Current concepts of molecular events during bovine and porcine spermatozoa capacitation

Archives of Andrology

Volumn 53, Issue 3, 2007, Pages 109-123

  Vadnais, Melissa L ^a   Galantino Homer, Hannah L ^b   Althouse, Gary C ^b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Bovine; Capacitation; Lipid rafts; Porcine; Signal transduction; Spermatozoa

Indexed keywords

ADENYLATE CYCLASE; BICARBONATE; CALCIUM; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; ION; MEMBRANE LIPID;

ACROSOME; AUTOCRINE EFFECT; CALCIUM TRANSPORT; CELL LEVEL; CELL MEMBRANE; COW; EJACULATION; ENERGY METABOLISM; EXOCYTOSIS; FERTILIZATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIPID MEMBRANE; LIPID RAFT; MEMBRANE POTENTIAL; MOLECULAR BIOLOGY; NONHUMAN; PHYSIOLOGY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; SPERMATOZOON CAPACITATION; SPERMATOZOON MATURATION; SWINE; ZONA PELLUCIDA;

1-ALKYL-2-ACETYLGLYCEROPHOSPHOCHOLINE ESTERASE; ADENYLATE CYCLASE; ANIMALS; BICARBONATES; CALCIUM; CARRIER PROTEINS; CATTLE; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENERGY METABOLISM; HEPARIN; MALE; MEMBRANE LIPIDS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PLATELET ACTIVATING FACTOR; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SPERM CAPACITATION; SPERM MATURATION; SWINE;

EID: 79961199040     PISSN: 01485016     EISSN: 15210375     Source Type: Journal    
DOI: 10.1080/01485010701329386     Document Type: Review

References (157)

1. Adams, C. and Chang, M. (1962) The effect of delayed mating on fertilisation in the rabbit. J Exp Zool 151:155-158.
2. 2+ uptake by mouse spermatozoa in vitro correlates with changing functional potential. J Reprod Fertil 99:187-194.
3. Adeoya-Osiguwa, S. and Fraser, L. (2002) Capacitation state-dependent changes in adenosine receptors and their regulation of adenylyl cyclase/cAMP. Mol Reprod Devel 63:245-255.
4. Albarracin, J., Mogas, T., Palomo, M., Pena, A., Rigau, T. and Rodriguez-Gil, J. (2004) In vitro capacitation and acrosome reaction of dog spermatozoa can be feasibly attained in a defined medium without glucose. Reprod Domest Anim 39 (3):129-135.
5. i2 protein subunit, has a capacitative effect on human spermatozoa. Biol Reprod 64:1653-1659.
6. Althouse, G. C. (1992) Biochemical composition of the spermatozoal plasma membrane in normal and heat-stressed boars. Ph.D. Thesis, Iowa State University, USA.
7. Arnoult, C., Kazam, I., Visconti, P., Kopf, G., Villaz, M. and Florman, H. (1999) Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. PNAS 96:6757-6762.
8. Austin, C. (1951) Observations on the penetration of the sperm into the mammalian egg. Austral J Sci Res Series B 4:581-589.
9. Austin, C. (1952) The 'capacitation' of the mammalian sperm. Nature 170:326.
10. Austin, C. (1985) Sperm maturation in the male and female genital tracts. In: Biology of Fertilization. Monroy, A., (Ed). New York: Academic Press, pp 121-155.
11. Baldi, E., Casano, R., Falsetti, C., Krausz, C., Maggi, M. and Forti, G. (1991) Intracellular calcium accumulation and responsiveness to progesterone in capacitating human spermatozoa. Journal of Andrology 12:323-330.
12. +-activated NADPH oxidase in testis, spleen, and lymph nodes. J Biol Chem 276:37594-37601.
13. Baumber, J., Sabeur, K., Vo, A. and Ball, B. A. (2003) Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 60:1239-1247.
14. Bavister, B. (1973) Capacitation of golden hamster spermatozoa during incubation in culture medium. J Reprod Fertil 35:161-163.
15. Bize, I., Santander, G., Cabello, P., Driscoll, D. and Sharpe, C. (1991) Hydrogen peroxide is involved in hamster sperm capacitation in vitro. Biol Reprod 44:398-403.
