Fibrous sheath of mammalian spermatozoa

Microscopy Research and Technique

Volumn 61, Issue 1, 2003, Pages 103-115

  Eddy, Edward M ^a   Toshimori, Kiyotaka ^b   O'Brien, Deborah A ^c  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

^b UNIVERSITY OF MIYAZAKI   (Japan)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

Author keywords

AKAP; Cytoskeleton; GAPDS; Glycolysis; Signal transduction; Sperm motility

Indexed keywords

CELL SIGNALING; ENZYMES; MAMMALS; SCAFFOLDS (BIOLOGY);

AKAP; CYTOSKELETAL STRUCTURES; CYTOSKELETONS; DEGREE OF FLEXIBILITY; GLYCERALDEHYDE 3-PHOSPHATE DEHYDROGENASE-S; GLYCERALDEHYDE-3-PHOSPHATE DEHYDROGENASE; GLYCOLYSIS; GLYCOLYTIC PATHWAYS; SPERM MOTILITY; SPERMATOGENIC CELLS;

SIGNAL TRANSDUCTION;

CELL PROTEIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP DEPENDENT PROTEIN KINASE ANCHORING PROTEIN; GLUTATHIONE TRANSFERASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GUANOSINE TRIPHOSPHATASE; HEXOKINASE; INTERMEDIATE FILAMENT PROTEIN; PROTEIN AKAP3; PROTEIN AKAP4; PROTEIN TAKAP 80; RHO FACTOR; RHOPHILIN; ROPPORIN; UNCLASSIFIED DRUG;

ACROSOME REACTION; ANIMAL CELL; ARTICLE; AXONEME; CELL STRUCTURE; ENZYME ACTIVITY; FLAGELLUM; GENE EXPRESSION; GLYCOLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; SIGNAL TRANSDUCTION; SPERMATOGENESIS; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION; SPERMATOZOON MOTILITY; ZONA PELLUCIDA;

ANIMALIA; MAMMALIA;

EID: 0037405197     PISSN: 1059910X     EISSN: None     Source Type: Journal    
DOI: 10.1002/jemt.10320     Document Type: Article

References (129)

