Skip to main content

Oocyte Maturation in Amphibians

  • Chapter
Oogenesis

Part of the book series: Developmental Biology ((DEBO,volume 1))

Abstract

Although the amphibian oocyte possesses a vast store of structural and regulatory components, the oocyte itself is extremely repressed in terms of its rate of protein synthesis. It can remain in this repressed state for a period of months or years, as it grows in the ovary by virtue of deposition of yolk platelets. The quiescent state of oocyte metabolism is broken when the process of oocyte maturation is initiated by hormones. Studies over many years have demonstrated that in vivo the epithelial layer of follicle cells surrounding each oocyte is stimulated by pituitary-derived luteinizing hormone (LH) to synthesize and secrete progesterone, which acts directly on the oocyte to induce maturation of the oocyte into an unfertilized egg (Masui, 1967; Mailer and Krebs, 1980). The interaction of progesterone with the isolated oocyte appears to be a sufficient trigger for a normal oocyte maturation response, as judged by cytological analysis and by the ability of isolated oocytes responding to exogenously applied progesterone to undergo normal embryonic development (Smith et al., 1968; Drury and Schorderet-Slatkine, 1975).

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

eBook
USD 16.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 109.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Allende, C. C., Bravo, R., and Allende, J. E., 1977, Comparison of in vivo and in vitro properties of cyclic adenosine 3′:5′-monophosphate phosphodiesterase of amphibian oocytes,J. Biol. Chem. 252:4662–4666.

    PubMed  CAS  Google Scholar 

  • Boyer, J., Belle, R., Huchon, D., and Ozon, R., 1980, in ovo protein kinase activity during progesterone-induced maturation of Xenopus Jaevis oocytes, in: Steroids and TheirMechanismof Action in Non-mammalianVertebrates (G. Delrio and J. Brachet, eds.), pp. 85–92, Raven Press, New York.

    Google Scholar 

  • Cassci, D., and Selinger, Z., 1977, Mechanism of adenylate cyclase activation by cholera toxin: Inhibition of GTP hydrolysis at the regulatory site, Proc. Natl. Acad. Sci. USA 74:3307–3311.

    Article  Google Scholar 

  • Cassci, D., Levkovitz, H., and Selinger, Z., 1977, The regulatory GTPase cycle of turkey erythrocyte adenylate cyclase,J. Cyclic Nucleotide Res. 3:393–406.

    Google Scholar 

  • Cheung, W. Y., 1980, Calmodulin plays a pivotal role in cellular regulation, Science 207:19–27.

    Article  PubMed  CAS  Google Scholar 

  • Cicirelli, M. F., Robinson, K. R., and Smith, L. D., 1983, Internal pH of Xenopus oocytes: A study of the mechanism and role of pH changes during meiotic maturation, Dev. Biol. 100:133–146.

    Article  PubMed  CAS  Google Scholar 

  • Cohen, P., 1982, The role of protein phosphorylation in neural and hormonal control of cellular activity, Nature 296:613–620.

    Article  PubMed  CAS  Google Scholar 

  • DeRobertis, E. M., Partington, G. A., Longthorne, R. F., and Gurdon, J. B., 1977, Somatic nuclei in amphibian oocytes: Evidence for selective gene expression,J. Embryol. Exp. Morphol. 40:199–214.

    CAS  Google Scholar 

  • Drury, K. C., and Schorderet-Slatkine, S., 1975, Effects of cycloheximide on the “autocataly-tic” nature of the maturation promoting factor (MPF) in oocytes of Xenopus Jaevis, Cell 4:269–274.

    Article  PubMed  CAS  Google Scholar 

  • Duncan, R., and McConkey, E. H., 1982, Rapid alterations in initiation rate and recruitment of inactive RNA are temporally correlated with S6 phosphorylation, Eur. J. Biochem. 123:539–544.

    Article  PubMed  CAS  Google Scholar 

  • Echeverria, M., Orellana, O., Jedlicki, E., Plaza, M., Allende, C., and Allende, J., 1981, Regulation of a cyclic nucleotide phosphodiesterase from Xenopus laevis ovary by calmodulin and calcium, Biochem. Int. 2:539–545.

