Tales from the Tail: What Do We Really Know about Sperm Motility?

Journal of Andrology

Volumn 24, Issue 6, 2003, Pages 790-803

  Turner, Regina M ^a,b  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATE; DYNEIN ADENOSINE TRIPHOSPHATASE;

AXONEME; CALCIUM SIGNALING; CELL COMPARTMENTALIZATION; CELL ULTRASTRUCTURE; FERTILITY; FIBER; FIBROUS SHEATH; FLAGELLUM; GENETIC DISORDER; MALE INFERTILITY; MITOCHONDRIAL MEMBRANE; MITOCHONDRIAL SHEATH; OUTER DENSE FIBER; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SPERM ACTIVATED MOTILITY; SPERM HYPERACTIVATED MOTILITY; SPERMATOZOON MOTILITY; SPERMATOZOON TAIL;

EID: 0242541073     PISSN: 01963635     EISSN: None     Source Type: Journal    
DOI: 10.1002/j.1939-4640.2003.tb03123.x     Document Type: Review

References (161)

1. Afzelius BA. A human syndrome caused by immotile cilia. Science. 1976;193:317-319.
2. Afzelius BA, Eliasson R. Flagellar mutants in man: on the heterogeneity of the immotile-cilia syndrome. J Ultrastruct Res. 1979;69:43-52.
3. Aitken RJ, Ross A, Lees MM. Analysis of sperm function in Kartagener's syndrome. Fertil Steril. 1983;40:696-698.
4. Arden GB, Fox B. Increased incidence of abnormal nasal cilia in patients with retinitis pigmentosa. Nature. 1979;279:534-536.
5. 2+ channels by adhesion to the egg zona pellucida. Proc Natl Acad Sci USA. 1996;93:13004-13009.
6. Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci USA. 1999;96:6757-6762.
7. Arnoult C, Villaz M, Florman HM. Pharmacological properties of the T-type Ca2+ current of mouse spermatogenic cells. Mol Pharmacol. 1998;53:1104-1111.
8. Barak Y, Goldman S, Gonen Y, Nevo Z, Bartoov B, Kogosowski A. Does glucose affect fertilization, development and pregnancy rates of human in-vitro fertilized oocytes? Hum Reprod. 1998;13(suppl 4):203-211.
9. Bartoloni L, Blouin JL, Pan Y, et al. Mutations in the DNAH11 (axonemal heavy chain dynein type II) gene cause one form of situs inversus totalis and most likely primary ciliary dyskinesia. Proc Natl Acad Sci USA. 2002;99:10282-10286.
10. Bendahmane M, Lynch C II, Tulsiani DR. Calmodulin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa. Arch Biochem Biophys. 2001;390:1-8.
11. Benoff S. Voltage dependent calcium channels in mammalian spermatozoa. Front Biosci. 1998;3:D1220-1240.
12. Blouin JL, Meeks M, Radhakrishna U, et al. Primary ciliary dyskinesia: a genome-wide linkage analysis reveals extensive locus heterogeneity. Eur J Hum Genet. 2000;8:109-118.
13. Boatman DE, Robbins RS. Bicarbonate: carbon-dioxide regulation of sperm capacitation, hyperactivated motility, and acrosome reactions. Biol Reprod. 1991;44:806-813.
14. Boughman JA, Vernon M, Shaver KA. Usher syndrome: definition and estimate of prevalence from two high-risk populations. J Chronic Dis. 1983;36:595-603.
15. Boyle CA, Khoury MJ, Katz DF, Annest JL, Kresnow MJ, DeStefano F, Schrader SM. The relation of computer-based measures of sperm morphology and motility to male infertility. Epidemiology. 1992;3:239-246.
16. Bradley MP, Geelan A, Leitch V, Goldberg E. Cloning, sequencing, and characterization of LDH-C4 from a fox testis cDNA library. Mol Reprod Dev. 1996;44:452-459.
17. Brohmann H, Pinnecke S, Hoyer-Fender S. Identification and characterization of new cDNAs encoding outer dense fiber proteins of rat sperm. J Biol Chem. 1997;272:10327-10332.
