The "switching on" of mammalian spermatozoa: molecular events involved in promotion and regulation of capacitation

Molecular Reproduction and Development

Volumn 77, Issue 3, 2010, Pages 197-208

  Fraser, Lynn R ^a  

^a KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE CYCLASE; ALBUMIN; CALCIUM; CYCLIC AMP; PHOSPHODIESTERASE; TYROSINE;

ACROSOME REACTION; CELL MEMBRANE; CULTURE MEDIUM; EJACULATION; ENVIRONMENT; FERTILIZATION; IN VITRO STUDY; IN VIVO STUDY; MAMMAL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY;

ANIMALS; MALE; MAMMALS; SPERM CAPACITATION; SPERMATOZOA;

MAMMALIA;

EID: 76649091227     PISSN: 1040452X     EISSN: 10982795     Source Type: Journal    
DOI: 10.1002/mrd.21124     Document Type: Review

References (88)

1. 2+- dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol Reprod Dev 44:111-120.
2. Adeoya-Osiguwa SA, Fraser LR. 2002. Capacitation state-dependent changes in adenosine receptors and their regulation of adenylyl cyclase/cAMP. Mol Reprod Dev 63:245-255.
3. Adeoya-Osiguwa SA, Fraser LR. 2003. Calcitonin acts as a first messenger to regulate adenylyl cyclase/cAMP and mammalian sperm function. Mol Reprod Dev 65:228-236.
4. 2- and β-adrenergic receptors in mammalian spermatozoa. Hum Reprod 21:1555-1563.
5. Arcelay E, Salicioni AM, Wertheimer E, Visconti PE. 2008. Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int J Dev Biol 52:463-472.
6. Asano A, Selvaraj V, Buttke DE, Nelson JL, Green KM, Evans JE, Travis AJ. 2009. Biochemical characterization of membrane fractions in murine sperm: Identification of three distinct subtypes of membrane rafts. J Cell Physiol 218:537-548.
7. Austin CR. 1951. Observations on the penetration of the sperm into the mammalian egg. Aust J Sci Res B 4:581-596.
8. Austin CR. 1952. The "capacitation" of the mammalian sperm. Nature 170:326.
9. Baxendale RW, Fraser LR. 2003a. Evidence for multiple distinctly localized adenylyl cyclase isoforms in mammalian spermatozoa. Mol Reprod Dev 66:181-189.
10. s. Mol Reprod Dev 65:104-113.
11. Baxendale RW, Fraser LR. 2005. Mammalian sperm phosphodiesterases and their involvement in receptor-mediated cell signalling important for capacitation. Mol Reprod Dev 71: 495-508.
12. Bedford JM, Chang MC. 1962. Removal of decapacitation factor from seminal plasma by high speed centrifugation. Am J Physiol 202:179-181.
13. Bentley JK, Garbers DL, Domino SE, Noland TD, Van Dop C. 1986. Spermatozoa contain a guanine nucleotide-binding protein ADP-ribosylated by pertussis toxin. Biochem Biophys Res Commun 138:728-734.
14. Buck J, Sinclair ML, Schapal L, Cann MJ, Levin LR. 1999. Cytosolic adenylyl cyclase defines a unique signalling molecule in mammals. Proc Natl Acad Sci USA 96:79-84.
15. Chang MC. 1951. Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697-698.
16. 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.
17. Choi YH, Toyoda Y. 1998. Cyclodextrin removes cholesterol from mouse sperm and induces capacitation in a protein-free medium. Biol Reprod 59:1328-1333.
18. Cross NL. 1998. Role of cholesterol in sperm capacitation. Biol Reprod 59:7-11.
19. Cross NL. 1999. Effects of methyl-beta-cyclodextrin on the acrosomal responsiveness of human sperm. Mol Reprod Dev 53:92-98.
20. Cross NL. 2004. Reorganization of lipid rafts during capacitation of human sperm. Biol Reprod 71:1367-1373.
21. Da Ros VG, Maldera JA, Willis WD, Cohen DJ, Goulding EH, Gelman DM, Rubinstein M, Eddy EM, Cuasnicu PS. 2008. Impaired sperm fertilizing ability in mice lacking cysteine-rich secretory protein 1 (CRISP1). Dev Biol 320:12-18.
22. 2+-ATPase in human sperm capacitation. J Reprod Fertil 102: 107-116.
