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Possible participation of calmodulin in the decondensation of nuclei isolated from guinea pig spermatozoa

Published online by Cambridge University Press:  26 November 2009

Armando Zepeda-Bastida ,
Natalia Chiquete-Felix ,
Juan Ocampo-López ,
Salvador Uribe-Carvajal  and
Adela Mújica
Armando Zepeda-Bastida
Affiliation:
Departamento de Biología Celular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), PC 07360, México, D. F., México.
Natalia Chiquete-Felix
Affiliation:
Departamento de Biología Celular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), PC 07360, México, D. F., México.
Juan Ocampo-López
Affiliation:
Departamento de Biología Celular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), PC 07360, México, D. F., México.
Salvador Uribe-Carvajal
Affiliation:
Instituto de Fisiología Celular, Universidad Nacional Autónoma de México, México D. F., México.
Adela Mújica*
Affiliation:
Departamento de Biología Celular, CINVESTAV-IPN. Av. Instituto Politécnico Nacional No. 2508, México, D. F., México. Departamento de Biología Celular, Centro de Investigación y de Estudios Avanzados del Instituto Politécnico Nacional (CINVESTAV-IPN), PC 07360, México, D. F., México.
*
All correspondence to: Adela Mújica. Departamento de Biología Celular, CINVESTAV-IPN. Av. Instituto Politécnico Nacional No. 2508, México, D. F., México. Tel: +5255 5747 3992. Fax: +5255 5747 3393. e-mail: adelam@cell.cinvestav.mx
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Summary

The guinea pig spermatozoid nucleus contains actin, myosin, spectrin and cytokeratin. Also, it has been reported that phalloidin and/or 2,3-butanedione monoxime retard the sperm nuclear decondensation caused by heparin, suggesting a role for F-actin and myosin in nuclear stability. The presence of an F-actin/myosin dynamic system in these nuclei led us to search for proteins usually related to this system. In guinea pig sperm nuclei we detected calmodulin, F-actin, the myosin light chain and an actin-myosin complex. To define whether calmodulin participates in nuclear-dynamics, the effect of the calmodulin antagonists W5, W7 and calmidazolium was tested on the decondensation of nuclei promoted by either heparin or by a Xenopus laevis egg extract. All antagonists inhibited both the heparin- and the X. laevis egg extract-mediated nuclear decondensation. Heparin-mediated decondensation was faster and led to loss of nuclei. The X. laevis egg extract-promoted decondensation was slower and did not result in loss of the decondensed nuclei. It is suggested that in guinea pig sperm calmodulin participates in the nuclear decondensation process.

Keywords

CalmidazoliumHeparinMyosin–actin complexW7Xenopus laevis
Type
Research Article
Information
Zygote , Volume 18 , Issue 3 , August 2010 , pp. 217 - 229
Copyright
Copyright © Cambridge University Press 2009

