1491-1499.
19. Bellve AR. 1979. The molecular biology of mammalian spermatogenesis. Oxford Rev Reprod Biol 1: 159-261.
20. Bellve AR, Anderson E, Hanley Bowdoin L. 1975. Synthesis and amino acid composition of basic proteins in mammalian sperm nuclei. Dev Biol 47: 349-365.
21. Ben-Aharon I, Brown PR, Etkovitz N, Eddy EM, Shalgi R. 2005. The expression of calpain 1 and calpain 2 in spermatogenic cells and spermatozoa of the mouse. Reproduction 129: 435-442. (Pubitemid 40542169)
22. Ben-Aharon I, Brown PR, Shalgi R, Eddy EM. 2006. Calpain 11 is unique to mouse spermatogenic cells. Mol Reprod Dev 73: 767-773.
23. Bi M, Hickox JR, Winfrey VP, Olson GE, Hardy DM. 2003. Processing, localization and binding activity of zonadhesin suggest a function in sperm adhesion to the zona pellucida during exocytosis of the acrosome. Biochem J 375(Part 2): 477-488. (Pubitemid 37315457)
24. Biggiogera M, Fakan S, Leser G, Martin TE, Gordon J. 1990. Immunoelectron microscopical visualization of ribonucleoproteins in the chromatoid body of mouse spermatids. Mol Reprod Dev 26: 150-158. (Pubitemid 20192139)
25. Bilbe G, Delabie J, Bruggen J, Richener H, Asselbergs FA, Cerletti N, Sorg C, Odink K, Tarcsay L, Wiesendanger W, DeWolf-Peeters C, Shipman R. 1992. Restin: A novel intermediate filament-associated protein highly expressed in the Reed-Sternberg cells of Hodgkin's disease. EMBO J 11: 2103-2113.
26. Bleil JD, Wassarman PM. 1990. Identification of a ZP3-binding protein on acrosome-intact mouse sperm by photoaffinity crosslinking. Proc Natl Acad Sci USA 87: 5563-5567. (Pubitemid 20260221)
27. Brahmaraju M, Shoeb M, Laloraya M, Kumar PG. 2004. Spatio-temporal organization of Vam6P and SNAP on mouse spermatozoa and their involvement in sperm-zona pellucida interactions. Biochem Biophys Res Commun 318: 148-155. (Pubitemid 38526258)
28. Braun RE. 1998. Post-transcriptional control of gene expression during spermatogenesis. Semin Cell Dev Biol 9: 483-489. (Pubitemid 128350676)
29. Breucker H, Schafer E, Holstein AF. 1985. Morphogenesis and fate of the residual body in human spermiogenesis. Cell Tissue Res 240: 303-309. (Pubitemid 15087047)
30. Brown CR, Harrison RA. 1978. The activation of proacrosin in spermatozoa from ram bull and boar. Biochim Biophys Acta 526: 202-217.
31. Buffone MG, Foster JA, Gerton GL. 2008a. The role of the acrosomal matrix in fertilization. Int J Dev Biol 52: 511-522.
32. Buffone MG, Zhuang T, Ord TS, Hui L, Moss SB, Gerton GL. 2008b. Recombinant mouse sperm ZP3-binding protein (ZP3R/sp56) forms a high order oligomer that binds eggs and inhibits mouse fertilization in vitro. J Biol Chem 283: 12438-12445.
33. Burgos MH, Fawcett DW. 1955. Studies on the fine structure of the mammalian testis. I. Differentiation of the spermatids in the cat (Felis domestica). J Biophys Biochem Cytol 1: 287-300.
34. Burgos MH, Gutierrez LS. 1986. The Golgi complex of the early spermatid in guinea pig. Anat Rec 216: 139-145.
35. Burkin HR, Zhao L, Miller DJ. 2004. CASK is in the mammalian sperm head and is processed during epididymal maturation. Mol Reprod Dev 68: 500-506. (Pubitemid 39090422)
36. Butscheid Y, Chubanov V, Steger K, Meyer D, Dietrich A, Gudermann T. 2006. Polycystic kidney disease and receptor for egg jelly is a plasma membrane protein of mouse sperm head. Mol Reprod Dev 73: 350-360. (Pubitemid 43262050)
37. Cairns BR, Schlichter A, Erdjument-Bromage H, Tempst P, Kornberg RD, Winston F. 1999. Two functionally distinct forms of the RSC nucleosome- remodeling complex, containing essential AT hook. BAH, and bromodomains. Mol Cell 4: 715-723.
38. Caron N, Veilleux S, Boissonneault G. 2001. Stimulation of DNA repair by the spermatidal TP1 protein. Mol Reprod Dev 58: 437-443. (Pubitemid 32179152)
39. Catena R, Ronfani L, Sassone-Corsi P, Davidson I. 2006. Changes in intranuclear chromatin architecture induce bipolar nuclear localization of histone variant H1T2 in male haploid spermatids. Dev Biol 296: 231-238. (Pubitemid 44061765)
40. Chalmel F, Rolland AD, Niederhauser-Wiederkehr C, Chung SS, Demougin P, Gattiker A, Moore J, Patard JJ, Wolgemuth DJ, Jegou B, Primig M. 2007. The conserved transcriptome in human and rodent male gametogenesis. Proc Natl Acad Sci USA 104: 8346-8351. (Pubitemid 47175490)
41. Chapin RE, Wine RN, Harris MW, Borchers CH, Haseman JK. 2001. Structure and control of a cell-cell adhesion complex associated with spermiation in rat seminiferous epithelium. J Androl 22: 1030-1052.
42. Chen JL, Longo FJ. 1996. Expression and localization of DNA topo-isomerase II during rat spermatogenesis. Mol Reprod Dev 45: 61-71. (Pubitemid 26300188)
43. Chennathukuzhi VM, Kurihara Y, Bray JD, Hecht NB. 2001. Trax (translin-associated factor X), a primarily cytoplasmic protein, inhibits the binding of TB-RBP (translin) to RNA. J Biol Chem 276: 13256-13263. (Pubitemid 37385256)
44. Chennathukuzhi V, Stein JM, Abel T, Donlon S, Yang S, Miller JP, All-man DM, Simmons RA, Hecht NB. 2003. Mice deficient for testisbrain RNA-binding protein exhibit a coordinate loss of TRAX, reduced fertility, altered gene expression in the brain, and behavioral changes. Mol Cell Biol 23: 6419-6434. (Pubitemid 37075755)
45. Chesneau V, Prat A, Segretain D, Hospital V, Dupaix A, Foulon T, Jegou B, Cohen P. 1996. NRD convertase: A putative processing endoprotease associated with the axoneme and the manchette in late spermatids. J Cell Sci 109(Part 11): 2737-2745. (Pubitemid 26388358)
46. Cho C, Willis WD, Goulding EH, Jung-Ha H, Choi YC, Hecht NB, Eddy EM. 2001. Haploinsufficiency of protamine-1 or-2 causes infertility in mice. Nat Genet 28: 82-86. (Pubitemid 32409348)
47. Cho C, Jung-Ha H, Willis WD, Goulding EH, Stein P, Xu Z, Schultz RM, Hecht NB, Eddy EM. 2003. Protamine 2 deficiency leads to sperm DNA damage and embryo death in mice. Biol Reprod 69: 211-217. (Pubitemid 36806824)
48. Cho YS, Chennathukuzhi VM, Handel MA, Eppig J, Hecht NB. 2004. The relative levels of translin-associated factor X (TRAX) and testis brain RNA-binding protein determine their nucleocytoplasmic distribution in male germ cells. J Biol Chem 279: 31514-31523. (Pubitemid 39037820)
49. Cho YS, Iguchi N, Yang J, Handel MA, Hecht NB. 2005. Meiotic messenger RNA and noncoding RNA targets of the RNA-binding protein Translin (TSN) in mouse testis. Biol Reprod 73: 840-847. (Pubitemid 41356145)
50. Choi HS, Lee SH, Kim H, Lee Y. 2008. Germ cell-specific gene 1 targets testis-specific poly(A) polymerase to the endoplasmic reticulum through protein-protein interactions. FEBS Lett 582: 1203-1209.
51. Choudhary SK, Wykes SM, Kramer JA, Mohamed AN, Koppitch F, Nelson JE, Krawetz SA. 1995. A haploid expressed gene cluster exists as a single chromatin domain in human sperm. J Biol Chem 270: 8755-8762.
52. Chuma S, Hiyoshi M, Yamamoto A, Hosokawa M, Takamune K, Nakatsuji N. 2003. Mouse Tudor Repeat-1 (MTR-1) is a novel component of chromatoid bodies/nuages in male germ cells and forms a complex with snRNPs. Mech Dev 120: 979-990. (Pubitemid 37205042)
53. Churikov D, Zalenskaya IA, Zalensky AO. 2004. Male germline-specific histones in mouse and man. Cytogenet Genome Res 105: 203-214. (Pubitemid 38979681)
54. Clermont Y. 1991. Four decades of research on the biology of the male reproductive system: A few landmarks. Ann NY Acad Sci 637: 17-25.
55. Clermont Y, Leblond CP. 1955. Spermiogenesis of man, monkey, ram and other mammals as shown by the periodic acid-Schiff technique. Am J Anat 96: 229-253.
56. Clermont Y, Rambourg A. 1978. Evolution of the endoplasmic reticulum during rat spermiogenesis. Am J Anat 151: 191-211. (Pubitemid 8292368)
57. Clermont Y, Einberg E, Leblond CP, Wagner S. 1955. The perforato-rium; an extension of the nuclear membrane of the rat spermatozoon. Anat Rec 121: 1-12.
58. Clermont Y, Lalli M, Rambourg A. 1981. Ultrastructural localization of nicotinamide adenine dinucleotide phosphatase (NADPase), thia-mine pyrophosphatase (TPPase), and cytidine monophosphatase (CMPase) in the Golgi apparatus of early spermatids of the rat. Anat Rec 201: 613-622. (Pubitemid 12244585)
59. Clermont Y, Oko R, Hermo L. 1990. Immunocytochemical localization of proteins utilized in the formation of outer dense fibers and fibrous sheath in rat spermatids: An electron microscope study. Anat Rec 227: 447-457 (Pubitemid 20222177)
60. Clermont Y, Rambourg A, Hermo L. 1992. Segregation of secretory material in all elements of the Golgi apparatus in principal epithelial cells of the rat seminal vesicle. Anat Rec 232: 349-358.
61. Clermont Y, Oko R, Hermo L. 1993. Cell biology of mammalian spermiogenesis. In: Desjardin C, Ewing LL, editors. Cell and molecular biology of the testis. New York: Oxford University Press. pp. 332-376.
62. Clermont Y, Rambourg A, Hermo L. 1994. Connections between the various elements of the cis-and mid-compartments of the Golgi apparatus of early rat spermatids. Anat Rec 240: 469-480. (Pubitemid 24350482)
63. Cobb J, Reddy RK, Park C, Handel MA. 1997. Analysis of expression and function of topoisomerase I and II during meiosis in male mice. Mol Reprod Dev 46: 489-498. (Pubitemid 27149084)
64. Cohen N, Wassarman PM. 2001. Association of egg zona pellucida glycoprotein mZP3 with sperm protein sp56 during fertilization in mice. Int J Dev Biol 45: 569-576. (Pubitemid 32452753)
65. Cole A, Meistrich ML, Cherry LM, Trostle-Weige PK. 1988. Nuclear and manchette development in spermatids of normal and azh/azh mutant mice. Biol Reprod 38: 385-401.
66. Conrad M, Moreno SG, Sinowatz F, Ursini F, Kolle S, Roveri A, Briel-meier M, Wurst W, Maiorino M, Bornkamm GW. 2005. The nuclear form of phospholipid hydroperoxide glutathione peroxidase is a protein thiol peroxidase contributing to sperm chromatin stability. Mol Cell Biol 25: 7637-7644. (Pubitemid 41170125)
67. Coonrod SA, Herr JC, Westhusin ME. 1996. Inhibition of bovine fertilization in vitro by antibodies to SP-10. J Reprod Fertil 107: 287-297. (Pubitemid 126687003)
68. Cotman M, Jezek D, Fon Tacer K, Frangez R, Rozman D. 2004. A functional cytochrome P450 lanosterol 14 alpha-demethylase CYP51 enzyme in the acrosome: Transport through the Golgi and synthesis of meiosis-activating sterols. Endocrinology 145: 1419-1426. (Pubitemid 38281027)
69. Courtens JL, Courot M, Flechon JE. 1976. The perinuclear substance of boar, bull ram and rabbit spermatozoa. J Ultrastruct Res 57: 54-64.
