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. 1997 Feb 15;322(Pt 1):267–272. doi: 10.1042/bj3220267

Involvement of the Ca2+/calmodulin-dependent protein kinase II pathway in the Ca2+-mediated regulation of the capacitative Ca2+ entry in Xenopus oocytes.

F Matifat 1, F Fournier 1, T Lorca 1, J P Capony 1, G Brûlé 1, T Collin 1
PMCID: PMC1218187  PMID: 9078272

Abstract

Activation of the phosphoinositide transduction pathway induces capacitative Ca2+ entry in Xenopus oocytes. This can also be evoked by intracellular injection of Ins(1,4.5)P3, external application of thapsigargin and/or incubation in a Ca2+-free medium. Readmission of Ca2+ to voltage-clamped, thapsigargin-treated Xenopus oocytes triggers Ca2+-dependent Cl- current variations that reflect capacitative Ca2+ entry. Inhibition of Ca2+/calmodulin-dependent protein kinase II (CaMKII) by specific peptides markedly increased the amplitude of the transients, suggesting an involvement of the CaMKII pathway in the regulation of capacitative Ca2+ entry. Biochemical studies provide evidence for the activation of CaMKII in response to the development of capacitative Ca2+ entry. In effect, a CaMKII assay in vivo allows us to postulate that readmission of Ca2+ to thapsigargin-treated oocytes can induce a burst of CaMKII activity. Finally, analysis of the Cl- transient kinetics at high resolution of time suggests that CaMKII inhibition blocks the onset of the inactivation process without affecting the activation rate. We therefore postulate that CaMKII might participate in a negative feedback regulation of store-depletion-evoked Ca2+ entry in Xenopus oocytes.