16. Braun, T. (1975) The effect of divalent cations on bovine spermatozoal adenylate cyclase activity. J Cyclic Nucleo Res 1:227-281.
17. Breitbart, H. (2003): Signaling pathways in sperm capacitation and acrosome reaction. Cell Mol Biol 49:321-327.
18. Breitbart, H., Rubinstein, S. and Etkovitz, N. (2006) Sperm capacitation is regulated by the crosstalk between protein kinase A and C. Mol and Cell Endocrinol Signal. 252(1-2):247-249.
19. Brener, E., Rubinstein, S., Cohen, G., Shternall, K., Rivlin, J. and Breitbart, H. (2003) Remodeling of the actin cytoskeleton during mammalian sperm capacitation and acrosome reaction. Biol Reprod 68:837-845.
20. Calvete, J., Ensslin, M., Mburu, J., Iborra, A., Martinez, P., Adermann, K., Waberski, D., Sanz, L., Topfer-Petersen, E., Weitze, K. et al. (1997) Monoclonal antibodies against boar sperm zona pellucida-binding protein AWN-1. Characterization of a continuous antigenic determinant and immunolocalization of AWN epitopes in inseminated sows. Biol Reprod 57:735-742.
21. + entry and control of flagellar function in sperm. PNAS 100:14864-14868.
22. Carr, D., Fujita, A., Stentz, C., Liberty, G., Olson, G. and 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.
23. Carrera, A., Moos, J., Ning, X., Gerton, G. L., Tesarik, J., Kopf, G. S. and Moss, S. B. (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.
24. Centurion, F., Vazquez, J. M., Calvete, J. J., Roca, J., Sanz, L., Parrilla, I., Garcia, E. M. and Martinez, E. A. (2003) Influence of porcine spermadhesins on the susceptibility of boar spermatozoa to high dilution. Biol Reprod 69:640-646.
25. Chang, M. (1951) Fertilising capacity of spermatozoa deposited into the fallopian tubes. Nature 168:697.
26. Chang, M. (1952) Fertilisability of rabbit ova and the effects of temperature in vitro on their subsequent fertilisation and activation in vivo. J Exp Zool 121:351-381.
27. Chang, M. (1957) A detrimental effect of seminal plasma on the fertilizing capacity of sperm. Nature 179:258-259.
28. Cohen, G., Rubinstein, S., Gur, Y. and Breitbart, H. (2004) Crosstalk between protein kinase A and C regulates phospholipase D and F-actin formation during sperm capacitation. Developl Biol 267:230-241.
29. Cross, N. L. (1998) Role of cholesterol in sperm capacitation. Biol Reprod 59:7-11.
30. Cross, N. L. (2004) Reorganization of lipid rafts during capacitation of human sperm. Biol Reprod 71:1367-1373.
31. Dacheux, J. L., Belghazi, M., Lanson, Y. and Dacheux, F. (2006) Human epididymal secretome and proteome. Molecular and Cellular Endocrinology 250(1-2):36-42.
32. Davis, B. (1976) Inhibitory effect of synthetic phospholipid vesicles containing cholesterol on the fertilizing ability of rabbit spermatozoa. Proc Soc Exp Biol Med 152:257-261.
33. Davis, B. (1981) Timing of fertilization in mammals: Sperm cholesterol/phospholipid ration as a determinant of the capacitation interval. Cell Biol 78:7560-7564.
34. De Jonge, C., Han, H., Lawrie, H., Mack, S. and Zaneveld, L. (1991) Modulation of the human sperm acrosome reaction by effectors of the adenylate cyclase/cyclic AMP second-messenger pathway. J Exp Zool 258:113-125.
35. de Lamirande, E., Leclerc, P. and Gagnon, C. (1997) Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 3:175-194.
36. - cotransporter in mouse sperm capacitation. J Biol Chem 278:7001-7009.
37. Dube, C., Leclerc, P., Reyes-Moreno, C. and Bailey, J. L. (2005) The proacrosin binding protein, sp32, is tyrosine phosphorylated during capacitation of pig sperm. J Androl 26:519-528.
38. Dukelow, W., Chernoff, H. and Williams, W. (1967) Properties of decapacitation factor and presence in various species. J Reprod Fertil 14:393-399.
