Artículo

Marín-Briggiler, C.I.; Jha, K.N.; Chertihin, O.; Buffone, M.G.; Herr, J.C.; Vazquez-Levin, M.H.; Visconti, P.E. "Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation" (2005) Journal of Cell Science. 118(9):2013-2022
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Abstract:

The mechanisms involved in the regulation of mammalian sperm motility are not well understood. Calcium ions (Ca 2+ ) have been suggested to play a key role in the maintenance of motility; nevertheless, how Ca 2+ modulates this process has not yet been completely characterized. Ca 2+ can bind to calmodulin and this complex regulates the activity of multiple enzymes, including Ca 2+ /calmodulin-dependent protein kinases (CaM kinases). Results from this study confirmed that the presence of Ca 2+ , in the incubation medium is essential for maintaining human sperm motility. The involvement of CaM kinases in Ca 2+ regulation of human sperm motility was evaluated using specific inhibitors (KN62 and KN93) or their inactive analogues (KN04 and KN92 respectively). Sperm incubation in the presence of KN62 or KN93 led to a progressive decrease in the percentage of motile cells; in particular, incubation with KN62 also reduced sperm motility parameters. These inhibitors did not alter sperm viability, protein tyrosine phosphorylation or the follicular fluid-induced acrosome reaction; however, KN62 decreased the total amount of ATP in human sperm. Immunological studies showed that Ca 2+ /calmodulin-dependent protein kinase IV (CaMKIV) is present and localizes to the human sperm flagellum. Moreover, CaMKIV activity increases during capacitation and is inhibited in the presence of KN62. This report is the first to demonstrate the presence of CaMKIV in mammalian sperm and suggests the involvement of this kinase in the regulation of human sperm motility.

Registro:

Documento: Artículo
Título:Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation
Autor:Marín-Briggiler, C.I.; Jha, K.N.; Chertihin, O.; Buffone, M.G.; Herr, J.C.; Vazquez-Levin, M.H.; Visconti, P.E.
Filiación:Instituto de Biología y Medicina Experimental, CONICET, Vuelta de Obligado 2490, 1428 Buenos Aires, Argentina
Center for Research in Contraception and Reproductive Health, Department of Cell Biology, University of Virginia, 1300 Jefferson Park Avenue, Charlottesville, VA 22908, United States
Laboratorio de Estudios en Reproducción, Av. Córdoba 2007, 1120 Buenos Aires, Argentina
Department of Veterinary and Animal Sciences, University of Massachusetts, 161 Holdsworth Way, Amherst, MA 01003, United States
Palabras clave:Calcium; Calmodulin; CaM kinases; Capacitation; Human sperm; Motility; 1 [n,o bis(5 isoquinolinesulfonyl) n methyltyrosyl] 4 phenylpiperazine; adenosine triphosphate; calcium ion; enzyme inhibitor; n [2 [[n [3 (4 chlorophenyl) 2 propenyl] n methylamino]methyl]phenyl] n (2 hydroxyethyl) 4 methoxybenzenesulfonamide; protein kinase; protein kinase (calcium,calmodulin); protein kinase inhibitor; protein tyrosine phosphatase; acrosome reaction; article; cell viability; complex formation; controlled study; culture medium; enzyme activity; enzyme inhibition; human; human cell; immunology; male; mammal; ovary follicle fluid; priority journal; protein binding; protein localization; protein phosphorylation; regulatory mechanism; spermatozoon capacitation; spermatozoon motility; spermatozoon tail; Acrosome Reaction; Adenosine Triphosphate; Blotting, Western; Ca(2+)-Calmodulin Dependent Protein Kinase; Calcium; Culture Media; Dose-Response Relationship, Drug; Electrophoresis; Enzyme Inhibitors; Humans; Ions; Male; Microscopy, Fluorescence; Sperm Capacitation; Sperm Motility; Spermatozoa; Time Factors; Mammalia
Año:2005
Volumen:118
Número:9
Página de inicio:2013
Página de fin:2022
DOI: http://dx.doi.org/10.1242/jcs.02326
Título revista:Journal of Cell Science
Título revista abreviado:J. Cell Sci.
