Snake venoms as a source of compounds modulating sperm physiology: Secreted phospholipases A2 from Oxyuranus scutellatus scutellatus impact sperm motility, acrosome reaction and in vitro fertilization in mice

Biochimie

Volumn 92, Issue 7, 2010, Pages 826-836

  Escoffier, Jessica ^a,b   Couvet, Morgane ^b,c,d   de Pomyers, Harold ^e   Ray, Pierre F ^f,g   Sève, Michel ^b,c,d   Lambeau, Gérard ^g,h   De Waard, Michel ^a,b   Arnoult, Christophe ^a,b,g  

^a GRENOBLE INSTITUT DES NEUROSCIENCES   (France)

^b UNIV GRENOBLE ALPES   (France)

^c INSERM   (France)

^d Plateforme de protéomique médicale   (France)

^e Latoxan   (France)

^f GRENOBLE UNIVERSITY HOSPITAL   (France)

^g CNRS   (France)

^h UNIVERSITÉ CÔTE D'AZUR   (France)

Author keywords

Acrosome reaction; In vitro fertilization; Secreted phospholipase A2; Snake venom; Sperm motility

Indexed keywords

PHOSPHOLIPASE A2; SNAKE VENOM; REPTILIAN PROTEIN; SECRETORY PHOSPHOLIPASE A2;

ACROSOME REACTION; ANIMAL CELL; ARTICLE; CATALYSIS; CELL MEMBRANE; CONCENTRATION RESPONSE; CONTROLLED STUDY; EMBRYO DEVELOPMENT; FERTILIZATION IN VITRO; LIPID COMPOSITION; LIPID METABOLISM; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYURANUS SCUTELLATUS SCUTELLATUS; PHOSPHOLIPID MEMBRANE; PROTEOMICS; SNAKE; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; ANIMAL; BIOCATALYSIS; CHEMISTRY; COLUBRIDAE; CYTOLOGY; DRUG EFFECTS; ELAPIDAE; GEL CHROMATOGRAPHY; ISOLATION AND PURIFICATION; MALE; METABOLISM; SPERMATOZOON; VIPERIDAE;

ACROSOME REACTION; ANIMALS; BIOCATALYSIS; CHROMATOGRAPHY, GEL; COLUBRIDAE; ELAPIDAE; EMBRYONIC DEVELOPMENT; FERTILIZATION IN VITRO; LIPID METABOLISM; MALE; MICE; MOLECULAR WEIGHT; PHOSPHOLIPASES A2, SECRETORY; PROTEOMICS; REPTILIAN PROTEINS; SNAKE VENOMS; SPERM MOTILITY; SPERMATOZOA; VIPERIDAE;

EID: 77953536038     PISSN: 03009084     EISSN: 61831638     Source Type: Journal    
DOI: 10.1016/j.biochi.2010.03.003     Document Type: Article

References (52)