    CAS  Google Scholar 

  • Epel, D., 1978, Mechanisms of activation of sperm and egg during fertilization of sea urchin gametes, Curr. Top. Dev. Biol. 12:185–246.

    Article  PubMed  CAS  Google Scholar 

  • Finidori-Lepicard, J., Schorderet-Slatkine, S., Hanoune, J., and Baulieu, E. E., 1981, Progesterone inhibits membrane-bound adendylate cyclase in Xenopus laevis oocytes, Nature 292:255–257.

    Article  PubMed  CAS  Google Scholar 

  • Foulkes, J. G., and Mailer, J. L., 1982, in vivo action of protein phosphatase inhibitor-2 in Xenopus oocytes, FEBS Lett. 158:155–160.

    Article  Google Scholar 

  • Gerhart, J., Wu, M., and Kirschner, M. W., 1984, Cell cycle dynamics of an M-phase-specific cytoplasmic factor in Xenopus Jaevis oocytes and eggs,J. Cell Biol. 98:1247–1255.

    Article  PubMed  CAS  Google Scholar 

  • Godeau, J. F., Schorderet-Slatkine, S. Hubert, P., and Baulieu, E. E., 1978, Induction of maturation in Xenopus Jaevis oocytes by a steroid linked to a polymer, Proc. Natl. Acad. Sci. USA 75:2353–2357.

    Article  PubMed  CAS  Google Scholar 

  • Hanocq-Quertier, J., and Baltus, E., 1981, Phosphorylation of ribosomal proteins during maturation of Xenopus Jaevis oocytes, Eur. J. Biochem. 120:351–355.

    Article  PubMed  CAS  Google Scholar 

  • Hemmings, B. A., Resink, T., and Cohen, P., 1982, Activation of the MgATP-dependent protein phosphatase by glycogen synthase kinase 3 does involve a phosphorylation reaction, FEBS Lett. 150:319–324.

    Article  PubMed  CAS  Google Scholar 

  • Huang, F. L., and Glinsmann, W. H., 1976, Separation and characterization of two phosphorylation phosphatase inhibitors from rabbit skeletal muscle, Eur. J. Biochem. 70:419–426.

    Article  PubMed  CAS  Google Scholar 

  • Huchon, D., Ozon, R., Fischer, E. H., and Démaille, J. G., 1981a, The pure inhibitor of cyclic AMP-dependent protein kinase initiates Xenopus Jaevis meiotic maturation: A 4-step scheme for meiotic maturation, Mol. Cell. Endocrinol. 22:211–222.

    Article  PubMed  CAS  Google Scholar 

  • Huchon, D., Ozon, R., and Demaille, J. G., 1981b, Protein phosphatase-1 is involved in Xenopus oocyte maturation, Nature 294:358–359.

    Article  PubMed  CAS  Google Scholar 

  • Ishikawa, K., Hanaoka, Y., Kondo, Y., and Imai, K., 1977, Primary action of steroid hormone at the surface of amphibian oocyte in the induction of germinal vesicle breakdown, Mol. Cell. Endocrino J. 9:91–100.

    Article  CAS  Google Scholar 

  • Johnson, G. L., 1982, Cholera toxin action and the regulation of hormone-sensitive adenylate cyclase, in: Molecular Action of Toxins and Viruses (P. Cohen and P. Van Heyningen, eds.), pp. 33–49, Elsevier Biomedical Press, New York.

    Google Scholar 

  • Jordana, X., Allende, C. C., and Allende, J. E., 1981, Guanine nucleotides are required for progesterone inhibition of amphibian oocyte adenylate cyclase, Biochem. Int. 3:527–532.

    CAS  Google Scholar 

  • Kaltoff, H., Darmer, D., Towbin, H., Gordon, J., Amons, R., Moller, W., and Richter, D., 1982, Ribosomal protein S6 from Xenopus Jaevis ovaries, Eur. J. Biochem. 122:439–443.

