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Ultrastructural changes in the follicular epithelium of Ceratophrys cranwelli previtellogenic oocytes

Published online by Cambridge University Press:  01 August 2007

E.I. Villecco ,
M.E. Mónaco  and
S.S. Sánchez
E.I. Villecco
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) y Universidad Nacional de Tucumán (UNT), Chacabuco 461, 4000, San Miguel de Tucumán, Tucumán, Argentina
M.E. Mónaco
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) y Universidad Nacional de Tucumán (UNT), Chacabuco 461, 4000, San Miguel de Tucumán, Tucumán, Argentina
S.S. Sánchez*
Affiliation:
Departamento de Biología del Desarrollo, Instituto Superior de Investigaciones Biológicas (INSIBIO), Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) y Universidad Nacional de Tucumán (UNT), Chacabuco 461, 4000, San Miguel de Tucumán, Tucumán, Argentina
*
All correspondence to: S.S. Sánchez, Departamento de Biología del Desarrollo, INSIBIO (CONICET-UNT), Chacabuco 461, 4000-San Miguel de Tucumán, Argentina. Tel: +54 81 4107214. Fax: +54 81 4247752 ext. 7004. e-mail: ssanchez@fbqf.unt.edu.ar
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Summary

In this work we carried out ultrastructural, autoradiographic and biochemical analyses of the follicular epithelium during C. cranwelli previtellogenesis. This study revealed that the follicular epithelium in early previtellogenesis is constituted of a single layer of squamous homogeneous cells. During mid-previtellogenesis two types of cells develop: dark cells and clear cells. The follicular dark cells are actively involved in the synthesis of RNA, which is transferred to the oocyte through the interface. In late previtellogenesis the dark cells show apoptotic characteristics such as chromatin condensation, DNA fragmentation and cytoplasm shrinkage. This process forms apoptotic bodies that seem to be engulfed by the oocyte. Our results show evidence that, during mid- and late C. cranwelli previtellogenesis, the follicular epithelium undergoes remodelling processes interacting with the oocyte.

Keywords

AmphibianApoptosisFollicular cellsPrevitellogenic oocyte
Type
Research Article
Information
Zygote , Volume 15 , Issue 3 , August 2007 , pp. 273 - 283
Copyright
Copyright © Cambridge University Press 2007

