Identification and function of exchange proteins activated directly by cyclic AMP (Epac) in mammalian spermatozoa

PLoS ONE

Volumn 7, Issue 5, 2012, Pages

  Miro Moran, Alvaro ^a   Jardin, Isaac ^a   Ortega Ferrusola, Cristina ^a   Salido, Gines M ^a   Peña, Fernando J ^a   Tapia, Jose A ^a   Aparicio, Ines M ^a  

^a UNIVERSITY OF EXTREMADURA   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

8 BROMO 2' O METHYLADENOSINE 3',5' CYCLIC AMP; ADENOSINE DERIVATIVE; ANTIPORTER; CALCIUM; CYCLIC NUCLEOTIDE; EXCHANGE PROTEIN ACTIVATED DIRECTLY BY CYCLIC AMP 1; EXCHANGE PROTEIN ACTIVATED DIRECTLY BY CYCLIC AMP 2; MEMBRANE PHOSPHOLIPID; RAP1 PROTEIN; UNCLASSIFIED DRUG; UVOMORULIN;

ACROSOME REACTION; ADULT; ANIMAL CELL; ARTICLE; CALCIUM MOBILIZATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME ACTIVATION; FERTILIZATION; GAMETE; HUMAN; MALE; MALE FERTILITY; NONHUMAN; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SPERMATOZOON; SPERMATOZOON CAPACITATION; SPERMATOZOON MOTILITY; STALLION; SWINE;

ACROSOME; ADULT; ANIMALS; CADHERINS; CALCIUM; CELL MEMBRANE; CYCLIC AMP; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HUMANS; INTRACELLULAR SPACE; MALE; PHOSPHOLIPIDS; PROTEIN TRANSPORT; RAP1 GTP-BINDING PROTEINS; SPERM CAPACITATION; SPERM MOTILITY; SPERMATOZOA; SUS SCROFA; YOUNG ADULT;

MAMMALIA;

EID: 84861470142     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0037713     Document Type: Article

References (47)

