Sperm activation: Role of reactive oxygen species and kinases

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 1, 2008, Pages 106-115

  de Lamirande, Eve ^a   O'Flaherty, Cristián ^b  

^a ROYAL VICTORIA HOSPITAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Capacitation; Protein phosphorylation; Reactive oxygen species; Signal transduction; Spermatozoa

Indexed keywords

ARGININE; CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; DISULFIDE; GLUTAMIC ACID; HYDROGEN PEROXIDE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; NITRIC OXIDE; PHOSPHOTRANSFERASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; REACTIVE OXYGEN METABOLITE; SERINE; SUPEROXIDE; THIOL DERIVATIVE; THREONINE; TYROSINE;

ACROSOME REACTION; CELL ACTIVATION; CELL FUNCTION; ENZYME ACTIVATION; ENZYME SUBSTRATE; EXOCYTOSIS; HUMAN; NONHUMAN; OOCYTE; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN MOTIF; REVIEW; SECOND MESSENGER; SIGNAL TRANSDUCTION; SPERM; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; ZONA PELLUCIDA;

CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; HUMANS; MALE; MITOGEN-ACTIVATED PROTEIN KINASE KINASES; PHOSPHORYLATION; PROTEIN KINASES; REACTIVE OXYGEN SPECIES; SPERM CAPACITATION; SPERMATOZOA;

EID: 38149095757     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2007.08.024     Document Type: Review

References (81)