70. Craig AW, Zirngibl R, Williams K, Cole LA, Greer PA. 2001. Mice devoid of fer protein-tyrosine kinase activity are viable and fertile but display reduced cortactin phosphorylation. Mol Cell Biol 21: 603-613. (Pubitemid 32037378)
71. Dass B, Tardif S, Park JY, Tian B, Weitlauf HM, Hess RA, Carnes K, Griswold MD, Small CL, Macdonald CC. 2007. Loss of polyadenylation protein tauCstF-64 causes spermatogenic defects and male infertility. Proc Natl Acad Sci USA 104: 20374-20379.
72. De Blas GA, Roggero CM, Tomes CN, Mayorga LS. 2005. Dynamics of SNARE assembly and disassembly during sperm acrosomal exocytosis. PLoS Biol 3: e323.
73. De Kretser DM, Kerr JB. 1988. The cytology of the testis. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven Press. pp. 837-932.
74. De Kretser DM, Kerr JB. 1994. The cytology of the testis In: Knobil E, Neill JD, editors. Physiology and reproduction. New York: Raven Press. pp. 1177-1290.
75. Dear TN, Boehm T. 1999. Diverse mRNA expression patterns of the mouse calpain genes Capn5. Capn6 and Capn11 during development. Mech Dev 89: 201-209.
76. Dear TN, Boehm T. 2001. Identification and characterization of two novel calpain large subunit genes. Gene 274: 245-252. (Pubitemid 32817142)
77. Dev A, Nayernia K, Meins M, Adham I, Lacone F, Engel W. 2007. Mice deficient for RNA-binding protein brunol1 show reduction of spermatogenesis but are fertile. Mol Reprod Dev 74: 1456-1464. (Pubitemid 47479963)
78. Donev RM, Sivasankar B, Mizuno M, Morgan BP. 2008. The mouse complement regulator CD59b is significantly expressed only in testis and plays roles in sperm acrosome activation and motility. Mol Immunol 45: 534-542. (Pubitemid 47332630)
79. Drabent B, Benavente R, Hoyer-Fender S. 2003. Histone H1t is not replaced by H1.1 or H1.2 in pachytene spermatocytes or spermatids of H1t-deficient mice. Cytogenet Genome Res 103: 307-313. (Pubitemid 38445995)
80. Dym M, Cavicchia JC. 1978. Functional morphology of the testis. Biol Reprod 18: 1-15. (Pubitemid 8297308)
81. Eddy EM. 1970. Cytochemical observations on the chromatoid body of the male germ cells. Biol Reprod 2: 114-128.
82. Eddy EM. 1988. The spermatozoon. In: Knobil E, Neill JD, editors. The physiology ofreproduction. New York: Raven Press. pp. 27-68.
83. Eddy E, O'Brien DA. 1994. The spermatozoon. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven Press. pp. 29-77.
84. Escalier D, Gallo JM, Albert M, Meduri G, Bermudez D, David G, Schrevel J. 1991. Human acrosome biogenesis: Immunodetection of proacrosin in primary spermatocytes and of its partitioning pattern during meiosis. Development 113: 779-788. (Pubitemid 21900317)
85. Farrington JE, Patel R, Ward WS. 1991. DNA attachment to the hamster sperm nuclear matrix and nuclear annulus. Ann NY Acad Sci 637: 164-174.
86. Fawcett DW. 1970. A comparative view of sperm ultrastructure. Biol Reprod 2(Suppl 2): 90-127.
87. Fawcett DW. 1974. Interactions between Sertoli cells and germ cells. In: Mancini RE, Martini L, editors. Male fertility and sterility. London: Academic Press. pp. 13-36.
88. Fawcett DW. 1975. Gametogenesis in the male: Prospects for its control. Symp Soc Dev Biol: 25-53.
89. Fawcett DW, Eddy EM, Phillips DM. 1970. Observations on the fine structure and relationships of the chromatoid body in mammalian spermatogenesis. Biol Reprod 2: 129-153.
90. Fawcett DW, Anderson WA, Phillips DM. 1971. Morphogenetic factors influencing the shape of the sperm head. Dev Biol 26: 220-251.
91. Figueroa J, Burzio LO. 1998. Polysome-like structures in the chromatoid body of rat spermatids. Cell Tissue Res 291: 575-579. (Pubitemid 28105006)
92. Forsbach A, Heinlein UA. 1998. Intratesticular distribution of cyritestin, a protein involved in gamete interaction. J Exp Biol 201 (Part 6): 861-867. (Pubitemid 28181263)
93. Foster JA, Klotz KL, Flickinger CJ, Thomas TS, Wright RM, Castillo JR, Herr JC. 1994. Human SP-10: Acrosomal distribution, processing, and fate after the acrosome reaction. Biol Reprod 51: 1222-1231.
94. Foster JA, Friday BB, Maulit MT, Blobel C, Winfrey VP, Olson GE, Kim KS, Gerton GL. 1997. AM67, a secretory component of the guinea pig sperm acrosomal matrix, is related to mouse sperm protein sp56 and the complement component 4-binding proteins. J Biol Chem 272: 12714-12722. (Pubitemid 27203370)
95. Fouquet JP. 1972. [Mechanism of spermatogenesis in hamsters: Meaning of relationship between Sertoli cells and spermatids]. C R Acad Sci Hebd Seances Acad Sci D 275: 2025-2028.
96. Fouquet J, Kann M, Soues S, Melki R. 2000. ARP1 in Golgi organisation and attachment of manchette microtubules to the nucleus during mammalian spermatogenesis. J Cell Sci 113(Part 5): 877-886. (Pubitemid 30168656)
97. Franke WW, Scheer U, Krohne G, Jarasch ED. 1981. The nuclear envelope and the architecture of the nuclear periphery. J Cell Biol 91: 39s-50s. (Pubitemid 12177859)
98. Fukuda M, Kuroda TS. 2002. Slac2-c (synaptotagmin-like protein homologue lacking C2 domains-c), a novel linker protein that interacts with Rab27, myosin Va/VIIa, and actin. J Biol Chem 277: 43096-43103. (Pubitemid 35285692)
99. Garde J, Roldan ER. 1996. rab 3-peptide stimulates exocytosis of the ram sperm acrosome via interaction with cyclic AMP and phospholipase A2 metabolites. FEBS Lett 391: 263-268. (Pubitemid 26259769)
100. Gawlik V, Schmidt S, Scheepers A, Wennemuth G, Augustin R, Aumuller G, Moser M, Al-Hasani H, Kluge R, Joost HG, Schurmann A. 2008. Targeted disruption of Slc2a8 (GLUT8) reduces motility and mitochondrial potential of spermatozoa. Mol Membr Biol 25: 224-235. (Pubitemid 351563941)
101. Geppert M, Bolshakov VY, Siegelbaum SA, Takei K, De Camilli P, Hammer RE, Sudhof TC. 1994. The role of Rab3A in neurotransmitter release. Nature 369: 493-497. (Pubitemid 24210570)
102. Gerard A, Nya AE, Egloff M, Domingo M, Degrelle H, Gerard H. 1991. Endocytosis of human sex steroid-binding protein in monkey germ cells. Ann N Y Acad Sci 637: 258-276.
103. Gomez O, Romero A, Terrado J, Mesonero JE. 2006. Differential expression of glucose transporter GLUT8 during mouse spermatogenesis. Reproduction 131: 63-70. (Pubitemid 43230704)
104. Govin J, Caron C, Lestrat C, Rousseaux S, Khochbin S. 2004. The role of histones in chromatin remodelling during mammalian spermiogenesis. Eur J Biochem 271: 3459-3469. (Pubitemid 39215336)
105. Govin J, Lestrat C, Caron C, Pivot-Pajot C, Rousseaux S, Khochbin S. 2006. Histone acetylation-mediated chromatin compaction during mouse spermatogenesis. Ernst Schering Res Found Workshop 57: 155-172.
106. Green DP. 1978. The activation of proteolysis in the acrosome reaction of guinea-pig sperm. J Cell Sci 32: 153-164. (Pubitemid 8392505)
107. Green GR, Balhorn R, Poccia DL, Hecht NB. 1994. Synthesis and processing of mammalian protamines and transition proteins. Mol Reprod Dev 37: 255-263. (Pubitemid 24086204)
108. Greer P. 2002. Closing in on the biological functions of Fps/Fes and Fer. Nat Rev Mol Cell Biol 3: 278-289. (Pubitemid 34619263)
109. Grimes SR. 2004. Testis-specific transcriptional control. Gene 343: 11-22.
110. Grimes SR Jr, Meistrich ML, Platz RD, Hnilica LS. 1977. Nuclear protein transitions in rat testis spermatids. Exp Cell Res 110: 31-39. (Pubitemid 8243330)
111. Grimes SR, Wilkerson DC, Noss KR, Wolfe SA. 2003. Transcriptional control of the testis-specific histone H1t gene. Gene 304: 13-21.
112. Grzmil P, Boinska D, Kleene KC, Adham I, Schluter G, Kamper M, Buyandelger B, Meinhardt A, Wolf S, Engel W. 2008. Prm3, the fourth gene in the mouse protamine gene cluster, encodes a conserved acidic protein that affects sperm motility. Biol Reprod 78: 958-967. (Pubitemid 351749291)
113. Gutti RK, Tsai-Morris CH, Dufau ML. 2008. Gonadotropin-regulated testicular helicase (DDX25), an essential regulator of spermatogenesis, prevents testicular germ cell apoptosis. J Biol Chem 283: 17055-17064.
114. Ha H, van Wijnen AJ, Hecht NB. 1997. Tissue-specific protein-DNA interactions of the mouse protamine 2 gene promoter. J Cell Biochem 64: 94-105. (Pubitemid 27081798)
115. Hall ES, Eveleth J, Jiang C, Redenbach DM, Boekelheide K. 1992. Distribution of the microtubule-dependent motors cytoplasmic dynein and kinesin in rat testis. Biol Reprod 46: 817-828.
116. Hamatani T, Tanabe K, Kamei K, Sakai N, Yamamoto Y, Yoshimura Y. 2000. A monoclonal antibody to human SP-10 inhibits in vitro the binding of human sperm to hamster oolemma but not to human Zona pellucida. Biol Reprod 62: 1201-1208. (Pubitemid 30238470)
117. Hao Z, Wolkowicz MJ, Shetty J, Klotz K, Bolling L, Sen B, Westbrook VA, Coonrod S, Flickinger CJ, Herr JC. 2002. SAMP32, a testis-specific, isoantigenic sperm acrosomal membrane-associated protein. Biol Reprod 66: 735-744. (Pubitemid 34193931)
118. Hardy DM, Garbers DL. 1995. A sperm membrane protein that binds in a species-specific manner to the egg extracellular matrix is homologous to von Willebrand factor. J Biol Chem 270: 26025-26028.
119. Hardy DM, Oda MN, Friend DS, Huang TT Jr. 1991. A mechanism for differential release of acrosomal enzymes during the acrosome reaction. Biochem J 275(Part 3): 759-766.
120. Hayasaka S, Terada Y, Suzuki K, Murakawa H, Tachibana I, Sankai T, Murakami T, Yaegashi N, Okamura K. 2008. Intramanchette transport during primate spermiogenesis: Expression of dynein, myosin Va, motor recruiter myosin Va. VIIa-Rab27a/b interacting protein, and Rab27b in the manchette during human and monkey spermiogenesis. Asian J Androl 10: 561-568. (Pubitemid 351865762)
121. Hazzouri M, Pivot-Pajot C, Faure AK, Usson Y, Pelletier R, Sele B, Khochbin S, Rousseaux S. 2000. Regulated hyperacetylation of core histones during mouse spermatogenesis: Involvement of histone deacetylases. Eur J Cell Biol 79: 950-960. (Pubitemid 32000729)
122. Hecht NB. 1995. The making of a spermatozoon: A molecular perspective. Dev Genet 16: 95-103.
123. Hecht NB. 1998. Molecular mechanisms of male germ cell differentiation. Bioessays 20: 555-561. (Pubitemid 28362301)
124. Hecht NB. 1999. Protamine gene expression: A model for post transcriptional gene regulation in male germ cells. In: Gagnon C, editor. The male gamete: From basic science to clinical applications. Vienna, IL: Cache River Press. pp. 5-10.
125. Hecht NB, Distel RJ, Yelick PC, Tanhauser SM, Driscoll CE, Goldberg E, Tung KS. 1988. Localization of a highly divergent mammalian testicular alpha tubulin that is not detectable in brain. Mol Cell Biol 8: 996-1000. (Pubitemid 18044895)
126. Heinlein UAO, Wallat S, Senftleben A, Lemaire L. 1994. Male germ cell-expressed mouse gene TAZ83 encodes a putative, cysteine-rich transmembrane protein (cyritestin) sharing homologies with snake toxins and sperm-egg fusion proteins. Dev Growth Differ 36: 49-58. (Pubitemid 24156323)
127. Hermo L, Clermont Y, Rambourg A. 1979. Endoplasmic reticulum-Golgi apparatus relationships in the rat spermatid. Anat Rec 193: 243-255. (Pubitemid 9133602)
128. Hermo L, Rambourg A, Clermont Y. 1980. Three-dimensional architecture of the cortical region of the Golgi apparatus in rat spermatids. Am J Anat 157: 357-373. (Pubitemid 10086118)
129. Hermo L, Oko R, Hecht NB. 1991. Differential post-translational modifications of microtubules in cells of the seminiferous epithelium of the rat: A light and electron microscope immunocytochemical study. Anat Rec 229: 31-50.