39. Ecroyd, H. W., Jones, R. C. and Aitken, R. J. (2003) Endogenous redox activity in mouse spermatozoa and its role in regulating the tyrosine phosphorylation events associated with sperm capacitation. Biol Reprod 69:347-354.
40. Ekhlasi-Hundrieser, M., Gohr, K., Wagner, A., Tsolova, M., Petrunkina, A. and Topfer-Petersen, E. (2005) Spermadhesin AQN1 is a candidate receptor molecule involved in the formation of the oviductal sperm reservoir in the pig. Biol Reprod 73:536-45.
41. Ericsson, R. (1967) Technology, physiology and morphology of spermatozoa capacitation. J Reprod Fertil Suppl 2:65-74.
42. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A. and Henson, P. M. (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85-90.
43. Fazeli, A. D. A., Watson, P. F. and Holt, W. V. (1999) Sperm-oviduct interaction: Induction of capacitation and preferential binding of uncapacitated spermatozoa to oviductal epithelial cells in porcine species. Biol Reprod 60:879-886.
44. Ficarro, S., Chertihin, O., Westbrook, V. A., White, F., Jayes, F., Kalab, P., Marto, J. A., Shabanowitz, J., Herr, J. C., Hunt, D. F. and Visconti, P. E. (2003) Phosphoproteome analysis of capacitated human sperm: Evidence of tyrosine phosphorylation of A kinase-anchoring protein 3 and valosin-containing protein/p97 during capacitation. J Biol Chem 278:11579-11589.
45. Flesch, F., Brouwers, J., Nievelstein, P., Verkleij, A., van Golde, L. and Gadella, B. (2001) Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Biol 114:3543-3555.
46. Florman, H., Corron, M., Kim, T. and Babcock, D. (1992) Activation of voltage-dependent calcium channels of mammalian sperm is required for zona pellucida-induced acrosomal exocytosis. Dev Biol 152:304-314.
47. Fraire-Zamora, J. J. and Gonzalez-Martinez, M. T. (2004) Effect of intracellular pH on the depolarization-evoked calcium influx in human sperm. Am J Physiol Cell Physiol 287:1688-1696.
48. Fraser, L. and Adeoya-Osiguwa, S. (1999) Modulation of adenylyl cyclase by FPP and adenosine involves stimulatory and inhibitory adenosine receptors and G proteins. Mol Reprod Devel 53:459-471.
49. Fraser, L. and Adeoya-Osiguwa, S. (2001) Fertilization promoting peptidea possible regulator of sperm function. Vitam Horm 63:1-28.
50. 2 in the atmosphere. J Reprod Fertil 33:159-161.
51. Fraser, L., Harrison, R. A. and Herod, J. (1990) Characterization of a decapacitation factor associated with epididymal mouse spermatozoa. J Reprod Fertil 89:135-148.
52. Fraser, L. and Quinn, P. (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.
53. Fraser, L. R., Pondel, M. D. and Vinson, G. P. (2001) Calcitonin, angiotensin II, and FPP significantly modulate mouse sperm function. Mol Hum Reprod 7:245-253.
54. Funahashi, H., Asano, A., Fujiwara, T., Nagai, T., Niwa, K. and Fraser, L. (2000) Both fertilization promoting peptide and adenosine stimulate capacitation but inhibit spontaneous acrosome loss in boar spermatozoa in vitro. Mol Reprod Develop 55:117-124.
55. Gadella, B. M. and Harrison, R. A. (2002) Capacitation induces cyclic adenosine 3′,5′ -monophosphate-dependent, but apoptosis-unrelated, exposure of animophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340-350.
56. Gadella, B. M. and Harrison, R. A. (2000) The capacitating agent bicarbonate induces protein kinase A-dependent changes in phospholipid transbilayer behavior in the sperm plasma membrane. Development. 127:2407-2420.
57. Gadella, B. M. and Harrison, R. A. (2002) Capacitation induces cyclic adenosine 3′,5′ -monophosphate-dependent, but apoptosis-unrelated, exposure of animophospholipids at the apical head plasma membrane of boar sperm cells. Biol Reprod 67:340-350.
58. Gadella, B. M. and van Gestel, R. A. (2004) Bicarbonate and its role in mammalian sperm function. Anim Reprod Sci 82-83:307-319.
