Sperm capacitation: A distant landscape glimpsed but unexplored

Molecular Human Reproduction

Volumn 19, Issue 12, 2013, Pages 785-793

  Aitken, R John ^a   Nixon, Brett ^a  

^a HUNTER MEDICAL RESEARCH INSTITUTE   (Australia)

Author keywords

Acrosome reaction; Fertilization; Sperm biochemistry; Sperm function; Spermatozoa

Indexed keywords

ALBUMIN; BICARBONATE; CHAPERONIN 60; CHOLESTEROL; CYCLIC AMP; FIBROBLAST GROWTH FACTOR RECEPTOR; HYALURONIDASE; HYDROGEN PEROXIDE; NITRIC OXIDE SYNTHASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SOMATOMEDIN RECEPTOR; SUPEROXIDE DISMUTASE; TYROSINE; TYROSINE KINASE RECEPTOR;

ACROSOME; ACROSOME REACTION; CELL INTERACTION; CELL MEMBRANE; CELL MOTILITY; CELL PH; EXOCYTOSIS; EXTRACELLULAR MATRIX; FERTILIZATION; HUMAN; MALE; MEMBRANE FLUIDITY; NONHUMAN; OOCYTE; OVULATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; REVIEW; SEMINAL PLASMA; SPERMATOZOON; SPERMATOZOON CAPACITATION; ZONA PELLUCIDA;

ACROSOME REACTION; FERTILIZATION; SPERM BIOCHEMISTRY; SPERM FUNCTION; SPERMATOZOA;

HUMANS; MEMBRANE FLUIDITY; OXIDATION-REDUCTION; PHOSPHORYLATION; REACTIVE OXYGEN SPECIES; SPERM CAPACITATION; SPERM-OVUM INTERACTIONS; TYROSINE;

EID: 84888996931     PISSN: 13609947     EISSN: 14602407     Source Type: Journal    
DOI: 10.1093/molehr/gat067     Document Type: Review

References (124)

