Skip to main content
The Journal of Cell Biology logoLink to The Journal of Cell Biology
. 1981 Jun 1;89(3):389–394. doi: 10.1083/jcb.89.3.389

Calmodulin triggers the resumption of meiosis in amphibian oocytes

PMCID: PMC2111798  PMID: 6265465

Abstract

The calcium-binding protein, calmodulin, has been purified from Xenopus laevis oocytes. This 18,500-dalton protein, pl 4.3, has two high- affinity calcium-binding sites per mole protein having a dissociation constant of 2.8 x 10(-6) M. Full-grown Xenopus oocytes, arrested in late G2 of the meiotic cell cycle, resumed meiosis when microinjected with 60-80 ng (3-4 pmol) of calmodulin in the form of a calcium- calmodulin complex. The timing of the meiotic events in these recipient oocytes was the same as that normally induced by progesterone. Xenopus ovarian calmodulin stimulated bovine brain phosphodiesterase (PDE) 3- to 10-fold in a calcium-dependent manner, but it had no apparent effect on ovarian PDE activity. A calcium-calmodulin-dependent protein kinase has been isolated from Xenopus oocytes using a calmodulin-Sepharose 4B affinity column. The possible role for this kinase in regulating the G2- M transition in oocytes has been discussed.

Full Text

The Full Text of this article is available as a PDF (578.7 KB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Baulieu E. E., Godeau F., Schorderet M., Schorderet-Slatkine S. Steroid-induced meiotic division in Xenopus laevis oocytes: surface and calcium. Nature. 1978 Oct 19;275(5681):593–598. doi: 10.1038/275593a0. [DOI] [PubMed] [Google Scholar]
  2. Cartaud A., Ozon R., Walsh M. P., Haiech J., Demaille J. G. Xenopus laevis oocyte calmodulin in the process of meiotic maturation. J Biol Chem. 1980 Oct 10;255(19):9404–9408. [PubMed] [Google Scholar]
  3. Cheung W. Y. Calmodulin plays a pivotal role in cellular regulation. Science. 1980 Jan 4;207(4426):19–27. doi: 10.1126/science.6243188. [DOI] [PubMed] [Google Scholar]
  4. Childers S. R., Siegel F. L. Isolation and purification of calcium-binding protein from electroplax of Electrophorus electricus. Biochim Biophys Acta. 1975 Sep 9;405(1):99–108. doi: 10.1016/0005-2795(75)90319-0. [DOI] [PubMed] [Google Scholar]
  5. Dedman J. R., Potter J. D., Jackson R. L., Johnson J. D., Means A. R. Physicochemical properties of rat testis Ca2+-dependent regulator protein of cyclic nucleotide phosphodiesterase. Relationship of Ca2+-binding, conformational changes, and phosphodiesterase activity. J Biol Chem. 1977 Dec 10;252(23):8415–8422. [PubMed] [Google Scholar]
  6. Head J. F., Mader S., Kaminer B. Calcium-binding modulator protein from the unfertilized egg of the sea urchin Arbacia punctulata. J Cell Biol. 1979 Jan;80(1):211–218. doi: 10.1083/jcb.80.1.211. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Klee C. B., Crouch T. H., Richman P. G. Calmodulin. Annu Rev Biochem. 1980;49:489–515. doi: 10.1146/annurev.bi.49.070180.002421. [DOI] [PubMed] [Google Scholar]
  8. Klee C. B., Krinks M. H. Purification of cyclic 3',5'-nucleotide phosphodiesterase inhibitory protein by affinity chromatography on activator protein coupled to Sepharose. Biochemistry. 1978 Jan 10;17(1):120–126. doi: 10.1021/bi00594a017. [DOI] [PubMed] [Google Scholar]
  9. Lin Y. M., Liu Y. P., Cheung W. Y. Cyclic 3':5'-nucleotide phosphodiesterase. Purification, characterization, and active form of the protein activator from bovine brain. J Biol Chem. 1974 Aug 10;249(15):4943–4954. [PubMed] [Google Scholar]
  10. Maller J. L., Butcher F. R., Krebs E. G. Early effect of progesterone on levels of cyclic adenosine 3':5'-monophosphate in Xenopus oocytes. J Biol Chem. 1979 Feb 10;254(3):579–582. [PubMed] [Google Scholar]
  11. Maller J. L., Krebs E. G. 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. 1977 Mar 10;252(5):1712–1718. [PubMed] [Google Scholar]
  12. Maller J. L., Krebs E. G. Regulation of oocyte maturation. Curr Top Cell Regul. 1980;16:271–311. doi: 10.1016/b978-0-12-152816-4.50012-1. [DOI] [PubMed] [Google Scholar]
  13. Maller J., Wu M., Gerhart J. C. Changes in protein phosphorylation accompanying maturation of Xenopus laevis oocytes. Dev Biol. 1977 Jul 15;58(2):295–312. doi: 10.1016/0012-1606(77)90093-8. [DOI] [PubMed] [Google Scholar]
