D-myo-inositol 1,4,5-trisphosphate 3-kinase A is activated by receptor activation through a calcium:calmodulin-dependent protein kinase II phosphorylation mechanism

EMBO Journal

Volumn 16, Issue 8, 1997, Pages 1943-1952

  Communi, David ^a   Vanweyenberg, Valérie ^a   Erneux, Christophe ^a  

^a FREE UNIVERSITY OF BRUSSELS   (Belgium)

Author keywords

Calcium; Calmodulin; Inositol phosphate; Kinase; Phosphorylation

Indexed keywords

1 [N,O BIS(5 ISOQUINOLINESULFONYL) N METHYLTYROSYL] 4 PHENYLPIPERAZINE; CARBACHOL; INOSITOL TRISPHOSPHATE 3 KINASE; OKADAIC ACID; PROTEIN KINASE (CALCIUM,CALMODULIN) II; THREONINE; URIDINE TRIPHOSPHATE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN CORTEX; CHO CELL; CONSENSUS SEQUENCE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVE SITE; GENETIC TRANSFECTION; IMMUNOPRECIPITATION; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALCIUM; CARBACHOL; CEREBRAL CORTEX; CHO CELLS; CRICETINAE; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; MALE; MUSCARINIC AGONISTS; OKADAIC ACID; PHOSPHORYLATION; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, PURINERGIC P2; THREONINE; URIDINE TRIPHOSPHATE;

ANIMALIA; CRICETINAE; CRICETULUS GRISEUS;

EID: 0030891857     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/16.8.1943     Document Type: Article

References (55)