130. Hermo L, Oko R, Morales CR. 1994. Secretion and endocytosis in the male reproductive tract: A role in sperm maturation. Int Rev Cytol 154: 106-189.
131. Herrero MB, Mandal A, Digilio LC, Coonrod SA, Maier B, Herr JC. 2005. Mouse SLLP1, a sperm lysozyme-like protein involved in sperm-egg binding and fertilization. Dev Biol 284: 126-142. (Pubitemid 41096729)
132. Hess RA, Miller LA, Kirby JD, Margoliash E, Goldberg E. 1993. Immunoelectron microscopic localization of testicular and somatic cytochromes c in the seminiferous epithelium of the rat. Biol Reprod 48: 1299-1308 (Pubitemid 23163149)
133. Heydecke D, Meyer D, Ackermann F, Wilhelm B, Gudermann T, Boekhoff I. 2006. The multi PDZ domain protein MUPP1 as a putative scaffolding protein for organizing signaling complexes in the acrosome of mammalian spermatozoa. J Androl 27: 390-404. (Pubitemid 43667987)
134. Ho HC, Tang CY, Suarez SS. 1999. Three-dimensional structure of the Golgi apparatus in mouse spermatids: A scanning electron microscopic study. Anat Rec 256: 189-194.
135. Honda A, Siruntawineti J, Baba T. 2002. Role of acrosomal matrix proteases in sperm-zona pellucida interactions. Hum Reprod Update 8: 405-412. (Pubitemid 35175202)
136. Hospital V, Chesneau V, Balogh A, Joulie C, Seidah NG, Cohen P, Prat A. 2000. N-arginine dibasic convertase (nardilysin) isoforms are soluble dibasic-specific metalloendopeptidases that localize in the cytoplasm and at the cell surface. Biochem J 349(Part 2): 587-597. (Pubitemid 30465794)
137. Howes L, Jones R. 2002. Interactions between zona pellucida glycoproteins and sperm proacrosin/acrosin during fertilization. J Reprod Immunol 53: 181-192. (Pubitemid 34569216)
138. Howes E, Pascall JC, Engel W, Jones R. 2001. Interactions between mouse ZP2 glycoprotein and proacrosin; a mechanism for secondary binding of sperm to the zona pellucida during fertilization. J Cell Sci 114(Part 22): 4127-4136. (Pubitemid 33115033)
139. Hughes J, Ward CJ, Aspinwall R, Butler R, Harris PC. 1999. Identification of a human homologue of the sea urchin receptor for egg jelly: A polycystic kidney disease-like protein. Hum Mol Genet 8: 543-549. (Pubitemid 29097343)
140. Hutt DM, Cardullo RA, Baltz JM, Ngsee JK. 2002. Synaptotagmin VIII is localized to the mouse sperm head and may function in acrosomal exocytosis. Biol Reprod 66: 50-56.
141. Hutt DM, Baltz JM, Ngsee JK. 2005. Synaptotagmin VI and VIII and syntaxin 2 are essential for the mouse sperm acrosome reaction. J Biol Chem 280: 20197-20203.
142. Igdoura SA, Herscovics A, Lal A, Moremen KW, Morales CR, Hermo L. 1999. Alpha-mannosidases involved in N-glycan processing show cell specificity and distinct subcompartmentalization within the Golgi apparatus of cells in the testis and epididymis. Eur J Cell Biol 78: 441-452. (Pubitemid 29385217)
143. Iguchi N, Tanaka H, Yomogida K, Nishimune Y. 2003. Isolation and characterization of a novel cDNA encoding a DNA-binding protein (Hils1) specifically expressed in testicular haploid germ cells. Int J Androl 26: 354-365. (Pubitemid 37521889)
144. Iguchi N, Tobias JW, Hecht NB. 2006a. Expression profiling reveals meiotic male germ cell mRNAs that are translationally up-and down-regulated. Proc Natl Acad Sci USA 103: 7712-7717. (Pubitemid 43752846)
145. Iguchi N, Yang S, Lamb DJ, Hecht NB. 2006b. An SNP in protamine 1: A possible genetic cause of male infertility? J Med Genet 43: 382-384.
146. Iida H, Yoshinaga Y, Tanaka S, Toshimori K, Mori T. 1999. Identification of Rab3A GTPase as an acrosome-associated small GTP-binding protein in rat sperm. Dev Biol 211: 144-155. (Pubitemid 29315828)
147. Ikawa M, Wada I, Kominami K, Watanabe D, Toshimori K, Nishimune Y, Okabe M. 1997. The putative chaperone calmegin is required for sperm fertility. Nature 387: 607-611. (Pubitemid 27249238)
148. Ikawa M, Nakanishi T, Yamada S, Wada I, Kominami K, Tanaka H, Nozaki M, Nishimune Y, Okabe M. 2001. Calmegin is required for fertilin alpha/beta heterodimerization and sperm fertility. Dev Biol 240: 254-261. (Pubitemid 33141122)
149. Imai-Senga Y, Sun-Wada GH, Wada Y, Futai M. 2002. A human gene. ATP6E1, encoding a testis-specific isoform of H(+)-ATPase subunit E. Gene 289: 7-12. (Pubitemid 34564480)
150. Imreh G, Hallberg E. 2000. An integral membrane protein from the nuclear pore complex is also present in the annulate lamellae: Implications for annulate lamella formation. Exp Cell Res 259: 180-190.
151. Inoue N, Ikawa M, Nakanishi T, Matsumoto M, Nomura M, Seya T, Okabe M. 2003. Disruption of mouse CD46 causes an accelerated spontaneous acrosome reaction in sperm. Mol Cell Biol 23: 2614-2622. (Pubitemid 36351040)
152. Ito C, Suzuki-Toyota F, Maekawa M, Toyama Y, Yao R, Noda T, Toshimori K. 2004. Failure to assemble the peri-nuclear structures in GOPC deficient spermatids as found in round-headed spermatozoa. Arch Histol Cytol 67: 349-360. (Pubitemid 40215908)
153. Jimenez A, Zu W, Rawe VY, Pelto-Huikko M, Flickinger CJ, Sutovsky P, Gustafsson JA, Oko R, Miranda-Vizuete A. 2004. Spermatocyte/spermatid-specific thioredoxin-3, a novel Golgi apparatus-associated thioredoxin, is a specific marker of aberrant spermatogenesis. J Biol Chem 279: 34971-34982. (Pubitemid 39328058)
154. Jones MH, Numata M, Shimane M. 1997. Identification and characterization of BRDT: A testis-specific gene related to the bromodomain genes RING3 and Drosophila fsh. Genomics 45: 529-534. (Pubitemid 27506127)
155. Kai M, Irie M, Okutsu T, Inoue K, Ogonuki N, Miki H, Yokoyama M, Migishima R, Muguruma K, Fujimura H, Kohda T, Ogura A, Kaneko-Ishino T, Ishino F. 2004. The novel dominant mutation Dspd leads to a severe spermiogenesis defect in mice. Biol Reprod 70: 1213-1221. (Pubitemid 38387735)
156. Kang-Decker N, Mantchev GT, Juneja SC, McNiven MA, van Deursen JM. 2001. Lack of acrosome formation in Hrb-deficient mice. Science 294: 1531-1533. (Pubitemid 33063925)
157. Kann ML, Fouquet JP. 1993. Association of spectrin with manchette microtubules in mammalian spermatids. Biol Cell 77: 311-313.
158. Kann ML, Soues S, Levilliers N, Fouquet JP. 2003. Glutamylated tubulin: Diversity of expression and distribution of isoforms. Cell Motil Cytoskeleton 55: 14-25. (Pubitemid 36514495)
159. Kashiwabara S, Arai Y, Kodaira K, Baba T. 1990. Acrosin biosynthesis in meiotic and postmeiotic spermatogenic cells. Biochem Biophys Res Commun 173: 240-245.
160. Kashiwabara S, Zhuang T, Yamagata K, Noguchi J, Fukamizu A, Baba T. 2000. Identification of a novel isoform of poly(A) polymerase. TPAP, specifically present in the cytoplasm of spermatogenic cells. Dev Biol 228: 106-115.
161. Kashiwabara S, Noguchi J, Zhuang T, Ohmura K, Honda A, Sugiura S, Miyamoto K, Takahashi S, Inoue K, Ogura A, Baba T. 2002. Regulation of spermatogenesis by testis-specific, cytoplasmic poly(A) polymerase TPAP. Science 298: 1999-2002. (Pubitemid 35425257)
162. Kato A, Nagata Y, Todokoro K. 2004. Delta-tubulin is a component of intercellular bridges and both the early and mature perinuclear rings during spermatogenesis. Dev Biol 269: 196-205. (Pubitemid 38471833)
163. Kessel RG. 1981. Origin, differentiation, distribution and possible functional role of annulate lamellae during spermatogenesis in Drosophila melanogaster. J Ultrastruct Res 75: 72-96.
164. Kessel RG. 1983. The structure and function ofannulate lamellae: Porous cytoplasmic and intranuclear membranes. Int Rev Cytol 82: 181-303.
165. Kessel RG. 1989. The annulate lamellae - From obscurity to spotlight. Electron Microsc Rev 2: 257-348.
166. Kido T, Namiki H. 2000. Expression of testicular fatty acid-binding protein PERF 15 during germ cell apoptosis. Dev Growth Differ 42: 359-366. (Pubitemid 30662892)
167. Kierszenbaum AL. 2001. Spermatid manchette: Plugging proteins to zero into the sperm tail. Mol Reprod Dev 59: 347-349.
168. Kierszenbaum AL. 2002. Intramanchette transport (IMT): Managing the making of the spermatid head, centrosome, and tail. Mol Reprod Dev 63: 1-4.
169. Kierszenbaum AL. 2006. Tyrosine protein kinases and spermatogenesis: Truncation matters. Mol Reprod Dev 73: 399-403. (Pubitemid 43376567)
170. Kierszenbaum AL, Tres LL. 1975. Structural and transcriptional features of the mouse spermatid genome. J Cell Biol 65: 258-270.
171. Kierszenbaum AL, Tres LL. 2004. The acrosome-acroplaxome-manchette complex and the shaping of the spermatid head. Arch Histol Cytol 67: 271-284.
172. Kierszenbaum AL, Gil M, Rivkin E, Tres LL. 2002. Ran, a GTP-binding protein involved in nucleocytoplasmic transport and microtubule nucleation, relocates from the manchette to the centrosome region during rat spermiogenesis. Mol Reprod Dev 63: 131-140. (Pubitemid 34831323)
173. Kierszenbaum AL, Rivkin E, Tres LL. 2003a. Acroplaxome, an F-actin-keratin-containing plate, anchors the acrosome to the nucleus during shaping of the spermatid head. Mol Biol Cell 14: 4628-4640. (Pubitemid 37444661)
174. Kierszenbaum AL, Rivkin E, Tres LL. 2003b. The actin-based motor myosin Va is a component of the acroplaxome, an acrosome-nuclear envelope junctional plate, and of manchette-associated vesicles. Cytogenet Genome Res 103: 337-344. (Pubitemid 38445999)
175. Kierszenbaum AL, Tres LL, Rivkin E, Kang-Decker N, van Deursen JM. 2004. The acroplaxome is the docking site of Golgi-derived myosin Va/Rab27a/b- containing proacrosomal vesicles in wild-type and Hrb mutant mouse spermatids. Biol Reprod 70: 1400-1410. (Pubitemid 38509688)
176. Kierszenbaum AL, Rivkin E, Tres LL. 2007. Molecular biology of sperm head shaping. Soc Reprod Fertil Suppl 65: 33-43.
177. Kierszenbaum AL, Rivkin E, Tres LL. 2008. Expression of Fer testis (FerT) tyrosine kinase transcript variants and distribution sites of FerT during the development of the acrosome-acroplaxome-manchette complex in rat spermatids. Dev Dyn 237: 3882-3891.
178. Kim ST, Moley KH. 2007. The expression of GLUT8. GLUT9a, and GLUT9b in the mouse testis and sperm. Reprod Sci 14: 445-455.
179. Kim KS, Foster JA, Gerton GL. 2001. Differential release of guinea pig sperm acrosomal components during exocytosis. Biol Reprod 64: 148-156.