    Article  Google Scholar 

  • Kishimoto, T., and Kanatani, H., 1976, Cytoplasmic factor responsible for germinal vesicle breakdown and meiotic maturation in starfish oocyte, Nature 260:321–322.

    Article  PubMed  CAS  Google Scholar 

  • Koski, K., and Klee, W. A., 1981, Opiates inhibit adenylate cyclase by stimulating GTP hydrolysis, Proc. Natl. Acad. Sci. USA 78:4185–4189.

    Article  PubMed  CAS  Google Scholar 

  • Lee, S. C., and Steinhardt, R. A., 1981, pH changes associated with meiotic maturation in oocytes of Xenopus Jaevis, Dev. Biol. 85:358–369.

    Article  PubMed  CAS  Google Scholar 

  • Lin, Y. M., and Cheung, W. Y., 1980, Ca+-dependent cyclic nucleotide phosphodiesterase, in: Calcium and Cell Function: Calmodulin (Y. Cheung, ed.), pp. 79–107, Academic Press, New York.

    Google Scholar 

  • Londos, C., Wolff, J., and Cooper, D. M. F., 1981, Adenosine as a regulator of adenylate cyclase, in: Purinergic Receptors (G. Burnstock, ed.), pp. 287–323, Chapman and Hall, New York.

    Chapter  Google Scholar 

  • Mailer, J. L., 1983, Interaction of steroids with the cyclic nucleotide system in amphibian oocytes, Adv. Cyclic Nucleotide Res. 15:295–336.

    Google Scholar 

  • Mailer, J. L., and Krebs, E. G., 1977, Progesterone-stimulated meiotic cell division in Xenopus oocytes: Induction by regulatory subunit and inhibition by catalytic subunit of adenosine 3′:5′-monophosphate-dependent protein kinase,J. Biol. Chem. 252:1712–1718.

    Google Scholar 

  • Mailer, J. L., and Krebs, E. G., 1980, Regulation of oocyte maturation, Curr. Top. Cell. Regul. 16:217–311.

    Google Scholar 

  • Mailer, J. L., and Sadler, S. E., 1981, Regulation of steroid induced cell division in amphibian oocytes by protein phosphorylation, Proc. Cold Spring Harbor Conf. Cell Prolif. 8:1127–1141.

    Google Scholar 

  • Mailer, J. L., Wu, M., and Gerhart, J. C., 1977, Changes in protein phosphorylation accompanying maturation of Xenopus laevis oocytes, Dev. Biol. 58:295–312.

    Article  Google Scholar 

  • Mailer, J. L., Butcher, F. R., and Krebs, E. G., 1979, Early effect of progesterone on levels of cyclic adenosine 3′:5′-monophosphate in Xenopus oocytes,J. Biol. Chem. 254:579–582.

    Google Scholar 

  • Martin-Perez, J., Mailer, J. L., and Thomas, G., 1984, Progesterone- and MPF-induced S6 phosphorylation during meiotic maturation of Xenopus laevis oocytes: in vivo and in vitro sites of phosphorylation, J. Biol. Chem. (submitted).

    Google Scholar 

  • Masui, Y., 1967, Relative roles of the pituitary, follicle cells and progesterone in the induction of oocyte maturation in Rana pipiens, J. Exp. Zool. 166:365–376.

    Article  PubMed  CAS  Google Scholar 

  • Masui, Y., and Markert, C. L., 1971, Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes,J. Exp. Zool. 177:129–146.

    Article  PubMed  CAS  Google Scholar 

  • Morrill, G. A., Schatz, F., Kostellow, A. B., and Poupko, J. M., 1977, Changes in cyclic AMP levels in the amphibian ovarian follicle following progesterone induction of meiotic maturation, Differentiation, 8:97–104.

    Article  PubMed  CAS  Google Scholar 

  • Mulner, O., Huchon, D., Thibier, C., and Ozon, R., 1979, Cyclic AMP synthesis in Xenopus laevis oocytes: Inhibition by progesterone, Biochim. Biophys. Acta 582:179–184.