18. Brokaw CJ. Flagellar movement: a sliding filament model. Science. 1972;178:455-462.
19. Brokaw CJ. Direct measurements of sliding between outer doublet microtubules in swimming sperm flagella. Science. 1989;243:1593-1596.
20. Brokaw CJ. Calcium sensors in sea urchin sperm flagella. Cell Motil Cytoskeleton. 1991;18:123-130.
21. Brown PA, Miki K, Harper DB, Eddy EM. A-kinase anchoring protein 4 binding proteins in the fibrous sheath of the sperm flagellum. Biol Reprod. 2003;68:2241-2248.
22. Bunch DO, Welch JE, Magyar PL, Eddy EM, O'Brien DA. Glyceraldehyde 3-phosphate dehydrogenase-S protein distribution during mouse spermatogenesis. Biol Reprod. 1998;58:834-841.
23. Burgos C, Maldonado C, Gerez de Burgos NM, Aoki A, Blanco A. Intracellular localization of the testicular and sperm-specific lactate dehydrogenase isozyme C4 in mice. Biol Reprod. 1995;53:84-92.
24. Burmester S, Hoyer-Fender S. Transcription and translation of the outer dense fiber gene (Odf1) during spermiogenesis in the rat: a study by in situ analyses and polysome fractionation. Mol Reprod Dev. 1996;45:10-20.
25. Burton KA, Treash-Osio B, Muller CH, Dunphy EL, McKnight GS. Deletion of type IIalpha regulatory subunit delocalizes protein kinase A in mouse sperm without affecting motility or fertilization. J Biol Chem. 1999;274:24131-24136.
26. Carr DW, Fujita A, Stentz CL, Liberty GA, Olson GE, Narumiya S. 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. 2001;276:17332-17338.
27. Carrera A, Gerton GL, Moss SB. The major fibrous sheath polypeptide of mouse sperm: structural and functional similarities to the A-kinase anchoring proteins. Dev Biol. 1994;165:272-284.
28. Carrera A, Moos J, Ning X, Gerton G, Tesarik J, Kopf G, Moss S. 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. 1996;180:284-296.
29. Chan PJ, Corselli JU, Patton WC, Jacobson JD, King A. Enhanced fertility after heat-induced hyperactivation. Fertil Steril. 1998;69:118-121.
30. Chemes HE, Brugo S, Zanchetti F, Carrere C, Lavieri JC. Dysplasia of the fibrous sheath: an ultrastructural defect of human spermatozoa associated with sperm immotility and primary sterility. Fertil Steril. 1987;48:664-669.
31. Clermont Y, Oko R, Hermo L. Immunocytochemical localization of proteins utilized in the formation of outer dense fibers and fibrous sheath in rat spermatids: an electron microscope study. Anat Rec. 1990;227:447-457.
32. Coghlan VM, Perrino BA, Howard M, Langeberg LK, Hicks JB, Gallatin WM, Scott JD. Association of protein kinase A and protein phosphatase 2B with a common anchoring protein. Science. 1995;267:108-111.
33. Du J, Tao J, Kleinhans FW, Mazur P, Critser JK. Water volume and osmotic behaviour of mouse spermatozoa determined by electron paramagnetic resonance. J Reprod Fertil. 1994;101:37-42.
34. Dutcher SK. Flagellar assembly in two hundred and fifty easy-to-follow steps. Trends Genet. 1995;11:398-404.
35. Eddy EM, Toshimori K, O'Brien DA. Fibrous sheath of mammalian spermatozoa. Microsc Res Tech. 2003;61:103-115.
36. Eliasson R, Mossberg B, Camner P, Afzelius B. The immotile cilia syndrome. N Engl J Med. 1977;297:1-6.
37. Fawcett DW. The anatomy of the mammalian spermatozoon with particular reference to the guinea pig. Z Zellforsch Mikrosk Anat. 1965;67:279-296.
38. Fawcett DW. The mammalian spermatozoon. Dev Biol. 1975;44:394-436.
39. Fawcett DW, Phillips DM. The fine structure and development of the neck region of the mammalian spermatozoon. Anat Rec. 1969;165:153-164.