180. Kim E, Baba D, Kimura M, Yamashita M, Kashiwabara S, Baba T. 2005. Identification of a hyaluronidase. Hyal5, involved in penetration of mouse sperm through cumulus mass. Proc Natl Acad Sci USA 102: 18028-18033. (Pubitemid 41798496)
181. Kistler MK, Sassone-Corsi P, Kistler WS. 1994. Identification of a functional cyclic adenosine 3′, 5′-monophosphate response element in the 5′-flanking region of the gene for transition protein 1 (TP1), a basic chromosomal protein of mammalian spermatids. Biol Reprod 51: 1322-1329. (Pubitemid 24354295)
182. Kitamura K, Tanaka H, Nishimune Y. 2003. Haprin, a novel haploid germ cell-specific RING finger protein involved in the acrosome reaction. J Biol Chem 278: 44417-144123 (Pubitemid 37377192)
183. Kitamura K, Iguchi N, Kaneko Y, Tanaka H, Nishimune Y. 2004. Characterization of a novel postacrosomal perinuclear theca-specific protein. CYPT1. Biol Reprod 71: 1927-1935. (Pubitemid 39586938)
184. Kitamura K, Nishimura H, Nishimune Y, Tanaka H. 2005a. Identification of human HAPRIN potentially involved in the acrosome reaction. J Androl 26: 511-518. (Pubitemid 40847864)
185. Kitamura K, Tanaka H, Nishimune Y. 2005b. The RING-finger protein haprin: Domains and function in the acrosome reaction. Curr Protein Pept Sci 6: 567-574. (Pubitemid 41723526)
186. Kleene KC. 2001. A possible meiotic function of the peculiar patterns of gene expression in mammalian spermatogenic cells. Mech Dev 106: 3-23.
187. Kleene KC, Flynn JF. 1987. Characterization of a cDNA clone encoding a basic protein. TP2, involved in chromatin condensation during spermiogenesis in the mouse. J Biol Chem 262: 17272-17277.
188. Koizumi H, Yamaguchi N, Hattori M, Ishikawa TO, Aoki J, Taketo MM, Inoue K, Arai H. 2003. Targeted disruption of intracellular type I platelet activating factor-acetylhydrolase catalytic subunits causes severe impairment in spermatogenesis. J Biol Chem 278: 12489-12494. (Pubitemid 36800237)
189. Komada M, McLean DJ, Griswold MD, Russell LD, Soriano P. 2000. E-MAP-115, encoding a microtubule-associated protein, is a retinoic acid-inducible gene required for spermatogenesis. Genes Dev 14: 1332-1342. (Pubitemid 30397077)
190. Kornfeld S, Mellman I. 1989. The biogenesis of lysosomes. Annu Rev Cell Biol 5: 483-525. (Pubitemid 19286692)
191. Kotaja N, Sassone-Corsi P. 2007. The chromatoid body: A germ-cell-specific RNA-processing centre. Nat Rev Mol Cell Biol 8: 85-90. (Pubitemid 46012017)
192. Kotaja N, Bhattacharyya SN, Jaskiewicz L, Kimmins S, Parvinen M, Filipowicz W, Sassone-Corsi P. 2006a. The chromatoid body of male germ cells: Similarity with processing bodies and presence of Dicer and microRNA pathway components. Proc Natl Acad Sci USA 103: 2647-2652. (Pubitemid 43306603)
193. Kotaja N, Lin H, Parvinen M, Sassone-Corsi P. 2006b. Interplay of PIWI/Argonaute protein MIWI and kinesin KIF17b in chromatoid bodies of male germ cells. J Cell Sci 119(Part 13): 2819-2825. (Pubitemid 44184018)
194. Kramer JA, McCarrey JR, Djakiew D, Krawetz SA. 1998. Differentiation: The selective potentiation of chromatin domains. Development 125: 4749-4755. (Pubitemid 29027204)
195. Kress C, Gautier-Courteille C, Osborne HB, Babinet C, Paillard L. 2007. Inactivation of CUG-BP1/CELF1 causes growth, viability, and spermatogenesis defects in mice. Mol Cell Biol 27: 1146-1157. (Pubitemid 46174574)
196. Kuramochi-Miyagawa S, Kimura T, Ijiri TW, Isobe T, Asada N, Fujita Y, Ikawa M, Iwai N, Okabe M, Deng W, Lin H, Matsuda Y, Nakano T. 2004. Mili, a mammalian member of piwi family gene, is essential for spermatogenesis. Development 131: 839-849. (Pubitemid 38263199)
197. Kurth BE, Klotz K, Flickinger CJ, Herr JC. 1991. Localization of sperm antigen SP-10 during the six stages of the cycle of the seminiferous epithelium in man. Biol Reprod 44: 814-821.
198. Laberge RM, Boissonneault G. 2005. On the nature and origin of DNA strand breaks in elongating spermatids. Biol Reprod 73: 289-296. (Pubitemid 41022788)
199. Lalli M, Clermont Y. 1981. Structural changes of the head components of the rat spermatid during late spermiogenesis. Am J Anat 160: 419-434. (Pubitemid 11154948)
200. Leblond CP, Clermont Y. 1952. Definition of the stages of the cycle of the seminiferous epithelium in the rat. Ann NY Acad Sci 55: 548-573.
201. Leduc F, Maquennehan V, Nkoma GB, Boissonneault G. 2008a. DNA damage response during chromatin remodeling in elongating spermatids of mice. Biol Reprod 78: 324-332. (Pubitemid 351159988)
202. Leduc F, Nkoma GB, Boissonneault G. 2008b. Spermiogenesis and DNA repair: A possible etiology of human infertility and genetic disorders. Syst Biol Reprod Med 54: 3-10.
203. Lee K, Haugen HS, Clegg CH, Braun RE. 1995. Premature translation of protamine 1 mRNA causes precocious nuclear condensation and arrests spermatid differentiation in mice. Proc Natl Acad Sci USA 92: 12451-12455. (Pubitemid 26014087)
204. Lee NP, Mruk DD, Xia W, Cheng CY. 2007. Cellular localization of sphingomyelin synthase 2 in the seminiferous epithelium of adult rat testes. J Endocrinol 192: 17-32. (Pubitemid 46444392)
205. Levesque D, Veilleux S, Caron N, Boissonneault G. 1998. Architectural DNA-binding properties of the spermatidal transition proteins 1 and 2. Biochem Biophys Res Commun 252: 602-609. (Pubitemid 28556823)
206. Lewis JD, Abbott DW, Ausio J. 2003. A haploid affair: Core histone transitions during spermatogenesis. Biochem Cell Biol 81: 131-140. (Pubitemid 37076235)
207. Li S, Goldberg E. 2000. A novel N-terminal domain directs membrane localization of mouse testis-specific calpastatin. Biol Reprod 63: 1594-1600.
208. Li YC, Hu XQ, Zhang KY, Guo J, Hu ZY, Tao SX, Xiao LJ, Wang QZ, Han CS, Liu YX. 2006. Afaf, a novel vesicle membrane protein, is related to acrosome formation in murine testis. FEBS Lett 580: 4266-4273. (Pubitemid 44037561)
209. Lin Q, Sirotkin A, Skoultchi AI. 2000. Normal spermatogenesis in mice lacking the testis-specific linker histone H1t. Mol Cell Biol 20: 2122-2128. (Pubitemid 30123827)
210. Lin YN, Roy A, Yan W, Burns KH, Matzuk MM. 2007. Loss of zona pellucida binding proteins in the acrosomal matrix disrupts acrosome biogenesis and sperm morphogenesis. Mol Cell Biol 27: 6794-6805. (Pubitemid 47483630)
211. Linder B, Bammer S, Heinlein UA. 1995. Delayed translation and posttranslational processing of cyritestin, an integral transmembrane protein of the mouse acrosome. Exp Cell Res 221: 66-72.
212. Longo FJ, Krohne G, Franke WW. 1987. Basic proteins of the perinuclear theca of mammalian spermatozoa and spermatids: A novel class of cytoskeletal elements. J Cell Biol 105: 1105-1120. (Pubitemid 18029836)
213. Mali P, Kaipia A, Kangasniemi M, Toppari J, Sandberg M, Hecht NB, Parvinen M. 1989. Stage-specific expression of nucleoprotein mRNAs during rat and mouse spermiogenesis. Reprod Fertil Dev 1: 369-382. (Pubitemid 20121836)
214. Mandal A, Klotz KL, Shetty J, Jayes FL, Wolkowicz MJ, Bolling LC, Coonrod SA, Black MB, Diekman AB, Haystead TA, Flickinger CJ, Herr JC. 2003. SLLP1, a unique, intra-acrosomal, non-bacteriolytic, c lysozyme-like protein of human spermatozoa. Biol Reprod 68: 1525-1537. (Pubitemid 36519755)
215. Marcon L, Boissonneault G. 2004. Transient DNA strand breaks during mouse and human spermiogenesis new insights in stage specificity and link to chromatin remodeling. Biol Reprod 70: 910-918. (Pubitemid 38387699)
216. Martianov I, Brancorsini S, Catena R, Gansmuller A, Kotaja N, Parvinen M, Sassone-Corsi P, Davidson I. 2005. Polar nuclear localization of H1T2, a histone H1 variant, required for spermatid elongation and DNA condensation during spermiogenesis. Proc Natl Acad Sci USA 102: 2808-2813. (Pubitemid 40299874)
217. Martinez-Menarguez JA, Geuze HJ, Ballesta J. 1996a. Evidence for a nonlysosomal origin of the acrosome. J Histochem Cytochem 44: 313-320. (Pubitemid 26102428)
218. Martinez-Menarguez JA, Geuze HJ, Ballesta J. 1996b. Identification of two types of beta-COP vesicles in the Golgi complex of rat spermatids. Eur J Cell Biol 71: 137-143. (Pubitemid 26348469)
219. Matsuda M, Kondo M, Kashiwabara S, Yoshihara M, Sutou S, Matsukuma S. 2004. Co-localization of Trax and Mea2 in Golgi complex of pachytene spermatocytes in the mouse. J Histochem Cytochem 52: 1245-1248. (Pubitemid 39097192)
220. Matsukuma S, Kondo M, Yoshihara M, Matsuda M, Utakoji T, Sutou S. 1999. Mea2/Golga3 gene is disrupted in a line of transgenic mice with a reciprocal translocation between Chromosomes 5 and 19 and is responsible for a defective spermatogenesis in homozygotes. Mamm Genome 10: 1-5. (Pubitemid 29389934)
221. Matsuoka Y, Miyagawa Y, Tokuhiro K, Kitamura K, Iguchi N, Maekawa M, Takahashi T, Tsujimura A, Matsumiya K, Okuyama A, Nishimune Y, Tanaka H. 2008. Isolation and characterization of the spermatid-specific Smrp1 gene encoding a novel manchette protein. Mol Reprod Dev 75: 967-975. (Pubitemid 351628582)
222. Maul GG. 1977. Nuclear pore complexes. Elimination and reconstruction during mitosis. J Cell Biol 74: 492-500. (Pubitemid 8153984)
223. Mayorga LS, Tomes CN, Belmonte SA. 2007. Acrosomal exocytosis, a special type of regulated secretion. IUBMB Life 59: 286-292.
224. Meetei AR, Ullas KS, Vasupradha V, Rao MR. 2002. Involvement of protein kinase A in the phosphorylation of spermatidal protein TP2 and its effect on DNA condensation. Biochemistry 41: 185-195. (Pubitemid 34049394)
225. Meistrich ML. 1993. Nuclear morphogenesis during spermiogenesis. In: de Kretser D, editor. Molecular biology of the male reproductive system. New York: Academic Press. pp. 67-97.
226. Meistrich ML, Trostle-Weige PK, Russell LD. 1990. Abnormal manchette development in spermatids of azh/azh mutant mice. Am J Anat 188: 74-86.
227. Meistrich ML, Mohapatra B, Shirley CR, Zhao M. 2003. Roles of transition nuclear proteins in spermiogenesis. Chromosoma 111: 483-488. (Pubitemid 36705630)
228. Meizel S. 1972. Biochemical detection and activation of an inactive form of a trypsin-like enzyme in rabbit testes. J Reprod Fertil 31: 459-462.