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References

Ancel, P & Vitemberger, P. (1948). Recherches dur le determinisme de la symétrie bilatérale dans l'oeuf des amphibians. Bull. Biol. Fr. Belg. Suppl. 31, 1–81.Google Scholar
Andreuccetti, P. (1992). An ultrastructural study of differentiation of pyriform cells and their contribution to oocyte growth in representative squamata. J. Morphol. 212 (1), 1–11.CrossRefGoogle ScholarPubMed
Andreuccetti, P., Limatola, E. & Ghiara, G. (1979). Secretory activity of pyriform cells during the oocyte growth in Lacerta sicula. J. Submicr. Cytol. 11, 369–77.Google Scholar
Bachvarova, R.M., Manova, K., Packer, A.I., Huang, E.J. & Besmer, P. (1992). Role of c-kit and its ligand in oocyte growth. In: Ovarian Cell Interactions (ed. Hsueh, A.J.W. & Schomberg, D.), pp. 25–37, Norwell, MA: Symposia.Google Scholar
Berry, S.J. (1985). RNA synthesis and storage during insect oogenesis. In: Browder, L.W. (ed.): Developmental Biology, a Comprehensive Synthesis.New York: Plenum Press, pp. 351–84.Google Scholar
Bonhag, P.F. (1958). Ovarian structure and vittelogenesis in insects. Annu. Rev. Entomol. 3, 137–60.CrossRefGoogle Scholar
Cabada, M.O., Sánchez Riera, A.N., Genta, H.D., Genta, S.B., Sánchez, S.S. & Barisone, G.A. (1996). Vitelline envelope formation during oogenesis in Bufo arenarum. Biocell 20, 77–86.Google ScholarPubMed
Callebaut, M. (1991). Pyriform-like and holding granulosa cells in the avian ovarian follicle wall. Eur. Arch. Biol. (Bruxelles) 102, 135–45.Google Scholar
Callebaut, M. and Van, Nassauw (1987). Demonstration by monoclonal antidemin of a myoid tissue coat in the preovulatory ovarian tunica albuginea of the turtle Pseudemys scripta elegans. Med. Sci. Res. 15, 1129–30.Google Scholar
Davidson, E. H. (1986). Gene Activity in Early Development, 3rd edn. Academic Press Inc. Orlando, Florida.Google Scholar
Del Pino, E.M. (1989). Marsupial frogs. Scientific American 260 (5), 110–8.CrossRefGoogle Scholar
Dumont, J.N. (1972). Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J. Morphol. 136, 153–80.CrossRefGoogle ScholarPubMed
Dumont, J.N. (1978). Oogenesis in Xenopus laevis (Daudin). VI. The route of injected tracer transport in the follicle and developing oocyte. J. Exp. Zool. 204, 193–217.CrossRefGoogle ScholarPubMed
Dumont, J.N. & Brummet, A.R. (1978). Oogenesis in Xenopus laevis (Daudin). V. Relationships between developing oocytes and their investing follicular tissues. J. Morphol. 155, 73–98.CrossRefGoogle ScholarPubMed
Filosa, S. (1973). Biological and cytological aspects of the ovarian cycle in Lacerta sicula. Mon. Zool. Ital. 7, 151–65.Google Scholar
Fortune, J.E. (1983). Steroid production by Xenopus ovarian follicles at different developmental stages. Dev. Biol. 99, 502–9.CrossRefGoogle ScholarPubMed
Frens, G. (1973). Controlled nucleation for the regulation of the particle size in monodisperse gold solutions. Nature Phys. Sci. 241, 29.CrossRefGoogle Scholar
Hernandez, A.G. & Bahr, J.M. (2003). Role of FSH and epidermal growth factor (EGF) in the initiation of steroidogenesis in granulosa cells associated with follicular selection in chicken ovaries. Reproduction 125, 683–91.CrossRefGoogle ScholarPubMed
Hope, J., Humphries, A.A. & Bourne, G.H. (1963). Ultrastructural studies on developing oocytes of the salamander Triturus viridescens. Ultrastruct. Res. 9, 302–24.CrossRefGoogle Scholar
Hughes, F.M. Jr, Gorospe, W.C. (1991). Biochemical identification of apoptosis (programmed cell death) in granulosa cells: evidence for a potential mechanism underlying follicular atresia. Endocrinology 129 (5), 2415–22.CrossRefGoogle ScholarPubMed
Kemp, N.E. (1956). Electron microscopy of Rana pipiens oocytes. J. Biophys. Biochem. Cytol. 2, 282–91.CrossRefGoogle Scholar
King, R.C. & Devine, R.L. (1958). Oogenesis in adult Drosophila melanogaster. Growth 22, 299–326.Google Scholar
Kloc, M., Dougherty, M.T., Bilinski, S., Chan, A.P., Brey, E., King, M.L., Patrick, C.W. Jr & Etkin, L.D. (2002). Three-dimensional ultrastructural analysis of RNA distribution within germinal granules of Xenopus. Dev Biol. 241 (1), 79–93.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
Monroy, A., Parisi, E. & Rosati, F. (1983). On the segregation of the germ and somatic cell lines in the embryo. Differentiation 23, 179–83.CrossRefGoogle ScholarPubMed
Motta, C.M., Filosa, S. & Andreuccetti, P. (1995). Role of pyriform cells during the growth of oocytes in the lizard Podarcis sicula. J. Exp. Zool. 273, 256–67.CrossRefGoogle Scholar
Motta, C.M., Filosa, S. & Andreuccetti, P. (1996). Regression of the epithelium in late previtellogenic follicles of Podarcis sicula: a case of apoptosis. J. Exp. Zool. 276, 233–41.3.0.CO;2-O>CrossRefGoogle Scholar
Motta, C.M., Tammaro, S., Cicale, A., Indolfi, P., Iodice, C., Spagnuolo, M.S. & Filosa, S. (2001). Storage in the yolk platelets of low mw DNA produced by the regressing follicle cells. Mol. Reprod. Dev. 59, 422–30.CrossRefGoogle Scholar
Nezis, I.P., Vassilis, M., Mpakou, V, Stravopodis, D.M., Papassideri, I.S., Mammali, I. & Margaritis, L.H. (2003). Modes of programmed cell death during Ceratitis capitata oogenesis. Tissue & Cell 35, 113–9.CrossRefGoogle ScholarPubMed
Purcell, S.M. & Keller, R. (1993). A different type of amphibian mesoderm morphogenesis in Ceratophrys ornata. Development 117 (1), 307–17.CrossRefGoogle ScholarPubMed
Redshaw, M.R. (1972). The hormonal control of the amphibian ovary. Am. Zool. 12, 289–306.CrossRefGoogle Scholar
Robinson, D.N., Kant, K. & Cooley, L. (1994). Morphogenesis of Drosophila ovarian ring canals. Development 120, 2015–25.CrossRefGoogle ScholarPubMed
Sánchez, S.S. & Villecco, E.I. (2003). Reproductive biology and phylogeny of anura. Chapter 3, pp. 27–71. Oogenesis (ed.) B.J.M. Jamieson Publishers, Science Publishers, Inc., Enfield, New Hampshire, USA.Google Scholar
Sánchez Riera, A.N., Sánchez, S.S. and Cabada, M.O. (1988). RNA metabolism in the follicle cells of Bufo arenarum oocytes. Micr. Electr. Biol. Cell. 12, 149–76.Google ScholarPubMed
Schoenfelder, M, Schams, D, Einspanier, R. (2003). Steroidogenesis during in vitro maturation of bovine cumulus oocyte complexes and possible effects of tri-butyltin on granulosa cells. J. Steroid Biochem. Mol. Biol. 84, 291–300.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, 87–97.CrossRefGoogle ScholarPubMed
Tinsley, R.C., Loumont, C. & Kobel, H.R. (1996). Geographical distribution and ecology. In: The Biology of Xenopus. Tinsley, R.C. & Kobel, H.R. (eds). Oxford. Oxford University Press, pp. 35–39.Google Scholar
Villecco, E.I. (1998). Ovogénesis en anfibios: interacciones celulares. Doctoral dissertation, Universidad Nacional de Tucumán, Tucumán, Argentina.Google Scholar
Villecco, E.I., Aybar, M.J., Sanchez, S.S. & 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, 76–85.3.0.CO;2-2>CrossRefGoogle 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.CrossRefGoogle ScholarPubMed
Wartenberg, S. & Gusek, W. (1960). Electron microscopic research on the fine structure of the ovarian ovum and the follicular epithelium of amphibia. Expt. Cell. Res. 19, 199.CrossRefGoogle ScholarPubMed