40. Fraser LR, Quinn PJ. A glycolytic product is obligatory for initiation of the sperm acrosome reaction and whiplash motility required for fertilization in the mouse. J Reprod Fertil. 1981;61:25-65.
41. Fujita A, Nakamura K, Kato T, et al. Ropporin, a sperm-specific binding protein of rhophilin, that is localized in the fibrous sheath of sperm flagella. J Cell Sci. 2000;113:103-112.
42. Fulcher KD, Welch JE, Klapper DG, O'Brien DA, Eddy EM. Identification of a unique mu-class glutathione S-transferase in mouse spermatogenic cells. Mol Reprod Dev. 1995;42:415-424.
43. Gaddum-Rosse P. Some observations on sperm transport through the uterotubal junction of the rat. Am J Anat. 1981;160:333-341.
44. Gastmann O, Burfeind P, Gunther E, Hameister H, Szpirer C, Hoyer-Fender S. Sequence, expression, and chromosomal assignment of a human sperm outer dense fiber gene. Mol Reprod Dev. 1993;36:407-418.
45. Gibbons IR, Rowe A. Dynein: a protein with adenosine triphosphate activity from cilia. Science. 1965;149:424.
46. Gibson F, Walsh J, Mburu P, et al. A type VII myosin encoded by the mouse deafness gene shaker-1. Nature. 1995;374:62-64.
47. Guichard C, Harricane MC, Lafitte JJ, Godard P, Zaegel M, Tack V, Lalau G, Bouvagnet P. Axonemal dynein intermediate-chain gene (DNAII) mutations result in situs inversus and primary ciliary dyskinesia (Kartagener syndrome). Am J Hum Genet. 2001;68:1030-1035.
48. Hasson T, Heintzelman MB, Santos-Sacchi J, Corey DP, Mooseker MS. Expression in cochlea and retina of myosin VIIa, the gene product defective in Usher's syndrome type 1B. Proc Natl Acad Sci USA. 1995;92:9815-9819.
49. Hinsch KD, Habermann B, Just I, Hinsch E, Pfisterer S, Schill WB, Aktories K. ADP-ribosylation of Rho proteins inhibits sperm motility. FEBS Lett. 1993;334:32-36.
50. Ho HC, Granish KA, Suarez SS. Hyperactivated motility of bull sperm is triggered at the axoneme by Ca2+ and not cAMP. Dev Biol. 2002;250:208-217.
51. Ho HC, Suarez SS. Hyperactivation of mammalian spermatozoa: function and regulation. Reproduction. 2001;122:519-526.
52. Holzbaur EL, Vallee RB. DYNEINS: molecular structure and cellular function. Annu Rev Cell Biol. 1994;10:339-372.
53. Hoshi K, Tsukikawa S, Sato A. Importance of Ca2+, K+ and glucose in the medium for sperm penetration through the human zona pellucida. Tohoku J Exp Med. 1991;165:99-104.
54. Hoyer-Fender S, Burfeind P, Hameister H. Sequence of mouse Odf1 cDNA and its chromosomal localization: extension of the linkage group between human chromosome 8 and mouse chromosome 15. Cytogenet Cell Genet. 1995;70:200-204.
55. Hoyer-Fender S, Petersen C, Brohmann H, Rhee K, Wolgemuth DJ. Mouse Odf2 cDNAs consist of evolutionary conserved as well as highly variable sequences and encode outer dense fiber proteins of the sperm tail. Mol Reprod Dev. 1998;51:167-175.
56. Humphries P, Kenna P, Farrar J. On the molecular genetics of retinitis pigmentosa. Science. 1992;256:804-808.
57. Hunter DG, Fishman GA, Kretzer FL. Abnormal axonemes in X-linked retinitis pigmentosa. Arch Ophthalmol. 1988;106:362-368.
58. Hunter DG, Fishman GA, Mehta RS, Kretzer FL. Abnormal sperm and photoreceptor axonemes in Usher's syndrome. Arch Opthalmol. 1986;104:385-389.