23. de Lamirande E, Leclerc P, Gagnon C. 1997. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 3:175-194.
24. Devi KU, Jha K, Shivaji S. 1999. Plasma membrane-associated protein tyrosine phosphatase activity in hamster spermatozoa. Mol Reprod Dev 53:42-50.
25. Esposito G, Jaiswal BS, Xie F, Krajnc-Franken MA, Robben TJ, Strik AM, Kuil C, Philipsen RL, van Duin M, Conti M, Gossen JA. 2004. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc Natl Acad Sci USA 101:2993-2998.
26. Fisch JD, Behr B, Conti M. 1998. Enhancement of motility and acrosome reaction in human spermatozoa: Differential activation by type-specific phosphodiesterase inhibitors. Hum Reprod 13:1248-1254.
27. Flesch FM, Brouwers JFHM, Nievelstein PFEM, Verkleij AJ, Van Golde LMG, Colenbrander B, Gadella BM. 2001. Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114:3543-3555.
28. 2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev Biol 165:152-164.
29. Francis SH, Turko IV, Corbin JD. 2001. Cyclic nucleotide phosphodiesterases: Relating structure and function. Prog Nucleic Acid Res Mol Biol 65:1-52.
30. Fraser LR. 1984. Mouse sperm capacitation in vitro involves the loss of a surface-associated inhibitory component. J Reprod Fertil 72:373-384.
31. Fraser LR. 1998. Interactions between a decapacitation factor and mouse spermatozoa appear to involve fucose residues and a GPI-anchored receptor. Mol Reprod Dev 51:193-202.
32. Fraser LR, Adeoya-Osiguwa SA. 1999. Modulation of adenylyl cyclase by FPP and adenosine involves stimulatory and inhibitory adenosine receptors and G proteins. Mol Reprod Dev 53:459-471.
33. Fraser LR, Osiguwa OO. 2004. Human sperm responses to calcitonin, angiotensin II and fertilization-promoting peptide in prepared semen samples from normal donors and infertility patients. Hum Reprod 19:596-606.
34. Fraser LR, Harrison RAP, Herod JE. 1990. Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J Reprod Fertil 89:135-148.
35. 2+-regulating mechanisms that modulate bull sperm capacitation and acrosomal exocytosis as determined by chlortetracycline analysis. Mol Reprod Dev 40:233-241.
36. Fraser LR, Hosseini R, Hanyaloglu A, Talmor A, Dudley RK. 1997. TCP-11, the product of a mouse t-complex gene, plays a role in stimulation of capacitation and inhibition of the spontaneous acrosome reaction. Mol Reprod Dev 48:375-382.
37. Fraser LR, Adeoya-Osiguwa SA, Baxendale R. 2003. First messenger regulation of capacitation via G protein-coupled mechanisms: A tale of serendipity and discovery. Mol Hum Reprod 9:739-748.
38. Fraser LR, Adeoya-Osiguwa SA, Baxendale RW, Gibbons R. 2006. Regulation of mammalian sperm capacitation by endogenous molecules. Front Biosci 11:1636-1645.
39. Funahashi H, Asano A, Fujiwara T, Nagai T, Niwa K, Fraser LR. 2000a. Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in ejaculated boar spermatozoa in vitro. Mol Reprod Dev 55:117-124.
40. Funahashi H, Fujiwara T, Nagai T. 2000b. Modulation of the function of boar spermatozoa via adenosine and fertilization promoting peptide receptors reduces the incidence of polyspermic penetration into porcine oocytes. Biol Reprod 63:1157-1163.
41. Gadella BM, Harrison RAP. 2002. Capacitation induces cyclic adenosine 3′,5′-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340-350.
42. Galantino-Homer HL, Visconti PE, Kopf GS. 1997. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′,5′-monophosphate-dependent pathway. Biol Reprod 56:707-719.
43. Gibbons R, Adeoya-Osiguwa SA, Fraser LR. 2005. A mouse sperm decapacitation factor receptor is phosphatidylethanolamine-binding protein 1. Reproduction 130:497-508.