ISSN:00219533
CODEN:JNCSA
CAS:1 [n,o bis(5 isoquinolinesulfonyl) n methyltyrosyl] 4 phenylpiperazine, 127191-97-3; adenosine triphosphate, 15237-44-2, 56-65-5, 987-65-5; calcium ion, 14127-61-8; n [2 [[n [3 (4 chlorophenyl) 2 propenyl] n methylamino]methyl]phenyl] n (2 hydroxyethyl) 4 methoxybenzenesulfonamide, 139298-40-1; protein kinase (calcium,calmodulin), 97350-82-8; protein kinase, 9026-43-1; protein tyrosine phosphatase, 79747-53-8, 97162-86-2; Adenosine Triphosphate, 56-65-5; Ca(2+)-Calmodulin Dependent Protein Kinase, EC 2.7.1.123; Calcium, 7440-70-2; calmodulin-dependent protein kinase IV, EC 2.7.1.-; Culture Media; Enzyme Inhibitors; Ions
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_00219533_v118_n9_p2013_MarinBriggiler

Referencias:

  • Ahmad, K., Bracho, G.E., Wolf, D.P., Tash, J.S., Regulation of human sperm motility and hyperactivation components by calcium, calmodulin, and protein phosphatases (1995) Arch. Androl., 35, pp. 187-208
  • Aitken, R.J., Clarkson, J.S., Hulme, M.J., Henderson, C.J., Analysis of calmodulin acceptor proteins and the influence of calmodulin antagonists on human spermatozoa (1988) Gamete Res., 21, pp. 93-111
  • AOAC official method 968.08. Minerals in Animal Feed and Pet Food (2000) Official Methods of Analysis, 1, p. 40. , Association of Official Analytical Chemists 17th ed. (ed W. Horwitz) Washington DC: AOAC International
  • Baker, M.A., Hetherington, L., Ecroyd, H., Roman, S.D., Aitken, R.J., Analysis of the mechanism by which calcium negatively regulates the tyrosine phosphorylation cascade associated with sperm capacitation (2004) J. Cell Sci., 117, pp. 211-222
  • Bendahmane, M., Lynch II, C., Tulsiani, D.R., Calmodutin signals capacitation and triggers the agonist-induced acrosome reaction in mouse spermatozoa (2001) Arch. Biochem. Biophys., 390, pp. 1-8
  • Blaeser, F., Toppari, J., Heikinheimo, M., Yan, W., Wallace, M., Ho, N., Chatila, T.A., CaMKIV/Gr is dispensable for spermatogenesis and CREM-regulated transcription in male genn cells (2001) Am. J. Physiol. Endocrinol. Metab., 281, pp. E931-E937
  • Brokaw, C.J., Calcium sensors in sea urchin sperm flagella (1991) Cell Motil. Cytoskeleton, 18, pp. 123-130
  • Calvo, L., Vantman, D., Banks, S.M., Tezon, J., Koukoulis, G.N., Dennison, L., Sherins, R.J., Follicular fluid-induced acrosome reaction distinguishes a subgroup of men with unexplained infertility not identified by semen analysis (1989) Fertil. Steril., 52, pp. 1048-1054
  • Carrera, A., Moos, J., Ning, X.P., Gerton, G.L., Tesarik, J., Kopf, G.S., Moss, S.B., 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 (1996) Dev. Biol., 180, pp. 284-296
  • Eddy, E.M., O'Brien, D.A., The Spermatozoon (1994) The Physiology of Reproduction, 1, pp. 29-77. , (eds E. Knobil and J. D. Neill), New York: Raven Press
  • Ficarro, S., Chertihin, O., Westbrook, V.A., White, F., Jayes, F., Kalab, P., Marto, J.A., Hunt, D., Phosphoproteome analysis of human sperm. Evidence of tyrosine phosphorylation of AKAP 3 and valosin containing protein/P97 during capacitation (2003) J. Biol. Chem., 278, pp. 11579-11589
  • Fraser, L.R., Ionic control of sperm function (1995) Reprod. Fertil. Dev., 7, pp. 905-925