59. Irons MJ, Clermont Y. Formation of the outer dense fibers during spermiogenesis in the rat. Anat Rec. 1982;202:463-471.
60. Ishijima S, Baba SA, Mohri H, Suarez SS. Quantitative analysis of flagellar movement in hyperactivated and acrosome-reacted golden hamster spermatozoa. Mol Reprod Dev. 2002;61:376-384.
61. Jha KN, Shivaji S. Identification of the major tyrosine phosphorylated protein of capacitated hamster spermatozoa as a homologue of mammalian sperm a kinase anchoring protein. Mol Reprod Dev. 2002;61:258-270.
62. Johnson L, Foster JA, Haig-Ladewig L, VanScoy H, Moss SM, Gerton GL. Assembly of AKAP82, a protein kinase A anchor protein, into the fibrous sheath of mouse sperm. Dev Biol. 1997;192:340-350.
63. Katz DF, Yanagimachi R. Movement characteristics of hamster spermatozoa within the oviduct. Biol Reprod. 1980;22:759-764.
64. Kierszenbaum AL, Rivkin E, Fefer-Sadler S, Mertz JR, Tres LL. Purification, partial characterization, and localization of Sak57, an acidic intermediate filament keratin present in rat spermatocytes, spermatids, and sperm. Mol Reprod Dev. 1996;44:382-394.
65. Kim Y, Adham IM, Haack T, Kremling H, Engel W. Molecular cloning and characterization of the bovine and porcine outer dense fibers cDNA and organization of the bovine gene. Biol Chem Hoppe-Seyler. 1995;376:431-435.
66. Klauck TM, Faux MC, Labudda K, Langeberg LK, Jaken S, Scott JD. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science. 1996;27:1589-1591.
67. Leclerc P, de Lamirande E, Gagnon C. Cyclic adenosine 3′,5′ monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod. 1996;55:684-692.
68. Lievano A, Santi CM, Serrano CJ, Trevino CL, Bellve AR, Hernandez-Cruz A, Darszon A. T-type Ca2+ channels and alpha1E expression in spermatogenic cells, and their possible relevance to the sperm acrosome reaction. FEBS Lett. 1996;388:150-154.
69. Lindemann CB, Goltz JS. Calcium regulation of flagellar curvature and swimming pattern in Triton X-100 extracted rat sperm. Cell Motil Cytoskeleton. 1988;10:420-431.
70. Lindemann CB, Orlando A, Kanous KS. 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. 1992;102:249-260.
71. Linford E, Glover FA, Bishop C, Stewart DL. The relationship between semen evaluation methods and fertility in the bull. J Reprod Fertil. 1976;47:283-291.
72. Lopez-Gonzalez I, De La Vega-Beltran JL, Santi CM, Florman HM, Felix R, Darszon A. Calmodulin antagonists inhibit T-type Ca(2+) currents in mouse spermatogenic cells and the zona pellucida-induced sperm acrosome reaction. Dev Biol. 2001;236:210-219.
73. Luck D, Piperno G, Ramanis Z, Huang B. Flagellar mutants of Chlamydomonas: studies of radial spoke-defective strains by dikaryon and revertant analysis. Proc Natl Acad Sci USA. 1977;74:3456-3460.
74. Lunenfeld B, Insler V. Infertility: the dimension of the problem. In: Insler V, Lunenfeld B, eds. Infertility: Male and Female. Edinburgh: Churchill Livingstone; 1993:3-7.
75. Mahadevan MM, Miller MM, Moutos DM. Absence of glucose decreases human fertilization and sperm movement characteristics in vitro. Hum Reprod. 1997;12:119-123.
76. Mahony MC, Gwathmey T. Protein tyrosine phosphorylation during hyperactivated motility of cynomolgus monkey (Macaca fascicularis) spermatozoa. Biol Reprod. 1999;60:1239-1243.
77. Mandal A, Naaby-Hansen S, Wolkowicz MJ, et al. FSP95, A testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa. Biol Reprod. 1999;61:1184-1197.