1. Baba, H., Fuss, B., Urano, J., Poullet, P., Watson, J.B., Tamanoi, F. and Macklin, W.B. (1995) GapIII, a new brain-enriched member of the GTPase-activating protein family. J. Neurosci. Res., 41, 846-858.
2. Batty, I.R., Nahorski, S.R. and Irvine, R.F. (1985) Rapid formation of inositol 1,3,4,5-tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem. J., 232, 211-215.
3. Beltman, J., Sonnenburg, W.K. and Beavo, J.A. (1993) The role of protein phosphorylation in the regulation of cyclic nucleotide phosphodiesterase. Mol. Cell. Biochem., 127/128, 239-253.
4. Berridge, M.J. (1993) Inositol trisphosphate and calcium signalling. Nature, 361, 315-325.
5. 2+-dependent and -independent mechanisms. Biochem. J., 256, 697-701.
6. Burns, F., Zhao, A.Z. and Beavo, J.A. (1996) Cyclic nucleotide phosphodiesterases: gene complexity, regulation by phosphorylation, and physiological implications. Adv. Pharmacol., 36, 29-48.
7. Challiss, R.A.J. and Nahorski, S.R. (1990) Neurotransmitter and depolarization-stimulated accumulation of inositol 1,3,4,5-tetrakisphosphate mass in rat cerebral cortex slices. J. Neurochem., 54, 2138-2141.
8. + current in single internally perfused mouse lacrimal acinar cells. J. Membr. Biol., 109, 85-93.
9. Choi, K.Y., Kim, H.K., Lee, S.Y., Moon, K.H., Sim, S.S., Kim, J.W., Chung, H.K. and Rhee, S.G. (1990) Molecular cloning and expression of a complementary DNA for inositol 1,4,5-trisphosphate 3-kinase. Science, 248, 64-66.
10. Cohen, P., Holmes, C.F. and Tsukitani, Y. (1990) Okadaic acid: a new probe for the study of cellular regulation. Trends Biochem. Sci., 15, 98-102.
11. Communi, D., Vanweyenberg, V. and Erneux, C. (1994) Purification and biochemical properties of a high-molecular-mass inositol 1,4,5-trisphosphate 3-kinase isoenzyme in human platelets. Biochem. J., 298, 669-673.
12. Communi, D., Lecocq, R., Vanweyenberg, V. and Erneux, C. (1995) Active site labelling of inositol 1,4,5-trisphosphate 3-kinase A by phenylglyoxal. Biochem. J., 310, 109-115.
13. Communi ,D., Lecocq, R. and Erneux, C. (1996) Arginine 343 and 350 are two active site residues involved in substrate binding by human type I D-myo-inositol 1,4,5-trisphosphate 5-phosphatase. J. Biol. Chem., 271, 11676-11683.
14. Corton, J.M., Gillepie, J.G. and Hardie, G. (1994) Role of the AMP-activated protein kinase in the cellular stress response. Curr. Biol., 4, 315-324.
15. 2+ mobilization in permeabilized mouse L1210 lymphoma cells by inositol 2,4,5-trisphosphate and inositol 1,3,4,5-tetrakisphosphate. Biochem. J., 271, 549-553.
16. 4-binding protein as a member of the GAP1 family. Nature, 376, 527-530.
17. Erneux, C., Moreau, C., Vandermeers, A. and Takazawa, K. (1993) Interaction of calmodulin with a putative calmodulin-binding domain of inositol 1,4,5-trisphosphate 3-kinase. Eur. J. Biochem., 214, 497-501.
18. Florio, V.A., Sonnenburg, W.K., Johnson, R., Kwak, K.S., Jensen, G.S., Walsh, K.A. and Beavo, J.A. (1994) Phosphorylation of the 61-kDa calmodulin-stimulated cyclic nucleotide phosphodiesterase at serine 120 reduces its affinity for calmodulin. Biochemistry, 33, 8948-8954.
19. Gottesman, M.M. (1987) Chinese hamster ovary cells. Methods Enzymol., 151, 3-8.
20. Hajimohammadreza, I., Probert, A.W., Coughenour, L.L., Borosky, S.A., Marcoux, F.W., Boxer, P.A. and Wang, K.K.W. (1995) A specific inhibitor of calcium/calmodulin-dependent protein kinase-II provides neuroprotection against NMDA- and hypoxia/hypoglycemia-induced cell death. J. Neurosci., 15, 4093-4101.
21. Hanson, P.I., Meyer, T., Stryer, L. and Schulman, H. (1994) Dual role of calmodulin in autophosphorylation of multifunctional CaM kinase may underlie decoding of calcium signals. Neuron, 12, 943-956.
22. 2+/CaM-dependent protein kinase II. Proc. Natl Acad. Sci. USA, 85, 7001-7005.
23. Imboden, J.B. and Pattison, G. (1987) Regulation of inositol 1,4,5-trisphosphate kinase activity after stimulation of human T cell antigen receptor. J. Clin. Invest., 79, 1538-1541.