1. Aitken RJ, Gordon E, Harkiss D, Twigg JP, Milne P, Jennings Z, Irvine SD. 1998. Relative impact of oxidative stress on the functional competence and genomic integrity of human spermatozoa. Biol Reprod 59:1037-1046.
2. Amieux PS, Cummings DE, Motamed K, Brandon EP, Wailes LA, Le K, Idzerda RL, McKnight GS. 1997. Compensatory regulation of RIa protein levels in protein kinase A mutant mice. J Biol Chem 272:3993-3998.
3. Arora KK, Fanciulli M, Pedersen PL. 1990. Glucose phosphorylation in tumor cells: cloning, sequencing, and overexpression in active form of a full length cDNA encoding a mitochondrial bindable form of hexokinase. J Biol Chem 265:6481-6488.
4. Austin CR. 1985. Sperm maturation in the male and female genital tracts. In: Metz CB, Monroy A, editors. Biology of fertilization. New York: Academic Press. p 121-155.
5. Bedford JM, Calvin HI. 1974. Changes in -S-S- linked structures of the sperm tail during epididymal maturation, with comparative observations in sub-mammalian species. J Exp Zool 187:181-204.
6. Bishop AL, Hall A. 2000. Rho GTPases and their effector proteins. Biochem J 348(Pt 2):241-255.
7. Blake JA, Eppig JT, Richardson JE, Davisson MT. 2000. The mouse genome database (MGD): expanding genetic and genomic resources for the laboratory mouse. Nucleic Acids Res 28:108-111.
8. Boer PH, Adra CN, Lau Y-F, McBurney MW. 1987. The testis-specific phosphoglycerate kinase gene pgk-2 is a recruited retroposon. Mol Cell Biol 7:3107-3112.
9. Brito M, Figueroa J, Maldonado EU, Vera JC, Burzio LO. 1989. The major component of the rat sperm fibrous sheath is a phosphoprotein. Gamete Res 22:205-217.
10. Brooks DE. 1976. Activity and androgenic control of glycolytic enzymes in the epididymis and epididymal spermatozoa in the rat. Biochem J 156:527-537.
11. Brown-Woodman PD, White IG. 1976. Disruption of the metabolism, motility and morphology of spermatozoa by injection of α-chlorohydrin into rams. Aust J Biol Sci 29:545-555.
12. Brown-Woodman PD, Mohri H, Mohri T, Suter D, White IG. 1978. Mode of action of alpha-chlorohydrin as a male anti-fertility agent. Inhibition of the metabolism of ram spermatozoa by alpha-chlorohydrin and location of block in glycolysis. Biochem J 170:23-37.
13. Buck J, Sinclair ML, Cann MJ, Levin LR. 1999. Cytosolic adenylyl cyclase defines a unique signaling molecule in mammals. Proc Natl Acad Sci USA 96:79-84.
14. Buehr M, McLaren A. 1981. An electrophoretically detectable modification of glucosephosphate isomerase in mouse spermatozoa. J Reprod Fert 63:169-173.
15. Bunch DO, Welch JE, Magyar PL, Eddy EM, O'Brien DA. 1998. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol Reprod 58:834-841.
16. Burton KA, Treash-Osio B, Muller CH, Denphy EL, McKnight GS. 1999. Deletion of type II alpha regulatory subunit delocalizes protein kinase A in mouse sperm without affecting motility or fertilization. J Biol Chem 272:24131-24136.
17. Caldwell K, Blake ET, Sensabaugh GF. 1976. Sperm diaphorase: genetic polymorphism of a sperm-specific enzyme in man. Science 191:1185-1187.
18. Campbell E, Takahashi Y, Abramovitz M, Peretz M, Listowsky I. 1990. A distinct human testis and brain μ-class glutathione S-transferase: molecular cloning and characterization of a form present even in individuals lacking hepatic type-mu isoenzymes. J Biol Chem 265:9188-9193.
19. Carr DW, Stofko-Hahn RE, Fraser IDC, Bishop SM, Acott TS, Brennan RG, Scott JD. 1991. Interaction of the regulatory subunit (RII) of cAMP-dependent protein kinase with RII-anchoring proteins occurs through an amphipathic helix binding motif. J Biol Chem 266:14188-14192.
20. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. 2001. Identification of sperm-specific proteins that interact with A-kinase anchoring proteins in a manner similar to the type II regulatory subunit of PKA. J Biol Chem 276:17332-17338.
21. Carrera A, Gerton GL, Moss SB. 1994. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol 165:272-284.
