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Implication of gap junction coupling in amphibian vitellogenin uptake

Published online by Cambridge University Press:  01 May 2007

M.E. Mónaco
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO) y Universidad Nacional de Tucumán (UNT), Tucumán, Argentina
E.I. Villecco
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO) y Universidad Nacional de Tucumán (UNT), Tucumán, Argentina
S.S. Sánchez*
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO) y Universidad Nacional de Tucumán (UNT), Tucumán, Argentina
*
All correspondence to: Sara S. Sánchez, Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO) y Universidad Nacional de Tucumán (UNT), Chacabuco 461 – San Miguel de Tucumán, T4000ILI. Tucumán, Argentina. Tel: +54 381 4107214. Fax: +54 381 4247752 ext 7004. e-mail: [email protected]

Summary

The aim of the present study was to investigate the physiological role and the expression pattern of heterologous gap junctions during Xenopus laevis vitellogenesis. Dye transfer experiments showed that there are functional gap junctions at the oocyte/follicle cell interface during the vitellogenic process and that octanol uncouples this intercellular communication. The incubation of vitellogenic oocytes in the presence of biotinylated bovine serum albumin (b-BSA) or fluorescein dextran (FDX), showed that oocytes develop stratum of newly formed yolk platelets. In octanol-treated follicles no sign of nascent yolk sphere formation was observed. Thus, experiments in which gap junctions were downregulated with octanol showed that coupled gap junctions are required for endocytic activity. RT-PCR analysis showed that the expression of connexin 43 (Cx43) was first evident at stage II of oogenesis and increased during the subsequent vitellogenic stages (III, IV and V), which would indicate that this Cx is related to the process that regulates yolk uptake. No expression changes were detected for Cx31 and Cx38 during vitellogenesis. Based on our results, we propose that direct gap junctional communication is a requirement for endocytic activity, as without the appropriate signal from surrounding epithelial cells X. laevis oocytes were unable to endocytose VTG.