59. Galantino-Homer, H. L. and Kopf, G. S. (2000) Purification and identification of major bovine sperm proteins undergoing cAMP-dependent protein tyrosine phosphorylation during in vitro capacitation Biol Reprod (Suppl) 62:78.
60. Galantino-Homer, H., Florman, H., Storey, B., Dobrinski, I. and Kopf, G. S. (2004) Bovine sperm capacitation: Assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Mol Reprod Develop 67:487-500.
61. Galantino-Homer, H. L., Visconti, P. E. and Kopf, G. S. (1997) Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3,5′-monophosphate-dependent pathway. Biol. Reprod 56:707-719.
62. Galantino-Homer, H., Zeng, W., Megee, S. O., Dallmeyer, M., Voelkl, D. and Dobrinski, I. (2006) Effects of beta-cyclodextrin and cholesterol on porcine sperm viability and capacitation status following cold shock or incubation. Mol Reprod Develop 73:638-650.
63. Garbers, D. L. and Kopf, G. S. (1980) The regulation of spermatozoa by calcium and cyclic nucleotides. Adv Cyclic Nucleo Res 13:251-306.
64. Green, C., Cockle, S., Watson, P. and Fraser, L. (1996) A possible mechanism of action for ferilization promoting peptide, a TRH-related tripeptide that promotes capacitation and fertilizing ability in mammalian spermatozoa. Mol Reprod Develop 45:244-252.
65. Gu, W. and Hecht, N. (1996) Translation of a testis-specific Cu/Zn superoxide dismutase (SOD-1) mRNA is regulated by a 65-kilodalton protein which binds to its 5′ untranslated region. Mol Cell Biol 16:4535-4543.
66. Gur, Y., Breitbart, H., Lax, Y., Rubinstein, S. and Zamir, N. (1998) Angiotensin II induces acrosomal exocytosis in bovine spermatozoa. Am J Physiol Endocrinol Metab 275:87-93.
67. Gwathmey, T. M., Ignotz, G. G., Mueller, J. L., Manjunath, P. and Suarez, S. S. (2006) Bovine seminal plasma proteins PDC-109, BSP-A3, and BSP-30-kDa share functional roles in storing sperm in the oviduct 1. Biol Reprod 76:501-507.
68. Hammer, C., Jennings, L., Sojika, N. (1970) Cat (Feris catus L.) spermatozoa require capacitation. J Reprod Fertil 23:477-480.
69. Handrow, R., First, N., Parrish, J. (1989) Calcium requirement and increased association with bovine sperm during capacitation by heparin. J Exp Zool 252:174-182.
70. Hao, Z., Jha, K. N., Kim, Y.-H., Vemuganti, S., Westbrook, V. A., Chertihin, O., Markgraf, K., Flickinger, C. J., Coppola, M., Herr, J. C. and Visconti, P. E. (2004) Expression analysis of the human testis-specific serine/threonine kinase (TSSK) homologues. A TSSK member is present in the equatorial segment of human sperm. Mol Hum Reprod 10:433-444.
71. Harayama, H., Magargee, S., Kunze, E., Shidara, O., Iwamoto, E., Arikawa, S., Miyake, M., Kato, S. and Hammerstedt, R. (1999) Changes in epididymal protein anti-agglutinin on ejaculated boar spermatozoa during capacitation in vitro. Reprod Fertil Dev 11:193-199.
72. Harrison, R. (1996) Capacitation mechanisms, and the role of capacitation as seen in eutherian mammals. Reprod Fertil Dev 8:581-594.
73. Harrison, R. A. (1997) Sperm plasma membrane characteristics and boar semen fertility. J Reprod Fertil Suppl 52:195-211.
74. 2, an effector of capacitation, induced a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Develop 45:378-391.
75. Harrison, R. A. and Gadella, B. M. (2005) Bicarbonate-induced membrane processing in sperm capacitation. Theriogenology 63:342-351.
76. Harrison, R. A. and Millar, N. G. A. (2000) cAMP-dependent protein kinase control of plasma membrane lipid architecture in boar sperm. Mol Reprod Develop 55:220-228.
77. Hess, R. (1998) Spermatogenesis, overview. In: Encyclopedia of Reproduction. Knobil, E. and Neill, J., (Eds). San Diego: Academic Press, pp 539-545.