1. Aitken RJ. The capacitation-apoptosis highway: Oxysterols and mammalian sperm function. Biol Reprod 2011, 85, 9-12
2. Aitken RJ, Baker MA. Causes and consequences of apoptosis in spermatozoa; contributions to infertility and impacts on development. Int J Dev Biol 2013, 57, 265-27
3. Aitken RJ, McLaughlin EA. Molecular mechanisms of sperm capacitation: Progesterone-induced secondary calcium oscillations reflect the attainment of a capacitated state. Soc Reprod Fertil Suppl 2007, 63, 273-293
4. Aitken RJ, Paterson M, Fisher H, Buckingham DW, van Duin M. Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J Cell Sci 1995, 108, 2017-2025
5. Aitken RJ, BuckinghamDW, Harkiss D, Paterson M, Fisher H, Irvine DS. The extragenomic action of progesterone on human spermatozoa is influenced by redox regulated changes in tyrosine phosphorylation during capacitation. Mol Cell Endocrinol 1996, 117, 83-93
6. Aitken RJ, Fisher HM, Fulton N, Gomez E, Knox W, Lewis B, Irvine S. Reactive oxygen species generation by human spermatozoa is induced by exogenous NADPH and inhibited by the flavoprotein inhibitors diphenylene iodonium and quinacrine. Mol Reprod Dev 1997, 47, 468-482
7. Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS. A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci 1998a, 111, 645-656
8. Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine S. On the cellular mechanisms by which the bicarbonate ion mediates the extragenomic action of progesterone on human spermatozoa. Biol Reprod 1998b, 58, 186-196
9. Aitken RJ, Ryan AL, Curry BJ, Baker MA. Multiple forms of redox activity in populations of human spermatozoa. Mol Hum Reprod 2003, 9, 645-661
10. Aitken RJ, Ryan AL, BakerMA, McLaughlin EA. Redox activity associated with the maturation and capacitation of mammalian spermatozoa. Free Radic Biol Med 2004, 36, 994-1010
11. Aitken RJ, DeIuliis GN, Gibb Z, Baker MA. The Simmet lecture:newhorizons on an old landscape-oxidative stress,DNA damage and apoptosis in the male germ line. Reprod Domest Anim 2012a, 47 (Suppl 4), 7-14
12. Aitken RJ, Whiting S, De Iuliis GN, McClymont S, Mitchell LA, Baker MA. Electrophilic aldehydes generated by sperm metabolism activate mitochondrial reactive oxygen species generation and apoptosis by targeting succinate dehydrogenase. J Biol Chem 2012b, 287, 33048-33060
13. 2+ stores regulate different behaviors in human sperm. J Biol Chem 2013, 288, 6248-6258
14. Asquith KL, Baleato RM, McLaughlin EA, Nixon B, Aitken RJ. Tyrosine phosphorylation activates surface chaperones facilitating sperm-zona recognition. J Cell Sci 2004, 117, 3645-3657
15. Baillie HS, Pacey AA, Warren MA, Scudamore IW, Barratt CL. Greater numbers of human spermatozoa associate with endosalpingeal cells derived from the isthmus compared with those from the ampulla. Hum Reprod 1997, 12, 1985-1992
16. Baker MA, Hetherington L, Ecroyd H, Roman SD, Aitken RJ. Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation. J Cell Sci 2004, 117, 211-222
17. Baker MA, Hetherington L, Aitken RJ. Identification of SRC as a key PKA-stimulated tyrosine kinase involved in the capacitation-associated hyperactivation of murine spermatozoa. J Cell Sci 2006, 119, 3182-3192
18. Baker MA, Hetherington L, Curry B, Aitken RJ. Phosphorylation and consequent stimulation of the tyrosine kinase c-Abl by PKA in mouse spermatozoa; its implicationsduring capacitation.DevBiol2009, 333, 57-66
19. Battistone MA, Da Ros VG, Salicioni AM, Navarrete FA, Krapf D, Visconti PE, Cuasnicú PS. Functional human sperm capacitation requires both bicarbonate dependent PKA activation and down-regulation of Ser/Thr phosphatases by Src family kinases. Mol Hum Reprod 2013, 19, 570-580
20. Baumber J, Sabeur K, Vo A, Ball BA. Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 2003, 60, 1239-1247