Type
Research Articles
Copyright
Copyright © Cambridge University Press 2007

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References

Adler, E. & Woodruff, R. (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, 2232.3.0.CO;2-U>CrossRefGoogle ScholarPubMed
Ancel, P. & Vintemberger, P. (1948). Recherches sur le déterminisme des la symetrie bilaterale dans l'oeuf des amphibiens. Bull. Biol. Fr. Belg. Suppl. 31, 1181.Google Scholar
Anderson, K. & Woodruff, R. (2001). A gap junctionally transmitted epithelial cell signal regulates endocytic yolk uptake in Oncopeltus fasciatus. Dev. Biol. 239, 6878.CrossRefGoogle ScholarPubMed
Bolamba, D., Patiño, R., Yoshizaki, G. & Thomas, P. (2003). Changes in homologous and heterologous gap junction contacts during maturation-inducing hormone-dependent meiotic resumption in ovarian follicles of Atlantic croaker. Gen. Comp. Endocrinol. 131, 291–5.CrossRefGoogle ScholarPubMed
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
Browne, C.L. & Werner, W. (1984). Intercellular junctions between the follicle cells and oocytes of Xenopus laevis. J. Exp. Zool. 230, 105–13.CrossRefGoogle ScholarPubMed
Buccione, R., Schroeder, A.C. & Eppig, J.J. (1990). Interactions between somatic cells and germ cells throughout mammalian oogenesis. Biol. Reprod. 43, 543–7.CrossRefGoogle ScholarPubMed
Carabatsos, M.J., Sellitto, C., Goodenough, D.A. & Albertini, D.F. (2000). Oocyte–granulosa cell heterologous gap junctions are required for the coordination of nuclear and cytoplasmic meiotic competence. Dev. Biol. 226, 167–79.CrossRefGoogle ScholarPubMed
Cerda, 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
Chomczynski, P. & Sacchi, N. (1987). Single-step method of RNA isolation by acid guanidinium thiocyanate–phenol–chloroform extraction. Anal. Biochem. 162, 69.CrossRefGoogle ScholarPubMed
Chu, B. & Treistman, S.N. (1997). Modulation of two cloned potassium channels by 1-alkanols demonstrates different cutoffs. Alcohol Clin. Exp. Res. 21, 1103–7.Google ScholarPubMed
De Boer, T.P., Kok, B., Neuteboom, K.I., Spieker, N., De Graaf, J., Destree, O.H., Rook, M.B., Van Veen, T.A., Jongsma, H.J., Vos, M.A., De Bakker, J.M. & Van Der Heyden, M.A. (2005). Cloning and functional characterization of a novel connexin expressed in somites of Xenopus laevis. Dev. Dyn. 233, 864–71.CrossRefGoogle ScholarPubMed
De Boer, T.P., Van der Heyden, M.A. (2005). Xenopus connexins: how frogs bridge the gap. Differentiation 73, 330–40.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
Ebihara, L., Beyer, E.C., Swenson, K.I., Paul, D.L. & Goodenough, D.A. (1989). Cloning and expression of a Xenopus embryonic gap junction protein. Science 243, 1194–5.CrossRefGoogle ScholarPubMed
Fernández, S.N. & Ramos, I. (2003). Endocrinology of re-production. In: Reproductive Biology and Phylogeny of Anura, (ed. Jamieson, B.G.M.), pp. 73118. University of Queensland: Australia.Google Scholar
Fortune, J.E. (1983). Steroid production by Xenopus ovarian follicles at different developmental stages. Dev. Biol. 99, 502–9.CrossRefGoogle ScholarPubMed
Gimlich, R.L., Kumar, N.M., Gilula, N.B. (1988). Sequence and developmental expression of mRNA coding for a gap junction protein in Xenopus. J. Cell Biol. 107, 1065–73.CrossRefGoogle ScholarPubMed
Gimlich, R.L., Kumar, N.M., Gilula, N.B. (1990). Differential regulation of the levels of three gap junction mRNAs in Xenopus embryos. J. Cell Biol. 110, 597605.CrossRefGoogle ScholarPubMed
Goodenough, D.A., Goliger, J.A. & Paul, D.L. (1996). Connexins, connexons, and intercellular communication. Annu. Rev. Biochem. 65, 475502.CrossRefGoogle ScholarPubMed
Ho, S. (1987). Endocrinology of vitellogenesis. In Hormones and Reproduction in Fishes, Amphibians, and Reptiles (eds D. Norris & R. Jones), pp. 145–69. Plenum: New York.CrossRefGoogle Scholar
Kidder, G.M. & Mhawi, A.A. (2002). Gap junctions and ovarian folliculogenesis. Reproduction 123, 613–20.CrossRefGoogle ScholarPubMed
Kumar, N.M. & Gilula, N.B. (1996). The gap junction communication channel. Cell 84, 381–8.CrossRefGoogle ScholarPubMed
Landesman, Y., Postma, F.R., Goodenough, D.A. & Paul, D.L. (2003). Multiple connexins contribute to intercellular communication in the Xenopus embryo. J. Cell Sci. 116, 2938.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
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