22. Carrera A, Moos J, Ning XP, Gerton GL, Kopf GS, Moss SB. 1996. Regulation of protein tyrosine phosphorylation in human sperm by a calcium/calmodulin-dependent mechanism: identification of A kinase anchor proteins as major substrates for tyrosine phosphorylation. Dev Biol 180:284-296.
23. Catalano RD, Vlad M, Kennedy RC. 1997. Differential display to identify and isolate novel genes expressed during spermatogenesis. Hum Reprod 3:215-221.
24. Catalano RD, Hillhouse EW, Vlad M. 2001. Developmental expression and characterization of FS39, a testis complementary DNA encoding an intermediate filament-related protein of the sperm fibrous sheath. Biol Reprod 65:277-287.
25. Chemes HE. 2000. Phenotypes of sperm pathology: genetic and acquired forms in infertile men. J Androl 21:799-808.
26. Chemes HE, Olmedo SB, Carrere C, Oses R, Carizza C, Leisner N, Blaquier J. 1998. Ultrastructural pathology of the sperm flagellum: association between flagellar pathology and fertility prognosis in severely asthenozoospermic men. Hum Reprod 13:2521-2526.
27. Chen Y, Cann MJ, Litvin TN, Iourgenko V, Sinclair ML, Levin LR, Buck J. 2000. Soluble adenylyl cyclase as an evolutionarily conserved bicarbonate sensor. Science 289:625-628.
28. Cooper TG. 1984. The onset and maintenance of hyperactivated motility of spermatozoa in the mouse. Gamete Res 9:55-74.
29. Desseyn J-L, Burton KA, McKnight GS. 2000. Expression of a non-myristylated variant of the catalytic subunit of protein kinase A during male germ-cell development. Proc Natl Acad Sci USA 97:6433-6438.
30. Draveland E, Meizel S. 1981. Stimulation of hamster sperm capacitation and acrosome reaction in vitro by glucose and lactate and inhibition by the glycolytic inhibitor alpha-chlorohydrin. Gamete Res 4:515-523.
31. Eddy EM, O'Brien DA. 1994. The spermatozoon. In: Knobil E, Neill JD, editors. The physiology of reproduction. New York: Raven Press. p 29-77.
32. Eddy EM, O'Brien DA, Fenderson BA, Welch JE. 1991. Intermediate filament-like proteins in the fibrous sheath of the mouse sperm flagellum. Ann NY Acad Sci 637:224-239.
33. Eddy EM, Welch JE, Mori C, Fulcher KD, O'Brien DA. 1994. Role and regulation of spermatogenic cell-specific gene expression: enzymes of glycolysis. In: Bartke A, editor. Function of somatic cells in the testis. New York: Springer. p 362-372.
34. Edward YH, Grootegoed A. 1983. A sperm-specific enolase. J Reprod Fertil 68:305-310.
35. Edwards AS, Scott JD. 2000. A-kinase anchoring proteins: protein kinase A and beyond. Curr Opin Cell Biol 12:217-221.
36. El-Alfy M, Moshonas D, Moralies CR, Oko R. 1999. Molecular cloning and developmental expression of the major fibrous sheath protein (FS75) of rat sperm. J Androl 20:307-318.
37. Fawcett DW. 1975. The mammalian spermatozoon. Dev Biol 44:394-436.
38. Fenderson BA, Toshimori K, Muller CH, Lane TF, Eddy EM. 1988. Identification of a protein in the fibrous sheath of the sperm flagellum. Biol Reprod 38:345-357.
39. Ford WCL, Harrison A. 1983. The activity of glyceraldehyde 3-phosphate dehydrogenase in spermatozoa from different regions of the epididymis in laboratory rodents treated with α-chlorohydrin or 6-chloro-deoxyglucose. J Reprod Fertil 69:147-156.
40. Fraser LR, Herod JE. 1990. Expression of capacitation-dependent changes in chlortetracycline fluorescence patterns in mouse spermatozoa requires a suitable glycolysable substrate. J Reprod Fertil 88:611-621.
41. Fraser LR, Quinn PJ. 1981. A glycolytic product is obligatory for initiation of the sperm acrosome reaction and whiplash motility required for fertilization in the mouse. J Reprod Fertil 61:25-35.
42. Fujita A, Nakamura K, Kato T, Watanabe N, Ishizaki T, Kimura K, Mizoguchi A, Narumiya S. 2000. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Science 113:103-112.
43. Fulcher KD, Welch JE, Klapper DG, O'Brien DA, Eddy EM. 1995a. Identification of a unique μ-class glutathione S-transferase in mouse spermatogenic cells. Mol Reprod Dev 42:415-424.