1. Halliwell B., and Gutteridge J.M.C. Free Radicals in Biology and Medicine (1999), Clarendon Press, Oxford
2. Dröge W. Free radicals in the physiological control of cell function. Physiol. Rev. 82 (2001) 47-95
3. Filomeni G., Rotilio G., and Ciriolo M.R. Disulfide relays and phosphorylative cascades: partners in redox-mediated signaling pathways. Cell. Death Diff. 12 (2005) 1555-1563
4. de Lamirande E., and Gagnon C. The dark and the bright sides of reactive oxygen species on sperm function. In: Gagnon C. (Ed). The Male Gamete. From Basic Science to Clinical Applications (1998), Cache River Press, Vienna IL, USA 455-467
5. de Lamirande E., and Gagnon C. Impact of reactive oxygen species on spermatozoa: a balancing between beneficial and detrimental effects. Hum. Reprod. 10 (1995) 15-21
6. Aitken R.J. A free radical theory of male infertility. Reprod. Fertil. Dev. 6 (1994) 19-24
7. Sheppard F.R., Kelher M.R., Moore E.E., McLaughlin N.J.D., Banerjee A., and Silliman C.C. Structural organization of the neutrophil NADPH oxidase: phosphorylation and translocation during priming and activation. J. Leukoc. Biol. 78 (2005) 1025-1042
8. Quinn M.T., and Gauss K.A. Structure and regulation of the neutrophil respiratory burst oxidase: comparison with nonphagocyte oxidases. J. Leukoc. Biol. 76 (2004) 760-781
9. Sumimoto H., Miyano K., and Takeya R. Molecular composition and regulation of the Nox family NAD(P)H oxidases. Biochem. Biophys. Res. Comm. 338 (2005) 677-686
10. Herrero M.B., Perez Martinez S., Viggiano J.M., Polak J.M., and Gimeno M.F. Localization by indirect immunofluorescence of nitric oxidase synthase in mouse and human spermatozoa. Reprod. Fertil. Dev. 8 (1996) 931-934
11. Herrero M.B., de Lamirande E., and Gagnon C. Nitric oxide is a signaling molecule in spermatozoa. Curr. Pharm. Des. 9 (2003) 419-425
12. Lewis S.E.M., Donnelly E.T., Sterling E.S.L., Kennedy M.S., Thompson W., and Chakravarthy U. Nitric oxide synthase and nitrite production in human spermatozoa: evidence that endogenous nitric oxide is beneficial to sperm motility. Mol. Hum. Reprod. 2 (1996) 873-878
13. de Lamirande E., Leclerc P., and Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol. Hum. Reprod. 3 (1997) 175-194
14. O'Flaherty C., de Lamirande E., and Gagnon C. Positive role of reactive oxygen species in mammalian sperm capacitation triggering and modulation of phosphorylation events. Free Radic. Biol. Med. 41 (2006) 528-540
15. de Lamirande E., and Gagnon C. Redox control of changes in protein sulfhydryl levels during human sperm capacitation. Free Radic. Biol. Med. 35 (2003) 1271-1285
16. Sen C.K. Cellular thiols and redox-regulated signal transduction. Curr. Top. Cell. Regul. 36 (2000) 1-30
17. Eddy E.M., and O'Brien A.O. The spermatozoon. In: Knobil E., and Neill J.D. (Eds). The Physiology of Reproduction vol. 2 (1994), Raven Press, New York 29-77
18. Miller D., and Ostermeier G.C. Spermatozoal RNA: why is it there and what does it do?. Gynecol. Obstet. Fertil. 34 (2006) 840-846
19. Yanagimachi R. Mammalian fertilization. In: Knobil E., and Neill J.D. (Eds). The Physiology of Reproduction vol. 2 (1994), Raven Press, New York 189-317
20. Gagnon C., and de Lamirande E. Controls of sperm motility. In: De Jonge C., and Barratt C. (Eds). The Sperm Cell: Production, Maturation, Fertilization and Regeneration (2006), Cambridge University Press, Cambridge, UK 108-133
21. Robert M., and Gagnon C. Semenogelin I: a coagulum forming, multifunctional seminal vesicle protein. Cell. Mol. Life Sci. 55 (1999) 944-960
22. de Lamirande E. Semenogelin, the main protein of the human semen coagulum, regulates sperm function. Semin. Thromb. Homost. 33 (2007) 60-68
23. Chatterjee S., Laloraya M., and Kumar P.G. Free radical-induced liquefaction of ejaculated human semen: a new dimension in semen biochemistry. Arch. Androl. 38 (1997) 107-111
24. Jonsson M., Linse S., Frohm B., Lundwall A., and Malm J. Semenogelins I and II blind zinc and regulate the activity of prostate-specific antigen. Biochem. J. 387 (2005) 447-453
25. Ludwig M.L., and Marletta M.A. A new decoration for nitric oxide synthase-a Zn(Cys)4 site. Structure 7 (1999) R73-R79
26. Knapp L.T., and Klann E. Superoxide-induced stimulation of protein kinase C via thiol modification and modulation of zinc content. J. Biol. Chem. 275 (2000) 24136-24145
27. Gavella M., Lipovac V., Vicic M., and Sverko V. In vitro inhibition of superoxide anion production and superoxide dismutase activity by zinc in human spermatozoa. Int. J. Androl. 22 (1999) 266-274
28. Maret W. Zinc coordination environments in proteins determine zinc functions. J. Trace Elem. Med. Biol. 19 (2005) 7-12
29. Olds-Clarke P. Unresolved issues in mammalian fertilization. Int. Rev. Cyt. 232 (2003) 129-184
30. De Jonge C. Biological basis for human capacitation. Hum. Reprod. 11 (2005) 205-214