Pierantoni, R., Cobellis, G., Meccariello, R. & Fasano, S. (2002). Evolutionary aspects of cellular communication in the vertebrate hypothalamo–hypophysio–gonadal axis. Int. Rev. Cytol. 218, 69141.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, 146.CrossRefGoogle ScholarPubMed
Racowsky, C. & Satterlie, R.A. (1985). Metabolic, fluorescent dye and electrical coupling between hamster oocytes and cumulus cells during meiotic maturation in vivo and in vitro. Dev. Biol. 108, 191202.CrossRefGoogle ScholarPubMed
Redshaw, M.R. (1972). The hormonal control of the amphibian ovary. American Zoologist 12, 289306.CrossRefGoogle Scholar
Sánchez, S. & Villecco, E.I. (2003). Oogenesis. In Reproductive Biology and Phylogeny of Anura (ed. B.G.M. Jamieson), pp. 2772. University of Queensland: Australia.Google Scholar
Segretain, D. & Falk, M.M. (2004). Regulation of connexin biosynthesis, assembly, gap junction formation, and removal. Biochim. Biophys. Acta 1662, 321.CrossRefGoogle ScholarPubMed
Sohl, G. & Willecke, K. (2003). An update on connexin genes and their nomenclature in mouse and man. Cell. Commun. Adhes. 10, 173–80.CrossRefGoogle ScholarPubMed
Sretarugsa, P. & Wallace, R.A. (1997). The developing Xenopus oocyte specifies the type of gonadotropin-stimulated steroidogenesis performed by its associated follicle cells. Dev. Growth Differ. 39, 8797.CrossRefGoogle ScholarPubMed
Teunissen, B.E. & Bierhuizen, M.F. (2004). Transcriptional control of myocardial connexins. Cardiovasc. Res. 62, 246–55.CrossRefGoogle ScholarPubMed
Van Der Heyden, M.A., Roeleveld, L., Reneman, S., Peterson, J. & Destree, O.H. (2001). Regulated expression of the X. tropicalis connexin43 promoter. Cell. Commun. Adhes. 8, 293–8.CrossRefGoogle ScholarPubMed
Varriale, B., Pierantoni, R., Di Matteo, L., Minucci, S., Milone, M. & Chieffi, G. (1988). Relationship between estradiol-17 beta seasonal profile and annual vitellogenin content of liver, fat body, plasma, and ovary in the frog (Rana esculenta). Gen. Comp. Endocrinol. 69, 328–34.CrossRefGoogle ScholarPubMed
Villecco, E.I., Aybar, M.J., Genta, S.B., Sanchez, S.S. & Sanchez 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
Villecco, E.I., Aybar, M.J., Sanchez, S.S. and Sanchez Riera, A.N. (1996). Heterologous gap junctions between oocyte and follicle cells in Bufo arenarum: hormonal effects on their permeability and potential role in meiotic arrest. J. Exp. Zool. 276, 7685.3.0.CO;2-2>CrossRefGoogle Scholar
Waksmonski, S.L. & Woodruff, R.I. (2002). For uptake of yolk precursors, epithelial cell–oocyte gap junctional communication is required by insects representing six different orders. J. Insect Physiol. 48, 667–75.CrossRefGoogle ScholarPubMed
Wallace, R., 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. & Bergink, E.W. (1974). Amphibian vitellogenin: properties, hormonal regulation of hepatic synthesis and ovarian uptake, and conversion to yolk proteins. American Zoology 14, 1159–75.CrossRefGoogle Scholar
Wallace, R. & Dumont, J.N. (1968). The induced synthesis and transport of yolk proteins and their accumulation by the oocyte in Xenopus laevis. J. Cell Physiol. 72, 7389.CrossRefGoogle ScholarPubMed
Wallace, R., Misulovin, Z. & Wiley, H.S. (1980). Growth of anuran oocytes in serum-supplemented medium. Reprod. Nutr. Dev. 20, 699708.CrossRefGoogle ScholarPubMed
Wallace, R. (1985). Vitellogenesis and oocyte growth in nonmammalian vertebrates. Dev. Biol. 1, 127–77.Google ScholarPubMed
Wei, C.J., Xu, X., Lo, C.W. (2004). Connexins and cell signaling in development and disease. Annu. Rev. Cell. Dev. Biol. 20, 811–38.CrossRefGoogle ScholarPubMed
Willecke, K., Eiberger, J., Degen, J., Eckardt, D., Romualdi, A., Guldenagel, M., Deutsch, U. & Sohl, G. (2002). Structural and functional diversity of connexin genes in the mouse and human genome. Biol. Chem. 383, 725–37.CrossRefGoogle ScholarPubMed
Woodruff, R.I. & Tilney, L.G. (1998). Intercellular bridges between epithelial cells in the Drosophila ovarian follicle: a possible aid to localized signaling. Dev. Biol. 200, 8291.CrossRefGoogle ScholarPubMed
Yoshizaki, G., Patiño, R. & Thomas, P. (1994). Connexin messenger ribonucleic acids in the ovary of Atlantic croaker: molecular cloning and characterization, hormonal control, and correlation with appearance of oocyte maturational competence. Biol. Reprod. 51, 493503.CrossRefGoogle ScholarPubMed
Yoshizaki, G. & Patiño, R. (1995). Molecular cloning, tissue distribution, and hormonal control in the ovary of Cx41 mRNA, a novel Xenopus connexin gene transcript. Mol. Reprod. Dev. 42, 718.CrossRefGoogle ScholarPubMed