Guanine-nucleotide exchange factors (RAPGEF3/RAPGEF4) induce sperm membrane depolarization and acrosomal exocytosis in capacitated stallion sperm

Biology of Reproduction

Volumn 85, Issue 1, 2011, Pages 179-188

  McPartlin, L A ^a   Visconti, P E ^b   Bedford Guaus, S J ^a  

^a Department of Obstetrics Gynecology   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

Author keywords

Acrosome reaction; EPAC; PKA; PRKACA; RAPGEF; Sperm capacitation; Stallion sperm

Indexed keywords

ACROSIN; CALCIUM ION; CALCIUM IONOPHORE; CYCLIC AMP DEPENDENT PROTEIN KINASE; GUANINE NUCLEOTIDE EXCHANGE FACTOR; ION CHANNEL; PROGESTERONE; TYROSINE; VOLTAGE GATED CALCIUM CHANNEL;

ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL MEMBRANE; CELL MEMBRANE DEPOLARIZATION; CONTROLLED STUDY; EXOCYTOSIS; HORSE; HUMAN; IMMUNOFLUORESCENCE; MALE; MEMBRANE DEPOLARIZATION; MEMBRANE POTENTIAL; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; SOMATIC CELL; SPERM; SPERMATOZOON CAPACITATION; STALLION; ZONA PELLUCIDA;

ACROSOME; ANIMALS; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASE CATALYTIC SUBUNITS; DICHLORORIBOFURANOSYLBENZIMIDAZOLE; EXOCYTOSIS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; HORSES; MALE; MEMBRANE POTENTIALS; MICE; PHOSPHORYLATION; PROTEIN-TYROSINE KINASES; SIGNAL TRANSDUCTION; SPERM CAPACITATION; THIONUCLEOTIDES;

EQUIDAE;

EID: 79960118343     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.085555     Document Type: Article

References (49)