78. Hess, R., Jones, B., Marquez, B., Chen, Y., Ord, T., Kamenetsky, M., Miyamoto, C., Zippin, J., Kopf, G., Suarez, S. et al. (2005) The 'soluble' adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Develop Cell 9:249-259.
79. Hicks, J., Martinez-Manautou, J., Pedron, N. and Rosado, A. (1972) Metabolic changes in human spermatozoa related to capacitation. Fertil Steril 23:172-179.
80. Hildebrandt, J., Codina, J., Tash, J., Kirchick, H., Lipschultz, L., Sekura, R. and Birnbaumer, L. (1985) The membrane-bound spermatozoal adenylyl cyclase system does not share coupling characteristics with somatic cell adenylyl cyclases. Endocrinology 116:1357-1366.
81. Hunter, R. (1969) Capacitation in the golden hamster, with special reference to the influence of the uterine environment. J Reprod Fertil 20:223-237.
82. Hunter, R. and Hall, J. (1974a) Capacitation of boar spermatozoa: Synergism between uterine and tubal environments. J Exp Zool 188:203-214.
83. Hunter, R. and Hall, J. (1974b) Capacitation of boar spermatozoa: The influence of post-coital separation of the uterus and fallopian tubes. Anat Re 180:597-604.
84. Imai, H., Niwa, K. and Iritani, A. (1982) The importance of the presence of metabolizable sugars in a medium for in vitro fertilization of hamster eggs with postovulatory oviduct contents. J Exp Zool 220:261-265.
85. Jelinkova, P., Liberda, J., Manaskova, P., Ryslava, H., Jonakova, V. and Ticha, M. (2004) Mannan-binding proteins from boar seminal plasma. J Reprod Immunol 62:167-182.
86. Jha, K. N., Salicioni, A. M., Arcelay, E., Chertihin, O., Kumari, S., Herr, J. C. and Visconti, P. E. (2006) Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation. Mol Hum Reprod 12:781-789.
87. Johnston, D. S., Wooters, J., Kopf, G. S., Qiu, Y. and Roberts, K. D. (2005) Analysis of the human sperm proteome. Ann. N.Y. Acad. Sci 1061:190-202.
88. Jones, A. (1997) Metabolism of lactate by mature boar spermatozoa. Reprod Fertil Dev 9:227-232.
89. Kabouridis, P., Janzen, J., Magee, A. and Ley, S. (2000) Cholesterol depletion distrupts lipid rafts and modulates the activity of multiple signaling pathways in T lymphocytes. Eur J Immunol 30:954-963.
90. Kim, N., Day, B., Lim, J., Lee, H. and Chung, K. (1997) Effects of oviductal fluid and heparin on fertility and characteristics of porcine spermatozoa. Zygote 5:61-65.
91. King, R. S., Anderson, S. H. and Killian, G. J. (1994) Effect of bovine oviductal estrus-associated protein on the ability of sperm to capacitate and fertilize oocytes. J Androl 15:468-478.
92. Kopf, G. S. and Gerton, G. L. (1991) The mammalian sperm acrosome and the acrosome reaction. In: Elements of Mammalian Fertilization. Wassarman, P., (Ed). Boca Ratan: FL, CRC Press, pp 153-203.
93. Kopf, G. S., Woolkalis, M. and Gerton, G. L. (1986) Evidence for a guanine nucleotide-binding regulatory protein in invertebrate and mammalian sperm. J Biol Chem 261:7327-7331.
94. Leclerc, P., De Lamirande, E. and Gagnon, C. (1996) Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Rad Biol Med 22:643-656.
95. Lewis, B. and Aitkent, R. J. (2001) A redox-regulated tyrosine phosphorylation cascade in rat spermatozoa. J Androl 22:611-622.
96. Manjunath, P. and Therien, I. (2002) Role of seminal plasma phospholipidbinding proteins in sperm membrane lipid modification that occurs during capacitation. J Reprod Immunol 53:109-119.
97. Marquez, B. and Suarez, S. (2004) Different signaling pathways in bovine sperm regulate capacitation and hyperactivation. Biol Reprod 70:1626-1633.