44. Green CM, Cockle SM, Watson PF, Fraser LR. 1996. A possible mechanism of action for fertilization promoting peptide, a TRH-related tripeptide that promotes capacitation and fertilizing ability in mammalian spermatozoa. Mol Reprod Dev 45:244-252.
45. Hanoune J, Defer N. 2001. Regulation and role of adenylyl cyclase isoforms. Ann Rev Pharm Toxicol 41:145-174.
46. Harrison RAP. 2004. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 67:337-352.
47. Harrison RAP, Gadella BM. 2005. Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63:342-351.
48. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, Buck J, Moss SB. 2005. The 'soluble' adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 9:249-259.
49. Hildebrandt JD, Codina J, Tash JS, Kirchick HJ, Lipschultz L, Sekura RD, Birnbaumer L. 1985. The membrane-bound spermatozoal adenylyl cyclase system does not share coupling characteristics with somatic cell adenylyl cyclases. Endocrinology 116:1357-1366.
50. Ho K, Wolff CA, Suarez SS. 2009. CatSper-null spermatozoa are unable to ascend beyond the oviductal reservoir. Reprod Fertil Dev 21:345-350.
51. Jha KN, Salicioni AM, Arcelay E, Chertihin O, Kumari S, Herr JC, Visconti PE. 2006. Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation. Mol Hum Reprod 12:781-789.
52. Jin J, Jin N, Zheng H, Ro S, Tafolla D, Sanders KM, Yan W. 2007. Catsper3 and Catsper4 are essential for sperm hyperactivated motility and male fertility. Biol Reprod 77:37-44.
53. Kalab P, Peknicova J, Geussova G, Moos J. 1998. Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Mol Reprod Dev 51:304-314.
54. Kamenetsky M, Middelhaufe S, Bank EM, Levin LR, Buck J, Steegborn C. 2006. Molecular details of cAMP generation in mammalian cells: A tale of two systems. J Mol Biol 362:623-639.
55. Kierszenbaum AL, Rivkin E, Talmor-Cohen A, Shalgi R, Tres LL. 2009. Expression of full-length and truncated Fyn tyrosine kinase transcripts and encoded proteins during spermatogenesis and localization during acrosome biogenesis and fertilization. Mol Reprod Dev 76:832-843.
56. 2+ channel. Nature 439:737-740.
57. Kopf GS, Woolkalis MJ, Gerton GL. 1986. Evidence for a guanine nucleotide-binding regulatory protein in invertebrate and mammalian sperm. Identification by islet-activating protein-catalyzed ADP-ribosylation and immunochemical methods. J Biol Chem 261:7327-7331.
58. Kumar P, Meizel S. 2005. Nicotinic acetylcholine receptor subunits and associated proteins in human sperm. J Biol Chem 280:25928-25935.
59. Lai EC. 2003. Lipid rafts make for slippery platforms. J Cell Biol 162:365-370.
60. Lalancette C, Faure RL, Leclerc P. 2006. Identification of the proteins present in the bull sperm cytosolic fraction enriched in tyrosine kinase activity: A proteomic approach. Proteomics 6:4523-4540.
61. 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.
62. Lefievre L, de Lamirande E, Gagnon C. 2002. Presence of cyclic nucleotide phosphodiesterases PDE1A, existing as a stable complex with calmodulin, and PDE3A in human spermatozoa. Biol Reprod 67:423-430.
63. Levine N, Marsh DJ. 1971. Micropuncture studies of the electrochemical aspects of fluid and electrolyte transport in individual seminiferous tubules, the epididymis and the vas deferens in rats. J Physiol 213:557-570.
64. Livera G, Xie F, Garcia MA, Jaiswal B, Chen J, Law E, Storm DR, Conti M. 2005. Inactivation of the mouse adenylyl cyclase 3 gene disrupts male fertility and spermatozoon function. Mol Endocrinol 19:1277-1290.
65. Mayor S, Riezman H. 2004. Sorting GPI-anchored proteins. Nat Rev Mol Cell Biol 5:110-120.