1. Yanagimachi R. Mammalian Fertilization. In: Knobil E, Neill JD (eds.), The Physiology of Reproduction. New York, NY: Raven Press; 1994:189- 317.
2. Galantino-Homer HL, Visconti PE, Kopf GS. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3050-monophosphate-dependent pathway. Biol Reprod 1997; 56:707-719.
3. Visconti PE, Stewart-Savage J, Blasco A, Battaglia L, Miranda P, Kopf GS, Tezon JG. Roles of bicarbonate, cAMP, and protein tyrosine phosphorylation on capacitation and the spontaneous acrosome reaction of hamster sperm. Biol Reprod 1999; 61:76-84.
4. Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J, Kopf GS. Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated upregulation of protein tyrosine phosphorylation. Mol Hum Reprod 1999; 5:1017-1026.
5. Visconti PE, Galantino-Homer H, Ning X, Moore GD, Valenzuela JP, Jorgez CJ, Alvarez JG, Kopf GS. Cholesterol efflux-mediated signal transduction in mammalian sperm. Beta-cyclodextrins initiate transmembrane signaling leading to an increase in protein tyrosine phosphorylation and capacitation. J Biol Chem 1999; 274:3235-3242.
6. Visconti PE, Westbrook VA, Chertihin O, Demarco I, Sleight S, Diekman AB. Novel signaling pathways involved in sperm acquisition of fertilizing capacity. J Reprod Immunol 2002; 53:133-150.
7. Suarez SS. Control of hyperactivation in sperm. Hum Reprod Update 2008; 14:647-657.
8. Pommer AC, Rutllant J, Meyers SA. Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biol Reprod 2003; 68:1208-1214.
9. Ellington JE, Ball BA, Blue BJ, Wilker CE. Capacitation-like membrane changes and prolonged viability in vitro of equine spermatozoa cultured with uterine tube epithelial cells. Am J Vet Res 1993; 54:1505-1510.
10. Rathi R, Colenbrander B, Stout TA, Bevers MM, Gadella BM. Progesterone induces acrosome reaction in stallion spermatozoa via a protein tyrosine kinase dependent pathway. Mol Reprod Dev 2003; 64:120-128.
11. Christensen P, Whitfield CH, Parkinson TJ. In vitro induction of acrosome reactions in stallion spermatozoa by heparin and A23187. Theriogenology 1996; 45:1201-1210.
12. Meyers S, Kiu I, Overstreet J, Drobins E. Induction of acrosome reactions in stallion sperm by equine zona pellucida, porcine zona pellucida, and progesterone. Biol Reprod Mono 1995; 1:739-744.
13. Varner DD, Ward CR, Storey BT, Kenney RM. Induction and characterization of acrosome reaction in equine spermatozoa. Am J Vet Res 1987; 48:1383-1389.
14. Hinrichs K, Love CC, Brinsko SP, Choi YH, Varner DD. In vitrofertilization of in vitro-matured equine oocytes: effect of maturation medium, duration of maturation, and sperm calcium ionophore treatment, and comparison with rates of fertilization in vivo after oviductal transfer. Biol Reprod 2002; 67:256-262.
15. Zhang JJ, Muzs LZ, Boyle MS. In vitro fertilization of horse follicular oocytes matured in vitro. Mol Reprod Dev 1990; 26:361-365.
16. Dell'Aquila ME, Fusco S, Lacalandra GM, Maritato F. In vitro maturation and fertilization of equine oocytes recovered during the breeding season. Theriogenology 1996; 45:547-560.
17. Dell'Aquila ME, Cho YS, Minoia P, Traina V, Lacalandra GM, Maritato F. Effects of follicular fluid supplementation of in-vitro maturation medium on the fertilization and development of equine oocytes after invitro fertilization or intracytoplasmic sperm injection. Hum Reprod 1997; 12:2766-2772.
18. Dell'Aquila ME, Cho YS, Minoia P, Traina V, Fusco S, Lacalandra GM, Maritato F. Intracytoplasmic sperm injection (ICSI) versus conventional IVF on abattoir-derived and in vitro-matured equine oocytes. Theriogenology 1997; 47:1139-1156.
19. Choi YH, Okada Y, Hochi S, Braun J, Sato K, Oguri N. In vitro fertilization rate of horse oocytes with partially removed zonae. Theriogenology 1994; 42:795-802.
20. Alm H, Torner H, Blottner S, Nurnberg G, Kanitz W. Effect of sperm cryopreservation and treatment with calcium ionophore or heparin on in vitro fertilization of horse oocytes. Theriogenology 2001; 56:817-829.
21. McPartlin LA, Littell J, Mark E, Nelson JL, Travis AJ, Bedford-Guaus SJ. A defined medium supports changes consistent with capacitation in stallion sperm, as evidenced by increases in protein tyrosine phosphorylation and high rates of acrosomal exocytosis. Theriogenology 2008; 69:639-650.
22. Visconti PE, Kopf GS. Regulation of protein phosphorylation during sperm capacitation. Biol Reprod 1998; 59:1-6.
23. Visconti PE, Moore GD, Bailey JL, Leclerc P, Connors SA, Pan D, Olds-Clarke P, Kopf GS. Capacitation of mouse spermatozoa, II: protein tyrosine phosphorylation and capacitation are regulated by a cAMPdependent pathway. Development 1995; 121:1139-1150.
24. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS, Levin LR, Williams CJ, et al. The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Dev Cell 2005; 9:249-259.
25. Holz GG, Kang G, Harbeck M, Roe MW, Chepurny OG. Cell physiology of cAMP sensor Epac. J Physiol 2006; 577:5-15.
