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Xepac protein and IP3/Ca2+ pathway implication during Xenopus laevis vitellogenesis

Published online by Cambridge University Press:  26 July 2013

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, Argentina.
Melchor Emilio Luque
Affiliation:
Instituto Superior de Investigaciones Biológicas (CONICET), Universidad Nacional de Tucumán, Departamento de Biología del Desarrollo, San Miguel de Tucumán, Argentina.
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]

Summary

The objective of this study was to elucidate the signalling pathways initiated by cAMP once inside the Xenopus laevis oocyte, where it triggers and maintains vitellogenin endocytic uptake. Our results showed the presence of Xepac transcripts at all stages of oogenesis and we demonstrated that a cAMP analogue that exclusively activates Xepac, 8-CPT, was able to rescue the endocytic activity in oocytes with uncoupled gap junctions. Inhibition experiments for the IP3/Ca2+ signalling pathway showed either a complete inhibition or a significant reduction of the vitellogenic process. These results were confirmed with the rescue capability of the A-23187 ionophore in those oocyte batches in which the IP3/Ca2+ pathway was inhibited. Taking our findings into account, we propose that the cAMP molecule binds Xepac protein enabling it to activate the IP3/Ca2+ pathway, which is necessary to start and maintain X. laevis vitellogenin uptake.

