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Involvement of cAMP and calmodulin in endocytic yolk uptake during Xenopus laevis oogenesis

Published online by Cambridge University Press:  04 May 2011

Melchor Emilio Luque ,
María de los Angeles Serrano ,
María Eugenia Mónaco ,
Evelina Inés Villecco  and
Sara Serafina Sánchez
Melchor Emilio Luque
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, San Miguel de Tucumán
María de los Angeles Serrano
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, San Miguel de Tucumán
María Eugenia Mónaco
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, San Miguel de Tucumán
Evelina Inés Villecco
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, San Miguel de Tucumán
Sara Serafina Sánchez*
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, Chacabuco 461, T4000ILI San Miguel de Tucumán, Argentina.
*
All correspondence to: Sara Serafina Sánchez. Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, Chacabuco 461, T4000ILI San Miguel de Tucumán, Argentina. Tel: +54 381 4107214. Fax: +54 381 4247752. e-mail: [email protected]
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Summary

The aim of the present study was to show the participation and physiological role of calmodulin (CaM) and cAMP during vitellogenin endocytic uptake in the amphibian Xenopus laevis. The results showed a differential distribution of CaM in the ovary follicles during oogenesis. The CaM intracellular localization was not affected by gap junction's downregulation and CaM inhibition did not completely abolished the endocytic activity of oocytes. We showed that cAMP was able to completely rescue the endocytic competence in follicles in which gap junctional communication had been disrupted by octanol. Moreover cAMP was capable of restoring oocyte endocytic capability in the presence of octanol and stelazine, a CaM inhibitor. We propose that, in Vtg uptake regulation, cAMP is upstream of CaM during the endocytic signalling pathway.

Keywords

CalmodulincAMPSignalling pathwaysVitellogenesisXenopus laevis
Type
Research Article
Information
Zygote , Volume 21 , Issue 1 , February 2013 , pp. 1 - 9
Copyright
Copyright © Cambridge University Press 2011