    Article  PubMed  CAS  Google Scholar 

  • Mulner, O., Cartaud, A., and Ozon, R., 1980, Cyclic AMP phosphodiesterase activities in Xenopus laevis oocytes, Differentiation 16:31–39.

    Article  PubMed  CAS  Google Scholar 

  • Nielsen, P. J., Thomas, G., and Mailer, J. L., 1982, Increased phosphorylation of ribosomal protein S6 during meiotic maturation of Xenopus oocytes, Proc. Natl. Acad. Sci. USA 79:2937–2941.

    Article  PubMed  CAS  Google Scholar 

  • Nimmo, G. A., and Cohen, P., 1978, The regulation of glycogen metabolism: Purification and characterization of protein phosphatase inhibitor-1 from rabbit skeletal muscle, Eur. J. Biochem. 87:341–351.

    Article  PubMed  CAS  Google Scholar 

  • O’Connor, C. M., and Smith, L. D., 1976, Inhibition of oocyte maturation by theophylline: Possible mechanism of action, Dev. Biol. 52:318–322.

    Article  PubMed  Google Scholar 

  • Orellana, O., Allende, C. C., and Allende, J. E., 1981. Trypsin activates the calmodulin sensitive cyclic nucleotide phosphodiesterase of amphibian oocytes, Biochem Int. 3:663–668.

    CAS  Google Scholar 

  • Pouyssegur, J., Chambard, J. C., Franchi, A., Paris, S., and van Obberghen-Schilling, E., 1982, Growth factor activation of an amiloride-sensitive Na+/H+ exchange system in quiescent fibroblasts. Coupling to ribosomal protein S6 phosphorylation, Proc. Natl. Acad. Sci. USA 79:3935–3939.

    Article  PubMed  CAS  Google Scholar 

  • Reynhout, J. K., and Smith, L. D., 1974, Studies on the appearance and nature of a maturation-inducing factor in the cytoplasm of amphibian oocytes exposed to progesterone, Dev. Biol. 38:394–400.

    Article  PubMed  CAS  Google Scholar 

  • Richter, J. D., Wasserman, W. J., and Smith, L. D., 1982, The mechanism for increased protein synthesis during Xenopus oocyte maturation, Dev. Biol. 89:159–167.

    Article  PubMed  CAS  Google Scholar 

  • Sadler, S. E., and Mailer, J. L., 1981, Progesterone inhibits adenylate cyclase in Xenopus oocytes: Action on the guanine nucleotide regulatory protein,J. Biol. Chem. 256:6368–6373.

    PubMed  CAS  Google Scholar 

  • Sadler, S. E., and Mailer, J. L., 1982, Identification of a steroid receptor on the surface of Xen-opus oocytes by photoaffinity labeling,J. Biol. Chem. 257:355–361.

    PubMed  CAS  Google Scholar 

  • Sadler, S. E., and Mailer, J. L., 1983, Inhibition of Xenopus oocyte adenylate cyclase by progesterone and 2′,5′-dideoxyadenosine is associated with slowing of guanine nucleotide exchange,J. Biol. Chem. 258:7935–7941.

    PubMed  CAS  Google Scholar 

  • Sayhoun, N., Schmitges, C. J., Siegel, M. I., and Cuatrecasas, P., 1976, 2′-Deoxyadenosine-3’-monophosphate: A naturally occurring inhibitor of adenylate cyclase in amphibian and mammalian cells, Life Sci. 19:1961–1970.

    Article  Google Scholar 

  • Schorderet-Slatkine, S., Schorderet, M., and Baulieu, E. E., 1982, Cyclic AMP-mediated control of meiosis: Effects of progesterone, cholera toxin and membrane-active drugs in Xenopus laevis oocytes, Proc. Natl. Acad. Sci. USA, 79:850–854.

    Article  PubMed  CAS  Google Scholar 

  • Schulman, H., Huttner, W., and Grecngard, P., 1980, Calcium-dependent protein phosphorylation in mammalian brain and other tissues, in: Calcium and Cell Function, Vol. 1: Calmodulin, (W. Y. Cheung, ed.), pp. 219–252, Academic Press, New York.