21. Bavister BD. Capacitation of golden hamster spermatozoa during incubation in culture medium. J Reprod Fertil 1973, 35, 161-163
22. Beconi MT, Francia CR, Mora NG, Affranchino MA. Effect of natural antioxidants on frozen bovine semen preservation. Theriogenology 1993, 40, 841-851
23. Bennetts L, LinM, Aitken RJ. CyclicAMP-dependent tyrosine phosphorylation in tammar wallaby (Macropus eugenii) spermatozoa. J Exp Zool A Comp Exp Biol 2004, 301, 118-130
24. Bi Y, XuWM, Wong HY, Zhu H, Zhou ZM, ChanHC, Sha JH. NYD-SP27, a novel intrinsic decapacitation factor in sperm. Asian J Androl 2009, 11, 229-239
25. Bize I, Santander G, Cabello P, Driscoll D, Sharpe C. Hydrogen peroxide is involved in hamster sperm capacitation in vitro. Biol Reprod 1991, 44, 398-403
26. Boerke A, Brouwers JF, Olkkonen VM, vande Lest CH, Sostaric E, Schoevers EJ, Helms JB, Gadella BM. Involvement of bicarbonate-induced radical signaling inoxysterol formation andsteroldepletionof capacitatingmammaliansperm during in vitro fertilization. Biol Reprod 2013, 88, 21
27. Breininger E, Beorlegui NB, O'Flaherty CM, Beconi MT. Alpha-tocopherol improves biochemical and dynamic parameters in cryopreserved boar semen. Theriogenology 2005, 63, 2126-2135
28. Breitbart H, Etkovitz N. Role and regulation of EGFR in actin remodeling in sperm capacitation and the acrosome reaction. Asian J Androl 2011, 13, 106-110
29. Brouwers JF, Boerke A, Silva PF, Garcia-Gil N, van Gestel RA, Helms JB, van de Lest CH, Gadella BM. Mass spectrometric detection of cholesterol oxidation in bovine sperm. Biol Reprod 2011, 85, 128-136
30. Choi YH, Landim-Alvarenga FC, Seidel GE Jr, Squires EL. Effect of capacitation of stallion sperm with polyvinylalcohol or bovine serum albumin on penetration of bovine zona-free or partially zona-removed equine oocytes. J Anim Sci 2003, 81, 2080-2087
31. Córdoba M, Mora N, Beconi MT. Respiratory burst and NAD(P)H oxidase activity are involved in capacitation of cryopreserved bovine spermatozoa. Theriogenology 2006, 65, 882-892
32. Cotton L, Gibbs GM, Sanchez-Partida LG, Morrison JR, de Kretser DM, O'Bryan MK. FGFR-1 [corrected] signaling is involved in spermiogenesis and sperm capacitation. J Cell Sci 2006, 119, 75-84
33. Davis BK. Interaction of lipidswith the plasma membrane of spermcells. I. The antifertilization action of cholesterol. Arch Androl 1980, 5, 249-254
34. Davis BK. Timing of fertilization in mammals: Sperm cholesterol/ phospholipid ratio as a determinant of the capacitation interval. Proc Natl Acad Sci USA 1981, 78, 7560-7564
35. Davis BK, Byrne R, Hungund B. Studies on the mechanism of capacitation. II. Evidence for lipid transfer between plasma membrane of rat sperm and serum albumin during capacitation in vitro. Biochim Biophys Acta 1979, 558, 257-266
36. de Lamirande E, Gagnon C. Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic Biol Med 1993a, 14, 157-166
37. de Lamirande E, Gagnon C. A positive role for the superoxide anion in triggering hyperactivation and capacitation of human spermatozoa. Int J Androl 1993b, 16, 21-25
38. de Lamirande E, Gagnon C. The extracellular signal-regulated kinase (ERK) pathway is involved in human sperm function and modulated by the superoxide anion. Mol Hum Reprod 2002, 8, 124-135
39. Dona' G, Fiore C, Andrisani A,AmbrosiniG, Brunati A, Ragazzi E, ArmaniniD, Bordin L,ClariG. Evaluation of correct endogenous reactive oxygen species content for human sperm capacitation and involvement of the NADPH oxidase system. Hum Reprod 2011, 26, 3264-3273
40. Dun MD, Mitchell LA, Aitken RJ, Nixon B. Sperm-zona pellucida interaction: Molecular mechanisms and the potential for contraceptive intervention. Handb Exp Pharmacol 2010, 198, 139-178