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References

Adler, E.L. & Woodruff, R.I. (2000). Varied effects of 1-octanol on gap junctional communication between ovarian epithelial cells and oocytes of Oncopeltus fasciatus, Hyalophora cecropia, and Drosophila melanogaster. Arch. Insect Biochem. Physiol. 43, 22–32.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Anderson, K.L. & Woodruff, R.I. (2001). A gap junctionally transmitted epithelial cell signal regulates endocytic yolk uptake in Oncopeltus fasciatus. Dev. Biol. 239, 68–78.CrossRefGoogle ScholarPubMed
Bedner, P., Niessen, H., Odermatt, B., Kretz, M., Willecke, K. & Harz, H. (2006). Selective permeability of different connexin channels to the second messenger cyclic AMP. J. Biol. Chem. 281, 6673–81.CrossRefGoogle Scholar
Brooks, R.A. & Woodruff, R.I. (2004). Calmodulin transmitted through gap junctions stimulates endocytic incorporation of yolk precursors in insect oocytes. Dev. Biol. 271, 339–49.CrossRefGoogle ScholarPubMed
Cerdá, J.L., Petrino, T.R. & Wallace, R.A. (1993). Functional heterologous gap junctions in Fundulus ovarian follicles maintain meiotic arrest and permit hydration during oocyte maturation. Dev. Biol. 160, 228–35.CrossRefGoogle ScholarPubMed
Chen, J., Chi, M.M., Moley, K.H. & Downs, S.M. (2009). cAMP pulsing of denuded mouse oocytes increases meiotic resumption via activation of AMP-activated protein kinase. Reproduction 138, 759–70.CrossRefGoogle ScholarPubMed
Chien, Y.H. & Dawid, I.B. (1984) Isolation and characterization of calmodulin genes from Xenopus laevis. Mol. Cell Biol. 4, 507–13.Google ScholarPubMed
Cicirelli, M.F. & Smith, L.D. (1986) Calmodulin synthesis and accumulation during oogenesis and maturation of Xenopus laevis oocytes. Dev. Biol. 113, 174–81.CrossRefGoogle ScholarPubMed
Curran, J.E. & Woodruff, R.I. (2007) Passage of 17 kDa calmodulin through gap junctions of three vertebrate species. Tissue Cell 39, 303–9.CrossRefGoogle ScholarPubMed
Dumont, J.N. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–79.CrossRefGoogle ScholarPubMed
Eppig, J.J. & Downs, S.M. (1984). Chemical signals that regulate mammalian oocyte maturation. Biol. Reprod. 30, 1–11.CrossRefGoogle ScholarPubMed
Giaume, C., Tabernero, A. & Medina, J.M. (1997). Metabolic trafficking through astrocytic gap junctions. Glia 21,114–23.3.0.CO;2-V>CrossRefGoogle ScholarPubMed
Kam, Y., Kim, D.Y., Koo, S.K. & Joe, C.O. (1998). Transfer of second messengers through gap junction connexin 43 channels reconstituted in liposomes. Biochim. Biophys. Acta 1372 384–8.CrossRefGoogle ScholarPubMed
Lawrence, T.S., Beers, W.H. & Gilula, N.B. (1978). Transmission of hormonal stimulation by cell-to-cell communication. Nature 272, 501–06.CrossRefGoogle ScholarPubMed
Manes, M.E. & Nieto, O.L. (1983). A fast and reliable celloidin-paraffin embedding technique for yolked amphibian embryos. Mikroskopie. 40, 341–3.Google ScholarPubMed
Marilley, D., Robyr, D., Schild-Poulter, C. & Wahli, W. (1998). Regulation of the vitellogenin gene B1 promoter after transfer into hepatocytes in primary cultures. Mol. Cell Endocrinol. 141, 79–93.CrossRefGoogle ScholarPubMed
Medeiros, M.N., Mendonça, L.H., Hunter, A.L., Paiva-Silva, G.O., Mello, F.G., Henze, I.P., Masuda, H., Maya-Monteiro, C.M. & Machado, E.A. (2004). The role of lipoxygenase products on the endocytosis of yolk proteins in insects: participation of cAMP. Arch. Insect Biochem. Physiol. 55, 178–87.CrossRefGoogle ScholarPubMed
Mónaco, M.E., Villecco, E.I. & Sánchez, S.S. (2007). Implication of gap junction coupling in amphibian vitellogenin uptake. Zygote. 15, 149–57.CrossRefGoogle ScholarPubMed
Patiño, R. & Purkiss, R.T. (1993). Inhibitory effects of n-alkanols on the hormonal induction of maturation in follicle-enclosed Xenopus oocytes: implications for gap junctional transport of maturation-inducing steroid. Gen. Comp. Endocrinol. 91, 189–98.CrossRefGoogle ScholarPubMed
Polzonetti-Magni, A.M., Mosconi, G., Soverchia, L., Kikuyama, S. & Carnevali, O. (2004). Multihormonal control of vitellogenesis in lower vertebrates. Int. Rev. Cytol. 239, 1–46.CrossRefGoogle ScholarPubMed
Rossello, R.A. & Kohn, H.D. (2010). Cell communication and tissue engineering. Commun. Integr. Biol. 3, 53–6.CrossRefGoogle ScholarPubMed
Saez, J.C., Connor, J.A., Spray, D.C. & Bennett, M.V. (1989). Hepatocyte gap junctions are permeable to the second messenger, inositol 1,4,5-trisphosphate, and to calcium ions. Proc. Natl. Acad. Sci. 86, 2708–12.CrossRefGoogle Scholar
Tsafriri, A., Chun, S.Y., Zhang, R., Hsueh, A.J. & Conti, M. (1996). Oocyte maturation involves compartmentalization and opposing changes of cAMP levels in follicular somatic and germ cells: studies using selective phosphodiesterase inhibitors. Dev. Biol. 178, 393–402.CrossRefGoogle ScholarPubMed
Tucciarone, L.M. & Lanclos, K.D. (1982). Effect of calmodulin inhibitor, stelazine, on the endocytosis of vitellogenin and transglutaminase activity in Xenopus laevis oocytes. Mol. Cell. Biochem. 45, 159–61.CrossRefGoogle ScholarPubMed
Villecco, E.I., Aybar, M.J., Genta, S.B., Sánchez, S.S. & Sánchez Riera, A.N. (2000). Effect of gap junction uncoupling in full-grown Bufo arenarum ovarian follicles: participation of cAMP in meiotic arrest. Zygote 8, 171–9.CrossRefGoogle ScholarPubMed
Wall, D.A. & Patel, S. (1987). The intracellular fate of vitellogenin in Xenopus oocytes is determined by its extracellular concentration during endocytosis. J. Biol. Chem. 262, 14779–89.CrossRefGoogle ScholarPubMed
Wallace, R.A., Misulovin, Z. & Etkin, L.D. (1981). Full-grown oocytes from Xenopus laevis resume growth when placed in culture. Proc. Natl. Acad. Sci. USA 78, 3078–82.CrossRefGoogle ScholarPubMed
Wallace, R.A., Misulovin, Z. & Wiley, H.S. (1980). Growth of anuran oocytes in serum-supplemented medium. Reprod. Nutr. Dev. 20 (3A), 699–708.CrossRefGoogle ScholarPubMed
Wallace, R.A. (1985). Vitellogenesis and oocyte growth in non mammalian vertebrates. Dev. Biol. 1, 127–77.Google Scholar
Wallace, R.A., Opresko, L., Wiley, H.S. & Selman, K. (1983). The oocyte as an endocytic cell. Ciba Found. Symp. 98, 228–48.Google ScholarPubMed
Wasserman, W.J. & Smith, L.D. (1981). Calmodulin triggers the resumption of meiosis in amphibian oocytes. J. Cell Biol. 89, 389–94.CrossRefGoogle ScholarPubMed
Zmora, N., Sagi, A., Zohar, Y. & Chung, J.S. (2009). Molt-inhibiting hormone stimulates vitellogenesis at advanced ovarian developmental stages in the female blue crab, Callinectes sapidus 2: novel specific binding sites in hepatopancreas and cAMP as a second messenger. Saline Systems, 5, 6.CrossRefGoogle Scholar