1. Gadella BM, Tsai PS, Boerke A, Brewis IA, (2008) Sperm head membrane reorganisation during capacitation. Int J Dev Biol 52: 473-480.
2. Harrison RA, (2004) Rapid PKA-catalysed phosphorylation of boar sperm proteins induced by the capacitating agent bicarbonate. Mol Reprod Dev 67: 337-352.
3. Gadella BM, Van Gestel RA, (2004) Bicarbonate and its role in mammalian sperm function. Anim Reprod Sci 82-83: 307-319.
4. Litvin TN, Kamenetsky M, Zarifyan A, Buck J, Levin LR, (2003) Kinetic properties of "soluble" adenylyl cyclase. Synergism between calcium and bicarbonate. J Biol Chem 278: 15922-15926.
5. Wuttke MS, Buck J, Levin LR, (2001) Bicarbonate-regulated soluble adenylyl cyclase. JOP 2: 154-158.
6. Bravo MM, Aparicio IM, Garcia-Herreros M, Gil MC, Pena FJ, et al. (2005) Changes in tyrosine phosphorylation associated with true capacitation and capacitation-like state in boar spermatozoa. Mol Reprod Dev 71: 88-96.
7. Bragado MJ, Aparicio IM, Gil MC, Garcia-Marin LJ, (2010) Protein kinases A and C and phosphatidylinositol 3 kinase regulate glycogen synthase kinase-3A serine 21 phosphorylation in boar spermatozoa. J Cell Biochem 109: 65-73.
8. Breitbart H, (2002) Role and regulation of intracellular calcium in acrosomal exocytosis. J Reprod Immunol 53: 151-159.
9. Bos JL, (2006) Epac proteins: multi-purpose cAMP targets. Trends Biochem Sci 31: 680-686.
10. Gloerich M, Bos JL, (2010) Epac: defining a new mechanism for cAMP action. Annu Rev Pharmacol Toxicol 50: 355-375.
11. Breckler M, Berthouze M, Laurent AC, Crozatier B, Morel E, et al. (2011) Rap-linked cAMP signaling Epac proteins: compartmentation, functioning and disease implications. Cell Signal 23: 1257-1266.
12. Rehmann H, Das J, Knipscheer P, Wittinghofer A, Bos JL, (2006) Structure of the cyclic-AMP-responsive exchange factor Epac2 in its auto-inhibited state. Nature 439: 625-628.
13. Roscioni SS, Elzinga CR, Schmidt M, (2008) Epac: effectors and biological functions. Naunyn Schmiedebergs Arch Pharmacol 377: 345-357.
14. Shibasaki T, Takahashi H, Miki T, Sunaga Y, Matsumura K, et al. (2007) Essential role of Epac2/Rap1 signaling in regulation of insulin granule dynamics by cAMP. Proc Natl Acad Sci U S A 104: 19333-19338.
15. Dzhura I, Chepurny OG, Kelley GG, Leech CA, Roe MW, et al. (2010) Epac2-dependent mobilization of intracellular Ca2+ by glucagon-like peptide-1 receptor agonist exendin-4 is disrupted in beta-cells of phospholipase C-epsilon knockout mice. J Physiol.
16. Branham MT, Mayorga LS, Tomes CN, (2006) Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway. J Biol Chem 281: 8656-8666.
17. McPartlin LA, Visconti PE, Bedford-Guaus SJ, (2011) Guanine-Nucleotide Exchange Factors (RAPGEF3/RAPGEF4) Induce Sperm Membrane Depolarization and Acrosomal Exocytosis in Capacitated Stallion Sperm. Biol Reprod 85 (1): 179-188.
18. Amano R, Lee J, Goto N, Harayama H, (2007) Evidence for existence of cAMP-Epac signaling in the heads of mouse epididymal spermatozoa. J Reprod Dev 53: 127-133.
19. Aivatiadou E, Ripolone M, Brunetti F, Berruti G, (2009) cAMP-Epac2-mediated activation of Rap1 in developing male germ cells: RA-RhoGAP as a possible direct down-stream effector. Mol Reprod Dev 76: 407-416.
20. Branham MT, Bustos MA, De Blas GA, Rehmann H, Zarelli VE, et al. (2009) Epac activates the small G proteins Rap1 and Rab3A to achieve exocytosis. J Biol Chem 284: 24825-24839.
21. Kinukawa M, Oda S, Shirakura Y, Okabe M, Ohmuro J, et al. (2006) Roles of cAMP in regulating microtubule sliding and flagellar bending in demembranated hamster spermatozoa. FEBS Lett 580: 1515-1520.
22. Aivatiadou E, Mattei E, Ceriani M, Tilia L, Berruti G, (2007) Impaired fertility and spermiogenetic disorders with loss of cell adhesion in male mice expressing an interfering Rap1 mutant. Mol Biol Cell 18: 1530-1542.
23. Marin-Briggiler CI, Veiga MF, Matos ML, Echeverria MF, Furlong LI, et al. (2008) Expression of epithelial cadherin in the human male reproductive tract and gametes and evidence of its participation in fertilization. Mol Hum Reprod 14: 561-571.