  14. Masui Y., Markert C. L. Cytoplasmic control of nuclear behavior during meiotic maturation of frog oocytes. J Exp Zool. 1971 Jun;177(2):129–145. doi: 10.1002/jez.1401770202. [DOI] [PubMed] [Google Scholar]
  15. Masui Y., Meyerhof P. G., Miller M. A., Wasserman W. J. Roles of divalent cations in maturation and activation of vertebrate oocytes. Differentiation. 1977 Oct 20;9(1-2):49–57. doi: 10.1111/j.1432-0436.1977.tb01518.x. [DOI] [PubMed] [Google Scholar]
  16. Means A. R., Dedman J. R. Calmodulin--an intracellular calcium receptor. Nature. 1980 May 8;285(5760):73–77. doi: 10.1038/285073a0. [DOI] [PubMed] [Google Scholar]
  17. Moreau M., Doree M., Guerrier P. Electrophoretic introduction of calcium ions into the cortex of Xenopus laevis oocytes triggers meiosis neinitiation. J Exp Zool. 1976 Sep;197(3):443–449. doi: 10.1002/jez.1401970318. [DOI] [PubMed] [Google Scholar]
  18. Morrill G. A., Schatz F., Kostellow A. B., Poupko J. M. Changes in cyclic AMP levels in the amphibian ovarian follicle following progesterone induction of meiotic maturation. Effect of phosphodiesterase inhibitors and exogenous calcium on germinal vesicle breakdown. Differentiation. 1977 Aug 11;8(2):97–104. doi: 10.1111/j.1432-0436.1977.tb00925.x. [DOI] [PubMed] [Google Scholar]
  19. O'Connor C. M., Smith L. D. Inhibition of oocyte maturation by theophylline: possible mechanism of action. Dev Biol. 1976 Sep;52(2):318–322. doi: 10.1016/0012-1606(76)90249-9. [DOI] [PubMed] [Google Scholar]
  20. RAAFLAUB J. Applications of metal buffers and metal indicators in biochemistry. Methods Biochem Anal. 1956;3:301–325. doi: 10.1002/9780470110195.ch10. [DOI] [PubMed] [Google Scholar]
  21. Sanui H. Measurement of inorganic orthophosphate in biological materials: extraction properties of butyl acetate. Anal Biochem. 1974 Aug;60(2):489–504. doi: 10.1016/0003-2697(74)90259-0. [DOI] [PubMed] [Google Scholar]
  22. Schulman H., Greengard P. Ca2+-dependent protein phosphorylation system in membranes from various tissues, and its activation by "calcium-dependent regulator". Proc Natl Acad Sci U S A. 1978 Nov;75(11):5432–5436. doi: 10.1073/pnas.75.11.5432. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Speaker M. G., Butcher F. R. Cyclic nucleotide fluctuations during steroid induced meiotic maturation of frog oocytes. Nature. 1977 Jun 30;267(5614):848–850. doi: 10.1038/267848a0. [DOI] [PubMed] [Google Scholar]
  24. Waisman D. M., Stevens F. C., Wang J. H. Purification and characterization of a Ca2+-binding protein in Lumbricus terrestris. J Biol Chem. 1978 Feb 25;253(4):1106–1113. [PubMed] [Google Scholar]
  25. Wallace R. A., Jared D. W., Dumont J. N., Sega M. W. Protein incorporation by isolated amphibian oocytes. 3. Optimum incubation conditions. J Exp Zool. 1973 Jun;184(3):321–333. doi: 10.1002/jez.1401840305. [DOI] [PubMed] [Google Scholar]
  26. Wasserman W. J., Masui Y. Initiation of meiotic maturation in Xenopus laevis oocytes by the combination of divalent cations and ionophore A23187. J Exp Zool. 1975 Sep;193(3):369–375. doi: 10.1002/jez.1401930313. [DOI] [PubMed] [Google Scholar]
  27. Wasserman W. J., Pinto L. H., O'Connor C. M., Smith L. D. Progesterone induces a rapid increase in [Ca2+]in of Xenopus laevis oocytes. Proc Natl Acad Sci U S A. 1980 Mar;77(3):1534–1536. doi: 10.1073/pnas.77.3.1534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Watterson D. M., Harrelson W. G., Jr, Keller P. M., Sharief F., Vanaman T. C. Structural similarities between the Ca2+-dependent regulatory proteins of 3':5'-cyclic nucleotide phosphodiesterase and actomyosin ATPase. J Biol Chem. 1976 Aug 10;251(15):4501–4513. [PubMed] [Google Scholar]
  29. Welsh M. J., Dedman J. R., Brinkley B. R., Means A. R. Calcium-dependent regulator protein: localization in mitotic apparatus of eukaryotic cells. Proc Natl Acad Sci U S A. 1978 Apr;75(4):1867–1871. doi: 10.1073/pnas.75.4.1867. [DOI] [PMC free article] [PubMed] [Google Scholar]

Articles from The Journal of Cell Biology are provided here courtesy of The Rockefeller University Press

RESOURCES