1. Auger J., Kunstmann J.M., Czyglik F., Jouannet P. Decline in semen quality among fertile men in Paris during the past 20 years. N. Engl. J. Med. 1995, 332:281-285.
2. Sharpe R.M., Skakkebaek N.E. Are oestrogens involved in falling sperm counts and disorders of the male reproductive tract?. Lancet 1993, 341:1392-1395.
3. Esposito G., Jaiswal B.S., Xie F., Krajnc-Franken M.A., Robben T.J., Strik A.M., Kuil C., Philipsen R.L., van Duin M., Conti M., Gossen J.A. Mice deficient for soluble adenylyl cyclase are infertile because of a severe sperm-motility defect. Proc. Natl. Acad. Sci. U.S.A. 2004, 101:2993-2998.
4. Escalier D. Knockout mouse models of sperm flagellum anomalies. Hum. Reprod. Update 2006, 12:449-461.
5. Dieterich K., Soto R.R., Faure A.K., Hennebicq S., Ben Amar B., Zahi M., Perrin J., Martinez D., Sele B., Jouk P.S., Ohlmann T., Rousseaux S., Lunardi J., Ray P.F. Homozygous mutation of AURKC yields large-headed polyploid spermatozoa and causes male infertility. Nat. Genet. 2007, 39:661-665.
6. Salicioni A.M., Platt M.D., Wertheimer E.V., Arcelay E., Allaire A., Sosnik J., Visconti P.E. Signalling pathways involved in sperm capacitation. Soc. Reprod. Fertil. Suppl. 2007, 65:245-259.
7. Jungnickel M.K., Sutton K.A., Florman H.M. In the beginning: lessons from fertilization in mice and worms. Cell 2003, 114:401-404.
8. Flockerzi V., Oeken H.J., Hofmann F., Pelzer D., Cavalie A., Trautwein W. Purified dihydropyridine-binding site from skeletal muscle t-tubules is a functional calcium channel. Nature 1986, 323:66-68.
9. Inoue N., Ikawa M., Isotani A., Okabe M. The immunoglobulin superfamily protein Izumo is required for sperm to fuse with eggs. Nature 2005, 434:234-238.
10. Hugues M., Romey G., Duval D., Vincent J.P., Lazdunski M. Apamin as a selective blocker of the calcium-dependent potassium channel in neuroblastoma cells: voltage-clamp and biochemical characterization of the toxin receptor. Proc. Natl. Acad. Sci. U.S.A. 1982, 79:1308-1312.
11. Bourinet E., Soong T.W., Sutton K., Slaymaker S., Mathews E., Monteil A., Zamponi G.W., Nargeot J., Snutch T.P. Splicing of alpha 1A subunit gene generates phenotypic variants of P- and Q-type calcium channels. Nat. Neurosci. 1999, 2:407-415.
12. Ménez A., Gillet D., Grishin E. Recent Research Developments on Toxins from Bacteria and Other Organisms 2005, Research Signpost, Trivandrum, India. L. D.Gillet (Ed.).
13. Rouault M., Rash L.D., Escoubas P., Boilard E., Bollinger J., Lomonte B., Maurin T., Guillaume C., Canaan S., Deregnaucourt C., Schrevel J., Doglio A., Gutierrez J.M., Lazdunski M., Gelb M.H., Lambeau G. Neurotoxicity and other pharmacological activities of the snake venom phospholipase A2 OS2: the N-terminal region is more important than enzymatic activity. Biochemistry 2006, 45:5800-5816.
14. Shilov I.V., Seymour S.L., Patel A.A., Loboda A., Tang W.H., Keating S.P., Hunter C.L., Nuwaysir L.M., Schaeffer D.A. The Paragon Algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell Proteomics 2007, 6:1638-1655.
15. Lambeau G., Barhanin J., Schweitz H., Qar J., Lazdunski M. Identification and properties of very high affinity brain membrane-binding sites for a neurotoxic phospholipase from the taipan venom. J. Biol. Chem. 1989, 264:11503-11510.
16. Francis B., Gutierrez J.M., Lomonte B., Kaiser I.I. Myotoxin II from Bothrops asper (Terciopelo) venom is a lysine-49 phospholipase A2. Arch. Biochem. Biophys. 1991, 284:352-359.
17. Valentin E., Lambeau G. What can venom phospholipases A(2) tell us about the functional diversity of mammalian secreted phospholipases A(2)?. Biochimie 2000, 82:815-831.