229. Meizel S, Deamer DW. 1978. The pH of the hamster sperm acrosome. J Histochem Cytochem 26: 98-105. (Pubitemid 8287278)
230. Mendoza-Lujambio I, Burfeind P, Dixkens C, Meinhardt A, Hoyer-Fender S, Engel W, Neesen J. 2002. The Hook1 gene is non-functional in the abnormal spermatozoon head shape (azh) mutant mouse. Hum Mol Genet 11: 1647-1658. (Pubitemid 34812260)
231. Mengual L, Ballesca JL, Ascaso C, Oliva R. 2003. Marked differences in protamine content and P1/P2 ratios in sperm cells from percoll fractions between patients and controls. J Androl 24: 438-447. (Pubitemid 39571800)
232. Merisko EM. 1989. Annulate lamellae: An organelle in search of a function. Tissue Cell 21: 343-354.
233. Michaut M, Tomes CN, De Blas G, Yunes R, Mayorga LS. 2000. Calcium-triggered acrosomal exocytosis in human spermatozoa requires the coordinated activation of Rab3A and N-ethylmalei-mide-sensitive factor. Proc Natl Acad Sci USA 97: 9996-10001.
234. Miller DJ, Gong X, Shur BD. 1993. Sperm require beta-N-acetylgluco- saminidase to penetrate through the egg zona pellucida. Development 118: 1279-1289. (Pubitemid 23252415)
235. Miller MG, Mulholland DJ, Vogl AW. 1999. Rat testis motor proteins associated with spermatid translocation (dynein) and spermatid flagella (kinesin-II). Biol Reprod 60: 1047-1056.
236. Mizuno M, Harris CL, Johnson PM, Morgan BP. 2004. Rat membrane cofactor protein (MCP; CD46) is expressed only in the acrosome of developing and mature spermatozoa and mediates binding to immobilized activated C3. Biol Reprod 71: 1374-1383. (Pubitemid 39249825)
237. Mizuno M, Harris CL, Suzuki N, Matsuo S, Morgan BP. 2005. Expression of CD46 in developing rat spermatozoa: Ultrastructural localization and utility as a marker of the various stages of the seminiferous tubuli. Biol Reprod 72: 908-915. (Pubitemid 40404265)
238. Mochida K, Tres LL, Kierszenbaum AL. 1998. Isolation of the rat spermatid manchette and its perinuclear ring. Dev Biol 200: 46-56. (Pubitemid 28374691)
239. Mochida K, Rivkin E, Gil M, Kierszenbaum AL. 2000a. Keratin 9 is a component of the perinuclear ring of the manchette of rat spermatids. Dev Biol 227: 510-519.
240. Mochida K, Tres LL, Kierszenbaum AL. 2000b. Structural features of the 26S proteasome complex isolated from rat testis and sperm tail. Mol Reprod Dev 57: 176-184.
241. Mollenhauer HH, Morre DJ, Vanderwoude WJ. 1976. Endoplasmic reticulum-Golgi apparatus associations in maize root tips. Mikros-kopie 31: 257-272.
242. Monesi V. 1965. Synthetic activities during spermatogenesis in the mouse RNA and protein. Exp Cell Res 39: 197-224.
243. Morales C, Clermont Y. 1982. Evolution of Sertoli cell processes invading the cytoplasm of rat spermatids. Anat Rec 203: 233-244. (Pubitemid 12078924)
244. Morales CR, Wu XQ, Hecht NB. 1998. The DNA/RNA-binding protein. TB-RBP, moves from the nucleus to the cytoplasm and through intercellular bridges in male germ cells. Dev Biol 201: 113-123.
245. Morales P, Pizarro E, Kong M, Jara M. 2004. Extracellular localization of proteasomes in human sperm. Mol Reprod Dev 68: 115-124. (Pubitemid 38420526)
246. Moreno RD, Sepulveda MS, de Ioannes A, Barros C. 1998. The polysulphate binding domain of human proacrosin/acrosin is involved in both the enzyme activation and spermatozoa-zona pellucida interaction. Zygote 6: 75-83. (Pubitemid 128566360)
247. Moreno RD, Ramalho-Santos J, Chan EK, Wessel GM, Schatten G. 2000a. The Golgi apparatus segregates from the lysosomal/acrosomal vesicle during rhesus spermiogenesis: Structural alterations. Dev Biol 219: 334-349. (Pubitemid 30152609)
248. Moreno RD, Ramalho-Santos J, Sutovsky P, Chan EK, Schatten G. 2000b. Vesicular traffic and golgi apparatus dynamics during mammalian spermatogenesis: Implications for acrosome architecture. Biol Reprod 63: 89-98. (Pubitemid 30429389)
249. Moreno RD, Palomino J, Schatten G. 2006. Assembly of spermatid acrosome depends on microtubule organization during mammalian spermiogenesis. Dev Biol 293: 218-227.
250. Mori E, Baba T, Iwamatsu A, Mori T. 1993. Purification and characterization of a 38-kDa protein, sp38, with zona pellucida-binding property from porcine epididymal sperm. Biochem Biophys Res Commun 196: 196-202. (Pubitemid 23309493)
251. Morozova KN, Gubanova NV, Kiseleva EV. 2005. [Structural organization and possible functional role of annulate lamellae containing cytoplasmic pores]. Tsitologiia 47: 667-678.
252. Moussa F, Oko R, Hermo L. 1994. The immunolocalization of small nuclear ribonucleoprotein particles in testicular cells during the cycle of the seminiferous epithelium of the adult rat. Cell Tissue Res 278: 363-378. (Pubitemid 24315108)
253. Mylonis I, Drosou V, Brancorsini S, Nikolakaki E, Sassone-Corsi P, Giannakouros T. 2004. Temporal association of protamine 1 with the inner nuclear membrane protein lamin B receptor during spermiogenesis. J Biol Chem 279: 11626-11631. (Pubitemid 38401664)
254. Nagamori I, Sassone-Corsi P. 2008. The chromatoid body of male germ cells: Epigenetic control and miRNA pathway. Cell Cycle 7: 3503-3508.
255. NagDas SK, Winfrey VP, Olson GE. 1996. Identification of hydrolase binding activities of the acrosomal matrix of hamster spermatozoa. Biol Reprod 55: 1405-1414.
256. Nakanishi T, Ikawa M, Yamada S, Toshimori K, Okabe M. 2001. Alkalinization of acrosome measured by GFP as a pH indicator and its relation to sperm capacitation. Dev Biol 237: 222-231. (Pubitemid 32844317)
257. Nayernia K, Reim K, Oberwinkler H, Engel W. 1994. Diploid expression and translational regulation of rat acrosin gene. Biochem Biophys Res Commun 202: 88-93. (Pubitemid 24252569)
258. Nayernia K, Adham I, Kremling H, Reim K, Schlicker M, Schluter G, Engel W. 1996. Stage and developmental specific gene expression during mammalian spermatogenesis. Int J Dev Biol 40: 379-383. (Pubitemid 26151283)
259. Nayernia K, Adham IM, Shamsadin R, Muller C, Sancken U, Engel W. 2002. Proacrosin-deficient mice and zona pellucida modifications in an experimental model of multifactorial infertility. Mol Hum Reprod 8: 434-440. (Pubitemid 34567921)
260. Nayernia K, Vauti F, Meinhardt A, Cadenas C, Schweyer S, Meyer BI, Schwandt I, Chowdhury K, Engel W, Arnold HH. 2003. Inactivation of a testis-specific Lis1 transcript in mice prevents spermatid differentiation and causes male infertility. J Biol Chem 278: 48377-48385. (Pubitemid 37523293)
261. Nemoto Y, Wenk MR, Watanabe M, Daniell L, Murakami T, Ringstad N, Yamada H, Takei K, De Camilli P. 2001. Identification and characterization of a synaptojanin 2 splice isoform predominantly expressed in nerve terminals. J Biol Chem 276: 41133-41142. (Pubitemid 37373269)
262. Nian H, Fan C, Liao S, Shi Y, Zhang K, Liu Y, Han C. 2007. RNF151, a testis-specific RING finger protein, interacts with dysbindin. Arch Biochem Biophys 465: 157-163. (Pubitemid 47283989)
263. Nicander L. 1967. An electron microscopical study of cell contacts in the seminiferous tubules of some mammals. Z Zellforsch Mikrosk Anat 83: 375-397.
264. Nicander L, Ploen L. 1969. Fine structure of spermatogonia and primary spermatocytes in rabbits. Z Zellforsch Mikrosk Anat 99: 221-234.
265. Nishimura H, Cho C, Branciforte DR, Myles DG, Primakoff P. 2001. Analysis of loss of adhesive function in sperm lacking cyritestin or fertilin beta. Dev Biol 233: 204-213. (Pubitemid 32411305)
266. Noland TD. 1990. Regulation of acrosomal matrix dispersion in digitonin-permeabilized guinea pig spermatozoa. Biol Reprod 42: 252-259.
267. Noland TD, Friday BB, Maulit MT, Gerton GL. 1994. The sperm acrosomal matrix contains a novel member of the pentaxin family of calcium-dependent binding proteins. J Biol Chem 269: 32607-32614.
268. Novikoff PM, Novikoff AB, Quintana N, Hauw JJ. 1971. Golgi apparatus. GERL, and lysosomes of neurons in rat dorsal root ganglia, studied by thick section and thin section cytochemistry. J Cell Biol 50: 859-886.
269. Nuzzo NA, Anderson RA Jr, Zaneveld LJ. 1990. Proacrosin activation and acrosin release during the guinea pig acrosome reaction. Mol Reprod Dev 25: 52-60.
270. O'Brien DA, Gabel CA, Welch JE, Eddy EM. 1991. Mannose 6-phosphate receptors: Potential mediators of germ cell-Sertoli cell interactions. Ann NY Acad Sci 637: 327-339.
271. Obermann H, Raabe I, Balvers M, Brunswig B, Schulze W, Kirchh-off C. 2005. Novel testis-expressed profilin IV associated with acrosome biogenesis and spermatid elongation. Mol Hum Reprod 11: 53-64. (Pubitemid 40331003)
272. Oko R, Clermont Y. 1988. Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol Reprod 39: 673-687.
273. Oko R, Clermont Y. 1991. Origin and distribution ofperforatorial proteins during spermatogenesis of the rat: An immunocytochemical study. Anat Rec 230: 489-501.
274. Oke BO, Suarez-Quian CA. 1992. Partitioning of the Golgi apparatus in rat primary and secondary spermatocytes during meiosis. Anat Rec 233: 245-256.
275. Oko R, Morales CR. 1994. A novel testicular protein, with sequence similarities to a family of lipid binding proteins, is a major component of the rat sperm perinuclear theca. Dev Biol 166: 235-245. (Pubitemid 24374761)
276. Oko R, Moussakova L, Clermont Y. 1990. Regional differences in composition of the perforatorium and outer periacrosomal layer of the rat spermatozoon as revealed by immunocytochemistry. Am J Anat 188: 64-73. (Pubitemid 20135808)
277. Oko R, Hermo L, Chan PT, Fazel A, Bergeron JJ. 1993. The cytoplasmic droplet of rat epididymal spermatozoa contains saccular elements with Golgi characteristics. J Cell Biol 123: 809-821. (Pubitemid 23333571)
278. Oko R, Korley R, Murray MT, Hecht NB, Hermo L. 1996a. Germ cellspecific DNA and RNA binding proteins p48/52 are expressed at specific stages of male germ cell development and are present in the chromatoid body. Mol Reprod Dev 44: 1-13. (Pubitemid 26132078)
279. Oko RJ, Jando V, Wagner CL, Kistler WS, Hermo LS. 1996b. Chromatin reorganization in rat spermatids during the disappearance of testis-specific histone. H1t, and the appearance of transition proteins TP1 and TP2. Biol Reprod 54: 1141-1157.
280. Oliva R. 2006. Protamines and male infertility. Hum Reprod Update 12: 417-435. (Pubitemid 43923415)
281. Olson GE. 1979. Isolation of the fibrous sheath and perforatorium of rat spermatozoa. In: Fawcett DW, Bedford SJ, editors. The spermatozoon. Baltimore: Urban and Schwarzenberg. pp. 395-400.
282. Olson GE, Winfrey V. 1991. Structure-function relationships in the sperm acrosome. Ann N Y Acad Sci 637: 240-257.
283. Olson GE, Winfrey VP. 1994. Structure of acrosomal matrix domains of rabbit sperm. J Struct Biol 112: 41-48.
284. Olson GE, Hamilton DW, Fawcett DW. 1976. Isolation and characterization of the perforatorium of rat spermatozoa. J Reprod Fertil 47: 293-297.
285. Olson GE, Winfrey VP, Davenport GR. 1988. Characterization of matrix domains of the hamster acrosome. Biol Reprod 39: 1145-1158.
