Skip to main content
Proceedings of the National Academy of Sciences of the United States of America logoLink to Proceedings of the National Academy of Sciences of the United States of America
. 1991 Mar 15;88(6):2232–2235. doi: 10.1073/pnas.88.6.2232

Inositol trisphosphate receptor: phosphorylation by protein kinase C and calcium calmodulin-dependent protein kinases in reconstituted lipid vesicles.

C D Ferris 1, R L Huganir 1, D S Bredt 1, A M Cameron 1, S H Snyder 1
PMCID: PMC51204  PMID: 1848697

Abstract

We have previously demonstrated that the inositol 1,4,5-trisphosphate (IP3) receptor is phosphorylated by cyclic AMP-dependent protein kinase (PKA). In the present study, phosphorylation of IP3 receptors has been examined with purified receptor protein reconstituted in liposomes to remove detergent that can inhibit protein kinases. The IP3 receptor is stoichiometrically phosphorylated by protein kinase C (PKC) and Ca2+ calmodulin-dependent protein kinase II (CaM kinase II) as well as by PKA. Phosphorylation by the three enzymes is additive and involves different peptide sequences. Phosphorylation by PKC, which is stimulated by Ca2+ and diacylglycerol, and by CaM kinase II, which requires Ca2+, provides means whereby Ca2+ and diacylglycerol, formed during inositol phospholipid turnover, may regulate IP3 receptor physiology.