  • Gringhuis, S.I., de Leij, L.F., Wayman, G.A., Tokumitsu, H., Vellenga, E., The Ca 2+ /calmodulin-dependent kinase type IV is involved in the CD5-mediated signaling pathway in human T lymphocytes (1997) J. Biol. Chem., 272, pp. 31809-31820
  • Gross, M.K., Toscano, D.G., Toscano Jr., W.A., Calmodulin-mediated adenylate cyclase from mammalian sperm (1987) J. Biol. Chem., 262, pp. 8672-8676
  • Hidaka, H., Yokokura, H., Molecular and cellular pharmacology of a calcium/calmodulin-dependent protein kinase II (CaM kinase II) inhibitor, KN-62, and proposal of CaM kinase phosphorylation cascades (1996) Adv. Pharmacol., 36, pp. 193-219
  • Ho, H.C., Granish, K.A., Suarez, S.S., Hyperactivated motility of bull sperm is triggered at the axoneme by Ca 2+ and not cAMP (2002) Dev. Biol., 250, pp. 208-217
  • Hook, S.S., Means, A.R., Ca 2+ /CaM-dependent kinases: From activation to function (2001) Annu. Rev. Pharmacol. Toxicol., 41, pp. 471-505
  • Johnson, J., Bierle, B.M., Gallicano, G.I., Capco, D.G., Calcium/calmodulin-dependent protein kinase II and calmodulin: Regulators of the meiotic spindle in mouse eggs (1998) Dev. Biol., 204, pp. 464-477
  • Kalab, P., Visconti, P., Leclerc, P., Kopf, G.S., p95, the major phosphotyrosine-containing protein in mouse spermatozoa, is a hexokinase with unique properties (1994) J. Biol. Chem., 269, pp. 3810-3817
  • Laemmli, U.K., Cleavage of structural proteins during the assembly of the head of bacteriophage T4 (1970) Nature, 227, pp. 680-685
  • Lindemann, C.B., Goltz, J.S., Calcium regulation of flagellar curvature and swimming pattern in triton X-100-extracted rat sperm (1988) Cell Motil. Cytoskeleton, 10, pp. 420-431
  • Lindemann, C.B., Gardner, T.K., Westbrook, E., Kanous, K.S., The calcium-induced curvature reversal of rat sperm is potentiated by cAMP and inhibited by anti-calmodulin (1991) Cell Motil. Cytoskeleton, 20, pp. 316-324
  • Lopez-Gonzalez, I., de la Vega-Beltran, J.L., Santi, C.M., Florman, H.M., Felix, R., Darszon, A., Calmodulin antagonists inhibit T-type Ca 2+ currents in mouse spermatogenic cells and the zona pellucida-induced sperm acrosome reaction (2001) Dev. Biol., 236, pp. 210-219
  • Lorca, T., Crazalegui, F.H., Fesquet, D., Cavadore, J.C., Mery, J., Means, A., Doree, M., Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs (1993) Nature, 366, pp. 270-273
  • Luconi, M., Baldi, E., How do sperm swim? Molecular mechanisms underlying sperm motility (2003) Cell Mol. Biol., 49, pp. 357-369
  • Luconi, M., Krausz, C., Forti, G., Baldi, E., Extracellular calcium negatively modulates tyrosine phosphorylation and tyrosine kinase activity during capacitation of human spermatozoa (1996) Biol. Reprod., 55, pp. 207-216
  • Mandal, A., Naaby-Hansen, S., Wolkowicz, M.J., Klotz, K., Shelly, J., Retief, J.D., Coonrod, S.A., Cesar, F., FSP95, a testis-specific 95-kilodalton fibrous sheath antigen that undergoes tyrosine phosphorylation in capacitated human spermatozoa (1999) Biol. Reprod., 61, pp. 1184-1197
  • Marin-Briggiler, C.I., Vazquez-Levin, M.H., Gonzalez-Echeverria, F., Blaquier, J.A., Tezon, J.G., Miranda, P.V., Strontium supports human sperm capacitation but not follicular fluid-induced acrosome reaction (1999) Biol. Reprod., 61, pp. 673-680
  • Marin-Briggiler, C.I., Gonzalez-Echeverria, F., Buffone, M., Calamera, J.C., Tezon, J.G., Vazquez-Levin, M.H., Calcium requirements for human sperm function in vitro (2003) Fertil. Steril., 79, pp. 1396-1403