31. Ford W.C.L. Regulation of sperm function by reactive oxygen species. Hum. Reprod. Updat. 10 (2004) 387-399
32. Liguori L., de Lamirande E., Minelli A., and Gagnon C. Various protein kinases regulate sperm acrosome reaction and the associated phosphorylation of Tyr residues and of the Thr-Glu-Tyr motif. Mol. Hum. Reprod. 11 (2005) 211-221
33. de Lamirande E., Harakat A., and Gagnon C. Human sperm capacitation induced by biological fluids and progesterone, but not by NADH or NADPH, is associated with the production of superoxide anion. J. Androl. 19 (1998) 215-225
34. O'Flaherty C., de Lamirande E., and Gagnon C. Reactive oxygen species modulate independent protein phosphorylation pathways during human sperm capacitation. Free Radic. Biol. Med. 40 (2006) 1045-1055
35. Herrero M.B., Chatterjee S., Lefièvre L., de Lamirande E., and Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radic. Biol. Med. 29 (2000) 522-536
36. de Lamirande E., Tsai C., Harakat A., and Gagnon C. Involvement of reactive oxygen species in human sperm acrosome reaction induced by A23187, lysophosphatidylcholine, and biological fluid ultrafiltrates. J. Androl. 19 (1998) 585-594
37. Thundathil J., de Lamirande E., and Gagnon C. Different signal transduction pathways are involved during human sperm capacitation induced by biological and pharmacological agents. Mol. Hum. Reprod. 8 (2002) 811-816
38. +2 divergences. J. Androl. 25 (2004) 573-585
39. de Lamirande E., and Gagnon C. Involvement of the extracellular signal regulated protein kinase pathway in human sperm function; Involvement of the superoxide anion. Mol. Hum. Reprod. 8 (2002) 124-135
40. O'Flaherty C., de Lamirande E., and Gagnon C. Phosphorylation of the arginine-X-X-(serine/threonine) motif in human sperm capacitation: modulation and protein kinase dependency. Mol. Hum. Reprod. 10 (2004) 355-363
41. O'Flaherty C., de Lamirande E., and Gagnon C. Reactive oxygen species and protein kinases modulate the level of phospho-MEK-like proteins during human sperm capacitation. Biol. Reprod. 73 (2005) 94-105
42. Thundathil J., de Lamirande E., and Gagnon C. Nitric oxide regulates the phosphorylation of the threonine-glutamine-tyrosine motif in proteins of human spermatozoa during capacitation. Biol. Reprod. 68 (2003) 1290-1298
43. Lefièvre L., Jha K.N., de Lamirande E., Visconti P.E., and Gagnon C. Activation of protein kinase A during human sperm capacitation and acrosome reaction. J. Androl. 23 (2002) 709-716
44. Visconti P.E., Moore G.D., Bailey J.L., Leclerc P., Connors S.A., Pan D., Olds-Clarke P., and Kopf G.S. Capacitation of mouse spermatozoa: II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121 (1995) 1139-1150
45. Leclerc P., de Lamirande E., and Gagnon C. cAMP-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol. Reprod. 55 (1996) 684-692
46. Leclerc P., and de Lamirande E. Regulation of protein tyrosine phosphorylation and human sperm capacitation by reactive oxygen derivatives. Free Radic. Biol. Med. 22 (1997) 643-656
47. Carrera A., Moos J., Ning X.P., Gerton G.L., Tesarik J., and Kopf G.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. 180 (1996) 284-296
48. de Lamirande E., and Gagnon C. A positive role for the superoxide in the triggering of human sperm hyperactivation and capacitation. Int. J. Androl. 16 (1993) 21-25
49. de Lamirande E., and Gagnon C. Human sperm hyperactivation and capacitation as parts of an oxidative process. Free Radic. Biol. Med. 14 (1993) 157-166
50. Herrero M.B., de Lamirande E., and Gagnon C. Nitric oxide regulates human sperm capacitation and protein tyrosine phosphorylation in vitro. Biol. Reprod. 61 (2000) 575-581
51. O'Flaherty C., Beorelgui B., and Beconi M.T. Reactive oxygen species requirements for bovine sperm capacitation and acrosome reaction. Theriogenology 52 (1999) 289-301
52. O'Flaherty C., Rodriguez P., and Srivastava S. l-Arginine promotes capacitation and acrosome reaction in cryopreserved bovine spermatozoa. Biochim. Biophys. Acta 1674 (2004) 215-221
53. de Lamirande E., and Gagnon C. Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic. Biol. Med. 18 (1995) 487-496
54. Zhang H., and Zheng R. Promotion of human sperm capacitation by superoxide anion. Free Radic. Res. 24 (1996) 261-268
55. Aitken R.J., Harkiss D., Knox W., Paterson M., and Irvine D.S. A novel signal transduction cascade in capacitating human spermatozoa characterized by a redox-regulated cAMP-mediated induction of tyrosine phosphorylation. J. Cell Sci. 111 (1998) 645-656
56. Harrison R.A.P. Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol. Reprod. Dev. 67 (2004) 337-352
57. Luconi M., Krausz C., Forti G., and Baldi E. Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa. Biol. Reprod. 55 (1996) 207-216
