Development, Vol 121, Issue 4 1139-1150, Copyright © 1995 by Company of Biologists

JOURNAL ARTICLES

Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway

PE Visconti, GD Moore, JL Bailey, P Leclerc, SA Connors, D Pan, P Olds-Clarke and GS Kopf
Department of Obstetrics and Gynecology, University of Pennsylvania School of Medicine, Philadelphia 19104-6080, USA.

In the accompanying report (Visconti, P.E., Bailey, J.L., Moore, G.D., Pan, D., Olds-Clarke, P. and Kopf, G.S. (1995) Development, 121, 1129-1137) we demonstrated that the tyrosine phosphorylation of a subset of mouse sperm proteins of M(r) 40,000-120,000 was correlated with the capacitation state of the sperm. The mechanism by which protein tyrosine phosphorylation is regulated in sperm during this process is the subject of this report. Cauda epididymal sperm, when incubated in media devoid of NaHCO3, CaCl2 or bovine serum albumin do not display the capacitation-associated increases in protein tyrosine phosphorylation of this subset of proteins. This NaHCO3, CaCl2 or bovine serum albumin requirement for protein tyrosine phosphorylation can be completely overcome by the addition of biologically active, but not inactive, cAMP analogues. Addition of the active cAMP analogues to sperm incubated in media devoid of NaHCO3, CaCl2 or bovine serum albumin overcomes the inability of these media to support capacitation, as assessed by the ability of the cells to acquire the pattern B chlortetracycline fluorescence, to undergo the zona pellucida-induced acrosome reaction and, in some cases, to fertilize metaphase II-arrested eggs in vitro. The effects of the cAMP analogues to enhance protein tyrosine phosphorylation and to promote capacitation appears to be at the level of the cAMP-dependent protein kinase (PKA), since two specific inhibitors of this enzyme (H-89 and Rp-cAMPS) block the capacitation-dependent increases in protein tyrosine phosphorylation in sperm incubated in media supporting capacitation. Capacitation, as assessed by the aforementioned endpoints, also appears to be inhibited by H-89 in a concentration-dependent manner. These results provide further evidence for the interrelationship between protein tyrosine phosphorylation and the appearance of the capacitated state in mouse sperm. They also demonstrate that both protein tyrosine phosphorylation and capacitation appear to be regulated by cAMP/PKA. Up-regulation of protein tyrosine phosphorylation by cAMP/PKA in sperm is, to our knowledge, the first demonstration of such an interrelationship between tyrosine kinase/phosphatase and PKA signaling pathways.
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				K. P. Roberts, J. A. Wamstad, K. M. Ensrud, and D. W. Hamilton Inhibition of Capacitation-Associated Tyrosine Phosphorylation Signaling in Rat Sperm by Epididymal Protein Crisp-1 Biol Reprod, August 1, 2003; 69(2): 572 - 581. [Abstract] [Full Text] [PDF]

				N. L. Cross Decrease in Order of Human Sperm Lipids During Capacitation Biol Reprod, August 1, 2003; 69(2): 529 - 534. [Abstract] [Full Text] [PDF]

				N. Cormier and J. L. Bailey A Differential Mechanism Is Involved During Heparin- and Cryopreservation-Induced Capacitation of Bovine Spermatozoa Biol Reprod, July 1, 2003; 69(1): 177 - 185. [Abstract] [Full Text] [PDF]

				H. W. Ecroyd, R. C. Jones, and R. J. Aitken Endogenous Redox Activity in Mouse Spermatozoa and Its Role in Regulating the Tyrosine Phosphorylation Events Associated with Sperm Capacitation Biol Reprod, July 1, 2003; 69(1): 347 - 354. [Abstract] [Full Text] [PDF]

				K.J. de Vries, T. Wiedmer, P.J. Sims, and B.M. Gadella Caspase-Independent Exposure of Aminophospholipids and Tyrosine Phosphorylation in Bicarbonate Responsive Human Sperm Cells Biol Reprod, June 1, 2003; 68(6): 2122 - 2134. [Abstract] [Full Text] [PDF]

				H.-T. Zeng and D. R. P. Tulsiani Calmodulin antagonists differentially affect capacitation-associated protein tyrosine phosphorylation of mouse sperm components J. Cell Sci., May 15, 2003; 116(10): 1981 - 1989. [Abstract] [Full Text] [PDF]

				A. M. Petrunkina, K. Simon, A.-R. Gunzel-Apel, and E. Topfer-Petersen Specific Order in the Appearance of Protein Tyrosine Phosphorylation Patterns Is Functionally Coordinated With Dog Sperm Hyperactivation and Capacitation J Androl, May 1, 2003; 24(3): 423 - 437. [Abstract] [Full Text] [PDF]

				G. Wennemuth, A. E. Carlson, A. J. Harper, and D. F. Babcock Bicarbonate actions on flagellar and Ca2+-channel responses: initial events in sperm activation Development, April 1, 2003; 130(7): 1317 - 1326. [Abstract] [Full Text] [PDF]