78. Matzuk MM, Lamb DJ. Genetic dissection of mammalian fertility pathways. Nat Cell Biol. 2002;4(suppl):S41-49.
79. Mei X, Singh I, Erlichman J, Orr G. 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. 1997;246:425-432.
80. Miki K, Eddy EM. Identification of tethering domains for protein kinase A type I alpha regulatory subunits on sperm fibrous sheath protein FSC1. J Biol Chem. 1998;273:34384-34390.
81. Miki K, Willis W, Brown P, Goulding E, Fulcher K, Eddy E. Targeted disruption of the AKAP4 gene causes defects in sperm flagellum and motility. Dev Biol. 2002;248:331-342.
82. Milisav I. Dynein and dynein-related genes. Cell Motil Cytoskeleton. 1998;39:261-272.
83. Morales CR, Oko R, Clermont Y. Molecular cloning and developmental expression of an mRNA encoding the 27 kDa outer dense fiber protein of rat spermatozoa. Mol Reprod Dev. 1994;37:229-240.
84. Mori C, Nakamura N, Welch JE, Gotoh H, Goulding EH, Fujioka M, Eddy EM. 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. 1998;49:374-385.
85. Moss SB, Turner RM, Burkert KL, VanScoy Butt H, Gerton GL. Conservation and function of a bovine sperm A-kinase anchor protein homologous to mouse AKAP82. Biol Reprod. 1999;61:335-342.
86. Nakamura K, Fujita A, Murata T, et al. 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. 1999;445:9-13.
87. Narayan D, Krishnan SN, Upender M, Ravikumar TS, Mahoney MJ, Dolan TF, Teebi AS, Haddad GG. Unusual inheritance of primary ciliary dyskinesia (Kartagener's syndrome). J Med Genet. 1994;31:493-496.
88. Narisawa S, Hecht NB, Goldberg E, Boatright KM, Reed JC, Millan JL. Testis-specific cytochrome c-null mice produce functional sperm but undergo early testicular atrophy. Mol Cell Biol. 2002;22:5554-5562.
89. Oko R, Clermont Y. Light microscopic immunocytochemical study of fibrous sheath and outer dense fiber formation in the rat spermatid. Anat Rec. 1989;225:46-55.
90. Olbrich H, Haffner K, Kispert A, et al. Mutations in DNAH5 cause primary ciliary dyskinesia and randomization of left-right asymmetry. Nat Genet. 2002;30:143-144.
91. Pennarun G, Escudier E, Chapelin C, et al. Loss-of-function mutations in a human gene related to Chlamydomonas reinhardtii dynein IC78 result in primary ciliary dyskinesia. Am J Hum Genet. 1999;65:1508-1519.
92. Pickett BW. Reproductive evaluation of the stallion. In: Mckinnon Ao, Voss JI, eds. Equine Reproduction. Philadelphia: Lea and Febiger; 1992:755-759.
93. FLA10 to reach the distal part of flagella in Chlamydomonas. J Cell Biol. 1996;133:371-379.
94. Porter ME, Johnson KE. Dynein structure and function. Annu Rev Cell Biol. 1989;5:119-151.
95. Porter ME, Sale WS. The 9 + 2 axoneme anchors multiple inner arm dyneins and a network of kinases and phosphatases that control motility. J Cell Biol. 2000;151:F37-42.
96. Quill TA, Ren D, Clapham DE, Garbers DL. A voltage-gated ion channel expressed specifically in spermatozoa. Proc Natl Acad Sci USA. 2001;98:12527-12531.
97. Quinn P, Moinipanah R, Steinberg JM, Weathersbee PS. Successful human in vitro fertilization using a modified human tubal fluid medium lacking glucose and phosphate ions. Fertil Steril. 1995;63:922-924.
98. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE. A sperm ion channel required for sperm motility and male fertility. Nature. 2001;413:603-609.
99. Roberts SJ. Infertility in male animals. In: Roberts SJ, ed. Veterinary Obstetrics and Genital Diseases: Theriogenology. Woodstock: SJ Roberts; 1986.