286. Pan J, Goodheart M, Chuma S, Nakatsuji N, Page DC, Wang PJ. 2005. RNF17, a component of the mammalian germ cell nuage, is essential for spermiogenesis. Development 132: 4029-4039. (Pubitemid 41488853)
287. Paniagua R, Nistal M, Amat P, Rodriguez MC. 1986. Ultrastructural observations on nucleoli and related structures during human spermatogenesis. Anat Embryol (Berl) 174: 301-306. (Pubitemid 16043636)
288. Parrish RF, Polakoski KL. 1979. Mammalian sperm proacrosin-acrosin system. Int J Biochem 10: 391-395.
289. Parvinen M. 2005. The chromatoid body in spermatogenesis. Int J Androl 28: 189-201. (Pubitemid 41075936)
290. Pasten C, Morales P, Kong M. 2005. Role of the sperm proteasome during fertilization and gamete interaction in the mouse. Mol Reprod Dev 71: 209-219. (Pubitemid 40605059)
291. Penttila TL, Parvinen M, Paranko J. 2003. Microtubule-associated epithelial protein E-MAP-115 is localized in the spermatid manchette. Int J Androl 26: 166-174. (Pubitemid 36718208)
292. Petrie RG Jr, Morales CR. 1992. Receptor-mediated endocytosis of testicular transferrin by germinal cells of the rat testis. Cell Tissue Res 267: 45-55.
293. Pires-daSilva A, Nayernia K, Engel W, Torres M, Stoykova A, Chowdhury K, Gruss P. 2001. Mice deficient for spermatid perinuclear RNA-binding protein show neurologic, spermatogenic, and sperm morphological abnormalities. Dev Biol 233: 319-328. (Pubitemid 32467679)
294. Pirhonen A, Linnala-Kankkunen A, Maenpaa PH. 1994. Identification of phosphoseryl residues in protamines from mature mammalian spermatozoa. Biol Reprod 50: 981-986. (Pubitemid 24116031)
295. Pouresmaeili F, Morales CR, Oko R. 1997. Molecular cloning and structural analysis of the gene encoding PERF 15 protein present in the perinuclear theca of the rat spermatozoa. Biol Reprod 57: 655-659. (Pubitemid 27349929)
296. Pradeepa MM, Rao MR. 2007. Chromatin remodeling during mammalian spermatogenesis: Role of testis specific histone variants and transition proteins. Soc Reprod Fertil Suppl 63: 1-10.
297. Prescott SM, Zimmerman GA, Stafforini DM, McIntyre TM. 2000. Platelet-activating factor and related lipid mediators. Annu Rev Biochem 69: 419-445.
298. Qin X, Krumrei N, Grubissich L, Dobarro M, Aktas H, Perez G, Halperin JA. 2003. Deficiency of the mouse complement regulatory protein mCd59b results in spontaneous hemolytic anemia with platelet activation and progressive male infertility. Immunity 18: 217-227. (Pubitemid 36262997)
299. Qin X, Dobarro M, Bedford SJ, Ferris S, Miranda PV, Song W, Bronson RT, Visconti PE, Halperin JA. 2005. Further characterization of reproductive abnormalities in mCd59b knockout mice: A potential new function of mCd59 in male reproduction. J Immunol 175: 6294-6302. (Pubitemid 41598868)
300. Ramalho-Santos J, Moreno RD. 2001. Targeting and fusion proteins during mammalian spermiogenesis. Biol Res 34: 147-152. (Pubitemid 32952130)
301. Ramalho-Santos J, Moreno RD, Wessel GM, Chan EK, Schatten G. 2001. Membrane trafficking machinery components associated with the mammalian acrosome during spermiogenesis. Exp Cell Res 267: 45-60. (Pubitemid 32579140)
302. Ranpura SA, Deshmukh U, Reddi PP. 2008. NF45 and NF90 in murine seminiferous epithelium: Potential role in SP-10 gene transcription. J Androl 29: 186-197. (Pubitemid 351345716)
303. Rattner JB, Olson G. 1973. Observations on the fine structure of the nuclear ring of the mammalian spermatid. J Ultrastruct Res 43: 438-444.
304. Reddi PP, Flickinger CJ, Herr JC. 1999. Round spermatid-specific transcription of the mouse SP-10 gene is mediated by a 294-base pair proximal promoter. Biol Reprod 61: 1256-1266.
305. Reddi PP, Shore AN, Acharya KK, Herr JC. 2002. Transcriptional regulation of spermiogenesis: Insights from the study of the gene encoding the acrosomal protein SP-10. J Reprod Immunol 53: 25-36.
306. Reddi PP, Urekar CJ, Abhyankar MM, Ranpura SA. 2007. Role of an insulator in testis-specific gene transcription. Ann N Y Acad Sci 1120: 95-103.
307. Richardson RT, Batova IN, Widgren EE, Zheng LX, Whitfield M, Marzluff WF, O'Rand MG. 2000. Characterization of the histone H1-binding protein. NASP, as a cell cycle-regulated somatic protein. J Biol Chem 275: 30378-30386.
308. Richardson RT, Alekseev OM, Grossman G, Widgren EE, Thresher R, Wagner EJ, Sullivan KD, Marzluff WF, O'Rand MG. 2006. Nuclear autoantigenic sperm protein (NASP), a linker histone chaperone that is required for cell proliferation. J Biol Chem 281: 21526-21534. (Pubitemid 44115489)
309. Rivkin E, Cullinan EB, Tres LL, Kierszenbaum AL. 1997. A protein associated with the manchette during rat spermiogenesis is encoded by a gene of the TBP-1-like subfamily with highly conserved ATPase and protease domains. Mol Reprod Dev 48: 77-89. (Pubitemid 27347041)
310. Rivkin E, Eddy EM, Willis WD, Goulding EH, Suganuma R, Yanagimachi R, Kierszenbaum AL. 2005. Sperm tail abnormalities in mutant mice with neo(r) gene insertion into an intron of the keratin 9 gene. Mol Reprod Dev 72: 259-271. (Pubitemid 41099415)
311. Rozman D. 2000. Lanosterol 14alpha-demethylase (CYP51) - A cholesterol biosynthetic enzyme involved in production of meiosis activating sterols in oocytes and testis - A minireview. Pflugers Arch 439(3 Suppl): R56-R57.
312. Rozman D, Fink M, Fimia GM, Sassone-Corsi P, Waterman MR. 1999. Cyclic adenosine 3′, 5′-monophosphate(cAMP)/cAMP-responsive element modulator (CREM)-dependent regulation of cholesterogenic lanosterol 14alpha-demethylase (CYP51) in spermatids. Mol Endocrinol 13: 1951-1962. (Pubitemid 30645267)
313. Rozman D, Cotman M, Frangez R. 2002. Lanosterol 14alpha-demeth-ylase and MAS sterols in mammalian gametogenesis. Mol Cell Endocrinol 187: 179-187. (Pubitemid 34436947)
314. Russell L, Frank B. 1978. Ultrastructural characterization of nuage in spermatocytes of the rat testis. Anat Rec 190: 79-97. (Pubitemid 8269779)
315. Russell LD, Russell JA, MacGregor GR, Meistrich ML. 1991. Linkage of manchette microtubules to the nuclear envelope and observations of the role of the manchette in nuclear shaping during spermiogenesis in rodents. Am J Anat 192: 97-120.
316. Ryan KJ, McCaffery JM, Wente SR. 2003. The Ran GTPase cycle is required for yeast nuclear pore complex assembly. J Cell Biol 160: 1041-1053.
317. Saade M, Irla M, Govin J, Victorero G, Samson M, Nguyen C. 2007. Dynamic distribution of Spatial during mouse spermatogenesis and its interaction with the kinesin KIF17b. Exp Cell Res 313: 614-626. (Pubitemid 46201812)
318. Sadek CM, Jimenez A, Damdimopoulos AE, Kieselbach T, Nord M, Gustafsson JA, Spyrou G, Davis EC, Oko R, van der Hoorn FA, Miranda-Vizuete A. 2003. Characterization of human thioredoxin-like 2. A novel microtubule-binding thioredoxin expressed predominantly in the cilia of lung airway epithelium and spermatid manchette and axoneme. J Biol Chem 278: 13133-13142. (Pubitemid 36805602)
319. Salanova M, Chun SY, Iona S, Puri C, Stefanini M, Conti M. 1999. Type 4 cyclic adenosine monophosphate-specific phosphodiesterases are expressed in discrete subcellular compartments during rat spermiogenesis. Endocrinology 140: 2297-2306. (Pubitemid 30636471)
320. Sarg B, Chwatal S, Talasz H, Lindner HH. 2009. Testis-specific linker histone H1t is multiply phosphorylated during spermato-genesis. Identification of phosphorylation sites. J Biol Chem 284: 3610-3618.
321. Sasagawa I, Matsuki S, Suzuki Y, Iuchi Y, Tohya K, Kimura M, Nakada T, Fujii J. 2001. Possible involvement of the membranebound form of peroxiredoxin 4 in acrosome formation during spermiogenesis of rats. Eur J Biochem 268: 3053-3061. (Pubitemid 32862991)
322. Sasaki S, Shionoya A, Ishida M, Gambello MJ, Yingling J, Wynshaw-Boris A, Hirotsune S. 2000. A LIS1/NUDEL/cytoplasmic dynein heavy chain complex in the developing and adult nervous system. Neuron 28: 681-696. (Pubitemid 32038064)
323. Sasao T, Itoh N, Takano H, Watanabe S, Wei G, Tsukamoto T, Kuzumaki N, Takimoto M. 2004. The protein encoded by cancer/testis gene D40/AF15q14 is localized in spermatocytes, acrosomes of spermatids and ejaculated spermatozoa. Reproduction 128: 709-716. (Pubitemid 40028547)
324. Sassone-Corsi P. 2005. Transcription factors governing male fertility. Andrologia 37: 228-229.
325. Saunders PT, Millar MR, Maguire SM, Sharpe RM. 1992. Stage-specific expression of rat transition protein 2 mRNA and possible localization to the chromatoid body of step 7 spermatids by in situ hybridization using a nonradioactive riboprobe. Mol Reprod Dev 33: 385-391.
326. Schmidt S, Joost HG, Schurmann A. 2009. GLUT8, the enigmatic intracellular hexose transporter. Am J Physiol Endocrinol Metab 296: E614-E618.
327. Schneider M, Forster H, Boersma A, Seiler A, Wehnes H, Sinowatz F, Neumuller C, Deutsch MJ, Walch A, Hrabe de Angelis M, Wurst W, Ursini F, Roveri A, Maleszewski M, Maiorino M, Conrad M. 2009. Mitochondrial glutathione peroxidase 4 disruption causes male infertility. FASEB J 23: 3233-3242.
328. Schultz MC. 1990. Three structures associated with the nucleolus in male rat germinal cells: Round body, coiled body, and ''nubecula'' and general presence of round body at male meiosis. Am J Anat 189: 11-23.
329. Schultz MC, Leblond CP. 1990. Nucleolar structure and synthetic activity during meiotic prophase and spermiogenesis in the rat. Am J Anat 189: 1-10.
330. Schultz MC, Hermo L, Leblond CP. 1984. Structure, development, and cytochemical properties of the nucleolus-associated "round body" in rat spermatocytes and early spermatids. Am J Anat 171: 41-57. (Pubitemid 14028768)
331. Schumacher JM, Lee K, Edelhoff S, Braun RE. 1995. Spnr, a murine RNA-binding protein that is localized to cytoplasmic microtubules. J Cell Biol 129: 1023-1032.
332. Schumacher JM, Artzt K, Braun RE. 1998. Spermatid perinuclear ribonucleic acid-binding protein binds microtubules in vitro and associates with abnormal manchettes in vivo in mice. Biol Reprod 59: 69-76. (Pubitemid 28304355)
333. Schurmann A, Koling S, Jacobs S, Saftig P, Krauss S, Wennemuth G, Kluge R, Joost HG. 2002. Reduced sperm count and normal fertility in male mice with targeted disruption of the ADP-ribosylation factor-like 4 (Arl4) gene. Mol Cell Biol 22: 2761-2768. (Pubitemid 34262996)
334. Segretain D. 1989. Endocytosis in spermatids during spermiogenesis of the mouse. Biol Cell 67: 289-298. (Pubitemid 20022769)
335. Segretain D, Roussel C. 1988. Endocytic origin for periaxonemal vesicles along the flagellum during mouse spermiogenesis. Gamete Res 21: 451-463. (Pubitemid 19185287)
336. Seidah NG, Day R, Hamelin J, Gaspar A, Collard MW, Chretien M. 1992. Testicular expression of PC4 in the rat: Molecular diversity of a novel germ cell-specific Kex2/subtilisin-like proprotein convertase. Mol Endocrinol 6: 1559-1570.
337. Setchell BP. 1978. The mammalian testis. London: Paul Elek.
338. Shamsadin R, Adham IM, Nayernia K, Heinlein UA, Oberwinkler H, Engel W. 1999. Male mice deficient for germ-cell cyritestin are infertile. Biol Reprod 61: 1445-1451.
