A novel signal transduction cascade in capacitating human spermatozoa characterised by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation

Journal of Cell Science

Volumn 111, Issue 5, 1998, Pages 645-656

  Aitken, R J ^a   Harkiss, D ^a   Knox, W ^a   Paterson, M ^a   Irvine, D S ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

cAMP; Reactive oxygen species; Spermatozoa; Tyrosine phosphorylation

Indexed keywords

CATALASE; CYCLIC AMP; DEOXYGLUCOSE; MERCAPTOETHANOL; N [2 (4 BROMOCINNAMYLAMINO)ETHYL] 5 ISOQUINOLINESULFONAMIDE; PROGESTERONE; REACTIVE OXYGEN METABOLITE; TYROSINE;

ARTICLE; HUMAN; HUMAN CELL; MALE; OXIDATION REDUCTION REACTION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SPERMATOZOON CAPACITATION;

MAMMALIA;

EID: 0031890532     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.111.5.645     Document Type: Article

References (53)

1. 2+ dependent ATPase activity, stimulated by decapacitation factor and calmodulin, in mouse sperm. Mol. Reprod. Dev. 44, 111-120.
2. Ahuja, K. K. (1985). Inhibitors of glycoprotein biosynthesis block fertilization in the hamster. Gamete Res. 11, 179-189.
3. Aitken, R. J. (1997). Molecular mechanisms regulating human spens function. Mol. Human Reprod. 3, 169-173.
4. Aitken, R. J. and Clarkson, J. S. (1987). Cellular basis of defective sperm function and its association with the genesis of reactive oxygen species by human spermatozoa. J. Reprod. Fertil. 81, 459-469.
5. Aitken, R. J., Buckingham, D., Brindle, J., Gomez, E., Baker, G. and Irvine, D. S. (1995a). Analysis of sperm movement in relation to the oxidative stress created by leucocytes in washed sperm preparations and seminal plasma. Human Reprod. 10, 2061-2071.
6. Aitken, R. J., Buckingham, D. W., Harkiss, D., Fisher, H., Paterson, M. and Irvine, D. S. (1996a). The extragenomic action of progesterone on human spermatozoa is influenced by redox regulated changes in tyrosine phosphorylation during capacitation. Mol. Cell. Endocrinol. 117, 83-93.
7. Aitken, R. J., Buckingham, D. W. and Huang, G.-F. (1993). Analysis of the responses of human spermatozoa to A23187 employing a novel technique to monitor the acrosome reaction. J. Androl. 14, 132-141.
8. Aitken, R. J., Buckingham, D. W. and Irvine, D. S. (1996b). The extragenomic action of progesterone on human spermatozoa: evidence for a ubiquitous response that is rapidly down-regulated. Endocrinology 137, 3999-4009.
9. Aitken, R. J., Buckingham, D. W. and West, K. M. (1992). Reactive oxygen species and human spermatozoa; analysis of the cellular mechanisms involved in luminol- and lucigenin-dependent chemiluminescence. J. Cell. Physiol. 151, 466-477.
10. Aitken, R. J., Fisher, H., Fulton, N., Knox, W. and Lewis, B. (1997a). 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. 47, 468-482.
11. Aitken, R. J., Harkiss, D., Knox, W., Paterson, M. and Irvine, D. S. (1997b). On the cellular mechanisms by which the bicarbonate ion mediates the extragenomic action of progesterone on human spermatozoa. Biol. Reprod. (in press).
12. Aitken, R. J., Paterson, M., Fisher, H., Buckingham, D. W. and van Duin, M. (1995). Redox regulation of tyrosine phosphorylation in human spermatozoa and its role in the control of human sperm function. J. Cell Sci. 108, 2017-2025.
13. Bergamo, P., Venditti P., Talevi R., Sansone G. and Abrescia P. (1993). Two rat middle-piece coating antigens are lost upon in vitro capacitation. Cell. Physiol. Biochem. 3, 146-156.
14. Biggers, J. D., Whitten, W. K., Whittingham, D. G. (1971). The culture of mouse embryos in vitro. In Methods in Mammalian Embryology (ed. J. C. Daniel Jr.), pp. 86-116. Freeman. San Francisco.
15. Blackmore, P. F., Beebe, S. J., Danforth, D. R. and Alexander, N. (1990). Progesterone and 17-hydroxyprogesterone: novel stimulators of calcium influx in human sperm. J Biol. Chem. 265, 1376-1380.
16. Carrera, A., Moos, J., Ning, X. P., 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.
17. de Lamirande, E. and Gagnon, C. (1993). Human sperm hyperactivation as part of an oxidative process. Free Rad. Biol. Med. 314, 157-166.
18. Demaurex, N., Downey, G. P., Waddell, T. K. and Grinstein, S. (1996) Intracellular pH regulation during spreading of human neutrophits. J. Cell Biol. 133, 1391-1402
19. 2+ are initiated by the zona pellucida during acrosomal exocytosis. Dev. Biol. 165, 152-164.
20. Fraser, L. R. and Herod, J. E. (1990). Expression of capacitation-dependent changes in chlorotetracycline fluorescence patterns in mouse spermatozoa requires a suitable glycolysable substrate. J. Reprod. Fertil. 88, 611-621.
21. 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. Re-prod. 56, 707-719.
22. Gomez, E., Buckingham, D. W., Brindle, J., Lanzafame, F., Irvine. D. S. and Aitken, R. J. (1996). Development of an image analysis system to monitor the retention of residual cytoplasm by human spermatozoa: correlation with biochemical markers of the cytoplasmic space. oxidative stress and sperm function. J. Androl. 17, 276-287.