    Google Scholar 

  • Smith, L. D., 1981, Frog oocytes and sea urchin eggs: Steroid hormones and sperm induce similar events, in: Progress in Developmental Biology (H. W. Sauer, ed.), pp. 35–48, Gustav Fischer Verlag, Stuttgart and New York.

    Google Scholar 

  • Smith, L. D., and Ecker, R. E., 1971, The interaction of steroids with Rana pipiens oocytes in the induction of maturation, Dev. Biol. 25:233–247.

    Google Scholar 

  • Smith, L. D., Ecker, R. E., and Subtelny, S., 1968, In vitro induction of physiological maturation in Rana pipiens oocytes removed from the ovarian follicles, Dev. Biol. 17:627–643.

    Article  PubMed  CAS  Google Scholar 

  • Speaker, M. G., and Butcher, F. R., 1977, Cyclic nucleotide fluctuations during steroid-induced meiotic maturation of frog oocytes, Nature (London) 267:848–849.

    Article  CAS  Google Scholar 

  • Stith, B. J., and Mailer, J. L., 1984, The effect of insulin on intracellular pH and ribosomal protein S6 phosphorylation in oocytes of Xenopus laevis, Dev. Biol. 102:79–89.

    Article  PubMed  CAS  Google Scholar 

  • Sunkara, P. S., Wright, D. A., and Rao, P. N., 1979, Mitotic factors from mammalian cells induce germinal vesicle breakdown and chromosome condensation in amphibian oocytes, Proc. Natl. Acad. Sci. USA 76:2799–2802.

    Article  PubMed  CAS  Google Scholar 

  • Thomas, G., Martin-Perez, J., Scigmann, M., and Otto, A. M., 1982, The effect of serum, EGF, PGF2a and insulin on S6 phosphorylation and the initiation of protein and DNA synthesis, Cell 30:235–242.

    Article  PubMed  CAS  Google Scholar 

  • Wang, J. H., Stull, J. T., Huang, T. S., and Krebs, E. G., 1976, A study of the autoactivation of rabbit muscle Phosphorylase kinase,J. Biol. Chem. 251:4521–4527.

    PubMed  CAS  Google Scholar 

  • Wasserman, W. J., and Masui, Y., 1975, Effects of cycloheximide on a cytoplasmic factor initiation meiotic maturation in Xenopus oocytes, Exp. Cell. Res. 91:381–388.

    Article  PubMed  CAS  Google Scholar 

  • Wasserman, W. J., and Smith, L. D., 1981, Calmodulin triggers the resumption of meiosis in amphibian oocytes,J. Cell. Biol. 89:389–394.

    Article  PubMed  CAS  Google Scholar 

  • Wasserman, W. J., Pinto, L. H., O’Connor, C. M., and Smith, L. D., 1980, Progesterone induces a rapid increase in (Ca++)in of Xenopus laevis oocytes, Proc. Natl. Acad. Sci. USA 77:1534–1536.

    Article  PubMed  CAS  Google Scholar 

  • Wasserman, W. J., Richter, J. D., and Smith, L. D., 1982, Protein synthesis during maturation-promoting factor and progesterone-induced maturation in Xenopus oocytes, Dev. Biol. 89:152–158.

    Article  PubMed  CAS  Google Scholar 

  • Wu, M., and Gerhart, J. C., 1980, Partial purification and characterization of the maturation-promoting factor from eggs of Xenopus laevis, Dev. Biol. 79:465–477.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 1985 Plenum Press, New York

About this chapter

Cite this chapter

Maller, J.L. (1985). Oocyte Maturation in Amphibians. In: Browder, L.W. (eds) Oogenesis. Developmental Biology, vol 1. Springer, Boston, MA. https://doi.org/10.1007/978-1-4615-6814-8_6

Download citation

  • DOI: https://doi.org/10.1007/978-1-4615-6814-8_6

  • Publisher Name: Springer, Boston, MA

  • Print ISBN: 978-1-4615-6816-2

  • Online ISBN: 978-1-4615-6814-8

  • eBook Packages: Springer Book Archive

Publish with us

Policies and ethics