Calcium-calmodulin and pH regulate protein tyrosine phosphorylation in stallion sperm

Reproduction

Volumn 144, Issue 4, 2012, Pages 411-422

  Gonzalez Fernandez L ^a   Macias Garcia B ^a   Velez, I C ^a   Varner, D D ^a   Hinrichs, K ^a  

^a TEXAS A AND M UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BICARBONATE; BOVINE SERUM ALBUMIN; CALCIUM; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN INHIBITOR; CARBON DIOXIDE; N (6 AMINOHEXYL) 5 CHLORO 1 NAPHTHALENESULFONAMIDE; PROTEIN TYROSINE KINASE;

AIR; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CULTURE MEDIUM; DOSE RESPONSE; ENVIRONMENTAL ASPECTS AND RELATED PHENOMENA; ESTRUS; FEMALE; INCUBATION TIME; MALE; MARE; NONHUMAN; PH; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SPERM; SPERMATOZOON CAPACITATION; STALLION; UTERUS;

ANIMALS; CALCIUM; CALCIUM SIGNALING; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; CALMODULIN; CHELATING AGENTS; EGTAZIC ACID; ENZYME INHIBITORS; HORSES; HYDROGEN-ION CONCENTRATION; MALE; PHOSPHOPROTEINS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; SEMEN; SPERM CAPACITATION; SPERMATOZOA; SULFONAMIDES; TYROSINE;

EID: 84867187308     PISSN: 14701626     EISSN: 17417899     Source Type: Journal    
DOI: 10.1530/REP-12-0067     Document Type: Article

References (44)