41. Dun MD, Smith ND, Baker MA, Lin M, Aitken RJ, Nixon B. The chaperonin containing TCP1 complex (CCT/TRiC) is involved in mediating sperm-oocyte interaction. J Biol Chem 2011, 286, 36875-36887
42. Ecroyd HW, Jones RC, Aitken RJ. Endogenous redox activity in mouse spermatozoa and its role in regulating the tyrosine phosphorylation events associated with sperm capacitation. Biol Reprod 2003, 69: 347-354
43. Ecroyd H, Asquith KL, Jones RC, Aitken RJ. The development of signal transduction pathways during epididymal maturation is calcium dependent. Dev Biol 2004, 268, 53-63
44. Edwards RG. Maturation in vitro of human ovarian oö cytes. Lancet 1965, 2, 926-929
45. Edwards RG. Oocyte and follicle quality and success with IVF. Reprod Biomed Online 2002, 3, 263-264
46. Edwards RG. An astonishing journey into reproductive genetics since the 1950's. Reprod Nutr Dev 2005, 45, 299-306
47. Edwards RG, Talbert L, Israelstam D, Nino HN, Johnson MH. Diffusion chamber for exposing spermatozoa to human uterine secretions. Am J Obstet Gynecol 1968, 102, 388-396
48. Edwards RG, Bavister BD, Steptoe PC. Early stages of fertilization in vitro of human oocytes matured in vitro. Nature 1969, 221, 632-635
49. Flesch FM, Colenbrander B, van Golde LM, Gadella BM. Capacitation induces tyrosine phosphorylation of proteins in the boar sperm plasma membrane. Biochem Biophys Res Commun 1999, 262, 787-792
50. Florman HM, Jungnickel MK, Sutton KA. Regulating the acrosome reaction. Int J Dev Biol 2008, 52, 503-510
51. Gadella BM, Tsai PS, Boerke A, Brewis IA. Sperm head membrane reorganisation during capacitation. Int J Dev Biol 2008, 52, 473-480
52. Galantino-Homer HL, Visconti PE, Kopf GS. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway. Biol Reprod 1997, 56, 707-719
53. Griveau JF, Renard P, Le Lannou D. An in vitro promoting role for hydrogen peroxide in human sperm capacitation. Int J Androl 1994, 17, 300-307
54. Harayama H, Noda T, Ishikawa S, Shidara O. Relationship between cyclic AMP-dependent protein tyrosine phosphorylation and extracellular calcium during hyperactivation of boar spermatozoa. Mol Reprod Dev 2012, 79, 727-739
55. Hecht D, Zick Y. Selective inhibition of protein tyrosine phosphatase activities by H2O2 and vanadate in vitro. Biochem Biophys Res Commun 1992, 188, 773-779
56. Herrero MB, de Lamirande E, Gagnon C. Tyrosine nitration in human spermatozoa: A physiological function of peroxynitrite, the reaction product of nitric oxide and superoxide. MolHumReprod 2001, 7, 913-921
57. Ho HC, Suarez SS. Characterization of the intracellular calcium store at the base of the sperm flagellum that regulates hyperactivated motility. Biol Reprod 2003, 68, 1590-1596
58. Hunter RH. Sperm release from oviduct epithelial binding is controlled hormonally by peri-ovulatory graafian follicles. Mol Reprod Dev 2008, 75, 167-174
59. Huszar G, Vigue L, Oehninger S. Creatine kinase immunocytochemistry of human sperm-hemizona complexes: Selective binding of sperm with mature creatine kinase-staining pattern. Fertil Steril 1994, 61, 136-142
60. Huszar G, Ozkavukcu S, Jakab A,Celik-Ozenci C, Sati GL, Cayli S. Hyaluronic acid binding ability of human sperm reflects cellular maturity and fertilizing potential: Selection of sperm for intracytoplasmic sperm injection. Curr Opin Obstet Gynecol 2006, 18, 260-267
61. Huszar G, Jakab A, Sakkas D, Ozenci CC, Cayli S, Delpiano E, Ozkavukcu S. Fertility testing and ICSI sperm selection by hyaluronic acid binding: Clinical and genetic aspects. Reprod Biomed Online 2007, 14, 650-663
62. IckowiczD, Finkelstein M, Breitbart H. Mechanismof spermcapacitation andthe acrosome reaction: Role of protein kinases. Asian J Androl 2012, 14, 816-8211
63. Inoue N, Satouh Y, Ikawa M, Okabe M, Yanagimachi R. Acrosome-reacted mouse spermatozoa recovered from the perivitelline space can fertilize other eggs. Proc Natl Acad Sci USA 2011, 108, 20008-20011