44. Fulcher KD, Mori C, Welch JE, O'Brien DA, Klapper DG, Eddy EM. 1995b. Characterization of Fsc1 cDNA for a mouse sperm fibrous sheath component. Biol Reprod 52:41-49.
45. Fundele R, Winking H, Illmensee K, Jagerbauer E-M. 1987. Developmental activation of phosphoglycerate mutase-2 in the testis of the mouse. Dev Biol 124:562-566.
46. Gillis BA, Tamblyn TA. 1984. Association of bovine sperm aldolase with sperm subcellular components. Biol Reprod 31:25-35.
47. Gitlitis VK, Toh BH, Loveland KL, Sentry JH. 2000. The glycolytic enzyme enolase is present in sperm tail and displays nucleotide-dependent association with microtubules. Eur J Cell Biol 79:104-111.
48. Grootegoed JA, Jansen R, van der Molen HJ. 1986. Effect of glucose on ATP dephosphorylation in rat spermatids. J Reprod Fertil 77:99-107.
49. Guthrie CR, Skålhegg BS, McKnight GS. 1997. Two novel brain-specific splice variants of the murine C-beta gene of cAMP-dependent protein kinase. J Biol Chem 272:29560-29565.
50. Han JR, Yiu GK, Hecht NB. 1995. Testis/brain RNA-binding protein attaches translationally repressed and transported mRNAs to microtubules. Proc Natl Acad Sci USA 92:9550-9554.
51. Hinsch KD, Habermann B, Just I, Hinsch E, Pfisterer S, Schill WB, Aktories K. 1993. ADP-ribosylation of Rho proteins inhibits sperm motility. FEBS Lett 334:32-36.
52. Horowitz JM, Toeg H, Orr GA. 1984. Characterization and localization of cAMP-dependent protein kinases in rat caudal epididymal sperm. J Biol Chem 259:832-838.
53. Hoshi K, Tsukikawa S, Sato A. 1991. Importance of Ca2+, K+ and glucose in the medium for sperm penetration through the human zona pellucida. Tohoku J Exp Med 165:99-104.
54. Irons MJ, Clermont Y. 1982. Kinetics of fibrous sheath formation in the rat spermatid. Am J Anat 165:121-130.
55. Johnson LR, Foster JA, Haig-Ladewig L, VanScoy H, Rubin C, Moss SB, Gerton GB. 1997. Assembly of AKAP82, a protein kinase A anchor protein, into the fibrous sheath of mouse sperm. Dev Biol 192:340-350.
56. Jones AR. 1978. The antifertility actions of α-chlorohydrin in the male. Life Sci 23:1625-1646.
57. Jones AR, Cooper TG. 1999. A re-appraisal of the post-testicular action and toxicity of chlorinated antifertility compounds. Int J Androl 22:130-138.
58. Katzen HM. 1967. The multiple forms of mammalian hexokinase and their significance to the action of insulin. In: Weber G, editor. Advances in enzyme regulation, vol. 5. New York: Pergamon Press. p 335-356.
59. Katzen HM, Solerman DD, Cirillo VJ. 1968. Tissue distribution and physiological significance of multiple forms of hexokinase. Ann NY Acad Sci 151:351-358.
60. Kim YH, McFarlane JR, Almahbobi G, Stanton PG, Temple-Smith PD, De Kretser DM. 1995. Isolation and partial characterization of rat sperm tail fibrous sheath proteins and comparison with rabbit and human spermatozoa using a polyclonal antiserum. J Reprod Fertil 104:107-114.
61. Kopf GS, Ning XP, Visconti PE, Purdon M, Galantino-Homer H, Fornés. 1999. Signaling mechanisms controlling mammalian sperm fertilization competence and activation. In: Gagnon C, editor. The male gamete: from basic science to clinical applications. Vienna, IL: Cache River Press. p 106-118.
62. Leclerc P, De Lamirande E, Gagnon C. 1996. Cyclic adenosine 3',5' monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod 55:684-692.
63. Lin RY, Moss SB, Rubin CS. 1995. Characterization of S-AKAP, a novel developmentally regulated A kinase anchor protein of male germ cells. J Biol Chem 270:27804-27811.
64. Lindemann CB, Orlando A, Kanous KS. 1972. The flagellar beat of rat sperm is organized by the interaction of two functionally distinct populations of dynein bridges with a stable central axonemal partition. J Cell Sci 102:249-260.
65. Listowsky I, Rowe JD, Patskovsky YV, Tchaikovskaya T, Shintani N, Novikova E, Nieves E. 1998. Human testicular glutathione S-transferases: insights into tissue-specific expression of the diverse subunit classes. Chem Biol Interact 111-112:103-112.