1. Austin CR 1951 Observations on the penetration of the sperm in the mammalian egg. Australian Journal of Scientific Research. Ser. B: Biological Sciences 4 581-596. (doi:10.1071/BI9510581)
2. Baker MA, Hetherington L, Ecroyd H, Roman SD & Aitken RJ 2004 Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation. Journal of Cell Science 117 211-222. (doi:10.1242/jcs.00842)
3. Baumber J, Sabeur K, Vo A & Ball BA 2003 Reactive oxygen species promote tyrosine phosphorylation and capacitation in equine spermatozoa. Theriogenology 60 1239-1247. (doi:10.1016/S0093-691X(03)00144-4)
4. Boerke A, Tsai PS, Garcia-Gil N, Brewis IA & Gadella BM 2008 Capacitation-dependent reorganization of microdomains in the apical sperm head plasma membrane: functional relationship with zona binding and the zona-induced acrosome reaction. Theriogenology 70 1188-1196. (doi:10.1016/j.theriogenology. 2008.06.021)
5. Brinsko SP, Varner DD & Blanchard TL 1991 The effect of uterine lavage performed four hours post insemination on pregnancy rate in mares. Theriogenology 35 1111-1119. (doi:10.1016/0093-691X(91)90358-K)
6. Carrera A, Moos J, Ning XP, Gerton GL, Tesarik J, Kopf GS & Moss SB 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. Developmental Biology 180 284-296. (doi:10.1006/dbio.1996.0301)
7. Chan PJ & Dukelow WR 1985 Calmodulin level changes associated with cyclic AMP treatment in cultured squirrel monkey oocytes and sperm. Zoological Science 2 219-223.
8. Chang MC 1951 Fertilizing capacity of spermatozoa deposited into the fallopian tubes. Nature 168 697-698. (doi:10.1038/168697b0)
9. Choi YH, Okada Y, Hochi S, Braun J, Sato K & Oguri N 1994 In vitro fertilization rate of horse oocytes with partially removed zonae. Theriogenology 42 795-802. (doi:10.1016/0093-691X(94)90448-R)
10. Crivici A & Ikura M 1995 Molecular and structural basis of target recognition by calmodulin. Annual Review of Biophysics and Biomolecular Structure 24 85-116. (doi:10.1146/annurev.bb.24.060195.000505)
11. Demarco IA, Espinosa F, Edwards J, Sosnik J, De la Vega-Beltran JL, Hockensmith JW, Kopf GS, Darszon A & Visconti PE 2003 Involvement of a Na+/HCO-3 cotransporter in mouse sperm capacitation. Journal of Biological Chemistry 278 7001-7009. (doi:10.1074/jbc.M206284200)
12. Foster ML, Varner DD, Hinrichs K, Teague S, Lacaze K, Blanchard TL & Love CC 2011 Agreement between measures of total motility and membrane integrity in stallion sperm. Theriogenology 75 1499-1505. (doi:10.1016/j.theriogenology. 2010.12.011)
13. Galantino-Homer HL, Visconti PE & Kopf GS 1997 Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′5′-monophosphate-dependent pathway. Biology of Reproduction 56 707-719. (doi:10.1095/biolreprod56.3.707)
14. Galantino-Homer HL, Florman HM, Storey BT, Dobrinski I & Kopf GS 2004 Bovine sperm capacitation: assessment of phosphodiesterase activity and intracellular alkalinization on capacitation-associated protein tyrosine phosphorylation. Molecular Reproduction and Development 67 487-500. (doi:10.1002/mrd.20034)
15. Go KJ & Wolf DP 1985 Albumin-mediated changes in sperm sterol content during capacitation. Biology of Reproduction 32 145-153. (doi:10.1095/ biolreprod32.1.145)
16. Hess KC, Jones BH, Marquez B, Chen Y, Ord TS, Kamenetsky M, Miyamoto C, Zippin JH, Kopf GS, Suarez SS et al. 2005 The "soluble" adenylyl cyclase in sperm mediates multiple signaling events required for fertilization. Developmental Cell 9 249-259. (doi:10.1016/j.devcel.2005.06.007)
17. Kalab P, Peknicova J, Geussova G & Moos J 1998 Regulation of protein tyrosine phosphorylation in boar sperm through a cAMP-dependent pathway. Molecular Reproduction and Development 51 304-314. (doi:10.1002/(SICI)1098- 2795(199811)51:3〈304::AID-MRD10〉3.0.CO;2-2)
18. Laemmli UK 1970 Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227 680-685. (doi:10.1038/227680a0)
19. Leclerc P, Sirard MA, Chafouleas JG & Lambert RD 1992 Decrease in calmodulin concentrations during heparin-induced capacitation in bovine spermatozoa. Journal of Reproduction and Fertility 94 23-32. (doi:10.1530/jrf.0.0940023)
20. 2+, cyclic 3′,5′ adenosine monophosphate, the superoxide anion, and tyrosine phosphorylation pathways in the regulation of human sperm capacitation. Journal of Andrology 19 434-443.
21. Li LY, Meintjes M, Graff KJ, Paul JB, Denniston RS & Godke RA 1995 In vitro fertilization and development of in vitro-matured oocytes aspirated from pregnant mares. Biology of Reproduction Monograph 1 309-317.
22. Loux SC, Crawford KR, Norris JD, Ing NH, Reynolds EA, Love CC, Varner DD, Velez IC, Thornton ER, Choi YH et al. 2010 The CatSper ion channel and hyperactivated motility of horse spermatozoa. Animal Reproduction Science 121S 180. (doi:10.1016/j.anireprosci.2010.04.089)