339. Shang E, Salazar G, Crowley TE, Wang X, Lopez RA, Wolgemuth DJ. 2004. Identification of unique, differentiation stage-specific patterns of expression of the bromodomain-containing genes Brd2. Brd3, Brd4, and Brdt in the mouse testis. Gene Expr Patterns 4: 513-519. (Pubitemid 38992392)
340. Shang E, Nickerson HD, Wen D, Wang X, Wolgemuth DJ. 2007. The first bromodomain of Brdt, a testis-specific member of the BET subfamily of double-bromodomain-containing proteins, is essential for male germ cell differentiation. Development 134: 3507-3515. (Pubitemid 350028369)
341. Shetty J, Wolkowicz MJ, Digilio LC, Klotz KL, Jayes FL, Diekman AB, Westbrook VA, Farris EM, Hao Z, Coonrod SA, Flickinger CJ, Herr JC. 2003. SAMP14, a novel, acrosomal membrane-associated, glycosylphosphatidylinositol- anchored member of the Ly-6/uroki-nase-type plasminogen activator receptor superfamily with a role in sperm-egg interaction. J Biol Chem 278: 30506-30515. (Pubitemid 36994554)
342. Shibata N, Tsunekawa N, Okamoto-Ito S, Akasu R, Tokumasu A, Noce T. 2004. Mouse RanBPM is a partner gene to a germline specific RNA helicase, mouse vasa homolog protein. Mol Reprod Dev 67: 1-7. (Pubitemid 37467331)
343. Shirley CR, Hayashi S, Mounsey S, Yanagimachi R, Meistrich ML. 2004. Abnormalities and reduced reproductive potential of sperm from Tnp1-and Tnp2-null double mutant mice. Biol Reprod 71: 1220-1229. (Pubitemid 39249807)
344. Singh J, Rao MR. 1987. Interaction of rat testis protein. TP, with nucleic acids in vitro. Fluorescence quenching, UV absorption, and thermal denaturation studies. J Biol Chem 262: 734-740. (Pubitemid 17005245)
345. Smith CE, Hermo L, Fazel A, Lalli MF, Bergeron JJ. 1990. Ultrastructural distribution of NADPase within the Golgi apparatus and lysosomes ofmammalian cells. Prog Histochem Cytochem 21: 1-120. (Pubitemid 20278362)
346. Smrzka OW, Delgehyr N, Bornens M. 2000. Tissue-specific expression and subcellular localisation of mammalian delta-tubulin. Curr Biol 10: 413-416. (Pubitemid 30213390)
347. Soderstrom KO. 1981. Annulate lamellae in the spermatids of the rat. Z Mikrosk Anat Forsch 95: 845-854.
348. Soderstrom KO, Parvinen M. 1976. Transport ofmaterial between the nucleus, the chromatoid body and the Golgi complex in the early spermatids of the rat. Cell Tissue Res 168: 335-342.
349. Sonnack V, Failing K, Bergmann M, Steger K. 2002. Expression of hyperacetylated histone H4 during normal and impaired human spermatogenesis. Andrologia 34: 384-390. (Pubitemid 35463785)
350. Soues S, Kann ML, Fouquet JP, Melki R. 2003. The cytosolic chaperonin CCT associates to cytoplasmic microtubular structures during mammalian spermiogenesis and to heterochromatin in germline and somatic cells. Exp Cell Res 288: 363-373. (Pubitemid 36959952)
351. Steinberger A, Dighe RR, Diaz J. 1984. Testicular peptides and their endocrine and paracrine functions. Arch Biol Med Exp (Santiago) 17: 267-271.
352. Su D, Novoselov SV, Sun QA, Moustafa ME, Zhou Y, Oko R, Hatfield DL, Gladyshev VN. 2005. Mammalian selenoprotein thioredoxin-glutathione reductase. Roles in disulfide bond formation and sperm maturation. J Biol Chem 280: 26491-26498. (Pubitemid 41022246)
353. Suarez-Quian CA, An Q, Jelesoff N, Dym M. 1991. The Golgi apparatus of rat pachytene spermatocytes during spermatogenesis. Anat Rec 229: 16-26.
354. Sun-Wada GH, Imai-Senga Y, Yamamoto A, Murata Y, Hirata T, Wada Y, Futai M. 2002. A proton pump ATPase with testis-specific E1-subunit isoform required for acrosome acidification. J Biol Chem 277: 18098-18105. (Pubitemid 34967624)
355. Sun CN, Chew EC, White HJ. 1977. Cytoplasmic annulate lamellae and intranuclear membranes in human spermatids and sperm. Cell Biol Int Rep 1: 345-351.
356. Susi FR, Clermont Y. 1970. Fine structural modifications of the rat chromatoid body during spermiogenesis. Am J Anat 129: 177-191.
357. Susi FR, Leblond CP, Clermont Y. 1971. Changes in the golgi apparatus during spermiogenesis in the rat. Am J Anat 130: 251-267.
358. Sutovsky P, Manandhar G, McCauley TC, Caamano JN, Sutovsky M, Thompson WE, Day BN. 2004. Proteasomal interference prevents zona pellucida penetration and fertilization in mammals. Biol Reprod 71: 1625-1637. (Pubitemid 39403259)
359. Sutton KA, Jungnickel MK, Florman HM. 2008. A polycystin-1 controls postcopulatory reproductive selection in mice. Proc Natl Acad Sci USA 105: 8661-8666.
360. Tanaka SS, Toyooka Y, Akasu R, Katoh-Fukui Y, Nakahara Y, Suzuki R, Yokoyama M, Noce T. 2000. The mouse homolog of Drosophila Vasa is required for the development of male germ cells. Genes Dev 14: 841-853. (Pubitemid 30215003)
361. Tanaka H, Iguchi N, Isotani A, Kitamura K, Toyama Y, Matsuoka Y, Onishi M, Masai K, Maekawa M, Toshimori K, Okabe M, Nishi-mune Y. 2005. HANP1/H1T2, a novel histone H1-like protein involved in nuclear formation and sperm fertility. Mol Cell Biol 25: 7107-7119. (Pubitemid 41105908)
362. Tang XM, Lalli MF, Clermont Y. 1982. A cytochemical study of the Golgi apparatus of the spermatid during spermiogenesis in the rat. Am J Anat 163: 283-294. (Pubitemid 12114506)
363. Tanii I, Araki S, Toshimori K. 1994. Intra-acrosomal organization of a 90-kilodalton antigen during spermiogenesis in the rat. Cell Tissue Res 277: 61-67. (Pubitemid 24196396)
364. Tarsounas M, Pearlman RE, Moens PB. 2001. CLIP-50 immunolocali-zation during mouse spermiogenesis suggests a role in shaping the sperm nucleus. Dev Biol 236: 400-410. (Pubitemid 32756993)
365. Taulman PD, Haycraft CJ, Balkovetz DF, Yoder BK. 2001. Polaris, a protein involved in left-right axis patterning, localizes to basal bodies and cilia. Mol Biol Cell 12: 589-599.
366. Tesarik J, Drahorad J, Testart J, Mendoza C. 1990. Acrosin activation follows its surface exposure and precedes membrane fusion in human sperm acrosome reaction. Development 110: 391-400. (Pubitemid 20330515)
367. Thiery G, Rambourg A. 1976. A new staining technique for studying thick sections in the electron microscope. J Microsc Biol Cell 26: 03-106.
368. Thorne-Tjomsland G, Clermont Y, Hermo L. 1988. Contribution of the Golgi apparatus components to the formation of the acrosomic system and chromatoid body in rat spermatids. Anat Rec 221: 591-598.
369. Thorne-Tjomsland G, Clermont Y, Tang XM. 1991. Glucose-6-phosphatase activity of endoplasmic reticulum and Golgi apparatus in spermatocytes and spermatids of the rat: An electron microscopic cytochemical study. Biol Cell 71: 33-41.
370. Tice LW, Barrnett RJ. 1963. The Fine Structural Localization of Some Testicular Phosphatases. Anat Rec 147: 43-63.
371. Tomes CN, Michaut M, De Blas G, Visconti P, Matti U, Mayorga LS. 2002. SNARE complex assembly is required for human sperm acrosome reaction. Dev Biol 243: 326-338. (Pubitemid 34218934)
372. Tomes CN, De Blas GA, Michaut MA, Farre EV, Cherhitin O, Visconti PE, Mayorga LS. 2005. alpha-SNAP and NSF are required in a priming step during the human sperm acrosome reaction. Mol Hum Reprod 11: 43-51. (Pubitemid 40331002)
373. Toshimori K, Yoshinaga K, Tanii I, Wakayama T, Saxena DK, Ohoka T. 2001. Protein expression and cell organelle behavior in spermatogenic cells. Kaibogaku Zasshi 76: 267-279. (Pubitemid 33773872)
374. Toyooka Y, Tsunekawa N, Takahashi Y, Matsui Y, Satoh M, Noce T. 2000. Expression and intracellular localization of mouse Vasa-homologue protein during germ cell development. Mech Dev 93: 139-149. (Pubitemid 30216503)
375. Tres LL, Kierszenbaum AL. 1996. Sak57, an acidic keratin initially present in the spermatid manchette before becoming a component of paraaxonemal structures of the developing tail. Mol Reprod Dev 44: 395-407.
376. Tsai-Morris CH, Lei S, Jiang Q, Sheng Y, Dufau ML. 2004. Genomic organization and transcriptional analysis of gonadotropin-regulated testicular RNA helicase-GRTH/DDX25 gene. Gene 331: 83-94. (Pubitemid 38501595)
377. Tseden K, Topaloglu O, Meinhardt A, Dev A, Adham I, Muller C, Wolf S, Bohm D, Schluter G, Engel W, Nayernia K. 2007. Premature translation of transition protein 2 mRNA causes sperm abnormalities and male infertility. Mol Reprod Dev 74: 273-279. (Pubitemid 46147803)
378. Tubb B, Mulholland DJ, Vogl W, Lan ZJ, Niederberger C, Cooney A, Bryan J. 2002. Testis fascin (FSCN3): A novel paralog of the actinbundling protein fascin expressed specifically in the elongate spermatid head. Exp Cell Res 275: 92-109.
379. Tulsiani DR, Abou-Haila A, Loeser CR, Pereira BM. 1998. The biological and functional significance of the sperm acrosome and acrosomal enzymes in mammalian fertilization. Exp Cell Res 240: 151-164. (Pubitemid 28371096)
380. Vale RD, Reese TS, Sheetz MP. 1985. Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility. Cell 42: 39-50.
381. Venable ME, Olson SC, Nieto ML, Wykle RL. 1993. Enzymatic studies of lyso platelet-activating factor acylation in human neutrophils and changes upon stimulation. J Biol Chem 268: 7965-7975.
382. Vigodner M, Morris PL. 2005. Testicular expression of small ubiquitin-related modifier-1 (SUMO-1) supports multiple roles in sperma-togenesis: Silencing of sex chromosomes in spermatocytes, spermatid microtubule nucleation, and nuclear reshaping. Dev Biol 282: 480-492. (Pubitemid 40799337)
383. Vigodner M, Ishikawa T, Schlegel PN, Morris PL. 2006. SUMO-1, human male germ cell development, and the androgen receptor in the testis of men with normal and abnormal spermatogenesis. Am J Physiol Endocrinol Metab 290: E1022-E1033.
384. Vitale ML, Akpovi CD, Pelletier RM. 2009. Cortactin/tyrosine- phosphorylated cortactin interactions with f-actin and connexin 43 in mouse seminiferous tubules. Microsc Res Tech 72: 856-867.
385. Vydra G. 1980. Incidence of lamellae annulatae in testicular biopsy material. Morphol Igazsagugyi Orv Sz 20: 187-191. (Pubitemid 11201509)
386. Walden PD, Cowan NJ. 1993. A novel 205-kilodalton testis-specific serine/threonine protein kinase associated with microtubules of the spermatid manchette. Mol Cell Biol 13: 7625-7635.
387. Walden PD, Millette CF. 1996. Increased activity associated with the MAST205 protein kinase complex during mammalian spermiogenesis. Biol Reprod 55: 1039-1044.
388. Walden CM, Sandhoff R, Chuang CC, Yildiz Y, Butters TD, Dwek RA, Platt FM, van der Spoel AC. 2007. Accumulation of glucosylceramide in murine testis, caused by inhibition of beta-glucosidase 2: Implications for spermatogenesis. J Biol Chem 282: 32655-32664. (Pubitemid 350159292)
389. Walt H, Armbruster BL. 1984. Actin and RNA are components of the chromatoid bodies in spermatids of the rat. Cell Tissue Res 236: 487-490. (Pubitemid 14143350)
390. Wang JC. 2002. Cellular roles of DNA topoisomerases: A molecular perspective. Nat Rev Mol Cell Biol 3: 430-440. (Pubitemid 34685700)
391. Wang R, Sperry AO. 2008. Identification of a novel Leucine-rich repeat protein and candidate PP1 regulatory subunit expressed in developing spermatids. BMC Cell Biol 9: 9. (Pubitemid 351454851)
392. Wang PJ, McCarrey JR, Yang F, Page DC. 2001. An abundance of X-linked genes expressed in spermatogonia. Nat Genet 27: 422-426. (Pubitemid 32268424)
393. Wang HM, Song CC, Duan CW, Shi WX, Li CX, Chen DY, Wang YC. 2002. Effects of ubiquitin-proteasome pathway on mouse sperm capacitation, acrosome reaction and in vitro fertilization. Chin Sci Bull 47: 127-132.