  • Marquez, B., Suarez, S.S., Different signaling pathways in bovine sperm regulate capacitation and hyperactivation (2004) Biol. Reprod., 70, pp. 1626-1633
  • Means, A.R., Cruzalegui, F., LeMagueresse, B., Needleman, D.S., Slaughter, G.R., Ono, T., A novel Ca 2+ /calmodulin-dependent protein kinase and a male germ cell-specific calmodutin-binding protein are derived from the same gene (1991) Mol. Cell. Biol., 11, pp. 3960-3971
  • Mons, N., Guillou, J.L., Jaffard, R., The role of Ca 2+ /calmodulin-stimulable adenylyl cyclases as molecular coincidence detectors in memory formation (1999) Cell Mol. Life Sci., 55, pp. 525-533
  • Mortimer, S.T., Mortimer, D., Kinematics of human spermatozoa incubated under capacitating conditions (1990) J. Androl., 11, pp. 195-203
  • Osheroff, J.E., Visconti, P.E., Valenzuela, J.P., Travis, A.J., Alvarez, J., Kopf, G.S., 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 (1999) Mol. Hum. Reprod., 5, pp. 1017-1026
  • Plattner, H., Klauke, N., Calcium in ciliated protozoa: Sources, regulation, and calcium-regulated cell functions (2001) Int. Rev. Cytol., 201, pp. 115-208
  • Reyes, A., Martinez, R., Luna, M., Chavarria, M.E., Concentrations of calmodulin in sperm in relation to their motility in fertile euspermic and infertile asthenozoospermic men (1987) Int. J. Androl., 10, pp. 507-515
  • Rusnak, F., Mertz, P., Calcineurin: Form and function (2000) Physiol. Rev., 80, pp. 1483-1521
  • Serres, C., Feneux, D., Berthon, B., Decrease of internal free calcium and human sperm movement (1991) Cell Motil. Cytoskeleton, 18, pp. 228-240
  • Si, Y., Hyperactivation of hamster sperm motility by temperature-dependent tyrosine phosphorylation of an 80-kDa protein (1999) Biol. Reprod., 61, pp. 247-252
  • Si, Y., Olds-Clarke, P., Evidence for the involvement of calmodudin in mouse sperm capacitation (2000) Biol. Reprod., 62, pp. 1231-1239
  • Smith, E.F., Regulation of flagellar dynein by calcium and a role for an axonemal calmodulin and calmodulin-dependent kinase (2002) Mol. Biol. Cell, 13, pp. 3303-3313
  • Suarez, S., Woff, D., Meizel, S., Induction of the acrosome reaction in human spermatozoa by a fraction of human follicular fluid (1986) Gamete Res., 14, pp. 107-121
  • Tash, J.S., Bracho, G.E., Regulation of sperm motility: Emerging evidence for a major role for protein phosphatases (1994) J. Androl., 15, pp. 505-509
  • Tash, J.S., Krinks, M., Patel, J., Means, R.L., Klee, C.B., Means, A.R., Identification, characterization, and functional correlation of calmodulin-dependent protein phosphatase in sperm (1988) J. Cell Biol., 106, pp. 1625-1633
  • Turner, R.M., Tales from the tail: What do we really know about sperm motility? (2003) J. Androl., 24, pp. 790-803
  • Vijayaraghavan, S., Olson, G.E., NagDas, S., Winfrey, V.P., Carr, D.W., Subcellular localization of the regulatory subunits of cyclic adenosine 3′,5′-monophosphate-dependent protein kinase in bovine spermatozoa (1997) Biol. Reprod., 57, pp. 1517-1523
  • Visconti, P.E., Kopf, G.S., Regulation of protein phosphorylation during sperm capacitation (1998) Biol. Reprod., 59, pp. 1-6
  • Visconti, P.E., Bailey, J.L., Moore, G.D., Pan, D., Olds-Clarke, P., Kopf, G.S., Capacitation of mouse spermatozoa. I. Correlation between the capacitation state and protein tyrosine phosphorylation (1995) Development, 121, pp. 1129-1137