98. Mededovic, S. and Fraser, L. R. (2004) Angiotensin II stimulates cAMP production and protein tyrosine phosphorylation in mouse spermatozoa. Reproduction 127:601-612.
99. Mitra, K. and Shivaji, S. (2004) Novel tyrosine-phosphorylated post-pyruvate metabolic enzyme, dihydrolipoamide dehydrogenase, involved in capacitation of hamster spermatozoa. Biol Reprod 70:887-899.
100. Miyamoto, H. and Chang, M. (1973) The importance of serum albumin and metabolic intermediates for capacitation of spermatozoa and fertilization of mouse eggs in vitro. J Reprod Fertil 32:193-205.
101. Monks, N., Stein, D. and Fraser, L. (1986) Adenylate cyclase activity of mouse sperm during capacitation in vitro: Effect of calcium and a GTP analogue. Int J Androl 9:67-76.
102. Nikolopoulou, M., Soucek, D. and Vary, J. (1985) Changes in the lipid content of boar sperm plasma membranes during epididymal maturation. Biochim Biophys Acta 815:486-498.
103. Nimtz, M., Grabenhorst, E., Conradt, H. S., Sanz, L. and Calvete, J. J. (1999) Structural characterization of the oligosaccharide chains of native and crystallized boar seminal plasma spermadhesin PSP-I and PSP-II glycoforms. Eur J Biochem 265:703-718.
104. Odeh, A., Dascanio, J., Caceci, T., Bowen, J. and Eng, L. (2003) Effect of platelet-activating factor (PAF) on stallion sperm motility, capacitation and the acrosome reaction. Reproduction 126:605-613.
105. Okamura, N., Tajima, Y., Soejima, A., Masuda, H. and Sugita, Y. (1985) Sodium bicarbonate in seminal plasma stimulates the motility of mammalian spermatozoa through direct activation of adenylate cyclase. J Biol Chem 260:9699-9705.
106. Oliphant, G., Reynolds, A. and Thomas, T. (1985) Sperm surface components involved in the control of the acrosome reaction. Am J Anat 174:269-283.
107. Parrish, J., Susko-Parrish, J. and First, N. (1989) Capacitation of bovine sperm by heparin: Inhibitory effect of glucose and role of intracellular pH. Biol Reprod 41:683-699.
108. Parrish, J. J., Susko-Parrish, J. L., Uguz, C. and First, N. L. (1994) Differences in the role of cyclic adenosine 3′,5′-monophosphate during capacitation of bovine sperm by heparin or oviduct fluid. Biol Reprod 151:1099-1108.
109. Parrish, J., Susko-Parrish, J., Winer, M. and First, N. (1988) Capacitation of bovine sperm by heparin. Biol Reprod 38:1171-1180.
110. Perreault, S. and Rogers, B. (1982) Capacitation pattern of human sperm. Fertil Steril 38:258-260.
111. Pollard, J., Plante, C., King, W., Hansen, P., Betteridge, K. and Suarez, S. (1991) Fertilizing capacity of bovine sperm may be maintained by binding of oviductal epithelial cells. Biol Reprod 44:102-107.
112. Rana, A., Majumder, G., Misra, S. and Ghosh, A. (1991) Lipid changes of goat sperm plasma membrane during epididymal maturation. Biochim Biophys Acta 1061:185-196.
113. Roberts, K., Wamstad, J., Ensrud, K. and Hamilton, D. (2003) Inhibition of capacitation-associated tyrosine phosphorylation signaling in rat sperm by epididymal protein crisp-1. Biol Reprod 69:572-581.
114. Rodriguez Martinez, H., Ekstedt, E. and Einarsson, S. (1990) Acidification of epididymal fluid in the boar. Int J Androl 13:238-243.
115. Rogers, J. and Yanagimachi, R. (1975) Retardation of guinea pig sperm acrosome reaction by glucose: The possible importance of pyruvate and lactate metabolism in capacitation and the acrosome reaction. Biol Reprod 13:568-575.
116. 2 induces rapid activation of phospholipase A2 and renders boar spermatozoa capable of undergoing acrosomal exocytosis in response to progesterone. FEBS Lett 396:227-232.
117. Roudebush, W., Minhas, B., Ricker, D., Palmer, T. and Dodson, M (1990) Platelet activating factor enhances in vitro fertilization of rabbit oocytes. Amer J Obstet Gyneco 163:1670-1673.