64. Jin M, Fujiwara E, Kakiuchi Y, Okabe M, Satouh Y, Baba SA, Chiba K, Hirohashi N. Most fertilizing mouse spermatozoa begin their acrosome reaction before contact with the zona pellucida during in vitro fertilization. Proc Natl Acad Sci USA 2011, 108, 4892-4896
65. Johnson MH. Robert Edwards: The path to IVF. Reprod Biomed Online 2011, 23, 245-26
66. Kawano N, Yoshida K, Iwamoto T, Yoshida M. Ganglioside GM1 mediates decapacitation effects of SVS2 on murine spermatozoa. Biol Reprod 2008, 79, 1153-1159
67. Koppers AJ, Mitchell LA,Wang P, Lin M, Aitken RJ. Phosphoinositide 3-kinase signalling pathway involvement in a truncated apoptotic cascade associated with motility loss and oxidative DNA damage in human spermatozoa. Biochem J 2011, 436, 687-698
68. Krapf D, Arcelay E, Wertheimer EV, Sanjay A, Pilder SH, Salicioni AM, Visconti PE. Inhibition of Ser/Thr phosphatases induces capacitationassociated signaling in the presence of Src kinase inhibitors. J Biol Chem 2010, 285, 7977-7985
69. Langlais J, Zollinger M, Plante L, Chapdelaine A, Bleau G, Roberts KD. Localization of cholesteryl sulfate in human spermatozoa in support of a hypothesis for the mechanism of capacitation. Proc Natl Acad Sci USA 1981, 78, 7266-7270
70. Lax Y, Rubinstein S, Breitbart H. Epidermal growth factor induces acrosomal exocytosis in bovine sperm. FEBS Lett 1994, 339, 234-238
71. Leclerc P, de Lamirande E, Gagnon C. Regulation of protein-tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radic Biol Med 1997, 22, 643-656
72. Lewis B, Aitken RJ. A redox-regulated tyrosine phosphorylation cascade in rat spermatozoa. J Androl 2001, 22, 611-622
73. Lin MH, Lee RK, Hwu YM, Lu CH, Chu SL, Chen YJ, Chang WC, Li SH. SPINKL, a Kazal-type serine protease inhibitor-like protein purified from mouse seminal vesicle fluid, is able to inhibit sperm capacitation. Reproduction 2008, 136, 559-571
74. Lu CH, Lee RK, Hwu YM, Chu SL, Chen YJ, Chang WC, Lin SP, Li SH. SERPINE2, A serine protease inhibitor extensively expressed in adult male mouse reproductive tissues, may serve as a murine sperm decapacitation factor. Biol Reprod 2011, 84, 514-525
75. Luna C, Colás C, Pérez-Pé R, Cebrián-Pérez JA, Muiño-Blanco T. A novel epidermal growth factor-dependent extracellular signal-regulated MAP kinase cascade involved in sperm functionality in sheep. Biol Reprod 2012, 87, 93
76. Minetti M, Mallozzi C, Di Stasi AM. Peroxynitrite activates kinases of the src family and upregulates tyrosine phosphorylation signaling. Free Radic Biol Med 2002, 33, 744-754
77. Mitchell LA, Nixon B, Aitken RJ. Analysis of chaperone proteins associated with human spermatozoa during capacitation. Mol Hum Reprod 2007, 13, 605-613
78. Morales CR, Ni X, Smith CE, Inagaki N, Hermo L. ABCA17 Mediates sterol efflux from mouse spermatozoa plasma membranes. Histol Histopathol 2012, 27, 317-328
79. Musset B, Clark RA, DeCoursey TE, Petheo G.L.,Geiszt M.,Chen Y,Cornell JE, Eddy CA, Brzyski RG, El Jamali A. NOX5 In human spermatozoa: expression, function, and regulation. J Biol Chem2012, 287, 9376-9388
80. Nassar A, Mahony M, Morshedi M, Lin MH, Srisombut C, Oehninger S. Modulation of sperm tail protein tyrosine phosphorylation by pentoxifylline and its correlationwith hyperactivatedmotility. Fertil Steril 1999, 71, 919-923
81. Naz RK, Padman P. Identification of insulin-like growth factor (IGF)-1 receptor in human sperm cell. Arch Androl 1999, 43, 153-159
82. Ni Y, Zhou Y, Chen WY, Zheng M, Yu J, Li C, Zhang Y, Shi QX. Hongr ES1, a cauda epididymis-specific protein, is involved in capacitation of guinea pig sperm. Mol Reprod Dev 2009, 76, 984-993
83. Nixon B, Aitken RJ. The biological significance of detergent-resistant membranes in spermatozoa. J Reprod Immunol 2009, 83, 8-13