18. de Paula R.C., Castro H.C., Rodrigues C.R., Melo P.A., Fuly A.L. Structural and pharmacological features of phospholipases A2 from snake venoms. Protein Pept. Lett. 2009, 16:899-907.
19. Davidson F.F., Dennis E.A. Evolutionary relationships and implications for the regulation of phospholipase A2 from snake venom to human secreted forms. J. Mol. Evol. 1990, 31:228-238.
20. Lomonte B., Angulo Y., Sasa M., Gutierrez J.M. The phospholipase A2 homologues of snake venoms: biological activities and their possible adaptive roles. Protein Pept. Lett. 2009, 16:860-876.
21. Singer A.G., Ghomashchi F., Le Calvez C., Bollinger J., Bezzine S., Rouault M., Sadilek M., Nguyen E., Lazdunski M., Lambeau G., Gelb M.H. Interfacial kinetic and binding properties of the complete set of human and mouse groups I, II, V, X, and XII secreted phospholipases A2. J. Biol. Chem. 2002, 277:48535-48549.
22. Nicolas J.P., Lin Y., Lambeau G., Ghomashchi F., Lazdunski M., Gelb M.H. Localization of structural elements of bee venom phospholipase A2 involved in N-type receptor binding and neurotoxicity. J. Biol. Chem. 1997, 272:7173-7181.
23. Beck L.H., Bonegio R.G., Lambeau G., Beck D.M., Powell D.W., Cummins T.D., Klein J.B., Salant D.J. M-type phospholipase A2 receptor as target antigen in idiopathic membranous nephropathy. N. Engl. J. Med. 2009, 361:11-21.
24. Rigoni M., Caccin P., Gschmeissner S., Koster G., Postle A.D., Rossetto O., Schiavo G., Montecucco C. Equivalent effects of snake PLA2 neurotoxins and lysophospholipid-fatty acid mixtures. Science 2005, 310:1678-1680.
25. Kirchhoff C., Schroter S. New insights into the origin, structure and role of CD52: a major component of the mammalian sperm glycocalyx. Cells Tissues Organs 2001, 168:93-104.
26. Janssen M.J., van de Wiel W.A., Beiboer S.H., van Kampen M.D., Verheij H.M., Slotboom A.J., Egmond M.R. Catalytic role of the active site histidine of porcine pancreatic phospholipase A2 probed by the variants H48Q, H48N and H48K. Protein Eng. 1999, 12:497-503.
27. dos Santos J.I., Soares A.M., Fontes M.R. Comparative structural studies on Lys49-phospholipases A(2) from Bothrops genus reveal their myotoxic site. J. Struct. Biol. 2009, 167:106-116.
28. Zhou X., Tan T.C., Valiyaveettil S., Go M.L., Kini R.M., Velazquez-Campoy A., Sivaraman J. Structural characterization of myotoxic ecarpholin S from Echis carinatus venom. Biophys. J. 2008, 95:3366-3380.
29. Silva P.F., Gadella B.M. Detection of damage in mammalian sperm cells. Theriogenology 2006, 65:958-978.
30. Gadella B.M., Harrison R.A. Capacitation induces cyclic adenosine 3',5'-monophosphate-dependent, but apoptosis-unrelated, exposure of aminophospholipids at the apical head plasma membrane of boar sperm cells. Biol. Reprod. 2002, 67:340-350.
31. Roldan E.R., Shi Q.X. Sperm phospholipases and acrosomal exocytosis. Front. Biosci. 2007, 12:89-104.
32. Roldan E.R., Fragio C. Phospholipase A2 activation and subsequent exocytosis in the Ca2+/ionophore-induced acrosome reaction of ram spermatozoa. J. Biol. Chem. 1993, 268:13962-13970.
33. Yuan Y.Y., Chen W.Y., Shi Q.X., Mao L.Z., Yu S.Q., Fang X., Roldan E.R. Zona pellucida induces activation of phospholipase A2 during acrosomal exocytosis in guinea pig spermatozoa. Biol. Reprod 2003, 68:904-913.
34. Pietrobon E.O., Soria M., Dominguez L.A., Monclus M.L., Fornes M.W. Simultaneous activation of PLA2 and PLC are required to promote acrosomal reaction stimulated by progesterone via G-proteins. Mol. Reprod. Dev. 2005, 70:58-63.
35. Shi Q.X., Chen W.Y., Yuan Y.Y., Mao L.Z., Yu S.Q., Chen A.J., Ni Y., Roldan E.R. Progesterone primes zona pellucida-induced activation of phospholipase A2 during acrosomal exocytosis in guinea pig spermatozoa. J. Cell Physiol. 2005, 205:344-354.