118. Shadan, S., James, P., Howes, E. and Jones, R. (2004) Cholesterol efflux alters lipid raft stability and distribution during capacitation of boar spermatozoa. Biol Reprod 71:253-265.
119. Soupart, P. (1967) Studies on the hormonal control of rabbit sperm capacitation. J Reprod Fertil Suppl 2:49-64.
120. Suarez, S. (2002) Formation of a reservoir of sperm in the oviduct. Reprod Dom Anim 37:140-143.
121. Suarez, S. and Ho, H. (2003) Hyperactivated motility in sperm. Reprod Dom Anim 38:119-124.
122. Suarez, S. and Pacey, A. (2006) Sperm transport in the female reproductive tract. Human Reprod Update 12:23-37.
123. Sutton, K., Jungnickle. M. and Florman, H. (2003) Of fertility, cystic fibrosis, and the bicarbonate ion. Nature Cell Biol 5:857-859.
124. Suzuki, K., Asano, A., Eriksson, B., Niwa, K., Nagai, T. and Rodriguez-Martinez, H. (2002) Capacitation status and in vitro fertility of boar spermatozoa: Effects of seminal plasma, cumulus-oocyte-complexes-conditioned medium and hyaluronan. Int J Androl 25:84-93.
125. Tardif, S., Dube, C. and Bailey, J. L. (2003) Porcine sperm capacitation and tyrosine kinase activity are dependent on bicarbonate and calcium but protein tyrosine phosphorylation is only associated with calcium. Biol Reprod 68:207-213.
126. Tardif, S., Dube, C., Chevalier, S. and Bailey, J. L. (2001) Capacitation is associated with tyrosine phosphorylation and tyrosine kinase-like activity of pig sperm proteins. Biol Reprod 65:784-792.
127. Therien, I., Bleau, G., Manjunath, P. and Soubeyrand, S. (1995) Phosphatidylcholine-binding proteins of bovine seminal plasma modulate capacitation of spermatozoa by heparin. Biol Reprod 52:1372-1379.
128. Therien, I., Soubeyrand, S. and Manjunath, P. (1997) Major proteins of bovine seminal plasma modulate sperm capacitation by high-density lipoprotein. Biol Reprod 57:1080-1088.
129. Tienthai, P., Johannisson, A. and Rodriguez-Martinez, H. (2004) Sperm capacitation in the porcine oviduct. Anim Reprod Sci 80:131-146.
130. Tienthai, P., Kjellen, L., Pertoft, H., Suzuki, K. and Rodriguez Martinez, H. (2000) Localization and quantitation of hyaluronan and sulfated glycosaminoglycans in the tissues and intraluminal fluid of the pig oviduct. Reprod Fertil Dev 12:173-182.
131. Topfer Petersen, E., Romero, A., Varela, P., Ekhlasi Hundrieser, M., Dostalova, Z., Sanz, L. and Calvete, J. (1998) Spermadhesins: A new protein family. Facts, hypotheses and perspectives. Andrologia 30:217-224.
132. Topfer-Petersen, E., Ekhlasi-Hundrieser, M., Tsolova, M., Leeb, T., Kirchhoff, C. and Muller, P. (2005) Structure and function of secretory proteins of the male genital tract. Andrologia 37:202-204.
133. Travis, A. J., Jorgez, C. J., Merdiushev, T., Jones, B. H., Dess, D. M., Diaz-Cueto, L., Storey, B. T., Kopf, G. S. and Moss, S. B. (2001) Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem 276:7630-7636.
134. Travis, A. J. and Kopf, G. S. (2002) The role of cholesterol efflux in regulating the fertilization potential of mammalian spermatozoa. J Clin Invest 110:731-736.
135. Tsunoda, Y. and Chang, M. (1975) In vitro fertilization of rat and mouse eggs by ejaculated sperm and the effect of energy sources on in vitro fertilization of rat eggs. J Exp Zool 193:79-86.
136. Urner, F. and Sakkas, D. (2003) Protein phosphorylation in mammalian spermatozoa. Reproduction 125:17-26.
137. Ursini, F., Heim, S., Kiess, M., Maiorino, M., Roveri, A., Wissing, J. and Flohè, L. (1999) Dual function of the selenoprotein PHGPx during sperm maturation. Science 285:1393-1396.