24. Holz GG, (2004) Epac: A new cAMP-binding protein in support of glucagon-like peptide-1 receptor-mediated signal transduction in the pancreatic beta-cell. Diabetes 53: 5-13.
25. Chepurny OG, Leech CA, Kelley GG, Dzhura I, Dzhura E, et al. (2009) Enhanced Rap1 activation and insulin secretagogue properties of an acetoxymethyl ester of an Epac-selective cyclic AMP analog in rat INS-1 cells: studies with 8-pCPT-2′-O-Me-cAMP-AM. J Biol Chem 284: 10728-10736.
26. Harrison RA, Ashworth PJ, Miller NG, (1996) Bicarbonate/CO2, an effector of capacitation, induces a rapid and reversible change in the lipid architecture of boar sperm plasma membranes. Mol Reprod Dev 45: 378-391.
27. Flesch FM, Brouwers JF, Nievelstein PF, Verkleij AJ, van Golde LM, et al. (2001) Bicarbonate stimulated phospholipid scrambling induces cholesterol redistribution and enables cholesterol depletion in the sperm plasma membrane. J Cell Sci 114: 3543-3555.
28. Fazeli A, Hage WJ, Cheng FP, Voorhout WF, Marks A, et al. (1997) Acrosome-intact boar spermatozoa initiate binding to the homologous zona pellucida in vitro. Biol Reprod 56: 430-438.
29. Hong CY, Chiang BN, Ku J, Wei YH, Fong JC, (1985) Calcium antagonists stimulate sperm motility in ejaculated human semen. Br J Clin Pharmacol 19: 45-49.
30. Holz GG, Kang G, Harbeck M, Roe MW, Chepurny OG, (2006) Cell physiology of cAMP sensor Epac. J Physiol 577: 5-15.
31. Price LS, Hajdo-Milasinovic A, Zhao J, Zwartkruis FJ, Collard JG, et al. (2004) Rap1 regulates E-cadherin-mediated cell-cell adhesion. J Biol Chem 279: 35127-35132.
32. Yanagimachi R, (1994) Mammalian fertilization New York, USA Raven Press.
33. Gadella BM, Harrison RA, (2002) 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 67: 340-350.
34. Harkema W, Harrison RA, Miller NG, Topper EK, Woelders H, (1998) Enhanced binding of zona pellucida proteins to the acrosomal region of the intact boar spermatozoa in response to fertilizing conditions: a flow cytometric study. Biol Reprod 58: 421-430.
35. Zarintash RJ, Cross NL, (1996) Unesterified cholesterol content of human sperm regulates the response of the acrosome to the agonist, progesterone. Biol Reprod 55: 19-24.
36. Luconi M, Cantini G, Baldi E, Forti G, (2011) Role of a-kinase anchoring proteins (AKAPs) in reproduction. Front Biosci 16: 1315-1330.
37. Carr DW, Newell AE, (2007) The role of A-kinase anchoring proteins (AKaps) in regulating sperm function. Soc Reprod Fertil Suppl 63: 135-141.
38. Schmidt H, Kamp G, (2004) Induced hyperactivity in boar spermatozoa and its evaluation by computer-assisted sperm analysis. Reproduction 128: 171-179.
39. Fraser LR, McDermott CA, (1992) Ca(2+)-related changes in the mouse sperm capacitation state: a possible role for Ca(2+)-ATPase. J Reprod Fertil 96: 363-377.
40. Lawson C, Dorval V, Goupil S, Leclerc P, (2007) Identification and localisation of SERCA 2 isoforms in mammalian sperm. Mol Hum Reprod 13: 307-316.
41. Rufas O, Fisch B, Ziv S, Shalgi R, (2000) Expression of cadherin adhesion molecules on human gametes. Mol Hum Reprod 6: 163-169.
42. Angst BD, Marcozzi C, Magee AI, (2001) The cadherin superfamily. J Cell Sci 114: 625-626.
43. Espino J, Bejarano I, Ortiz A, Lozano GM, Garcia JF, et al. (2010) Melatonin as a potential tool against oxidative damage and apoptosis in ejaculated human spermatozoa. Fertil Steril 94: 1915-1917.
44. Gonzalez-Fernandez L, Ortega-Ferrusola C, Macias-Garcia B, Salido GM, Pena FJ, et al. (2009) Identification of protein tyrosine phosphatases and dual-specificity phosphatases in mammalian spermatozoa and their role in sperm motility and protein tyrosine phosphorylation. Biol Reprod 80: 1239-1252.
45. Laemmli UK, (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
46. Bradford MM, (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
47. Grynkiewicz G, Poenie M, Tsien RY, (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450.