84. Nixon B, Paul JW, Spiller CM, Attwell-Heap AG, Ashman LK, Aitken RJ. Evidence for the involvement of PECAM-1 in a receptor mediated signal-transduction pathway regulating capacitation-associated tyrosine phosphorylation in human spermatozoa. J Cell Sci 2005, 118, 4865-4877
85. Nixon B, MacIntyre DA, Mitchell LA, Gibbs GM, O'Bryan M, Aitken RJ. The identification of mouse sperm-surface-associated proteins and characterization of their ability to act as decapacitation factors. Biol Reprod 2006, 74, 275-287
86. Nixon B, Bielanowicz A, McLaughlin EA, Tanphaichitr N, Ensslin MA, Aitken RJ. Composition and significance of detergent resistant membranes in mouse spermatozoa. J Cell Physiol 2009, 218, 122-134
87. Nixon B, Bielanowicz A, Anderson AL, Walsh A, Hall T, McCloghry A, Aitken RJ. Elucidation of the signaling pathways that underpin capacitationassociated surface phosphotyrosine expression in mouse spermatozoa. J Cell Physiol 2010, 224, 71-83
88. Nixon B, Mitchell LA, Anderson AL, McLaughlin EA, O'Bryan MK, Aitken RJ. Proteomic and functional analysis of human sperm detergent resistant membranes. J Cell Physiol 2011, 226, 2651-2665
89. O'Flaherty C, Beconi M, Beorlegui N. Effect of natural antioxidants, superoxide dismutase and hydrogen peroxide on capacitation of frozen-thawed bull spermatozoa. Andrologia 1997, 29, 269-275
90. O'Flaherty CM, Beorlegui NB, Beconi MT. Reactive oxygen species requirements for bovine sperm capacitation and acrosome reaction. Theriogenology 1999, 52, 289-301
91. O'Flaherty C, Beorlegui N, Beconi MT. Participation of superoxide anion in the capacitation of cryopreserved bovine sperm. Int J Androl 2003, 26, 109-114
92. O'Flaherty C, de Lamirande E, Gagnon C. Phosphorylation of the Arginine-X-X-(Serine/Threonine) motif in human sperm proteins during capacitation: modulation and protein kinase A dependency. Mol Hum Reprod 2004, 10, 355-363
93. O'Flaherty C, de Lamirande E, Gagnon C. Reactive oxygen species and protein kinases modulate the level of phospho-MEK-like proteins during human sperm capacitation. Biol Reprod 2005, 73, 94-105
94. O'Flaherty C, de Lamirande E, Gagnon C. Reactive oxygen species modulate independent protein phosphorylation pathways during human sperm capacitation. Free Radic Biol Med 2006a, 40, 1045-1055
95. O'Flaherty C, de Lamirande E, Gagnon C. Positive role of reactive oxygen species in mammalian sperm capacitation: triggering and modulation of phosphorylation events. Free Radic Biol Med 2006b, 41, 528-540
96. Pacey AA, Ladbrook MB, Barratt CL, Cooke ID. The potential shortcomings of measuring hyperactivated motility by computer-aided sperm analysis when sperm motion is multiphasic. Hum Reprod Update 1997, 3, 185-193
97. Pommer AC, Rutllant J, Meyers SA. Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biol Reprod 2003, 68, 1208-1214
98. Pujianto DA, Curry BJ, Aitken RJ. Prolactin exerts a prosurvival effect on human spermatozoa via mechanisms that involve the stimulation of Akt phosphorylation and suppression of caspase activation and capacitation. Endocrinology 2010, 151, 1269-1279
99. Qi H, Moran MM, Navarro B, Chong JA, Krapivinsky G, Krapivinsky L, Kirichok Y, Ramsey IS, Quill TA, Clapham DE. All four CatSper ion channel proteins are required for male fertility and sperm cell hyperactivated motility. Proc Natl Acad Sci USA 2007, 104, 1219-1223
100. Redgrove KA, Anderson AL, Dun MD, McLaughlin EA, O'Bryan MK, Aitken RJ, Nixon B. Involvement of multimeric protein complexes in mediating the capacitation dependent binding of human spermatozoa to homologous zonae pellucidae. Dev Biol 2011, 356, 460-474
101. Redgrove KA, Nixon B, Baker MA, Hetherington L, Baker G, Liu DY, Aitken RJ. The molecular chaperone HSPA2 plays a key role in regulating the expression of sperm surface receptors that mediate sperm-egg recognition. PLoS One 2012, 7:e50851