66. Mahadevan MM, Miller MM, Moutos DM. 1997. Absence of glucose decreases human fertilization and sperm movement characteristics in vitro. Hum Reprod 12:119-123.
67. Mandal A, Naaby-Hansen S, Wolkowicz M, Klotz K, Shetty J, Retief J, Coonrod S, Kinter M, Sherman N, Cesar F, Flickinger C, Herr J. 1999. FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod 61:1184-1197.
68. McCarrey JR, Thomas K. 1987. Human testis-specific PGK gene lacks introns and possesses characteristics of a processed gene. Nature 326:501-505.
69. Mei X, Singh IS, Erlichman J, Orr GA. 1997. Cloning and characterization of a testis-specific, developmentally regulated A-kinase-anchoring protein (TAKAP-80) present on the fibrous sheath of rat sperm. Eur J Biochem 246:425-432.
70. Miki K, Eddy EM. 1998. Identification of tethering domains for protein kinase A type Ia regulatory subunits on sperm fibrous sheath protein FSC1. J Biol Chem 273:34384-34390.
71. Miki K, Eddy EM. 1999. Single amino acids determine specificity of binding of protein kinase A regulatory subunits by protein kinase A anchoring proteins. J Biol Chem 274:29057-29062.
72. Millan JL, Driscoll CE, LeVan KM, Goldberg E. 1987. Epitopes of human testis-specific lactate dehydrogenase deduced from a cDNA sequence. Proc Natl Acad Sci USA 84:5311-5315.
73. Mohri H, Mohri T, Ernster L. 1965. Isolation and enzymatic properties of the midpiece of bull spermatozoa. Exp Cell Res 38:217-246.
74. Moos J, Peknicová J, Geussova G, Philimonenko V, Hozák P. 1998. Association of protein kinase A type I with detergent-resistant structures of mammalian sperm cells. Mol Reprod Dev 50:79-85.
75. Mori C, Welch JE, Sakai Y, Eddy EM. 1992. In situ localization of spermatogenic cell-specific glyceraldehyde 3-phosphate dehydrogenase (Gapd-s) messenger ribonucleic acid in mice. Biol Reprod 46:859-868.
76. Mori C, Welch JE, Fulcher KD, O'Brien DA, Eddy EM. 1993. Unique hexokinase messenger ribonucleic acids lacking the porin-binding domain are developmentally expressed in mouse spermatogenic cells. Biol Reprod 49:191-203.
77. Mori C, Nakamura N, Welch JE, Shiota K, Eddy EM. 1996. Testis-specific expression ofmRNAs for a unique human type 1 hexokinase lacking the porin-binding domain. Mol Reprod Dev 44:14-22.
78. Mori C, Nakamura N, Welch JE, Gotoh H, Goulding EH, Fajioka M, Eddy EM. 1998. Mouse spermatogenic-cell specific type 1 hexokinase (mHk1-s) transcripts are expressed by alternative splicing from the mHk1 gene and the HK1-S protein is localized mainly in the sperm tail. Mol Reprod Dev 49:374-385.
79. Moss S, VanScoy H, Gerton GL. 1997. Mapping of a haploid transcribed and translated sperm-specific gene to the mouse X chromosome. Mamm Genome 8:37-38.
80. Nakamura M, Fujiwara A, Yasamasu I, Okinaga S, Arai K. 1982. Regulation of glucose metabolism by adenine nucleotides in round spermatids from rat testes. J Biol Chem 257:13945-13950.
81. Nakamura K, Fujita A, Murata T, Watanabe G, Mori C, Fujita J, Watanabe N, Ishizaki T, Yoshida O, Narumiya S. 1999. Rhophilin, a small GTPase Rho-binding protein, is abundantly expressed in the mouse testis and localized in the principal piece of the sperm tail. FEBS Lett 445:9-13.
82. Neill JM, Olds-Clarke P. 1987. A computer-assisted assay for mouse sperm hyperactivation demonstrates that bicarbonate but not bovine serum albumin is required. Gamete Res 18:121-140.
83. Oko R, Clermont Y. 1989. Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec 225:46-55.
84. Olson GE, Sammons DW. 1980. Structural chemistry of outer dense fibers of rat sperm. Biol Reprod 22:319-332.
85. Olson GE, Hamilton DW, Fawcett DW. 1976. Isolation and characterization of the fibrous sheath of rat epididymal sperm. Biol Reprod 14:517-530.
86. Pawson T, Scott JD. 1997. Signaling through scaffold, anchoring, and adaptor proteins. Science 278:2075-2080.