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References

Adelstein, R.S. (1980). Phosphorylation of muscle contractile proteins: introduction. Fed. Proc. 39, 1544–6.Google Scholar
Adelstein, R.S., Conti, M.A. & Pato, M.D. (1980). Regulation of myosin light chain kinase by reversible phosphorylation and calcium-calmodulin. Ann. NY Acad. Sci. 356, 142–9.Google Scholar
Bachs, O., Lanini, L., Serratosa, J., Coll, M.J., Bastos, R., Aligué, R., Rius, E. & Carafoli, E. (1990). Calmodulin-binding proteins in the nuclei of quiescent and proliferatively activated rat liver cells. J. Biol. Chem. 30, 18595–600.Google Scholar
Berruti, G., Anelli, G. & Camatini, M. (1985). The effects of anticalmodulin drugs on the ultrastructure of boar spermatozoa. Eur. J. Cell. Biol. 39, 147–52.Google ScholarPubMed
Bertanzon, F., Stevens, E.S., Toniolo, C. & Bonora, G.M. (1981). Interaction of the three main components of clupeine with glycosaminoglycans. Int. J. Pept. Protein. Res. 18, 312–7.Google Scholar
Bettinger, B.T., Gilbert, D.M. & Amberg, D.C. (2004). Actin up in the nucleus. Nature 5, 410–5.Google Scholar
Bezanehtak, H. & Swan, M.A. (1999). Study of demembranated, reactivated human spermatozoa with decondensed nuclei. J. Exp. Zool. 284, 789–97.Google Scholar
Blow, J.J. & Laskey, R.A. (1986). Initiation of DNA replication in nuclei and purified DNA by a cell free extract of Xenopus eggs. Cell 47, 577–87.Google Scholar
Crivici, A. & Ikura, M. (1995). Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24, 85–116.Google Scholar
Dedman, J.R., Welsh, M.J. & Means, A.R. (1978). Ca2+-dependent regulator: production and characterization of a monospecific antibody. J. Biol. Chem. 253, 7515–21.Google Scholar
Dedman, J.R. & Kaetzel, M.A. (1983). Calmodulin purification and fluorescent labeling. In Methods in Enzymology, (eds. Means, A.R. & O'Malley, B.W.), pp. 1–12. New York: Academic Press.Google Scholar
Diaz-Barriga, F., Carrizales, L., Yañez, L., Hernández, J.M., Robles, M.C.D., Palmer, E. & Saborio, J.L. (1989). Interaction of cadmium with actin microfilaments in vitro. Toxicol. In Vitro 3, 277–84.CrossRefGoogle ScholarPubMed
Eddy, E.M. (1988). The spermatozoon. In The Physiology of Reproduction, (eds. Knobil, E. & Neill, J.D.), pp. 27–68. New York: Raven Press.Google Scholar
Hernández, E.O., Trejo, R., Espinosa, A.M., González, A. & Mújica, A. (1994). Calmodulin binding proteins in the membrane vesicles released during the acrosome reaction and in the perinuclear material in isolated acrosome reacted sperm heads. Tissue Cell 26, 849–65.Google Scholar
Hernández-Montes, H., Iglesias, G. & Mújica, A. (1973). Selective solubilization of mammalian spermatozoa structures. Exp. Cell Res. 76, 437–40.CrossRefGoogle ScholarPubMed
Hincke, M.T. (1988). Conditions for improved adsorption of calmodulin to nitrocellulose: detection by 45Ca binding. Electrophoresis 9, 303–6.Google Scholar
Hutchison, C.J., Cox, R. & Ford, C.C. (1988). The control of DNA replication in a cell-free extract that recapitulates a basic cell cycle in vitro. Development 103, 553–66.Google Scholar
Jones, H.P., Lenz, R.W., Palevitz, B.A. & Cormier, M.J. (1980). Calmodulin localization in mammalian spermatozoa. Proc. Natl. Acad. Sci. USA 77, 2772–6.Google Scholar
Juárez-Mosqueda, M.L. & Mújica, M. (1999). A perinuclear theca substructure is formed during epididymal guinea pig sperm maturation and disappears in acrosome reacted cells. J. Struct. Biol. 128, 225–36.Google Scholar
Karnovsky, M.J. (1965). A formaldehyde–glutaraldehyde fixative of high osmolality for use in electron microscopy. J. Cell Biol. 27, 137A–8A.Google Scholar
Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680–5.Google Scholar
Leno, G.H. & Laskey, R.A. (1991). DNA replication in cell-free extracts from Xenopus laevis. Methods Cell Biol. 36, 561–79.CrossRefGoogle ScholarPubMed
Levinson, H., Moyer, K.E., Saggers, G.C. & Ehrlich, P.H. (2004). Calmodulin-myosin light chain kinase inhibition changes fibroblast-populated collagen lattice contraction, cell migration, focal adhesion formation and wound contraction. Wound Repair Regen. 12, 505–11.Google Scholar
Lohka, M.J. & Masaui, Y. (1983). Ectopic pro-opiolipomelanocortin: sequence of cDNA coding for β-melanocyte-stimulating hormone and β-endorphin. Science 220, 719–21.Google Scholar
Lowry, O.H., Rosebrough, N.J., Farr, A.L. & Randall, R.J. (1951). Protein measurement with the folin phenol reagent. J. Biol. Chem. 193, 265–75.Google Scholar