100. Rossman CM, Forrest JB, Ruffin RE, Newhouse MT. Immotile cilia syndrome in persons with and without Kartagener's syndrome. Am Rev Respir Dis. 1980;121:1011-1016.
101. Sakata Y, Saegusa H, Zong S, et al. Ca(v)2.3 (α 1E) Ca2+ channel participates in the control of sperm function. FEBS Lett. 2002;516:229-233.
102. Sale WS, Satir P. Direction of active sliding of microtubules in Tetrahymena cilia. Proc Natl Acad Sci USA. 1977;74:2045-2049.
103. San Augustin JT, Witman GB. Role of cAMP in the reactivation of demembranated ram spermatozoa. Cell Motil. Cytoskeleton 1994;27:206-218.
104. Satir P. Studies on cilia. 3: further studies on the cilium tip and a "sliding filament" model of ciliary motility. J Cell Biol. 1968;39:77-94.
105. Schalles U, Shao X, van der Hoorn FA, Oko R. Developmental expression of the 84-kDa ODF sperm protein: localization to both the cortex and medulla of outer dense fibers and to the connecting piece. Dev Biol. 1998;199:250-260.
106. Shao X, Tarnasky HA, Schalles U, Oko R, van der Hoorn FA. Interactional cloning of the 84-kDa major outer dense fiber protein Odf84: leucine zippers mediate associations of Odf84 and Odf27. J Biol Chem. 1997;272:6105-6113.
107. Shingyoji C, Murakami A, Takahashi K. Local reactivation of Triton-extracted flagella by iontophoretic application of ATP. Nature. 1977;265:269-270.
108. Si Y. Hyperactivation of hamster sperm motility by temperature-dependent tyrosine phosphorylation of an 80-kDa protein. Biol Reprod. 1999;61:247-252.
109. Si Y, Okuno M. The sliding of the fibrous sheath through the axoneme proximally together with microtubule extrusion. Exp Cell Res. 1993;208:170-174.
110. Si Y, Okuno M. Extrusion of microtubule doublet outer dense fibers 5-6 associating with fibrous sheath sliding in mouse sperm flagella. J Exp Zool. 1995;273:355-362.
111. Si Y, Okuno M. Role of tyrosine phosphorylation of flagellar proteins in hamster sperm hyperactivation. Biol Reprod. 1999;61:240-246.
112. Si Y, Olds-Clarke P. Evidence for the involvement of calmodulin in mouse sperm capacitation. Biol Reprod. 2000;62:1231-1239.
113. Skalhegg BS, Huang Y, Su T, Idzerda RL, McKnight GS, Burton KA. Mutation of the Calpha subunit of PKA leads to growth retardation and sperm dysfunction. Mol Endocrinol. 2002;16:630-639.
114. Smith EF. Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase. Mol Biol Cell. 2002;13:3303-3313.
115. Smith EF, Lefebvre PA. PFI6 encodes a protein with armadillo repeats and localizes to a single microtubule of the central apparatus in Chlamydomonas flagella. J Cell Biol. 1996;132:359-370.
116. Smith GD, Wolf DP, Trautman KC, da Cruz e Silva EF, Greengard P, Vijayaraghavan S. Primate sperm contain protein phosphatase 1, a biochemical mediator of motility. Biol Reprod. 1996;54:719-727.
117. Smith RJ, Berlin CI, Hejtmancik JF, et al. Clinical diagnosis of Usher's syndrome. Am J Med Genet. 1994;50:32-38.
118. Stauss CR, Votta TJ, Suarez SS. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol Reprod. 1995;53:1280-1285.
119. Storey BT, Kayne FJ. Energy metabolism of spermatozoa. V. The Embden-Myerhof pathway of glycolysis: activities of pathway enzymes in hypotonically treated rabbit epididymal spermatozoa. Fertil Steril. 1975;26:1257-1265.
120. Storey BT, Kayne FJ. Properties of pyruvate kinase and flagellar ATPase in rabbit spermatozoa: relation to metabolic strategy of the sperm cell. J Exp Zool. 1980;211:361-367.