26. Amano R, Lee J, Goto N, Harayama H. Evidence for existence of cAMPEpac signaling in the heads of mouse epididymal spermatozoa. J Reprod Dev 2007; 53:127-133.
27. Branham MT, Mayorga LS, Tomes CN. Calcium-induced acrosomal exocytosis requires cAMP acting through a protein kinase A-independent, Epac-mediated pathway. J Biol Chem 2006; 281:8656-8666.
28. Aivatiadou E, Ripolone M, Brunetti F, Berruti G. cAMP-Epac2-mediated activation of Rap1 in developing male germ cells: RA-RhoGAP as a possible direct down-stream effector. Mol Reprod Dev 2009; 76:407-416.
29. Walsh DA, Ashby CD, Gonzalez C, Calkins D, Fischer EH, Krebs EG. Purification and characterization of a protein inhibitor of adenosine 30,50-monophosphate-dependent protein kinases. J Biol Chem 1971; 246:1977- 1985.
30. Smolenski A, Bachmann C, Reinhard K, Honig-Leidi P, Jarchau T, Hoschuetzky H, Walter U. Analysis and regulation of vasodilatorstimulated phosphoprotein serine 239 phosphorylation in vitro and in intact cells using a phosphospecific monoclonal antibody. J Biol Chem 1998; 273:20029-20035.
31. Kang G, Chepurny OG, Malester B, Rindler MJ, Rehmann H, Bos JL, Schwede F, Coetzee WA, Holz GG. cAMP sensor Epac as a determinantof ATP-sensitive potassium channel activity in human pancreatic beta cells and rat INS-1 cells. J Physiol 2006; 573:595-609.
32. Travis AJ, Jorgez CJ, Merdiushev T, Jones BH, Dess DM, Diaz-Cueto L, Storey BT, Kopf GS, Moss SB. Functional relationships between capacitation-dependent cell signaling and compartmentalized metabolic pathways in murine spermatozoa. J Biol Chem 2001; 276:7630-7636.
33. Holmquist L. Surface modification of Beckman Ultra-Clear centrifuge tubes for density gradient centrifugation of lipoproteins. J Lipid Res 1982; 23:1249-1250.
34. Laemmli UK. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970; 227:680-685.
35. Arcelay E, Saliconi, AM, Wertheimer EV, Visconti PE. Identification of proteins undergoing tyrosine phosphorylation during mouse sperm capacitation. Int J Dev Biol 2008; 52:462-472.
36. Selvaraj V, Buttke DE, Asano A, McElwee JL, Wolff CA, Nelson JL, Klaus AV, Hunnicutt GR, Travis AJ. GM1 dynamics as a marker for membrane changes associated with the process of capacitation in murine and bovine spermatozoa. J Androl 2007; 28:588-599.
37. Jungnickel MK, Marrero H, Birnbaumer L, Lemos JR, Florman HM. Trp2 regulates entry of Ca2+ into mouse sperm triggered by egg ZP3. Nat Cell Biol 2001; 3:499-502.
38. Demarco IA, Espinosa F, Edwards J, Sosnik J, De La Vega-Beltran JL, Hockensmith JW, Kopf GS, Darszon A, Visconti PE. Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation. J Biol Chem 2003; 278:7001-7009.
39. Hernandez-Gonzalez EO, Sosnik J, Edwards J, Acevedo JJ, Mendoza-Lujambio I, Lopez-Gonzalez I, Demarco I, Wertheimer E, Darszon A, Visconti PE. Sodium and epithelial sodium channels participate in the regulation of the capacitation-associated hyperpolarization in mouse sperm. J Biol Chem 2006; 281:5623-5633.
40. Seino S, Shibasaki T. PKA-dependent and PKA-independent pathways for cAMP-regulated exocytosis. Physiol Rev 2005; 85:1303-1342.
41. Hernandez-Gonzalez EO, Trevino CL, Castellano LE, de la Vega-Beltran JL, Ocampo AY, Wertheimer E, Visconti PE, Darszon A. Involvement of cystic fibrosis transmembrane conductance regulator in mouse sperm capacitation. J Biol Chem 2007; 282:24397-24406.
42. Arnoult C, Kazam IG, Visconti PE, Kopf GS, Villaz M, Florman HM. Control of the low voltage-activated calcium channel of mouse sperm by egg ZP3 and by membrane hyperpolarization during capacitation. Proc Natl Acad Sci USA 1999; 96:6757-6762.
43. Ster J, De Bock F, Guerineau NC, Janossy A, Barrere-Lemaire S, Bos JL, Bockaert J, Fagni L. Exchange protein activated by cAMP (Epac) mediates cAMP activation of p38 MAPK and modulation of Ca2+dependent K+ channels in cerebellar neurons. Proc Natl Acad Sci U S A 2007; 104:2519-2524.
44. Kang G, Leech CA, Chepurny OG, Coetzee WA, Holtz GG. Role of the cAMP sensor Epac as a determinant of KATP channel ATP sensitivity in human pancreatic beta-cells and rat INS-1 cells. J Physiol 2008; 586:1307-1319.
45. Muňoz-Garay C, De la Vega-Beltran JL, Delgado R, Labarca P, Felix R, Darszon A. Inwardly rectifying K(+) channels in spermatogenic cells: functional expression and implication in sperm capacitation. Dev Biol 2001; 234:261-274.
46. Florman HM, Jungnickel MK, Sutton KA. Regulating the acrosome reaction. Int J Dev Biol 2008; 52:503-510.
47. Helms MN, Chen XJ, Ramosevac S, Eaton DC, Jain L. Dopamine regulation of amiloride-sensitive sodium channels in lung cells. Am J Physiol Lung Cell Mol Physiol 2006; 290:L710-L722.
48. Aromataris EC, Roberts ML, Barritt GJ, Rychkov GY. Glucagon activates Ca2+ and Cl- channels in rat hepatocytes. J Physiol 2006; 573:611-625.
49. Lishko PV, Kirichok Y. The role of Hv1 and CatSper channels in sperm activation. J Physiol 2010; 588:4667-4672.