23. Luconi M, Krausz C, Forti G & Baldi E 1996 Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa. Biology of Reproduction 55 207-216. (doi:10.1095/biolreprod55.1.207)
24. Marin-Briggiler CI, Gonzalez-Echeverria F, Buffone M, Calamera JC, Tezon JG & Vazquez-Levin MH 2003 Calcium requirements for human sperm function in vitro. Fertility and Sterility 79 1396-1403. (doi:10.1016/S0015-0282(03)00267-X)
25. Marin-Briggiler CI, Jha KN, Chertihin O, Buffone MG, Herr JC, Vazquez-Levin MH & Visconti PE 2005 Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. Journal of Cell Science 118 2013-2022. (doi:10.1242/jcs.02326)
26. McPartlin LA, Littell J, Mark E, Nelson JL, Travis AJ & Bedford-Guaus SJ 2008 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 69 639-650. (doi:10.1016/j.theriogenology.2007.11.016)
27. McPartlin LA, Suarez SS, Czaya CA, Hinrichs K & Bedford-Guaus SJ 2009 Hyperactivation of stallion sperm is required for successful in vitro fertilization of equine oocytes. Biology of Reproduction 81 199-206. (doi:10.1095/biolreprod.108.074880)
28. 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. Biology of Reproduction 85 179-188. (doi:10.1095/biolreprod.110.085555)
29. Nassar A, Mahony M, Morshedi M, Lin MH, Srisombut C & Oehninger S 1999 Modulation of sperm tail protein tyrosine phosphorylation by pentoxifylline and its correlation with hyperactivated motility. Fertility and Sterility 71 919-923. (doi:10.1016/S0015-0282(99)00013-8)
30. Naz RK & Rajesh PB 2004 Role of tyrosine phosphorylation in sperm capacitation/acrosome reaction. Reproductive Biology and Endocrinology 2 75. (doi:10.1186/1477-7827-2-75)
31. Osawa M, Swindells MB, Tanikawa J, Tanaka T, Mase T, Furuya T & Ikura M 1998 Solution structure of calmodulin-W-7 complex: the basis of diversity in molecular recognition. Journal of Molecular Biology 276 165-176. (doi:10.1006/jmbi.1997.1524)
32. Osheroff JE, Visconti PE, Valenzuela JP, Travis AJ, Alvarez J & Kopf GS 1999 Regulation of human sperm capacitation by a cholesterol efflux-stimulated signal transduction pathway leading to protein kinase A-mediated up-regulation of protein tyrosine phosphorylation. Molecular Human Reproduction 5 1017-1026. (doi:10.1093/molehr/5.11.1017)
33. Pallen CJ & Wang JH 1983 Calmodulin-stimulated dephosphorylation of p-nitrophenyl phosphate and free phosphotyrosine by calcineurin. Journal of Biological Chemistry 258 8550-8553. (Pubitemid 13026698)
34. Parrish JJ, Susko-Parrish JL & First NL 1989 Capacitation of bovine sperm by heparin: inhibitory effect of glucose and role of intracellular pH. Biology of Reproduction 41 683-699. (doi:10.1095/biolreprod41.4.683)
35. Pommer AC, Rutllant J & Meyers SA 2003 Phosphorylation of protein tyrosine residues in fresh and cryopreserved stallion spermatozoa under capacitating conditions. Biology of Reproduction 68 1208-1214. (doi:10.1095/biolreprod.102.011106)
36. Thomas AD, Meyers SA & Ball BA 2006 Capacitation-like changes in equine spermatozoa following cryopreservation. Theriogenology 65 1531-1550. (doi:10.1016/j.theriogenology.2005.08.022)
37. Uguz C, Vredenburgh WL & Parrish JJ 1994 Heparin-induced capacitation but not intracellular alkalinization of bovine sperm is inhibited by Rp-adenosine-3′,5′-cyclic monophosphorothioate. Biology of Reproduction 51 1031-1039. (doi:10.1095/biolreprod51.5.1031)
38. Visconti PE & Kopf GS 1998 Regulation of protein phosphorylation during sperm capacitation. Biology of Reproduction 59 1-6. (doi:10.1095/ biolreprod59.1.1)
39. Visconti PE, Bailey JL, Moore GD, Pan D, Olds-Clarke P & Kopf GS 1995 Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation. Development 121 1129-1137.
40. Visconti PE, Ning X, Fornes MW, Alvarez JG, Stein P, Connors SA & Kopf GS 1999 Cholesterol efflux-mediated signal transduction in mammalian sperm: cholesterol release signals an increase in protein tyrosine phosphorylation during mouse sperm capacitation. Developmental Biology 214 429-443. (doi:10.1006/dbio.1999.9428)
41. Visconti PE, Krapf D, de la Vega-Beltran JL, Acevedo JJ & Darszon A 2011 Ion channels, phosphorylation and mammalian sperm capacitation. Asian Journal of Andrology 13 395-405. (doi:10.1038/aja.2010.69)
42. Vredenburgh-Wilberg WL & Parrish JJ 1995 Intracellular pH of bovine sperm increases during capacitation. Molecular Reproduction and Development 40 490-502. (doi:10.1002/mrd.1080400413)
43. 2+-channel responses: initial events in sperm activation. Development 130 1317-1326. (doi:10.1242/dev.00353)
44. Wertheimer EV, Salicioni AM, Liu W, Trevino CL, Chavez J, Hernandez-Gonzalez EO, Darszon A & Visconti PE 2008 Chloride is essential for capacitation and for the capacitation-associated increase in tyrosine phosphorylation. Journal of Biological Chemistry 283 35539-35550. (doi:10.1074/jbc.M804586200)