138. Vadnais, M. L., Kirkwood, R., Spreche, R D. and Chou K (2005a) Effects of extender, incubation temperature, and added seminal plasma on capacitation of cryopreserved, thawed boar sperm as determined by chlortetracycline staining. Anim Reprod Sci 90:347-354.
139. Vadnais, M. L., Kirkwood, R. N., Tempelman, R. J., Sprecher, D. J. and Chou, K. (2005b) Effect of cooling and seminal plasma on the capacitation status of fresh boar sperm as determined using chlortetracycline assay. Anim Reprod Sci 87:121-132.
140. Vadnais, M. L. and Roberts, K. P. (2006) Effects of seminal plasma on cooling-induced capacitative changes in boar sperm. J Androl Ehead of print.
141. van Gestel, R., Helms, J., Brouwers, J. and Gadella, B. (2005) Effects of methyl-beta-cyclodextrin-mediated cholesterol depletion in porcine sperm compared to somatic cells. Mol Reprod Develop 72:386-395.
142. Visconti, P., Bailey, J., Moore, G., Pan, D., Olds-Clark, P. and Kopf, G. (1995) Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121:1129-1137.
143. Visconti, P., Galantino-Homer, H., Moore, G., Bailey, J., Ning, X., Fornes, M. and Kopf, G. (1998) The molecular basis of sperm capacitation. J Androl 19:242-248.
144. Visconti, P. and Kopf, G. (1998) Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 59:1-6.
145. Visconti, P. E., Ning, X., Fornes, M., Alvarez, J., Stein, P., Connors, S. and Kopf, G. S. (1999) Cholesterol efflux-mediated signal transduction in mammalian sperm: Cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Devel Biol 214:429-443.
146. Visconti, P. E., Westbrook, V. A., Chertihin, O., Demarco, I., Sleight, S. and Diekman, A. B. (2002) Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 53:133-150.
147. Vishwakarma, P. (1962) The ph and bicarbonate-ion content of the oviduct and uterine fluids. Fertil Steril 13:481-485.
148. Vredenburgh-Wilberg, W. and Parrish, J. (1995) Intracellular ph of bovine sperm increases during capacitation. Mol Reprod Develop 40:490-502.
149. + exchanger required for sperm motility and fertility. Nature Cell Biol 5:1117-1122.
150. Wang, X., Zhou, C., Shi, Q., Yuan, Y., Yu, M., Ajonuma, L., Ho, L., Lo, P., Tsang, L., Liu, Y. et al. (2003b) Involvement of CFTR in uterine bicarbonate secretion and the fertilizing capacity of sperm. Nature Cell Biol 5:902-906.
151. Watson, P. F. and Green, C. E. (2000). Cooling and capacitation of boar spermatozoa: What do they have in common? In: Boar Semen Preservation IV. Johnson, L. A. and Guthrie, H. D. (Eds). Lawrence: Allen Press, pp. 53-60.
152. Williams, A. C. and Ford, W. C. (2001) The role of glucose in supporting motility and capacitation in human spermatozoa. J Androl 22:680-695.
153. Wu, C., Stojanov, T., Chami, O., Ishii, S., Shimuzu, T., Li, A. and O'Neill, C. (2001) Evidence for the autocrine induction of capacitation of mammalian spermatozoa. J Biol Chem 276:26962-26968.
154. Xu, W., Ensrud, K. and Hamilton, D. (1997) The 26 kD protein recognized on rat cauda epididymal sperm by monoclonal antibody 4E9 has internal peptide sequence that is identical to the secreted form of epididymal protein E. Mol Reprod Develop 46:377-382.
155. Yamano, S., Yamazaki, J., Irahara, M., Tokumura, A., Nakagawa, K. and Saito, H. (2004) Human spermatozoa capacitated with progesterone or a long incubation show accelerated internalization by an alkyl ether lysophospholipid. Fertil Steril 81:605-610.
156. Zeng, Y., Clark, E. and Florman, H. (1995) Sperm membrane potential: Hyperpolarization during capacitation regulates zona pellucida-dependent acrosomal secretion. Dev Biol 171:554-563.
157. --dependent and arylaminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Develop Biol 173:510-520.