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Selected References

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  1. Berridge M. J. Capacitative calcium entry. Biochem J. 1995 Nov 15;312(Pt 1):1–11. doi: 10.1042/bj3120001. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Berridge M. J. Inositol trisphosphate and calcium signalling. Nature. 1993 Jan 28;361(6410):315–325. doi: 10.1038/361315a0. [DOI] [PubMed] [Google Scholar]
  3. DeLisle S., Blondel O., Longo F. J., Schnabel W. E., Bell G. I., Welsh M. J. Expression of inositol 1,4,5-trisphosphate receptors changes the Ca2+ signal of Xenopus oocytes. Am J Physiol. 1996 Apr;270(4 Pt 1):C1255–C1261. doi: 10.1152/ajpcell.1996.270.4.C1255. [DOI] [PubMed] [Google Scholar]
  4. Delisle S. The four dimensions of calcium signalling in Xenopus oocytes. Cell Calcium. 1991 Feb-Mar;12(2-3):217–227. doi: 10.1016/0143-4160(91)90022-7. [DOI] [PubMed] [Google Scholar]
  5. Dumont J. N. Oogenesis in Xenopus laevis (Daudin). I. Stages of oocyte development in laboratory maintained animals. J Morphol. 1972 Feb;136(2):153–179. doi: 10.1002/jmor.1051360203. [DOI] [PubMed] [Google Scholar]
  6. Ferris C. D., Huganir R. L., Bredt D. S., Cameron A. M., Snyder S. H. Inositol trisphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles. Proc Natl Acad Sci U S A. 1991 Mar 15;88(6):2232–2235. doi: 10.1073/pnas.88.6.2232. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Hashimoto Y., Soderling T. R. Calcium . calmodulin-dependent protein kinase II and calcium . phospholipid-dependent protein kinase activities in rat tissues assayed with a synthetic peptide. Arch Biochem Biophys. 1987 Feb 1;252(2):418–425. doi: 10.1016/0003-9861(87)90048-8. [DOI] [PubMed] [Google Scholar]
  8. Hoth M., Penner R. Depletion of intracellular calcium stores activates a calcium current in mast cells. Nature. 1992 Jan 23;355(6358):353–356. doi: 10.1038/355353a0. [DOI] [PubMed] [Google Scholar]
  9. Lorca T., Cruzalegui F. H., Fesquet D., Cavadore J. C., Méry J., Means A., Dorée M. Calmodulin-dependent protein kinase II mediates inactivation of MPF and CSF upon fertilization of Xenopus eggs. Nature. 1993 Nov 18;366(6452):270–273. doi: 10.1038/366270a0. [DOI] [PubMed] [Google Scholar]
  10. Lorca T., Labbé J. C., Devault A., Fesquet D., Capony J. P., Cavadore J. C., Le Bouffant F., Dorée M. Dephosphorylation of cdc2 on threonine 161 is required for cdc2 kinase inactivation and normal anaphase. EMBO J. 1992 Jul;11(7):2381–2390. doi: 10.1002/j.1460-2075.1992.tb05302.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Lupu-Meiri M., Beit-Or A., Christensen S. B., Oron Y. Calcium entry in Xenopus oocytes: effects of inositol trisphosphate, thapsigargin and DMSO. Cell Calcium. 1993 Feb;14(2):101–110. doi: 10.1016/0143-4160(93)90080-p. [DOI] [PubMed] [Google Scholar]
  12. Matifat F., Collin T., Humez S., Brûle G., Fournier F. Sensitization of InsP3-dependent calcium signalling through structural modification of voltage-dependent calcium channel: a physiological relevance of the calcium channel beta subunit. Biochem Biophys Res Commun. 1995 Mar 8;208(1):440–446. doi: 10.1006/bbrc.1995.1357. [DOI] [PubMed] [Google Scholar]
  13. Parker I., Yao Y. Relation between intracellular Ca2+ signals and Ca(2+)-activated Cl- current in Xenopus oocytes. Cell Calcium. 1994 Apr;15(4):276–288. doi: 10.1016/0143-4160(94)90067-1. [DOI] [PubMed] [Google Scholar]
  14. Parys J. B., Bezprozvanny I. The inositol trisphosphate receptor of Xenopus oocytes. Cell Calcium. 1995 Nov;18(5):353–363. doi: 10.1016/0143-4160(95)90051-9. [DOI] [PubMed] [Google Scholar]
  15. Parys J. B., Sernett S. W., DeLisle S., Snyder P. M., Welsh M. J., Campbell K. P. Isolation, characterization, and localization of the inositol 1,4,5-trisphosphate receptor protein in Xenopus laevis oocytes. J Biol Chem. 1992 Sep 15;267(26):18776–18782. [PubMed] [Google Scholar]
  16. Payne M. E., Fong Y. L., Ono T., Colbran R. J., Kemp B. E., Soderling T. R., Means A. R. Calcium/calmodulin-dependent protein kinase II. Characterization of distinct calmodulin binding and inhibitory domains. J Biol Chem. 1988 May 25;263(15):7190–7195. [PubMed] [Google Scholar]
  17. Pearson R. B., Kemp B. E. Protein kinase phosphorylation site sequences and consensus specificity motifs: tabulations. Methods Enzymol. 1991;200:62–81. doi: 10.1016/0076-6879(91)00127-i. [DOI] [PubMed] [Google Scholar]
  18. Petersen C. C., Berridge M. J. G-protein regulation of capacitative calcium entry may be mediated by protein kinases A and C in Xenopus oocytes. Biochem J. 1995 May 1;307(Pt 3):663–668. doi: 10.1042/bj3070663. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Petersen C. C., Berridge M. J. The regulation of capacitative calcium entry by calcium and protein kinase C in Xenopus oocytes. J Biol Chem. 1994 Dec 23;269(51):32246–32253. [PubMed] [Google Scholar]
  20. Phillips A. M., Bull A., Kelly L. E. Identification of a Drosophila gene encoding a calmodulin-binding protein with homology to the trp phototransduction gene. Neuron. 1992 Apr;8(4):631–642. doi: 10.1016/0896-6273(92)90085-r. [DOI] [PubMed] [Google Scholar]
  21. Putney J. W., Jr, Bird G. S. The inositol phosphate-calcium signaling system in nonexcitable cells. Endocr Rev. 1993 Oct;14(5):610–631. doi: 10.1210/edrv-14-5-610. [DOI] [PubMed] [Google Scholar]
  22. Putney J. W., Jr Capacitative calcium entry revisited. Cell Calcium. 1990 Nov-Dec;11(10):611–624. doi: 10.1016/0143-4160(90)90016-n. [DOI] [PubMed] [Google Scholar]
  23. Yao Y., Parker I. Inositol trisphosphate-mediated Ca2+ influx into Xenopus oocytes triggers Ca2+ liberation from intracellular stores. J Physiol. 1993 Aug;468:275–295. doi: 10.1113/jphysiol.1993.sp019771. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Zhang B. X., Zhao H., Muallem S. Ca(2+)-dependent kinase and phosphatase control inositol 1,4,5-trisphosphate-mediated Ca2+ release. Modification by agonist stimulation. J Biol Chem. 1993 May 25;268(15):10997–11001. [PubMed] [Google Scholar]
  25. Zweifach A., Lewis R. S. Rapid inactivation of depletion-activated calcium current (ICRAC) due to local calcium feedback. J Gen Physiol. 1995 Feb;105(2):209–226. doi: 10.1085/jgp.105.2.209. [DOI] [PMC free article] [PubMed] [Google Scholar]

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