121. Suarez SS, Katz DF, Owen DH, Andrew JB, Powell RL. Evidence for the function of hyperactivated motility in sperm. Biol Reprod. 1991;44:375-381.
122. Suarez SS, Osman RA. Initiation of hyperactivated flagellar bending in mouse sperm within the female reproductive tract. Biol Reprod. 1987;36:1191-1198.
123. Suarez SS, Vincenti L, Ceglia MW. Hyperactivated motility induced in mouse sperm by calcium ionophore A23187 is reversible. J Exp Zool. 1987;244:331-336.
124. Summers KE, Gibbons IR. Adenosine triphosphate-induced sliding of tnbules in trypsin-treated flagella of sea-urchin sperm. Proc Natl Acad Sci USA. 1971;68:3092-3096.
125. Tash JS. Protein phosphorylation: the second messenger signal transducer of flagellar motility. Cell Motil Cytoskeleton. 1989;14:332-339.
126. Tash JS, Bracho GE. Regulation of sperm motility: emerging evidence for a major role for protein phosphatases. J Androl. 1994;15:505-509.
127. Tash JS, Bracho GE. Identification of phosphoproteins coupled to initiation of motility in live epididymal mouse sperm. Biochem Biophys Res Commun. 1998;251:557-563.
128. Tash JS, Krinks M, Patel J, Means RL, Klee CB, Means AR. Identification, characterization and functional correlation of calmodulin-dependent protein phosphatase in sperm. J Cell Biol. 1988;106:1626-1633.
129. Tash JS, Means AR. Regulation of protein phosphorylation and motility of sperm by cyclic adenosine monophosphate and calcium. Biol Reprod. 1982;26:745-763.
130. Tash JS, Means AR. Cyclic adenosine 3′,5′ monophosphate, calcium and protein phosphorylation in flagellar motility. Biol Reprod. 1983;28:75-104.
131. Tash JS, Means AR. Ca2+ regulation of sperm axonemal motility. Methods Enzymol. 1987;139:808-823.
132. Travis AJ, Foster JA, Rosenbaum NA, Visconti PE, Gerton GL, Kopf GS, Moss SB. 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. 1998;9:263-276.
133. Tres LL, Kierszenbaum AL. Sak57, an acidic keratin initially present in the spermatid manchette before becoming a component of paraaxonemal structures of the developing tail. Mol Reprod Dev. 1996;44:395-407.
134. Turner RM, Eriksson RL, Gerton GL, Moss SB. Relationship between sperm motility and the processing and tyrosine phosphorylation of two human sperm fibrous sheath proteins, pro-hAKAP82 and hAKAP82. Mol Hum Reprod. 1999;5:816-824.
135. Turner RM, Johnson LJ, Haig-Ladewig L, Gerton GL, Moss SB. An X-linked gene encodes a major human sperm fibrous sheath protein, hAKAP82: genomic organization, protein kinase A-RII binding, and distribution of the precursor in the sperm tail. J Biol Chem. 1998;273:32135-32141.
136. Turner RM, Musse MP, Mandal A, et al. Molecular genetic analysis of two human sperm fibrous sheath proteins, AKAP4 and AKAP3, in men with dysplasia of the fibrous sheath. J Androl. 2001;22:302-315.
137. Urner F, Sakkas D. Glucose participates in sperm-oocyte fusion in the mouse. Biol Reprod. 1996;55:917-922.
138. Vijayaraghavan S, Goneli SA, Davey MP, Carr DW. Protein kinase A-anchoring inhibitor peptides arrest mammalian sperm motility. J Biol Chem. 1997;272:4747-4752.
139. Vijayaraghavan S, Liberty GA, Mohan J, Winfrey VP, Olson GE, Carr DW. Isolation and molecular characterization of AKAP110, a novel, sperm-specific protein kinase A-anchoring protein. Mol Endocrinol. 1999;13:705-717.
140. Vijayaraghavan S, Mohan J, Gray H, Khatra B, Carr DW. A role for phosphorylation of glycogen synthase kinase-3α in bovine sperm motility regulation. Biol Reprod. 2000;62:1647-1654.