23. Griveau, J. F., Renard, P. and Le Lannou, D. (1995). Superoxide anion production by human spermatozoa as a part of the lonophore-induced acrosome reaction process. Int. J. Androl. 18, 67-74.
24. 2 and vanadate vitro. Biochem. Biophys. Res. Commun. 188, 773-779.
25. 2 potentiates phosphorylation of novel putative substrates for the insulin receptor kinase in intact Fao cells. J. Biol. Chem. 264, 10126-10132.
26. + channel- evidence that gp9l-phox functions as an essential part of the channel. J. Biol. Chem. 270, 5909-5916.
27. Hirono, A. and Beutler, E. (1989). Alternative splicing of human glucose-6-phosphate dehydrogenase messenger RNA in different tissues. J. Clin. Invest. 83, 343-346.
28. Hyne, R. E. and Garbers, D. L. (1979). Regulation of guinea pig sperm adenylate cyclase by calcium. Biol. Reprod. 21, 1135-1142.
29. Kleinveld, H. A., Sluiter, W, Boonman, A. M. C., Swaak, A. J. G., Hack, C. E. and Koster, J. F. (1991). Differential stimulation of oxygen-free-radical-altered immunoglobulin G of the production of Superoxide and hydrogen peroxide by human polymorphonuclear leucocytes. Clin. Sci. 80, 385-391.
30. Langlais, J. and Roberts, K. D. (1985). A molecular membrane model of sperm capacitation and the acrosome reaction of mammalian spermatozoa. Gamete Res. 12, 183-224.
31. Leclerc, P., de Lamirande, E. and 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.
32. Leclerc, P., de Lamirande, E. and Gagnon, C. (1997). Regulation of protein-tyrosine phophorylation and human sperm capacitation by reactive oxygen derivatives. Free Rad. Biol. Med. 22, 643-656.
33. Leyton, L. and Saling, P. M. (1989). 95 kD sperm proteins bind ZP3 and serve as tyrosine kinase substrates in response to zona binding. Cell 57, 1123-1130.
34. MacLeod, J. (1943). The role of oxygen in the metabolism and motility of human spermatozoa. Am. J. Physiol. 138, 512-518.
35. Meizel, S. and Turner, K. O. (1996). Chloride efflux during the progesterone-initiated human sperm acrosome reaction is inhibited by lavendustin A. a tyrosine kinase inhibitor. J. Androl. 17, 327-330.
36. Monteiro, H. P. and Stern, A. (1996). Redox regulation of tyrosine phosphorylation-dependent signal transduction pathways. Free Rad. Biol. Med. 21, 323-333.
37. Naftalin, R. J. and Rist, R. J. (1993). The relationship between sugar metabolism. transport and Superoxide radical production in rat peritoneal macrophages. Biochim. Biophys. Acta 1148, 39-50.
38. + conductance of leukocytes. J. Biol. Chem. 269, 27280-27285.
39. Osman, R. A., Andria, M. L., Jones, A. D. and Meizel, M. (1989). Steroid induced exocytosis: the human sperm acrosome reaction. Biochim. Biophys. Res. Commun. 160, 828-34.
40. 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. 51, 1099-1 108.
41. Segal, A. W. (1995). The NADPH oxidase of phagocytic cells is an electron pump that alkalinizes the phagocytic vacuole. Protoplasma 184, 86-103.
42. Shibanuma, M., Kuroki, T. and Nose, K. (1988) Superoxide as a signal for increase in intracellular pH. J. Cell. Physiol. 136, 379-383.
43. Spungin, B. and Breitbart, H. (1996). Calcium mobilization and influx during sperm exocytosis. J. Cell Sci. 109, 1947-1955.
44. Suter, D., Chow, P.Y.W. and Martin, I. C. A. (1979). Maintenance of motility in human spermatozoa by energy derived through oxidative phosphorylation and addition of albumin. Biol. Reprod. 20, 505-510.
45. Tan, C. M., Xenoyannis, S. and Feldman, R. D. (1995). Oxidant stress enhances adenylyl cyclase activation. Circ. Res. 77, 710-717.
46. Traxinger, R. R. and Marshall, S. (1990). Suitability of 2-deoxyglucose for measuring initial rates of glucose uptake in isolated adipocytes. Biochem. Int. 22, 607-615.
47. Visconti, P. E., Moore, G. D., Bailey, J. L., Leclerc, P., Connors, S. A., Pan, D., Olds-Clarke, P. and Kopf, G. S. (1995) Capacitation in mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway. Development 121, 1139-1150
48. Yanagimachi, R. (1994) Mammalian fertilization. In The Physiology of Reproduction. Second Edition (ed. E. Knobil and J. D. Neill). pp. 189-317. Raven Press. New York. NY.
49. Yanagimachi, R., Yanagimachi, H. and Rogers, B. J. (1976). The use of zona free animal ova as a test system for the assessment of the femlizing capacity of human spermatozoa. Biol. Reprod. 15, 471-476.
50. Wassarman, P. (1988). Zona pellucida glyscoproteins. Ann. Rev. Biochem. 57, 415-442.
51. White, D. R. and Aitken, R. J. (1989). Relationship between calcium. cAMP. ATP and intracellular pH and the capacity to express hyperactivated motility by hamster spernmatozoa. Gamete Res. 22, 163-178.
52. World Health Organization (1992). WHO Laboratory Manual for the Examination of Human Semen and Semen-Cervical Mucus Interaction Cambridge University Press. Cambridge.
53. --dcpendent. and HCO: dependent and arylaiminobenzoate-dependent regulatory mechanisms and characterization of their roles in sperm capacitation. Dev. Biol. 173, 510-520.