102. Redgrove KA, Anderson AL, McLaughlin EA, O'Bryan MK, Aitken RJ, Nixon B. Investigation of the mechanisms by which the molecular chaperone HSPA2 regulates the expression of sperm surface receptors involved in human sperm-oocyte recognition. Mol Hum Reprod 2013, 19, 120-135
103. Reid AT, Redgrove K, Aitken RJ, Nixon B. Cellular mechanisms regulating sperm-zona pellucida interaction. Asian J Androl 2011, 13, 88-96
104. Rivlin J, Mendel J, Rubinstein S, Etkovitz N, Breitbart H. Role of hydrogen peroxide in sperm capacitation and acrosome reaction. Biol Reprod 2004, 70, 518-522
105. Roberts KD. Sterol sulfates in the epididymis; synthesis and possible function in the reproductive process. J Steroid Biochem 1987, 27, 337-341
106. Roberts PJ, Der CJ. Targeting the Raf-MEK-ERK mitogen-activated protein kinase cascade for the treatment of cancer. Oncogene 2007, 26: 3291-3310
107. Rodriguez PC, BeconiMT. Peroxynitrite participates in mechanisms involved in capacitation of cryopreserved cattle. Anim Reprod Sci 2009, 110, 96-107
108. Rodriguez PC, Valdez LB, Zaobornyj T, Boveris A, Beconi MT. Nitric oxide and superoxide anion production during heparin-induced capacitation in cryopreserved bovine spermatozoa. Reprod Domest Anim 2011, 46, 74-81
109. Roessner C, Paasch U, Glander HJ, Grunewald S. Activity of nitric oxide synthase in mature and immature human spermatozoa. Andrologia 2010, 42, 132-137
110. Roy SC, Atreja SK. Effect of reactive oxygen species on capacitation and associated protein tyrosine phosphorylation in buffalo (Bubalus bubalis) spermatozoa. Anim Reprod Sci 2008, 107, 68-84
111. Sagare-Patil V, Vernekar M, Galvankar M, Modi D. Progesterone utilizes the PI3K-AKT pathway in human spermatozoa to regulate motility and hyperactivation but not acrosome reaction. Mol Cell Endocrinol 2013, 374, 82-91
112. Silva SV, Soares AT, Batista AM,Almeida FC,Nunes JF, Peixoto CA, Guerra MM. Vitamin E (Trolox) addition to Tris-egg yolk extender preserves ram spermatozoon structure and kinematics after cryopreservation. Anim Reprod Sci 2012. doi, 10.1016/j.anireprosci.2012.12.002
113. Sion B, Grizard G, Boucher D. Quantitative analysis of desmosterol, cholesterol and cholesterol sulfate in semen by high-performance liquid chromatography. J Chromatogr A 2001, 935, 259-265
114. 2+ channel in a CatSper2-deficient infertile patient. Proc Natl Acad Sci USA 2013, 110, 6823-6828
115. Suarez SS. Regulation of sperm storage and movement in the mammalian oviduct. Int J Dev Biol 2008, 52, 455-462
116. Suarez SS, Pacey AA. Sperm transport in the female reproductive tract. Hum Reprod Update 2006, 12, 23-37
117. Takakura K, Beckman JS, MacMillan-Crow LA, Crow JP. Rapid and irreversible inactivation of protein tyrosine phosphatases PTP1B, CD45, and LAR by peroxynitrite. Arch Biochem Biophys 1999, 369, 197-207
118. Tan CM, Xenoyannis S, Feldman RD. Oxidant stress enhances adenylyl cyclase activation. Circ Res 1995, 77, 710-717
119. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMPdependent pathway. Development 1995, 121, 1139-1150
120. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezón JG. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 1999, 61, 76-84
121. 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
122. Yanagimachi R. Mammalian fertilization. In: Knobil E, Neill JD (eds). The Physiology of Reproduction, 2nd edn. New York: Raven Press, 1994, 189-317
123. Zhang H, Zheng RL. Promotion of human sperm capacitation by superoxide anion. Free Radic Res 1996, 24, 261-268
124. Zhu J, Massey JB, Mitchell-Leef D, Elsner CW, Kort HI, Roudebush WE. Platelet-activating factor acetylhydrolase activity affects sperm motility and serves as a decapacitation factor. Fertil Steril 2006, 85, 391-394