36. Fleming A.D., Yanagimachi R. Evidence suggesting the importance of fatty acids and the fatty acid moieties of sperm membrane phospholipids in the acrosome reaction of guinea pig spermatozoa. J. Exp. Zool. 1984, 229:485-489.
37. Llanos M.N., Morales P., Riffo M.S. Studies of lysophospholipids related to the hamster sperm acrosome reaction in vitro. J. Exp. Zool. 1993, 267:209-216.
38. Riffo M., Nieto A. Lysophosphatidylcholine induces changes in physicochemical, morphological, and functional properties of mouse zona pellucida: a possible role of phospholipase A2 in sperm-zona pellucida interaction. Mol. Reprod. Dev. 1999, 53:68-76.
39. Riffo M.S., Parraga M. Role of phospholipase A2 in mammalian sperm-egg fusion: development of hamster oolemma fusibility by lysophosphatidylcholine. J. Exp. Zool. 1997, 279:81-88.
40. A. Zalata, A. Hassan, A. Christophe, F. Comhaire, T. Mostafa, Cholesterol and desmosterol in two sperm populations separated on Sil-Select gradient, Int. J. Androl, in press, doi:. doi:10.1111/j.1365-2605.2009.00961.x.
41. Schaloske R.H., Dennis E.A. The phospholipase A2 superfamily and its group numbering system. Biochim. Biophys. Acta 2006, 1761:1246-1259.
42. Lambeau G., Ancian P., Nicolas J.P., Beiboer S.H., Moinier D., Verheij H., Lazdunski M. Structural elements of secretory phospholipases A2 involved in the binding to M-type receptors. J. Biol. Chem. 1995, 270:5534-5540.
43. Kumar J.R., Basavarajappa B.S., Arancio O., Aranha I., Gangadhara N.S., Yajurvedi H.N., Gowda T.V. Isolation and characterization of " Reprotoxin" , a novel protein complex from Daboia russelii snake venom. Biochimie 2008, 90:1545-1559.
44. Montell C. New light on TRP and TRPL. Mol. Pharmacol. 1997, 52(5):755-763. (GENERIC).
45. Buffone M.G., Verstraeten S.V., Calamera J.C., Doncel G.F. High cholesterol content and decreased membrane fluidity in human spermatozoa are associated with protein tyrosine phosphorylation and functional deficiencies. J. Androl. 2009, 30:552-558.
46. Gulaya N.M., Margitich V.M., Govseeva N.M., Klimashevsky V.M., Gorpynchenko I.I., Boyko M.I. Phospholipid composition of human sperm and seminal plasma in relation to sperm fertility. Arch. Androl 2001, 46:169-175.
47. Ollero M., Gil-Guzman E., Lopez M.C., Sharma R.K., Agarwal A., Larson K., Evenson D., Thomas A.J., Alvarez J.G. Characterization of subsets of human spermatozoa at different stages of maturation: implications in the diagnosis and treatment of male infertility. Hum. Reprod. 2001, 16:1912-1921.
48. Aksoy Y., Aksoy H., Altinkaynak K., Aydin H.R., Ozkan A. Sperm fatty acid composition in subfertile men. Prostaglandins Leukot. Essent. Fatty Acids 2006, 75:75-79.
49. Bao S., Miller D.J., Ma Z., Wohltmann M., Eng G., Ramanadham S., Moley K., Turk J. Male mice that do not express group VIA phospholipase A2 produce spermatozoa with impaired motility and have greatly reduced fertility. J. Biol. Chem. 2004, 279:38194-38200.
50. Masuda S., Murakami M., Matsumoto S., Eguchi N., Urade Y., Lambeau G., Gelb M.H., Ishikawa Y., Ishii T., Kudo I. Localization of various secretory phospholipase A2 enzymes in male reproductive organs. Biochim. Biophys. Acta 2004, 1686:61-76.
51. Silva P.F., Gadella B.M., Colenbrander B., Roelen B.A. Exposure of bovine sperm to pro-oxidants impairs the developmental competence of the embryo after the first cleavage. Theriogenology 2007, 67:609-619.
52. Grunewald S., Reinhardt M., Blumenauer V., Said T.M., Agarwal A., Abu H.F., Glander H.J., Paasch U. Increased sperm chromatin decondensation in selected nonapoptotic spermatozoa of patients with male infertility. Fertil. Steril. 2009, 92:572-577.