58. Luconi M., Krausz C., Barni T., Vannelli G.V., Forti G., and Baldi E. Progesterone stimulates p42 extracellular signal-regulated kinase (p42erk) in human spermatozoa. Mol. Hum. Reprod. 4 (1998) 251-258
59. Windmann C., Gibson S., Jarpe M.B., and Johnson G.L. Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human. Physiol. Rev. 79 (1999) 143-180
60. Miyata Y., and Nishida E. Distantly related cousins of MAP kinase: biochemical properties and possible physiological functions. Biochem. Biophys. Res. Commun. 266 (1999) 291-295
61. Westendorf J.M., Rao P.N., and Gerace L. Cloning of cDNA for M-phase phosphoproteins recognized by the MPM2 monoclonal antibody and determination of the phosphorylated state. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 714-718
62. Jha K.N., Salicioni A.M., Arcelay E., Chertihin O., Kumari S., Herr J.C., and Visconti P.E. Evidence for the involvement of proline-directed serine/threonine phosphorylation in sperm capacitation. Mol. Hum. Reprod. 12 (2006) 781-789
63. Suarez S.S., and Dai X. Hyperactivation enhanced mouse sperm capacity for penetrating viscoelastic media. Biol. Reprod. 46 (1992) 686-691
64. Stauss C.R., Votta T.J., and Suarez S.S. Sperm motility hyperactivation facilitates penetration of the hamster zona pellucida. Biol. Reprod. 53 (1995) 1280-1285
65. Revelli A., Soldati G., Costamagna C., Pellery O., Aldieri E., Massobrio M., Bosia A., and Ghogo D. Follicular fluid proteins stimulate nitric oxide (NO) synthesis in human sperm: a possible role for NO in acrosomal reaction. J. Cell. Physiol. 178 (1999) 85-92
66. de Lamirande E., and Gagnon C. Paradoxical effect of reagents for sulfhydryl and disulfide groups on human capacitation and superoxide production. Free Radic. Biol. Med. 25 (1998) 803-817
67. Kim J.R., Yoon H.W., Kwon K.-S., Lee S.-R., and Rhee S.G. Identification of proteins containing cystein residues that are sensitive to oxidation by hydrogen peroxide at neutral pH. Anal. Biochem. 283 (2000) 214-221
68. Salmen A., and Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid. Redox Signal. 7 (2005) 560-577
69. Lander H.M., Hajjar D.P., Hempstead B.L., Mirza U.A., Chait B.T., Campbell S., and Quillam L.A. A molecular redox switch on p21(ras): structural basis for the nitric oxide-p21(ras)interaction. J. Biol. Chem. 272 (1997) 4323-4326
70. Lander H.M., Milbank A.J., Tauras J.M., Hajjar D.P., Hempstead B.L., Schwartz G.D., Kreamer T.R., Mirza U.A., Chait B.T., Burk S.C., and Quillam L.A. Redox regulation of cell signalling. Nature 381 (2000) 380-381
71. Mitra K., and Shivaji S. Novel tyrosine-phosphorylated post-pyruvate metabolic enzyme, dihydrolipoamide dehydrogenase, involved in capacitation of hamster spermatozoa. Biol. Reprod. 70 (2004) 887-899
72. Mitra K., Rangaraj N., and Shivaji S. Novelty of the pyruvate metabolic enzyme dihydrolipoamide dehydrogenase in spermatozoa. J. Biol. Chem. 280 (2005) 25743-25753
73. Naaby-Hansen S., Mandal A., Wolkowicz M.J., Sen B., Westbrook V.A., Shetty J., Coonrod S.A., Klotz K.L., Kim Y.H., Bush L.A., Flickinger C.J., and Herr J.C. CABYR, a novel calcium-binding tyrosine phosphorylation-regulated fibrous sheath protein involved in capacitation. Dev. Biol. 242 (2002) 236-254
74. 2+. Biol. Reprod. 67 (2002) 301-307
75. Dubé C., Leclerc P., Baba T., Reyes-Moreno C., and Bailey J.L. The proacrosin binding protein, sp32, is tyrosine phosphorylated during capacitation of pig sperm. J. Androl. 26 (2005) 519-528
76. Bailey J.L., Tardif S., Dubé C., Beaulieu M., Reyes-Moreno C., Lefièvre L., and Leclerc P. Use of proteomics to study tyrosine kinase activity in capacitating boar sperm kinase activity and capacitation. Theriogenology 63 (2005) 599-614
77. Aitken R.J., Nixon B., Lin M., Koppers A.J., Lee Y.H., and Baker M.A. Proteomic changes in mammalian spermatozoa during epididymal maturation. Asian J. Androl. 9 (2007) 554-564
78. Herrero M.B., de Lamirande E., and Gagnon C. Tyrosine nitration in human spermatozoa: a physiological function of peroxynitrite, the reaction product of nitric oxide and superoxide. Mol. Hum. Reprod. 7 (2001) 913-921
79. Ficarro S., Chertihin O., Westbrook V.A., White F., Jayes F., Kabal P., Marto J.A., Shabanowitz J., Herr J.C., Hun D.F., and Visconti P.E. 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 (2003) 11579-11589
80. Bonduelle M., Wennerholm U.-B., Loft A., Tarlatzis B.C., Peters C., Henriet S., Mau C., Victorin-Cederquist A., Van Steirteghem A., Balaska A., Emberson J.R., and Sutcliffe A.G. A multi-centre cohort study on the physical health of 5-year-old children conceived after intracytoplasmic sperm injection, in vitro fertilization and natural conception. Hum. Reprod. 20 (2005) 413-419
81. Hansen M., Bower C., Milne E., de Klerk N., and Kurinczuk J. Assisted reproductive technologies and the risk of birth defects-a systematic review. Hum. Reprod. 20 (2005) 328-338