  • Visconti, P.E., Moore, G.D., Bailey, J.L., Leclerc, P., Connors, S.A., Pan, D., Olds-Clarke, P., Kopf, G.S., Capacitation of mouse spermatozoa. II. Protein tyrosine phosphorylation and capacitation are regulated by a cAMP-dependent pathway (1995) Development, 121, pp. 1139-1150
  • Visconti, P.E., Johnson, L.R., Oyaski, M., Fornes, M., Moss, S.B., Gerton, G.L., Kopf, G.S., Regulation, localization, and anchoring of protein kinase A subunits during mouse sperm capacitation (1997) Dev. Biol., 192, pp. 351-363
  • Visconti, P.E., Westbrook, V.A., Chertihin, O., Demarco, I., Sleight, S., Diekman, A.B., Novel signaling pathways involved in sperm acquisition of fertilizing capacity (2002) J. Reprod. Immunol., 53, pp. 133-150
  • Wasco, W.M., Orr, G.A., Function of calmodulin in mammalian sperm: Presence of a calmodulin-dependent cyclic nucleotide phosphodiesterase associated with demembranated rat caudal epididymal sperm (1984) Biochem. Biophys. Res. Commun., 118, pp. 636-642
  • (1999) WHO Laboratory Manual for the Examination of Human Semen and Ssperm-cervical Mucus Interaction, , WHO Cambridge, UK: Cambridge University Press
  • Wu, J.Y., Means, A.R., Ca 2+ /calmodulin-dependent protein kinase IV is expressed in spermatids and targeted to chromatin and the nuclear matrix (2000) J. Biol. Chem., 275, pp. 7994-7999
  • Wu, J.Y., Ribar, T.J., Cummings, D.E., Burton, K.A., McKnight, G.S., Means, A.R., Spermiogenesis and exchange of basic nuclear proteins are impaired in male germ cells lacking Camk4 (2000) Nat. Genet., 25, pp. 448-452
  • Wu, J.Y., Gonzalez-Robayna, I.J., Richards, J.S., Means, A.R., Female fertility is reduced in mice lacking Ca 2+ /calmodulin-dependent protein kinase IV (2000) Endocrinology, 141, pp. 4777-4783
  • Yanagimachi, R., Mammalian fertilization (1994) The Physiology of Reproduction, 1, pp. 189-317. , (eds E. Knobil and J. D. Neill), New York: Raven Press
  • Zeng, H., Tulsiani, D.R., Calmodulin antagonists differentially affect capacitation-associated protein tyrosine phosphorylation of mouse sperm components (2003) J. Cell Sci., 116, pp. 1981-1989

Citas:

---------- APA ----------
Marín-Briggiler, C.I., Jha, K.N., Chertihin, O., Buffone, M.G., Herr, J.C., Vazquez-Levin, M.H. & Visconti, P.E. (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(9), 2013-2022.
http://dx.doi.org/10.1242/jcs.02326
---------- CHICAGO ----------
Marín-Briggiler, C.I., Jha, K.N., Chertihin, O., Buffone, M.G., Herr, J.C., Vazquez-Levin, M.H., et al. "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, no. 9 (2005) : 2013-2022.
http://dx.doi.org/10.1242/jcs.02326
---------- MLA ----------
Marín-Briggiler, C.I., Jha, K.N., Chertihin, O., Buffone, M.G., Herr, J.C., Vazquez-Levin, M.H., et al. "Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation" . Journal of Cell Science, vol. 118, no. 9, 2005, pp. 2013-2022.
http://dx.doi.org/10.1242/jcs.02326
---------- VANCOUVER ----------
Marín-Briggiler, C.I., Jha, K.N., Chertihin, O., Buffone, M.G., Herr, J.C., Vazquez-Levin, M.H., et al. Evidence of the presence of calcium/calmodulin-dependent protein kinase IV in human sperm and its involvement in motility regulation. J. Cell Sci. 2005;118(9):2013-2022.
http://dx.doi.org/10.1242/jcs.02326