Luna, G.L. (1963). Manual of Histological Staining Methods of the Armed Forces. McGraw-Hill, N.Y. USA.250 pp..Google Scholar
Margossian, S.S. & Lowey, S. (1982). Preparation of myosin and its subfragments from rabbit skeletal muscle. Methods Enzymol. 85 (Pt B), 55–71.Google Scholar
Moreno-Fierros, L., Hernández, E.O., Salgado, Z.O. & Mújica, A. (1992). F-actin in guinea pig spermatozoa: its role in calmodulin translocation during acrosome reaction. Mol. Reprod. Dev. 33, 172–81.Google Scholar
Mújica, A. & Valdes-Ruiz, M.A. (1983). On the role of glucose in capacitation and acrosomal reaction of guinea pig sperm. Gamete Res. 8, 335–44.Google Scholar
Noland, T.D., Van Eldik, L.J., Garbers, D.L. & Burgers, W.H. (1985). Distribution of calmodulin-binding proteins in membranes from bovine epididymal spermatozoa. Gamete Res. 11, 297–303.Google Scholar
Ocampo, J., Mondragón, R., Roa-Espitia, A.L., Chiquete-Félix, N., Salgado, Z.O. & Mújica, A. (2005). Actin, myosin, cytokeratins and spectrin are components of the guinea pig sperm nuclear matrix. Tissue Cell 37, 293–308.Google Scholar
Olave, I.A., Reck-Peterson, S.L. & Crabtree, G.R. (2002). Nuclear actin and actin-related proteins in chromatin remodeling. Annu. Rev. Biochem. 71, 755–81.Google Scholar
Pastén-Hidalgo, K., Hernández-Rivas, R., Roa-Espitia, A.L., Sánchez-Gutiérrez, M., Martínez-Pérez, F., Monrroy, A.O., Hernández-González, E.O. & Mújica, A. (2008). Presence, processing and localization of mouse ADAM15 during sperm maturation and the role of its disintegrin domain during sperm–egg binding. Reproduction 136, 41–51.CrossRefGoogle ScholarPubMed
Pederson, T. & Aebi, U. (2003). Actin in the nucleus: what form and what for? J. Struct. Biol. 140, 3–9.Google Scholar
Pérez, H.E., Sánchez, N., Vidali, L., Hernández, J.M., Lara, M. & Sánchez, F. (1994). Actin isoforms in non-infected roots and symbiotic root nodules of Phaseolus vulgaris. Planta 193, 51–6.Google Scholar
Philimonenko, V.V., Zhao, J., Iben, S., Dingova, H., Kysela, K., Kahle, M., Zentgraf, H., Hofmann, W.A., Lanerolle, P., Hozak, P. & Grummt, I. (2004). Nuclear actin and myosin I are required for RNA polymerase I transcription. Nat. Cell Biol. 6, 1165–70.CrossRefGoogle ScholarPubMed
Pujol, M.J., Bosser, R., Vendrell, M., Serratosa, J. & Bachs, O. (1993). Nuclear calmodulin-binding proteins in rat neurons. J. Neurochem. 60, 1422–28.Google Scholar
Putkey, S.A., Kleerekoper, Q., Gaertner, T.R. & Waxham, M.N. (2003). A new role for IQ motif proteins in regulating calmodulin function. J. Biol. Chem. 278, 49667–70.Google Scholar
Sellers, J.R. (2000). Myosins: a diverse superfamily. Biochim. Biophys. Acta. 1496, 3–22.Google Scholar
Stevens, F.C. (1982). Calmodulin: an introduction. Can. J. Biochem. Cell Biol. 61, 906–10.Google Scholar
Stull, J.T., Tansey, M.G., Tang, D., Word, R.A. & Kamm, K.E. (1993). Phosphorylation of myosin light chain kinase: a cellular mechanism for Ca2+ desensitization. Mol. Cell. Biochem. 127 /128, 229–37.Google Scholar
Tomlinson, S., Macneil, S., Walker, S.W., Ollis, C.A., Merritt, J.E. & Brown, B.L. (1984). Calmodulin and cell function. Clin. Sci. 66, 497–508.Google Scholar
Towbin, H., Staenhelin, T. & Gordon, J. (1979). Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl. Acad. Sci. USA 76, 4350–4.Google Scholar
Trejo, R. & Mújica, A. (1990). Changes in calmodulin compartmentalization throughout capacitation and acrosome reaction in guinea pig spermatozoa. Mol. Reprod. Dev. 26, 366–76.Google Scholar
Ursitti, J.A. & Wade, J.B. (1993). Ultrastructure and immunocytochemistry of the isolated human erythrocyte membrane skeleton. Cell Motil. Cytoskeleton 25, 30–42.Google Scholar
Vendrell, M., Aligué, R., Bachs, O. & Serratosa, J. (1991). Presence of calmodulin and calmodulin-binding proteins in the nuclei of brian cells. J. Neurochem. 57, 622–8.Google Scholar
Vetter, S.W. & Leclerc, E. (2003). Novel aspects of calmodulin target recognition and activation. Eur. J. Biochem. 270, 404–14.Google Scholar
Wagner, P.D. (1982). Preparation and fractionation of myosin light chain and exchange of the essential light chain. Methods Enzymol. 85 (Pt B), 72–81.Google Scholar
Ward, W.S. & Coffey, D.S. (1991). DNA packaging and organization in mammalian spermatozoa: comparison with somatic cells. Biol. Reprod. 44, 569–74.Google Scholar
Yanagimachi, R. (1988). Mammalian fertilization. In The Physiology of Reproduction (eds. E. Knobil & J.D. Neill), pp. 135–85. New York: Raven Press.Google Scholar