				M. R. Nimmo and N. L. Cross Structural Features of Sterols Required to Inhibit Human Sperm Capacitation Biol Reprod, April 1, 2003; 68(4): 1308 - 1317. [Abstract] [Full Text] [PDF]

				A. C. Pommer, J. Rutllant, and S. A. Meyers Phosphorylation of Protein Tyrosine Residues in Fresh and Cryopreserved Stallion Spermatozoa under Capacitating Conditions Biol Reprod, April 1, 2003; 68(4): 1208 - 1214. [Abstract] [Full Text] [PDF]

				S. Ficarro, O. Chertihin, V. A. Westbrook, F. White, F. Jayes, P. Kalab, J. A. Marto, J. Shabanowitz, J. C. Herr, D. F. Hunt, et al. Phosphoproteome Analysis of Capacitated Human Sperm. EVIDENCE OF TYROSINE PHOSPHORYLATION OF A KINASE-ANCHORING PROTEIN 3 AND VALOSIN-CONTAINING PROTEIN/p97 DURING CAPACITATION J. Biol. Chem., March 21, 2003; 278(13): 11579 - 11589. [Abstract] [Full Text] [PDF]

				I. A. Demarco, F. Espinosa, J. Edwards, J. Sosnik, J. L. de la Vega-Beltran, J. W. Hockensmith, G. S. Kopf, A. Darszon, and P. E. Visconti Involvement of a Na+/HCO-3 Cotransporter in Mouse Sperm Capacitation J. Biol. Chem., February 21, 2003; 278(9): 7001 - 7009. [Abstract] [Full Text] [PDF]

				S.A. Adeoya-Osiguwa, S. Markoulaki, V. Pocock, S.R. Milligan, and L.R. Fraser 17{beta}-Estradiol and environmental estrogens significantly affect mammalian sperm function Hum. Reprod., January 1, 2003; 18(1): 100 - 107. [Abstract] [Full Text] [PDF]

				V. Fournier, P. Leclerc, N. Cormier, and J. L. Bailey Implication of Calmodulin-Dependent Phosphodiesterase Type 1 During Bovine Sperm Capacitation J Androl, January 1, 2003; 24(1): 104 - 112. [Abstract] [Full Text] [PDF]

				B. Maier, S. Medrano, S. B. Sleight, P. E. Visconti, and H. Scrable Developmental Association of the Synaptic Activity-Regulated Protein Arc with the Mouse Acrosomal Organelle and the Sperm Tail Biol Reprod, January 1, 2003; 68(1): 67 - 76. [Abstract] [Full Text] [PDF]

				M. Furusawa, T. Taira, S. M. M. Iguchi-Ariga, and H. Ariga AMY-1 Interacts with S-AKAP84 and AKAP95 in the Cytoplasm and the Nucleus, Respectively, and Inhibits cAMP-dependent Protein Kinase Activity by Preventing Binding of Its Catalytic Subunit to A-kinase-anchoring Protein (AKAP) Complex J. Biol. Chem., December 20, 2002; 277(52): 50885 - 50892. [Abstract] [Full Text] [PDF]

				H. Yukitake, M. Furusawa, T. Taira, S. M. M. Iguchi-Ariga, and H. Ariga AAT-1, a Novel Testis-specific AMY-1-binding Protein, Forms a Quaternary Complex with AMY-1, A-kinase Anchor Protein 84, and a Regulatory Subunit of cAMP-dependent Protein Kinase and Is Phosphorylated by Its Kinase J. Biol. Chem., November 15, 2002; 277(47): 45480 - 45492. [Abstract] [Full Text] [PDF]

				L. Lefievre, K. N. Jha, E. de Lamirande, P. E. Visconti, and C. Gagnon Activation of Protein Kinase A During Human Sperm Capacitation and Acrosome Reaction J Androl, September 1, 2002; 23(5): 709 - 716. [Abstract] [Full Text] [PDF]

				D. M. Hickox, G. Gibbs, J. R. Morrison, K. Sebire, K. Edgar, H.-H. Keah, K. Alter, K. L. Loveland, M. T.W. Hearn, D. M. de Kretser, et al. Identification of a Novel Testis-Specific Member of the Phosphatidylethanolamine Binding Protein Family, pebp-2 Biol Reprod, September 1, 2002; 67(3): 917 - 927. [Abstract] [Full Text] [PDF]

				L. Lefievre, E. de Lamirande, and C. Gagnon Presence of Cyclic Nucleotide Phosphodiesterases PDE1A, Existing as a Stable Complex with Calmodulin, and PDE3A in Human Spermatozoa Biol Reprod, August 1, 2002; 67(2): 423 - 430. [Abstract] [Full Text] [PDF]

				P. Leclerc and S. Goupil Regulation of the Human Sperm Tyrosine Kinase c-yes. Activation by Cyclic Adenosine 3',5'-Monophosphate and Inhibition by Ca2+ Biol Reprod, July 1, 2002; 67(1): 301 - 307. [Abstract] [Full Text] [PDF]