Type
Research Article
Copyright
Copyright © Cambridge University Press 2013 

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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, 2232.Google Scholar
Agius, E., Oelgeschläger, M., Wessely, O., Kemp, C. & De Robertis, E.M. (2000). Endodermal nodal-related signals and mesoderm induction in Xenopus. Development 127, 1173–83.Google Scholar
Anderson, K.L. & Woodruff, R.I. (2001). A gap junctionally transmitted epithelial cell signal regulates endocytic yolk uptake in Oncopeltus fasciatus. Dev. Biol. 78, 6878.Google Scholar
Arbuzova, a, Martushova, K., Hangyás-Mihályné, G., Morris, a J., Ozaki, S., Prestwich, G.D. & McLaughlin, S. (2000). Fluorescently labeled neomycin as a probe of phosphatidylinositol-4,5-bisphosphate in membranes. Biochim. Biophys. Acta 1464, 3548.Google Scholar
Bakouh, N., Chérif-Zahar, B., Hulin, P., Prié, D., Friedlander, G., Edelman, A. & Planelles, G. (2012). Functional interaction between CFTR and the sodium-phosphate co-transport type 2a in Xenopus laevis oocytes. PLoS One 7, e34879.Google Scholar
Bement, W.M. & Capco, D.G. (1990). Protein kinase C acts downstream of calcium at entry into the first mitotic interphase of Xenopus laevis. Cell Regul. 1, 315–26.Google Scholar
Bleasdale, J.E. & Fisher, S.K. (1993). Use of U-73122 as an inhibitor of phospholipase C-dependent processes. Neuroprotocols 3, 125–33.Google Scholar
de Boer, T.P. & van der Heyden, M. a G. (2005). Xenopus connexins: how frogs bridge the gap. Differentiation 73, 330–40.Google Scholar
Borland, G., Smith, B.O. & Yarwood, S.J. (2009). EPAC proteins transduce diverse cellular actions of cAMP. Brit. J. Pharmacol. 158, 7086.CrossRefGoogle ScholarPubMed
Breckler, M., Berthouze, M., Laurent, A.-C., Crozatier, B., Morel, E. & Lezoualc'h, F. (2011). Rap-linked cAMP signaling Epac proteins: compartmentation, functioning and disease implications. Cell. Signal. 23, 1257–66.Google Scholar
Brooks, R.A. & Woodruff, R.I. (2004). Calmodulin transmitted through gap junctions stimulates endocytic incorporation of yolk precursors in insect oocytes. Microscopy 271, 339–49.Google ScholarPubMed
Brown, P.T., Herbert, P. & Woodruff, R.I. (2010). Vitellogenesis in Oncopeltus fasciatus: PLC/IP3, DAG/PK-C pathway triggered by CaM. J. Insect Physiol. 56, 1300–5.Google Scholar
Bunney, T.D., Baxendale, R.W. & Katan, M. (2009). Regulatory links between PLC enzymes and Ras superfamily GTPases: signalling via PLCepsilon. Adv. Enzyme Regul. 49, 54–8.Google Scholar
Dascal, N. (1987). The use of Xenopus oocytes for the study of ion channel. Crit. Rev. Biochem. Mol. Biol. 22, 317–87.Google Scholar
Dascal, N. & Boton, R. (1990). Interaction between injected Ca2+ and intracellular Ca2+ stores in Xenopus oocytes. FEBS Letts 267, 22–4.Google Scholar
Decrock, E., Vinken, M., Bol, M., D'Herde, K., Rogiers, V., Vandenabeele, P., Krysko, D.V., Bultynck, G. & Leybaert, L. (2011). Calcium and connexin-based intercellular communication, a deadly catch? Cell Calcium 50, 310–21.Google Scholar
Dumont, J.N. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–79.Google Scholar
Edwards, S.J., Reader, K.L., Lun, S., Western, A., Lawrence, S., Mcnatty, K.P. & Juengel, J.L. (2008). The cooperative effect of growth and differentiation factor 9 and bone morphogenetic protein (BMP) 15 on granulosa cell function is modulated primarily through BMP receptor II. Endocrinology 149, 1026–30.Google Scholar
Gillo, B., Lass, Y., Nadler, E. & Oron, Y. (1987). Involvement of inositol 1,4,5-trisphosphate and calcium in the two-component response to acetylcholine in Xenopus oocytes. J. Physiol. 392, 349–61.Google Scholar
Gloerich, M. & Bos, J.L. (2010). Epac: defining a new mechanism for cAMP action. Ann. Rev. Pharmacol. Toxicol. 50, 355–75.CrossRefGoogle ScholarPubMed
Grandoch, M., Roscioni, S.S. & Schmidt, M. (2010). The role of Epac proteins, novel cAMP mediators, in the regulation of immune, lung and neuronal function. Brit. J. Pharmacol. 159, 265–84.Google Scholar
Hollywood, M., Sergeant, G., Thornbury, K. & MacHale, N. (2010). The PI-PLC inhibitor U-73122 is a potent inhibitor of the SERCA pump in smooth muscle. Brit. J. Pharmacol. 160, 1293–4.Google Scholar
Kawasaki, H. (1998). A family of cAMP-binding proteins that directly activate Rap1. Science 282, 2275–9.Google Scholar
Kidder, G.M. & Vanderhyden, B.C. (2010). Bidirectional communication between oocytes and follicle cells: ensuring oocyte developmental competence. Can. J. Physiol. Pharmacol. 88, 399413.CrossRefGoogle ScholarPubMed
Kwik, J., Boyle, S., Fooksman, D., Margolis, L., Sheetz, M.P. & Edidin, M. (2003). Membrane cholesterol, lateral mobility, and the phosphatidylinositol 4,5-bisphosphate-dependent organization of cell actin. Proc. Natl. Acad. Sci. USA 100, 13964–9.Google Scholar
Lambert, C.C. (2011). Signaling pathways in ascidian oocyte maturation: the roles of cAMP/Epac, intracellular calcium levels, and calmodulin kinase in regulating GVBD. Mol. Reprod. Dev. 78, 726–33.Google Scholar
