Levels of semenogelin in human spermatozoa decrease during capacitation: Involvement of reactive oxygen species and zinc

Human Reproduction

Volumn 25, Issue 7, 2010, Pages 1619-1630

  De Lamirande, E ^a,b   Lamothe, G ^a,b  

^a ROYAL VICTORIA HOSPITAL   (Canada)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

capacitation; human spermatozoa; nitric oxide; semenogelin; superoxide anion

Indexed keywords

CELL PROTEIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE INHIBITOR; OXYGEN; REACTIVE OXYGEN METABOLITE; SEMENOGELIN; SUPEROXIDE; SUPEROXIDE DISMUTASE; TYLOXAPOL; UNCLASSIFIED DRUG; ZINC;

ARTICLE; CELLULAR DISTRIBUTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNOBLOTTING; IMMUNOCYTOCHEMISTRY; MALE; PROTEIN FUNCTION; SPERMATOZOON CAPACITATION;

EID: 77955908178     PISSN: 02681161     EISSN: 14602350     Source Type: Journal    
DOI: 10.1093/humrep/deq110     Document Type: Article

References (53)

1. 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.
2. Andrews JC, Noland JP, Hammerstedt RH, Bavister BD. Role of zinc in hamster sperm capacitation. Biol Reprod 1994;51:1238-1247.
3. Biggers JD, Whitten WK, Whittingham DG. The culture of mouse embryos in vitro. In: Daniel JC (ed). Methods in Mammalian Embryology. USA: Freeman, San Francisco, 1971, 86-116.
4. Bjartell A, Malm J, Moller C, Gunnarsson M, Lundwall A, Lilja H. Distribution and tissue expression of semenogelin I and II in man as demonstrated by in situ hybridization and immunocytochemistry. J Androl 1996;17:17-26.
5. Chatterjee S, Laloraya M, Kumar PG. Free radical-induced liquefaction of ejaculated human semen: a new dimension in semen biochemistry. Arch Androl 1997;38:107-111.
6. Chiu PCN, Chung M-K, Tsang H-Y, Koistinen R, Koistinen H, Seppala M, Lee K-F, Yeung WSB. Glycodelin-S in human seminal plasma reduces cholesterol efflux and inhibits capacitation of spermatozoa. J Biol Chem 2005;280:25580-25589.
7. Cormier N, Sirard M-A, Bailey JL. Premature capacitation of bovine spermatozoa is initiated by cryopreservation. J Androl 1997;18:461-468.
8. Cross NL. Human seminal plasma prevents sperm from becoming acrosomally responsive to the agonist progesterone: cholesterol is the major inhibitor. Biol Reprod 1996;54:138-145.
9. Cross NL, Morales P, Overstreet JW, Hanson FW. Two simple methods for detecting the acrosome reaction in human sperm. Gamete Res 1986; 15:29-40.
10. De Jonge C. Biological basis for human capacitation. Hum Reprod 2005; 11:205-214.
11. De Lamirande E. Semenogelin, the main protein of the human semen coagulum, regulates sperm function. Semin Thromb Hemost 2007; 33:60-68.
12. De Lamirande E, Gagnon C. Human sperm hyperactivation in whole semen and its association with low superoxide scavenging capacity in seminal plasma. Fertil Steril 1993;59:1291-1295.
13. De Lamirande E, Gagnon C. Capacitation-associated production of superoxide anion by human spermatozoa. Free Radic Biol Med 1995; 18:487-496.
14. De Lamirande E, Lamothe G. Free radical-induced free radical production during human sperm activation. Free Radic Biol Med 2009;46: 502-510.
15. De Lamirande E, O'Flaherty C. Sperm activation: role of reactive oxygen species and kinases. Biochim Biophys Acta 2008;1784:106-115.
16. De Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997;3:175-194.
17. De Lamirande E, Yoshida K, Yoshiike M, Iwamoto T, Gagnon C. Semenogelin, the main protein of semen coagulum, inhibits human sperm capacitation by interfering with the superoxide anion generated during this process. J Androl 2001;22:672-679.
18. De Lamirande E, Lamothe G, Villemure M. Controls of superoxide and nitric oxide formation during human sperm capacitation. Free Radic Biol Med 2009;46:1420-1427.
19. Desnoyers L, Manjunath P. Major proteins of seminal plasma exhibit novel interactions with phospholipids. J Biol Chem 1992;267:10149-10155.
20. Dröge W. Free radicals in the physiological control of cell function. Physiol Rev 2001;82:47-95.
21. Edström AML, Malm J, Frohm B, Martellini JA, Giwercman A, Mörgelin M, Cole AM, Sørensen OE. The major bactericidal activity of human seminal plasma is zinc-dependent and derived from fragmentation of the semenogelins. J Immunol 2008;181:3413-3421.
22. Ek P, Malm J, Lilja H, Carlsson L, Ronquist G. Exogenous protein kinases A and C, but not endogenous prostasome associated protein kinase, phosphorylate semenogelins I and II from human semen. J Androl 2002;23:806-814.
23. Flori F, Ermeni L, Battista LaSala G, Nicoli A, Capone A, Focarelli R, Rosati F, Della Giovampaola C. The GPI-anchored CD52 antigen of the sperm surface interacts with semenogelin and participates in clot formation and liquefaction of human semen. Mol Reprod Dev 2008; 75:326-335.
24. Halliwell B, Gutteridge JMC. Free Radicals in Biology and Medicine, 4th edn. Oxford, UK: Oxford University Press, 2007, 851 pp.