394. Ward WS. 1994. The structure of the sleeping genome: Implications of sperm DNA organization for somatic cells. J Cell Biochem 55: 77-82.
395. Ward WS, Partin AW, Coffey DS. 1989. DNA loop domains in mammalian spermatozoa. Chromosoma 98: 153-159.
396. Ward CR, Faundes D, Foster JA. 1999a. The monomeric GTP binding protein, rab3a, is associated with the acrosome in mouse sperm. Mol Reprod Dev 53: 413-421. (Pubitemid 29309932)
397. Ward WS, Kimura Y, Yanagimachi R. 1999b. An intact sperm nuclear matrix may be necessary for the mouse paternal genome to participate in embryonic development. Biol Reprod 60: 702-706. (Pubitemid 29102403)
398. Watanabe D, Sawada K, Koshimizu U, Kagawa T, Nishimune Y. 1992. Characterization of male meiotic germ cell-specific antigen (Meg 1) by monoclonal antibody TRA 369 in mice. Mol Reprod Dev 33: 307-312.
399. Watanabe D, Yamada K, Nishina Y, Tajima Y, Koshimizu U, Nagata A, Nishimune Y. 1994. Molecular cloning of a novel Ca(2+)-binding protein (calmegin) specifically expressed during male meiotic germ cell development. J Biol Chem 269: 7744-7749. (Pubitemid 24217989)
400. Werner G, Werner K. 1995. Immunocytochemical localization of his-tone H4 in the chromatoid body of rat spermatids. J Submicrosc Cytol Pathol 27: 325-330.
401. West AP, Willison KR. 1996. Brefeldin A and mannose 6-phosphate regulation of acrosomic related vesicular trafficking. Eur J Cell Biol 70: 315-321.
402. Westbrook-Case VA, Winfrey VP, Olson GE. 1994. A domain-specific 50-kilodalton structural protein of the acrosomal matrix is processed and released during the acrosome reaction in the guinea pig. Biol Reprod 51: 1-13.
403. Westbrook-Case VA, Winfrey VP, Olson GE. 1995. Sorting of the domain-specific acrosomal matrix protein AM50 during spermio-genesis in the guinea pig. Dev Biol 167: 338-349.
404. Williams RM, Jones R. 1991. Binding of zona pellucida glycoproteins to sperm proacrosin. Biochem Soc Trans 19: 412S.
405. Willins DA, Liu B, Xiang X, Morris NR. 1997. Mutations in the heavy chain of cytoplasmic dynein suppress the nudF nuclear migration mutation of Aspergillus nidulans. Mol Gen Genet 255: 194-200. (Pubitemid 27336275)
406. Wolfsberg TG, Straight PD, Gerena RL, Huovila AP, Primakoff P, Myles DG, White JM. 1995. ADAM, a widely distributed and developmentally regulated gene family encoding membrane proteins with a disintegrin and metalloprotease domain. Dev Biol 169: 378-383.
407. Wolkowicz MJ, Shetty J, Westbrook A, Klotz K, Jayes F, Mandal A, Flickinger CJ, Herr JC. 2003. Equatorial segment protein defines a discrete acrosomal subcompartment persisting throughout acrosomal biogenesis. Biol Reprod 69: 735-745. (Pubitemid 37064602)
408. Wolkowicz MJ, Digilio L, Klotz K, Shetty J, Flickinger CJ, Herr JC. 2008. Equatorial segment protein (ESP) is a human alloantigen involved in sperm-egg binding and fusion. J Androl 29: 272-282. (Pubitemid 351669017)
409. Wu XQ, Hecht NB. 2000. Mouse testis brain ribonucleic acid-binding protein/translin colocalizes with microtubules and is immunopreci-pitated with messenger ribonucleic acids encoding myelin basic protein, alpha calmodulin kinase II, and protamines 1 and 2. Biol Reprod 62: 720-725.
410. Wu JY, Ribar TJ, Cummings DE, Burton KA, McKnight GS, Means AR. 2000. Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4. Nat Genet 25: 448-452.
411. Wu AT, Sutovsky P, Xu W, van der Spoel AC, Platt FM, Oko R. 2007. The postacrosomal assembly of sperm head protein, PAWP, is independent of acrosome formation and dependent on microtubular manchette transport. Dev Biol 312: 471-483. (Pubitemid 350183969)
412. Wykes SM, Krawetz SA. 2003. The structural organization of sperm chromatin. J Biol Chem 278: 29471-29477.
413. Xu M, Xiao J, Chen J, Li J, Yin L, Zhu H, Zhou Z, Sha J. 2003. Identification and characterization of a novel human testis-specific Golgi protein. NYD-SP12. Mol Hum Reprod 9: 9-17. (Pubitemid 36285139)
414. Yamagata K, Murayama K, Okabe M, Toshimori K, Nakanishi T, Kashiwabara S, Baba T. 1998. Acrosin accelerates the dispersal of sperm acrosomal proteins during acrosome reaction. J Biol Chem 273: 10470-10474. (Pubitemid 28227657)
415. Yamagata K, Nakanishi T, Ikawa M, Yamaguchi R, Moss SB, Okabe M. 2002. Sperm from the calmegin-deficient mouse have normal abilities for binding and fusion to the egg plasma membrane. Dev Biol 250: 348-357. (Pubitemid 35216420)
416. Yamaguchi N, Takanezawa Y, Koizumi H, Umezu-Goto M, Aoki J, Arai H. 2004. Expression of NUDEL in manchette and its implication in spermatogenesis. FEBS Lett 566: 71-76. (Pubitemid 38625935)
417. Yan W, Assadi AH, Wynshaw-Boris A, Eichele G, Matzuk MM, Clark GD. 2003a. Previously uncharacterized roles of platelet-activating factor acetylhydrolase 1b complex in mouse spermatogenesis. Proc Natl Acad Sci USA 100: 7189-7194. (Pubitemid 36706414)
418. Yan W, Ma L, Burns KH, Matzuk MM. 2003b. HILS1 is a spermatidspecific linker histone H1-like protein implicated in chromatin remodeling during mammalian spermiogenesis. Proc Natl Acad Sci USA 100: 10546-10551. (Pubitemid 37071915)
419. Yang J, Chennathukuzhi V, Miki K, O'Brien DA, Hecht NB. 2003.Mouse testis brain RNA-binding protein/translin selectively binds to the messenger RNA of the fibrous sheath protein glyceraldehyde 3-phosphate dehydrogenase-S and suppresses its translation in vitro. Biol Reprod 68: 853-859. (Pubitemid 36245829)
420. Yang XJ. 2004. Lysine acetylation and the bromodomain: A new partnership for signaling. Bioessays 26: 1076-1087.
421. Yang WX, Sperry AO. 2003. C-terminal kinesin motor KIFC1 participates in acrosome biogenesis and vesicle transport. Biol Reprod 69: 1719-1729.
422. Yang WX, Jefferson H, Sperry AO. 2006. The molecular motor KIFC1 associates with a complex containing nucleoporin NUP62 that is regulated during development and by the small GTPase RAN. Biol Reprod 74: 684-690.
423. Yao R, Ito C, Natsume Y, Sugitani Y, Yamanaka H, Kuretake S, Yana-gida K, Sato A, Toshimori K, Noda T. 2002. Lack of acrosome formation in mice lacking a Golgi protein. GOPC. Proc Natl Acad Sci USA 99: 11211-11216. (Pubitemid 34920904)
424. Yildiz Y, Matern H, Thompson B, Allegood JC, Warren RL, Ramirez DM, Hammer RE, Hamra FK, Matern S, Russell DW. 2006. Mutation of beta-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J Clin Invest 116: 2985-2994. (Pubitemid 44684483)
425. Yoshida T, Ioshii SO, Imanaka-Yoshida K, Izutsu K. 1994. Association of cytoplasmic dynein with manchette microtubules and spermatid nuclear envelope during spermiogenesis in rats. J Cell Sci 107(Part 3): 625-633. (Pubitemid 24091867)
426. Yoshinaga K, Toshimori K. 2003. Organization and modifications of sperm acrosomal molecules during spermatogenesis and epididy-mal maturation. Microsc Res Tech 61: 39-45. (Pubitemid 36457545)
427. Yu Z, Hecht NB. 2008. The DNA/RNA-binding protein, translin, binds microRNA122a and increases its in vivo stability. J Androl 29: 572-579.
428. Yu YE, Zhang Y, Unni E, Shirley CR, Deng JM, Russell LD, Weil MM, Behringer RR, Meistrich ML. 2000. Abnormal spermatogenesis and reduced fertility in transition nuclear protein 1-deficient mice. Proc Natl Acad Sci USA 97: 4683-4688. (Pubitemid 30238618)
429. Yu Z, Raabe T, Hecht NB. 2005. MicroRNA Mirn122a reduces expression of the posttranscriptionally regulated germ cell transition protein 2 (Tnp2) messenger RNA (mRNA) by mRNA cleavage. Biol Reprod 73: 427-433. (Pubitemid 41170197)
430. Yu Y, Xu W, Yi YJ, Sutovsky P, Oko R. 2006. The extracellular protein coat of the inner acrosomal membrane is involved in zona pellucida binding and penetration during fertilization: Characterization of its most prominent polypeptide (IAM38). Dev Biol 290: 32-43. (Pubitemid 43083601)
431. Yuan R, Primakoff P, Myles DG. 1997. A role for the disintegrin domain of cyritestin, a sperm surface protein belonging to the ADAM family, in mouse sperm-egg plasma membrane adhesion and fusion. J Cell Biol 137: 105-112. (Pubitemid 27167299)
432. Yunes R, Michaut M, Tomes C, Mayorga LS. 2000. Rab3A triggers the acrosome reaction in permeabilized human spermatozoa. Biol Reprod 62: 1084-1089. (Pubitemid 30173825)
433. Zhao M, Shirley CR, Yu YE, Mohapatra B, Zhang Y, Unni E, Deng JM, Arango NA, Terry NH, Weil MM, Russell LD, Behringer RR, Meistrich ML. 2001. Targeted disruption of the transition protein 2 gene affects sperm chromatin structure and reduces fertility in mice. Mol Cell Biol 21: 7243-7255. (Pubitemid 32953478)
434. Zhao M, Shirley CR, Hayashi S, Marcon L, Mohapatra B, Suganuma R, Behringer RR, Boissonneault G, Yanagimachi R, Meistrich ML. 2004. Transition nuclear proteins are required for normal chromatin condensation and functional sperm development. Genesis 38: 200-213. (Pubitemid 38590851)
435. Zhao L, Burkin HR, Shi X, Li L, Reim K, Miller DJ. 2007a. Complexin I is required for mammalian sperm acrosomal exocytosis. Dev Biol 309: 236-244. (Pubitemid 47361111)
436. Zhao L, Shi X, Li L, Miller DJ. 2007b. Dynamin 2 associates with com-plexins and is found in the acrosomal region of mammalian sperm. Mol Reprod Dev 74: 750-757. (Pubitemid 46676838)
437. Zhao L, Reim K, Miller DJ. 2008. Complexin-I-deficient sperm are subfertile due to a defect in zona pellucida penetration. Reproduction 136: 323-334.
438. Zhong J, Peters AH, Lee K, Braun RE. 1999. A double-stranded RNA binding protein required for activation of repressed messages in mammalian germ cells. Nat Genet 22: 171-174. (Pubitemid 29264812)
439. Zhou J, Du YR, Qin WH, Hu YG, Huang YN, Bao L, Han D, Mansouri A, Xu GL. 2009. RIM-BP3 is a manchette-associated protein essential for spermiogenesis. Development 136: 373-382.
440. Zhu H, Chan HC, Zhou Z, Li J, Yin L, Xu M, Cheng L, Sha J. 2004. A Gene Encoding Sialic-Acid-Specific 9-O-Acetylesterase Found in Human Adult Testis. J Biomed Biotechnol 2004: 130-136. (Pubitemid 39287732)
441. Zhuang T, Kashiwabara S, Noguchi J, Baba T. 2004. Transgenic expression of testis-specific poly(A) polymerase TPAP in wild-type and TPAP-deficient mice. J Reprod Dev 50: 207-213. (Pubitemid 40631820)