87. Rawe VY, Galaverna GD, Acosta AA, Olmedo SB, Chemes HE. 2001. Incidence of tail structure distortions associated with dysplasia of the fibrous sheath in human spermatozoa. Hum Reprod 16:879-886.
88. Reinton N, Haugen TB, Skålhegg BS, Hanson V, Jahnsen T. 1998. The gene encoding the C gamma catalytic subunit of cAMP-dependent protein kinase of ovine sperm flagella has a unique amonoterminal sequence. Genomics 49:290-297.
89. Reinton N, Ørstavik S, Haugen TB, Jahnsen K, Taskén K, Skålhegg BS. 2000. A novel isoform of human cyclic 3',5'-adenosine monophosphate-dependent protein kinase, Cα-s, localizes to sperm midpiece. Biol Reprod 63:607-611
90. Rowe JD, Tchaikovskaya T, Shintani N, Listowsky I. 1998a. Selective expression of a glutathione S-transferase subclass during spermatogenesis. J Androl 19:558-567.
91. Rowe JD, Patskovsky YV, Mastokovska LN, Novikova E, Listowsky I. 1998b. Rationale for reclassification of a distinctive subdivision of mammalian class Mu glutathione S-transferases that are primarily expressed in testis. J Biol Chem 273:9593-9601
92. Russell DL, Kim KH. 1996. Expression of triosephosphate isomerase transcripts in rat testis: evidence for retinol regulation and a novel germ cell transcript. Biol Reprod 55:11-18.
93. Sakai Y, Koyama Y-I, Fujimoto H, Nakamoto T, Yamashina S. 1986. Immunocytochemical study on fibrous sheath formation in mouse spermiogenesis using a monoclonal antibody. Anat Rec 215:119-126.
94. Sakai I, Sharief FS, Li S-L. 1987. Molecular cloning and nucleotide sequence of the cDNA for sperm-specific lactate dehydrogenase-C from mouse. Biochem J 242:619-922.
95. s and Ca1 isoforms of the catalytic subunit of cyclic 3',5'-adenosine monophosphate-dependent protein kinase in testicular cells. Biol Reprod 151-164.
96. San Agustin JT, Leszyk JD, Nuwaysir LM, Witman GB. 1998. The catalytic subunit of the cAMP-dependent protein kinase of ovine sperm flagella has a unique amino-terminal sequence. J Biol Chem 273:24874-24883.
97. Shalgi R, Seligman J, Kosower NS. 1989. Dynamics of the thiol status of rat spermatozoa during maturation: analysis with the fluorescent labeling agent monobromobimane. Biol Reprod 40:1037-1045.
98. Si Y, Okuno M. 1993. The sliding of the fibrous sheath through the axoneme proximally together with microtubule extrusion. Exp Cell Res 208:170-174.
99. Si Y, Okuno M. 1995. Extrusion of microtubule doublet outer dense fibers 5-6 associating with fibrous sheath sliding in mouse sperm flagella. J Exp Zool 273:355-362.
100. Si Y, Olds-Clarke P. 2000. Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol Reprod 62:1231-1239.
101. Sinclair ML, Wang X-Y, Mattia M, Conti M, Buck J, Wolgemuth DJ, Levin LR. 2000. Specific expression of soluble adenylyl cyclase in male germ cells. Mol Reprod Dev 56:6-11.
102. Smith GD, Wolf DP, Trautman KC, da Crez e Silva EF, Greengard P, Vijayaraghavan S. 1996. Primate sperm contain protein phosphatase 1, a biochemical mediator of motility. Biol Reprod 54:719-727.
103. Somlyo AP, Somlyo AV. 2000. Signal transduction by G-proteins, rho-kinase and protein phosphatase to smooth muscle and nonmuscle myosin II. J Physiol 522(Pt 2):177-185.
104. Sosa A, Altamirano E, Hernandez P, Rosado A. 1972. Developmental pattern of rat testis hexokinase. Life Sci 11:499-510.
105. Stevenson D, Jones AR. 1985. Production of (S)-3-chloroactaldehyde from (S)-α-chlorohydrin by boar spermatozoa and the inhibition of glyceraldehyde-3-phosphate dehydrogenase in vitro. J Reprod Fertil 74:157-165.
106. Storey BT, Kayne FJ. 1978. Energy metabolism of spermatozoa. VII. Interactions between lactate, pyruvate and malate as oxidative substrates for rabbit sperm mitochondria. Biol Reprod 18:527-536.
107. Storey BT, Kopf GS. 1991. Fertilization in the mouse II. Spermatozoa. In: Dunbar BS, O'Rand MG, editors. A comparative overview of mammalian fertilization. New York: Plenum Press. p 167-216.