25. Hayashi K, Yonemura S, Matsui T, Tsukita S, Tsukita S. Immunofluorescence detection of ezrin/radixin/moesin (ERM) proteins with their carboxyl-terminal threonine phosphorylated in cultured cells and tissues. Application of a novel fixation protocol using trichloroacetic acid (TCA) as fixative. J Cell Sci 1999; 112:1149-1158.
26. Herrero MB, Chatterjee S, Lefièvre L, de Lamirande E, Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radic Biol Med 2000a;29:522-536.
27. Herrero MB, de Lamirande E, Gagnon C. Nitric oxide regulates human sperm capacitation and protein tyrosine phosphorylation in vitro. Biol Reprod 2000b;61:575-581.
28. Herrero MB, de Lamirande E, Gagnon C. Nitric oxide is a signaling molecule in spermatozoa. Curr Pharm Des 2003;9:419-425.
29. Jonsson M, Linse S, Frohm B, Lundwall A, Malm J. Semenogelins I and II bind zinc and regulate the activity of prostate-specific antigen. Biochem J 2005;387:447-453.
30. Jonsson M, Lundwall A, Malm J. The semenogelins: proteins with functions beyond reproduction? Cell Mol Life Sci 2006;63:2886-2888.
31. Lilja H, Abrahamsson P-A, Lundwall A. Semenogelin, the predominant protein in human semen. Primary structure and identification of closely related proteins in the male accessory sex glands and on spermatozoa. J Biol Chem 1989;264:1894-1900.
32. Lundwall A, Bjartell A, Olsson A, Malm J. Semenogelin I and II, the predominant human seminal plasma proteins, are also expressed in non-genital tissues. Mol Hum Reprod 2002;8:805-810.
33. Kumar V, Hassan I, Kashav T, Singh TP, Yadav S. Heparin-binding proteins of human seminal plasma: purification and characterization. Mol Reprod Dev 2008;75:1767-1774.
34. Mandal A, Bhattacharyya AK. Sperm hyaluronidase activation by purified predominant and major basic human seminal coagulum proteins. Hum Reprod 1995;10:1745-1750.
35. Martellini JA, Cole AL, Venkataraman N, Quinn GA, Svoboda P, Gangrade BK, Pohl P, Sørensen OE, Cole AM. Cationic polypeptides contribute to the anti-HIV-1 activity of human seminal plasma. FASEB J 2009;23:3609-3618
36. Martínez-Heredia J, de Mateo S, Vidal-Taboada JM, Ballesca JL, Oliva R. Identification of proteomic differences in asthenozoospermic sperm samples. Hum Reprod 2008;23:783-791.
37. Mikkelsen RB, Wardman P. Biological chemistry of reactive oxygen and nitrogen and radiation-induced signal transduction mechanisms. Oncogene 2003;22:5734-5754.
38. 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.
39. 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.
40. Oshio S, Kaneko S, Iisuka R, Mohri H. Sialic acid in purified human sperm. Arch Androl 1987;18:225-230.
41. Peter A, Lilja H, Lundwall A, Malm J. Semenogelin I and semenogelin II, the major gel-forming proteins in human semen, are substrates for transglutaminase. Eur J Biochem 1998;252:216-221.
42. Plante M, de Lamirande E, Gagnon C. Reactive oxygen species released by activated neutrophils, but not by deficient spermatozoa, are sufficient to affect normal sperm motility. Fertil Steril 1994;62:387-393.
43. Robert M, Gagnon C. Sperm motility inhibitor from human seminal plasma: association with semen coagulum. Hum Reprod 1995; 10:2192-2197.
44. Robert M, Gagnon C. Semenogelin I: a coagulation forming multifunctional seminal vesicle protein. Cell Mol Life Sci 1999;55:944-960.
45. Suzuki K, Kise H, Nishioka J, Hayashi T. The interaction among protein C inhibitor, prostate-specific antigen, and the semenogelin system. Semin Thromb Hemost 2007;33:46-52.
46. Thundathil J, de Lamirande E, Gagnon C. Nitric oxide regulates the phosphorylation of the threonine-glutamine-tyrosine motif in proteins of human spermatozoa during capacitation. Biol Reprod 2003; 68:1291-1298.
47. Wang Z, Widgren EE, Richardson RT, O'Rand MG. Characterization of an eppin protein complex from human semen and spermatozoa. Biol Reprod 2007;77:476-484.
48. Wilcox S. The new antimicrobials: Cationic peptides. Biotechnol J 2004; 2:88-91.
49. World Health Organization. Laboratory Manual for the Examination of Human Semen and Semen-cervical Mucus Interaction, 4th edn. Cambridge, UK: Cambridge Univ Press, 1999.
50. Yeaman MR, Yount NY. Mechanisms of antimicrobial peptide action and resistance. Pharmacol Rev 2003;55:27-55.
51. Yoshida K, Kawano N, Yoshiike M, Yoshida M, Iwamoto T, Morisawa M. Physiological roles of semenogelin I and zinc in sperm motility and semen coagulation on ejaculation in humans. Mol Hum Reprod 2008;14:151-156.
52. Yoshida K, Krasznai ZT, Krasznai Z, Yoshiike M, Kawano N, Yoshida M, Morisawa M, Toth Z, Bazsáné ZK, Márián T et al. Functional implications of membrane modification with semenogelins for inhibition of sperm motility in humans. Cell Motil Cytoskeleton 2009;66: 99-108.
53. Zalensky AO, Yau P, Brenerman JW, Bradbury EM. The abundant 19-kilodalton protein associated with human sperm nuclei that is related to seminal plasma alpha-inhibin. Mol Reprod Dev 1993;36: 164-173.