Full text

PDF
2232

Images in this article

Selected References

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

  1. Berridge M. J. Inositol trisphosphate and diacylglycerol: two interacting second messengers. Annu Rev Biochem. 1987;56:159–193. doi: 10.1146/annurev.bi.56.070187.001111. [DOI] [PubMed] [Google Scholar]
  2. Berridge M. J., Irvine R. F. Inositol phosphates and cell signalling. Nature. 1989 Sep 21;341(6239):197–205. doi: 10.1038/341197a0. [DOI] [PubMed] [Google Scholar]
  3. Danoff S. K., Supattapone S., Snyder S. H. Characterization of a membrane protein from brain mediating the inhibition of inositol 1,4,5-trisphosphate receptor binding by calcium. Biochem J. 1988 Sep 15;254(3):701–705. doi: 10.1042/bj2540701. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Ferris C. D., Huganir R. L., Snyder S. H. Calcium flux mediated by purified inositol 1,4,5-trisphosphate receptor in reconstituted lipid vesicles is allosterically regulated by adenine nucleotides. Proc Natl Acad Sci U S A. 1990 Mar;87(6):2147–2151. doi: 10.1073/pnas.87.6.2147. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Ferris C. D., Huganir R. L., Supattapone S., Snyder S. H. Purified inositol 1,4,5-trisphosphate receptor mediates calcium flux in reconstituted lipid vesicles. Nature. 1989 Nov 2;342(6245):87–89. doi: 10.1038/342087a0. [DOI] [PubMed] [Google Scholar]
  6. Fukunaga K., Goto S., Miyamoto E. Immunohistochemical localization of Ca2+/calmodulin-dependent protein kinase II in rat brain and various tissues. J Neurochem. 1988 Oct;51(4):1070–1078. doi: 10.1111/j.1471-4159.1988.tb03070.x. [DOI] [PubMed] [Google Scholar]
  7. Furuichi T., Yoshikawa S., Miyawaki A., Wada K., Maeda N., Mikoshiba K. Primary structure and functional expression of the inositol 1,4,5-trisphosphate-binding protein P400. Nature. 1989 Nov 2;342(6245):32–38. doi: 10.1038/342032a0. [DOI] [PubMed] [Google Scholar]
  8. Huganir R. L., Miles K., Greengard P. Phosphorylation of the nicotinic acetylcholine receptor by an endogenous tyrosine-specific protein kinase. Proc Natl Acad Sci U S A. 1984 Nov;81(22):6968–6972. doi: 10.1073/pnas.81.22.6968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Ouimet C. C., McGuinness T. L., Greengard P. Immunocytochemical localization of calcium/calmodulin-dependent protein kinase II in rat brain. Proc Natl Acad Sci U S A. 1984 Sep;81(17):5604–5608. doi: 10.1073/pnas.81.17.5604. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Ross C. A., Meldolesi J., Milner T. A., Satoh T., Supattapone S., Snyder S. H. Inositol 1,4,5-trisphosphate receptor localized to endoplasmic reticulum in cerebellar Purkinje neurons. Nature. 1989 Jun 8;339(6224):468–470. doi: 10.1038/339468a0. [DOI] [PubMed] [Google Scholar]
  11. Satoh T., Ross C. A., Villa A., Supattapone S., Pozzan T., Snyder S. H., Meldolesi J. The inositol 1,4,5,-trisphosphate receptor in cerebellar Purkinje cells: quantitative immunogold labeling reveals concentration in an ER subcompartment. J Cell Biol. 1990 Aug;111(2):615–624. doi: 10.1083/jcb.111.2.615. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Supattapone S., Danoff S. K., Theibert A., Joseph S. K., Steiner J., Snyder S. H. Cyclic AMP-dependent phosphorylation of a brain inositol trisphosphate receptor decreases its release of calcium. Proc Natl Acad Sci U S A. 1988 Nov;85(22):8747–8750. doi: 10.1073/pnas.85.22.8747. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Supattapone S., Worley P. F., Baraban J. M., Snyder S. H. Solubilization, purification, and characterization of an inositol trisphosphate receptor. J Biol Chem. 1988 Jan 25;263(3):1530–1534. [PubMed] [Google Scholar]
  14. Uchida T., Filburn C. R. Affinity chromatography of protein kinase C-phorbol ester receptor on polyacrylamide-immobilized phosphatidylserine. J Biol Chem. 1984 Oct 25;259(20):12311–12314. [PubMed] [Google Scholar]
  15. Walaas S. I., Lai Y., Gorelick F. S., DeCamilli P., Moretti M., Greengard P. Cell-specific localization of the alpha-subunit of calcium/calmodulin-dependent protein kinase II in Purkinje cells in rodent cerebellum. Brain Res. 1988 Nov;464(3):233–242. doi: 10.1016/0169-328x(88)90029-0. [DOI] [PubMed] [Google Scholar]
  16. Walaas S. I., Nairn A. C., Greengard P. PCPP-260, a Purkinje cell-specific cyclic AMP-regulated membrane phosphoprotein of Mr 260,000. J Neurosci. 1986 Apr;6(4):954–961. doi: 10.1523/JNEUROSCI.06-04-00954.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Weeks G., Picciotto M., Nairn A. C., Walaas S. I., Greengard P. Purification and characterization of PCPP-260: a Purkinje cell-enriched cyclic AMP-regulated membrane phosphoprotein of Mr 260,000. Synapse. 1988;2(1):89–96. doi: 10.1002/syn.890020112. [DOI] [PubMed] [Google Scholar]
  18. Worley P. F., Baraban J. M., Colvin J. S., Snyder S. H. Inositol trisphosphate receptor localization in brain: variable stoichiometry with protein kinase C. Nature. 1987 Jan 8;325(7000):159–161. doi: 10.1038/325159a0. [DOI] [PubMed] [Google Scholar]
  19. Worley P. F., Baraban J. M., Supattapone S., Wilson V. S., Snyder S. H. Characterization of inositol trisphosphate receptor binding in brain. Regulation by pH and calcium. J Biol Chem. 1987 Sep 5;262(25):12132–12136. [PubMed] [Google Scholar]
  20. Yamamoto H., Maeda N., Niinobe M., Miyamoto E., Mikoshiba K. Phosphorylation of P400 protein by cyclic AMP-dependent protein kinase and Ca2+/calmodulin-dependent protein kinase II. J Neurochem. 1989 Sep;53(3):917–923. doi: 10.1111/j.1471-4159.1989.tb11792.x. [DOI] [PubMed] [Google Scholar]

Articles from Proceedings of the National Academy of Sciences of the United States of America are provided here courtesy of National Academy of Sciences

RESOURCES