Heparin- and superoxide anion-dependent capacitation of cryopreserved bovine spermatozoa: Requirement of dehydrogenases and protein kinases

References

• Yanagimachi R. Mammalian fertilization. The physiology of reproduction, E Knobil, JD Neill. Raven Press, New York 1994; 189–318
   Google Scholar
• de Lamirande E, Leclerc P, Gagnon C. Capacitation as a regulatory event that primes spermatozoa for the acrosome reaction and fertilization. Mol Hum Reprod 1997; 3: 175–194
   PubMed Web of Science ®Google Scholar
• Ford WC. Regulation of sperm function by reactive oxygen species. Hum Reprod Update 2004; 10: 387–399
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Beconi M, Beorlegui N. Effect of natural antioxidants, superoxide dismutase and hydrogen peroxide on capacitation of frozen-thawed bovine spermatozoa. Andrologia 1997; 29: 269–275
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Beorlegui N, Beconi M. Reactive oxygen species requirements in bovine sperm capacitation and acrosome reaction. Theriogenology 1999; 52: 289–301
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Beorlegui N, Beconi M. Role of superoxide anion in the cryopreserved bovine sperm capacitation. Int J Androl 2003; 26: 109–114
   PubMedGoogle Scholar
• Galantino-Homer HL, Visconti PE, Kopf GS. Regulation of protein tyrosine phosphorylation during bovine sperm capacitation by a cyclic adenosine 3′,5′-monophosphate-dependent pathway. Biol Reprod 1997; 56: 707–719
   PubMed Web of Science ®Google Scholar
• Lax Y, Rubinstein S, Breitbart H. Subcellular distribution of protein kinase C alpha and betaI in bovine spermatozoa, and their regulation by calcium and phorbol esters. Biol Reprod 1997; 56: 454–459
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Beorlegui N, Beconi M. Role of superoxide anion and hydrogen peroxide in bovine acrosome reaction. Andrology in the 21st century, B Robaire, H Chemes, C Morales. Medimond Publications, Milan 2001; 103–108
   Google Scholar
• Cohen G, Rubinstein S, Gur Y, Breitbart H. Crosstalk between protein kinase A and C regulates phospholipase D and F-actin formation during sperm capacitation. Dev Biol 2004; 267: 230–241
   PubMed Web of Science ®Google Scholar
• Rodriguez PC, O'Flaherty CM, Beconi MT, Beorlegui NB. Nitric oxide-induced capacitation of cryopreserved bull spermatozoa and assessment of participating regulatory pathways. Anim Reprod Sci 2005; 85: 231–242
   PubMed Web of Science ®Google Scholar
• O'Flaherty C, Breininger N, Beorlegui N, Beconi M. Acrosome reaction in bovine spermatozoa: Role of reactive oxygen species and lactate dehydrogenase C4. Biochim Biophys Acta 2005; 1726: 96–101
   PubMed Web of Science ®Google Scholar
• Baker M, Aitken RJ. The importance of redox regulated pathways in sperm cell biology. Mol Cell Endocrinol 2004; 126: 47–54
   Google Scholar
• Lewis B, Aitken RJ. A redox-regulated tyrosine phosphorylation cascade in rat spermatozoa. J Androl 2001; 22: 611–622
   PubMedGoogle Scholar
• O'Flaherty C, Beorlegui N, Beconi M. Lactate dehydrogenase-c4 is involved in heparin- and nadh-dependent bovine sperm capacitation. Andrologia 2002; 34: 91–97
   PubMed Web of Science ®Google Scholar
• Blanco A, Zinkham WH. Lactate dehydrogenase in human testes. Science 1963; 139: 601–602
   PubMed Web of Science ®Google Scholar
• Zinkham WH, Blanco A, Clowry J. An unusual isozyme of lactate dehydrogenase in mature testes: Localization, ontogeny and kinetic properties. Ann N Y Acad Sci 1964; 121: 571–588
   PubMed Web of Science ®Google Scholar
• Trinchero G, Pintos L, O'Flaherty C, Beconi M. Characterization of LDHX isoenzyme in bovine spermatozoa. Com Biol 1993; 11: 283–293
   Google Scholar
• Burkhart J, Ansary A, Mahling H. Localization of cytoplasmatic lactate dehydrogenase-X in spermatozoa. Arch Androl 1982; 9: 115–120
   PubMed Web of Science ®Google Scholar
• Blanco A, Burgos C, Gerez de Burgos NM, Montamat EE. Properties of testicular lactate dehydrogenase isoenzyme. Biochem J 1976; 153: 165–172
   PubMed Web of Science ®Google Scholar
• Pavlova S. Localization of lactate dehydrogenase X in the surface of bull spermatozoa. Biológia (Bratislava) 1987; 42: 253–257
   Web of Science ®Google Scholar
• Blanco A. On the functional significance of LDH-C4. Johns Hopkins Med J 1980; 146: 231–235
   PubMedGoogle Scholar