66. Nixon B, MacIntyre DA, Mitchell LA, Gibbs GM, O'Bryan M, Aitken RJ. 2006. The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol Reprod 74:275-287.
67. Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J, Kopf GS. 1999. Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation. Mol Hum Reprod 5: 1017-1026.
68. Pike LJ. 2009. The challenge of lipid rafts. J Lipid Res 50:S323-S328.
69. Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA, Clapham DE. 2007. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci USA 104:1219-1223.
70. Quill TA, Sugden SA, Rossi KL, Doolittle LK, Hammer RE, Garbers DL. 2003. Hyperactivated sperm motility driven by CatSper2 is required for fertilization. Proc Natl Acad Sci USA 100: 14869-14874.
71. Ren D, Navarro B, Perez G, Jackson AC, Hsu S, Shi Q, Tilly JL, Clapham DE. 2001. A sperm ion channel required for sperm motility and male fertility. Nature 413:603-609.
72. Rodriguez-Martinez H, Ekstedt E, Einarsson S. 1990. Acidification of epididymal fluid in the boar. Int J Androl 13:238-243.
73. Soderling SH, Beavo JA. 2000. Regulation of cAMP and cGMP signaling: New phosphodiesterases and new functions. Curr Opin Cell Biol 12:174-179.
74. Spehr M, Schwane K, Riffell JA, Barbour J, Zimmer RK, Neuhaus EM, Hatt H. 2004. Particulate adenylate cyclase plays a key role in human sperm olfactory receptor-mediated chemotaxis. J Biol Chem 279:40194-40203.
75. Spehr M, Schwane K, Riffell JA, Zimmer RK, Hatt H. 2006. Odorant receptors and olfactory-like signaling mechanisms in mammalian sperm. Mol Cell Endocrinol 250:128-136.
76. Suarez SS. 2008. Control of hyperactivation in sperm. Hum Reprod Update 14:647-657.
77. Sunahara RK, Taussig R. 2002. Isoforms of mammalian adenylyl cyclase: Multiplicities of signaling. Mol Interv 2:168-184.
78. van Gestel RA, Brewis IA, Ashton PR, Helms JB, Brouwers JF, Gadella BM. 2005. Capacitation dependent concentration of lipid rafts in the apical ridge head area of porcine sperm cells. Mol Hum Reprod 11:583-590.
79. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P, Kopf GS. 1995a. Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121:1129-1137.
80. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS. 1995b. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121:1139-1150.
81. Visconti PE, Galantino-Homer H, Ning X, Moore GD, Valenzuela JP, Jorgez CJ, Alvarez JG, Kopf GS. 1999a. Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J Biol Chem 274:3235-3242.
82. Visconti PE, Ning X, Fornes MW, Alvarez JG, Stein P, Connors SA, Kopf GS. 1999b. Cholesterol efflux-mediated signal transduction in mammalian sperm: Cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Dev Biol 214:429-443.
83. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezon JG. 1999c. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 61:76-84.
84. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. 2002. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 53:133-150.
85. Xie F, Garcia MA, Carlson AE, Schuh SM, Babcock DF, Jaiswal BS, Gossen JA, Esposito G, van Duin M, Conti M. 2006. Soluble adenylyl cyclase (sAC) is indispensable for sperm function and fertilization. Dev Biol 296:353-362.
86. Yanagimachi R. 1970. The movement of golden hamster spermatozoa before and after capacitation. J Reprod Fertil 23:193-196.
87. Yanagimachi R. 1994. Mammalian fertilization. In: Knobil E, Neill JD, editors. The Physiology of Reproduction, Vol. I, 2nd edition. New York: Raven Press, pp 189-317.
88. Zippin JH, Chen Y, Nahirney P, Kamenetsky M, Wuttke MS, Fischman DA, Levin LR, Buck J. 2003. Compartmentalization of bicarbonate-sensitive adenylyl cyclase in distinct signaling microdomains. FASEB J 17:82-84.