108. Suarez SS. 1996. Hyperactivated motility in sperm. J Androl 17:331-335.
109. Takai Y, Sasaki T, Matozaki T. 2001. Small GTP-binding proteins. Physiol Rev 81:153-208.
110. Travis AJ, Foster JA, Rosenbaum NA, Visconti PE, Gerton GL, Moss SB. 1998. Targeting of a germ cell-specific type 1 hexokinase lacking a porin-binding domain to the mitochondria as well as to the head and fibrous sheath of murine spermatozoa. Mol Biol Cell 9:263-276.
111. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, Diaz-Cueto L, Storey BT, Kopf GS, Moss SB. 2001. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem 276:7630-7636.
112. Turner RMO, Johnson LR, Haig-Ladewig L, Gerton GL, Moss SB. 1998. An X-linked gene encodes a major human sperm fibrous sheath protein, hAKAP82. J Biol Chem 273:32135-32141.
113. Turner RMO, Ericksson RLM, Gerton GL, Moss SB. 1999. Relationship between sperm motility and the processing and tyrosine phosphorylation of two human sperm fibrous sheath proteins, prohAKAP83 and hAKAP82. Mol Hum Reprod 5:816-824.
114. Urner F, Sakkas D. 1996. Glucose participates in sperm-oocyte fusion in the mouse. Biol Reprod 55:917-922.
115. Urner F, Leppens-Luisier G, Sakkas D. 2001. Protein tyrosine phosphorylation in sperm during gamete interaction in the mouse: the influence of glucose. Biol Reprod 64:1350-1357.
116. VandeVoort CA, Overstreet JW. 1995. Effects of glucose and other energy substrates on the hyperactivated motility of Macaque sperm and the zona pellucida-induced acrosome reaction. J Androl 16:327-333
117. Vijayaraghavan S, Goueli SA, Davey MP, Carr DW. 1977. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem 272:4747-4752.
118. Vijayaraghavan S, Stephens DT, Trautman K, Smith GD, Khatra B, da Crus e Silva EF, Greengard P. 1996. Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol Reprod 54:709-718.
119. Vijayaraghavan S, Olson GE, NagDas S, Winfrey VP, Carr DW. 1997. Subcellular localization of the regulatory subunits of cyclic adenosine 3',5'-monophosphate-dependent protein kinase in bovine spermatozoa. Biol Reprod 57:1517-1523.
120. Vijayaraghavan S, Liberty G, Mohan J, Winfrey V, Olson G, Carr D. 1999. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endo 13:705-717.
121. Virbasius JV, Scarpulla RC. 1988. Structure and expression ofrodent genes encoding the testis-specific cytochrome c. Differences in gene structure and evolution between somatic and testicular variants. J Biol Chem 263:6791-6796.
122. Visconti PE, Olds-Clarke P, Moss SB, Kalab P, Travis AJ, de las Heras M, Kopf GS. 1996. Properties and localization of a tyrosine phosphorylated form of hexokinase in mouse sperm. Mol Reprod Dev 43:82-93.
123. Visconti PE, Johnson LR, Oyaski M, Fornés M, Moss SB, Gerton GL, Kopf GS. 1997. Regulation, localization, and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev Biol 192:351-363.
124. Visconti PE, Galantino-Homer H, Moore GD, Bailey JL, Ning X, Fornes M, Kopf GS. 1998. The molecular basis of sperm capacitation. J Androl 19:242-248.
125. Watanabe G, Saito J, Madaule P, Ishizaki T, Fujisawa K, Morii N, Mukai H, Ono Y, Kakizuka A, Narumiya S. 1996. Protein kinase N (PKN) and PKN-related protein rhophilin as targets of small FT-Pase Rho. Science 271:645-648.
126. Welch JE, Schatte EC, O'Brien DA, Eddy EM. 1992. Expression of a glyceraldehyde 3-phosphate dehydrogenase gene specific to mouse spermatogenic cells. Biol Reprod 46:869-878.
127. Welch JE, Brown PR, O'Brien DA, Eddy EM. 1995. Genomic organization of a mouse glyceraldehyde 3-phosphate dehydrogenase gene (Gapd-s) expressed in post-meiotic spermatogenic cells. Dev Genet 16:179-189.
128. Welch JE, Brown PL, O'Brien DA, Magyar PL, Bunch DO, Eddy EM. 2000. Human glyceraldehyde 3-phosphate dehydrogenase-2 gene is expressed specifically in spermatogenic cells. J Androl 21:328-338.
129. Yanagimachi R. 1994. Mammalian fertilization. In: Knobil E, Neill J, editors. The physiology of reproduction. New York: Raven Press. p 189-317.