• Duan C, Goldberg E. Inhibition of lactate dehydrogenase C4 (LDH-C4) blocks capacitation of mouse sperm in vitro. Cytogenet Genome Res 2003; 103: 352–359
   PubMed Web of Science ®Google Scholar
• Brooks DE. Activity of androgenic control of enzymes associated with the tricarboxylic acid cycle, lipid oxidation and mitochondrial shuttles in the epididymis and epididymal spermatozoa of the rat. Biochem J 1978; 174: 741–752
   PubMed Web of Science ®Google Scholar
• Hammerstedt RH. Tritium release from [2–3H]d-glucose as a monitor of glucose consumption by bovine sperm. Biol Reprod 1975; 12: 545–551
   PubMed Web of Science ®Google Scholar
• Parrish JJ, Susko-Parrish J, Winer MA, First NL. Capacitation of bovine sperm by heparin. Biol Reprod 1988; 38: 1171–1180
   PubMed Web of Science ®Google Scholar
• Fraser L, Abeydeera L, Niwa K. Ca2+-regulating mechanisms that modulate bull sperm capacitation and acrosome exocytosis as determined by chlortetracycline analysis. Mol Reprod Dev 1995; 40: 233–241
   PubMed Web of Science ®Google Scholar
• Kornberb A, Horecker B. Glucose-6-phosphate dehydrogenase. Methods enzymol, S Colowick, N Kaplan. Academic Press, New York 1955; 1: 323–327
   Google Scholar
• Lohr G, Waller H. Glucose-6-phosphate dehydrogenase. Methods in enzymatic analysis, H Bergmeyer. Academic Press, New York 1974; 636–643
   Google Scholar
• Adinolfi A, Moratti R, Olezza S, Ruffo A. Control of the citric acid cycle by glyoxylate. The mechanism of inhibition of oxoglutarate dehydrogenase, isocitrate dehydrogenase and aconitate hydratase. Biochem J 1969; 114: 513–518
   PubMed Web of Science ®Google Scholar
• Parrish JJ, Susko-Parrish JL, Uguz C, First NL. Differences in the role of cyclic adenosine 3′,5′-monophosphate during capacitation of bovine sperm by heparin or oviduct fluid. Biol Reprod 1994; 51: 1099–1108
   PubMed Web of Science ®Google Scholar
• Tesarik J, Moos J, Mendoza C. Stimulation of protein tyrosine kinase phosphorylation by a progesterone receptor on the cell surface of human sperm. Endocrinology 1993; 133: 328–335
   PubMed Web of Science ®Google Scholar
• Finkel T. Oxygen radicals and signaling. Curr Opin Cell Biol 1998; 10: 248–253
   PubMed Web of Science ®Google Scholar
• Zhang H, Zheng R. Promotion of human sperm capacitation by superoxide anion. Free Radic Res 1996; 24: 261–268
   PubMed Web of Science ®Google Scholar
• Aitken RJ, Harkiss D, Knox W, Paterson M, Irvine DS. A novel signal transduction cascade in capacitating human spermatozoa characterized by a redox-regulated, cAMP-mediated induction of tyrosine phosphorylation. J Cell Sci 1998; 111: 645–656
   PubMed Web of Science ®Google Scholar
• Herrero MB, Chatterjee S, Lefièvre L, de Lamirande E, Gagnon C. Nitric oxide interacts with the cAMP pathway to modulate capacitation of human spermatozoa. Free Radic Biol Med 2000; 29: 522–536
   PubMed Web of Science ®Google Scholar
• 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 cAMP-dependent pathway. Development 1995; 121: 1139–1150
   PubMed Web of Science ®Google Scholar
• Leclerc P, de Lamirande E, Gagnon C. Cyclic adenosine 3′,5′monophosphate-dependent regulation of protein tyrosine phosphorylation in relation to human sperm capacitation and motility. Biol Reprod 1996; 55: 684–692
   PubMed Web of Science ®Google Scholar
• Chaudhry PS, Casillas ER. Calmodulin-stimulated cyclic nucleotide phosphodiesterases in plasma membranes of bovine epididymal spermatozoa. Arch Biochem Biophys 1988; 262: 439–444
   PubMed Web of Science ®Google Scholar
• Garbers DL, Lust WD, First N, Lardy HA. Effects of phosphodiesterase inhibitors and cyclic nucleotides on sperm respiration and motility. Biochemistry 1971; 10: 1825–1831
   Web of Science ®Google Scholar
• Tajik P, Niwa K. Effects of caffeine and/or heparin in a chemically defined medium with or without glucose on in vitro penetration of bovine oocytes and their subsequent development. Theriogenology 1998; 49: 771–777
   PubMed Web of Science ®Google Scholar
• Furuya S, Endo Y, Osumi K, Oba M, Suzuki S. Effects of modulators of protein kinase C on human sperm capacitation. Fertil Steril 1993; 59: 1285–1290
   PubMed Web of Science ®Google Scholar
• Pavlok A, Kubelka M, Peknicova J. The effect of various capacitation active compounds and capacitation time on the in vitro fertility and protein tyrosine phosphorylation profiles of bovine sperm. Zygote 2001; 9: 25–38
   PubMed Web of Science ®Google Scholar