Lee, S.J. & Han, J.-K. (2005). XEpac, a guanine nucleotide-exchange factor for Rap GTPase, is a novel hatching gland specific marker during the Xenopus embryogenesis. Dev. Dyn. 232, 1091–7.Google Scholar
Lienesch, L.A., Dumont, J.N. & Bantle, J.A. (2000). The effect of cadmium on oogenesis in Xenopus laevis. Environ. Health 41, 1651–8.Google Scholar
Luciano, A.M., Franciosi, F., Modina, S.C. & Lodde, V. (2011). Gap junction-mediated communications regulate chromatin remodeling during bovine oocyte growth and differentiation through cAMP-dependent mechanism(s). Biol. Reprod. 85, 1252–9.Google Scholar
Luque, M.E., Serrano, M.A., Mónaco, M.E., Villecco, E.I. & Sánchez, S.S. (2013). Involvement of cAMP and calmodulin in endocytic yolk uptake during Xenopus laevis oogenesis. Zygote 21, 19.CrossRefGoogle ScholarPubMed
Manes, M.E. & Nieto, O.L. (1983). A fast and reliable celloidin-paraffin embedding technique for yolked amphibian embryos. Mikroskopie 40 (11–12), 341–3.Google Scholar
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, 7993.Google Scholar
Mark, D.-O.D. & Fosket, J.K. (1994). Single-channel inositol 1,4,5-trisphosphate receptor currents revealed by patch clamp of isolated Xenopus oocyte nuclei. J. Biol. Chem. 269, 29375–8.Google Scholar
McGinnis, L.K., Carroll, D.J. & Kinsey, W.H. (2011). Protein tyrosine kinase signaling during oocyte maturation and fertilization. Mol. Reprod. Dev. 78, 831–45.Google Scholar
Mogami, H., Lloyd-Mills, C. & Gallacher, D.V. (1997). Phospholipase C inhibitor, U73122, releases intracellular Ca2+, potentiates Ins(1,4,5)P3-mediated Ca2+ release and directly activates ion channels in mouse pancreatic acinar cells. Biochem. J. 651, 645–51.Google Scholar
Mónaco, M.E., Villecco, E.I. & Sánchez, S.S. (2007). Implication of gap junction coupling in amphibian vitellogenin uptake. Zygote 15, 149–57.Google Scholar
Parekh, A.B., Foguet, M., Lubbert, H. & Stuhmer, W. (1993). Calcium oscillations and calcium influx in Xenopus oocytes expressing a novel 5-hydroxytryptamine receptor. J. Physiol. 469, 653–71.Google Scholar
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.Google Scholar
Pearson, R. a, Dale, N., Llaudet, E. & Mobbs, P. (2005). ATP released via gap junction hemichannels from the pigment epithelium regulates neural retinal progenitor proliferation. Neuron 46, 731–44.Google Scholar
Rasar, M.A. & Hammes, S.R. (2006). The physiology of the Xenopus laevis ovary. Methods Mol. Biol. 322, 1730.Google Scholar
de Rooij, J., Zwartkruis, F.J., Verheijen, M.H., Cool, R.H., Nijman, S.M., Wittinghofer, A. & Bos, J.L. (1998). Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 396, 474–7.Google Scholar
Shanker, A.K. (2008). Mode of action and toxicity of trace elements. In Trace Elements: Nutritional Benefits, Environmental Contamination, and Health Implications. (ed. Prasad, M.N.V.), John Wiley & Sons, Inc., pp. 525–56.Google Scholar
Stanton, J.L. & Green, D.P.L. (2001). A set of 840 mouse oocyte genes with well-matched human homologues. Mol. Hum. Reprod. 7, 521–43.Google Scholar
Von Stetina, J.R. & Orr-Weaver, T.L. (2011). Developmental control of oocyte maturation and egg activation in metazoan models. Cold Spring Harb. Perspect. Biol. 3, a005553.Google Scholar
Vallée, M., Aiba, K., Piao, Y., Palin, M.-F., Ko, M.S.H. & Sirard, M.-A. (2008). Comparative analysis of oocyte transcript profiles reveals a high degree of conservation among species. Reproduction 135, 439–48.Google Scholar
Van Schouwen, B., Selvaratnam, R., Fogolari, F. & Melacini, G. (2011). Role of dynamics in the autoinhibition and activation of the exchange protein directly activated by cyclic AMP (EPAC). J. Biol. Chem. 286, 42655–69.Google Scholar
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.Google Scholar
Walker, E.M., Bispham, J.R. & Hill, S.J. (1998). Nonselective effects of the putative phospholipase C inhibitor, U73122, on adenosine A1 receptor-mediated signal transduction events in Chinese hamster ovary cells. Biochem. Pharmacol. 56, 1455–62.Google Scholar
Wallace, R., Opresko, L., Wiley, H. & Selman, K. (1983). The oocyte as an endocytic cell. Ciba Found Symp. pp. 228–48.Google Scholar
Wallace, R.A. & Jared, D.W. (1976). Protein incorporation by isolated amphibian oocytes. V. Specificity for vitellogenin incorporation. J. Cell Biol. 69, 345–51.Google Scholar
Wallace, R.A., HO, T., Salter, D.W. & Jared, D.W. (1973). Protein incorporation by isolated amphibian oocytes. IV – the role of follicle cells and calcium during protein uptake. Exp. Cell Res. 82, 287–95.Google Scholar
Wallace, R.A., Misulovin, Z. & Wiley, H.S. (1980). Growth of anuran oocytes in serum-supplemented medium. Reprod. Nutr. Dev. 20, 699708.Google Scholar
Xiaodong, C., Zhenyu, J., Tamara, T. & Fang, M. (2008). Epac and PKA: a tale of two intracellular cAMP receptors. Acta Biochim. Biophys. Sin 40, 651–62.Google Scholar