141. Vijayaraghavan S, Stephens DT, Trautman K, Smith GD, Khatra B, da Cruz e Silva EF, Greengard P. Sperm motility development in the epididymis is associated with decreased glycogen synthase kinase-3 and protein phosphatase 1 activity. Biol Reprod. 1996;54:709-718.
142. Vijayaraghavan S, Trautman KD, Goueli SA, Carr DW. A tyrosine-phosphorylated 55-kilodalton motility-associated bovine sperm protein is regulated by cyclic adenosine 3′,5′-monophosphates and calcium. Biol Reprod. 1997;56:1450-1457.
143. Visconti P, Johnson L, Oyaski M, Fornes M, Moss S, Gerton G, Kopf G. Regulation, localization and anchoring of protein kinase A subunits during mouse sperm capacitation. Dev Biol. 1997;192:351-363.
144. Waite D, Steele R, Ross I, Wakefield JS, Mackay J, Wallace J. Cilia and sperm tail abnormalities in Polynesian bronchiectatics. Lancet. 1978;2:132-133.
145. Wallace MS. Canine reproduction: infertility in the male dog. Probl Vet Med. 1992;4:531-544.
146. Wargo MJ, Smith EF. Asymmetry of the central apparatus defines the location of active microtubule sliding in Chlamydomonas flagella. Proc Natl Acad Sci USA. 2003;100:137-142.
147. Weil D, Blanchard S, Kaplan J, et al. Defective myosin VIIA gene responsible for Usher syndrome type 1B. Nature. 1995;374:60-61.
148. Weinman S, Ores-Carton C, Rainteau D, Puszkin S. Immunoelectron microscopic localization of calmodulin and phospholipase A2 in spermatozoa. I. J Histochem Cytochem. 1986;34:1171-1179.
149. Wennemuth G, Westenbroek RE, Xu T, Hille B, Babcock DF. CaV2.2 and CaV2. 3 (N- and R-type) Ca2+ channels in depolarization-evoked entry of Ca2+ into mouse sperm. J Biol Chem. 2000;275:21210-21217.
150. Westenbroek RE, Babcock DF. Discrete regional distributions suggest diverse functional roles of calcium channel α1 subunits in sperm. Dev Biol. 1999;207:457-469.
151. Westhoff D, Kamp G. Glyceraldehyde 3-phosphate dehydrogenase is bound to the fibrous sheath of mammalian spermatozoa. J Cell Sci. 1997;110:1821-1829.
152. White DR, Aitken RJ. Relationship between calcium, cyclic AMP, ATP, and intracellular pH and the capacity of hamster spermatozoa to express hyperactivated motility. Gamete Res. 1989;22:163-177.
153. Wiesner B, Weiner J, Middendorff R, Hagen V, Kaupp UB, Weyand I. Cyclic nucleotide-gated channels on the flagellum control Ca2+ entry into sperm. J Cell Biol. 1998;142:473-484.
154. Williams AC, Ford WC. The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl. 2001;22:680-695.
155. Woolley DM. Striations in the peripheral fibers of rat and mouse spermatozoa. J Cell Biol. 1971;49:936-939.
156. World Health Organization. Prevention and Management of Infertility: Progress. Geneva: World Health Organization; 1990:15.
157. Yagi T, Kamiya R. Novel mode of hyper-oscillation in the paralyzed axoneme of Chlamydomonas mutant lacking the central-pair microtubules. Cell Motil Cytoskeleton. 1995;31:207-214.
158. Yanagimachi R. The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil. 1970;23:193-196.
159. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD, eds. The Physiology of Reproduction. 2nd ed. New York: Raven Press; 1994:189-317.
160. Zariwala M, Noone PG, Sannuti A, et al. Germline mutations in an intermediate chain dynein cause primary ciliary dyskinesia. Am J Respir Cell Mol Biol. 2001;25:577-583.
161. Zarsky HA, Cheng M, Van Der Hoorn FA. Novel RING finger protein OIP1 binds to conserved amino acid repeats in sperm tail protein ODF1. Biol Reprod. 2003;68:543-552.