24. Iredale, P.A. and Hill, S.J. (1993) Increases in intracellular calcium via activation of an endogenous P2-purinoreceptor in cultured CHO-K1 cells. Br. J. Pharmacol., 110, 1305-1310.
25. Irvine, R.F. (1991) Inositol tetrakisphosphate as a second messenger: confusions, contradictions, and a potential resolution. BioEssays, 13, 419-427.
26. Irvine, R.F., Moor, R.M., Pollock, W.K., Smith, P.M. and Wreggett, K.A. (1988) Inositol phosphates: proliferation, metabolism and function. Phil. Trans. R. Soc. Lond., 320, 281-298.
27. Ismailov, I.I., Fuller, C.M., Berdiev, B.K., Shlyonsky, V.G., Benos, D.J. and Barrett, K.E. (1996) A biological function for an 'orphan' messenger: D-myo-inositol 3,4,5,6-tetrakisphosphate selectively blocks epithelial calcium-activated chloride channels. Proc. Natl Acad. Sci. USA, 93, 10505-10509.
28. Ito, I., Hidaka, H. and Sugiyama, H. (1991) Effects of KN-62, a specific inhibitor of calcium/calmodulin-dependent protein kinase II, on long-term potentiation in the rat hippocampus. Neurosci. Lett., 121, 119-121.
29. Johnson, R.M., Wasilenko, W.J., Mattingly, R.R., Weber, M.J. and Garrison, J.C. (1989) Fibroblasts transformed with v-src show enhanced formation of an inositol tetrakisphosphate. Science, 246, 121-124.
30. King, W.G. and Rittenhouse, S.E. (1989) Inhibition of protein kinase C by staurosporine promotes elevated accumulations of inositol trisphosphates and tetrakisphosphates in human platelets exposed to thrombin. J. Biol. Chem., 264, 6070-6074.
31. Lee, S.Y., Sim, S.S., Kim, J.W., Moon, K.H., Kim, J.H. and Rhee, S.G. (1990) Purification and properties of D-myo-inositol 1,4,5-trisphosphate 3-kinase from rat brain. J. Biol. Chem., 265, 9434-9440.
32. 2+ release do not involve direct interaction of inositol 1,3,4,5-tetrakisphosphate with inositol trisphosphate-binding sites. Biochem. J., 314, 811-816.
33. Mailleux, P., Takazawa, K., Erneux, C. and Vanderhaeghen, J.-J. (1991) Inositol 1,4,5-trisphosphate 3-kinase distribution in the rat brain. High levels in the hippocampus CA1 pyramidal and cerebellar Purkinje cells suggest its involvement in some memory processes. Brain Res., 539, 203-210.
34. Mailleux, P., Takazawa, K., Albala, N., Erneux, C. and Vanderhaeghen, J.-J. (1992) Comparison of neuronal inositol 1,4,5-trisphosphate 3-kinase and receptor mRNA distributions in the human brain using in situ hybridization histochemistry. Neurosci. Lett., 137, 69-71.
35. + channels. Nature, 330, 653-655.
36. Roskoski, R., Jr (1979) Assays of protein kinase. Methods Enzymol., 99, 3-6.
37. 2+/calmodulin-dependent protein kinase. Neurochem. Res., 18, 65-77.
38. Schulman, H., Hanson, P.I. and Meyer, T. (1992) Decoding calcium signals by multifunctional CaM kinase. Cell Calcium, 13, 401-411.
39. Sim, S.S., Kim, J.W. and Rhee, S.G. (1990) Regulation of D-myo-inositol 1,4,5-trisphosphate 3-kinase by cAMP-dependent protein kinase and protein kinase C. J. Biol. Chem., 265, 10367-10372.
40. Soderling, T.R. (1990) Protein kinases. Regulation by autoinhibitory domains. J. Biol. Chem., 265, 1823-1826.
41. Takazawa, K. and Erneux, C. (1991) Identification of residues essential for catalysis and binding of calmodulin in rat brain inositol 1,4,5-trisphosphate 3-kinase. Biochem. J., 280, 125-129.
42. 2+/ calmodulin-sensitive inositol 1,4,5-trisphosphate 3-kinase in rat and bovine brain tissues. Biochem. Biophys. Res. Commun., 153, 632-641.
43. Takazawa, K., Lemos, M., Delvaux, A., Lejeune, C. Dumont, J.E. and Erneux, C. (1990a). Rat brain inositol 1,4,5-trisphosphate 3-kinase. Biochem. J., 268, 213-217.
44. 2+/calmodulin-sensitive inositol 1,4,5-trisphosphate 3-kinase. Biochem. J., 272, 107-112.
45. Takazawa, K., Perret, J., Dumont, J.E. and Erneux, C. (1991a) Molecular cloning and expression of a human brain inositol 1,4,5-trisphosphate 3-kinase. Biochem. Biophys. Res. Commun., 174, 529-535.
46. Takazawa, K., Perret, J., Dumont, J.E. and Erneux, C. (1991b) Molecular cloning and expression of a new putative inositol 1,4,5-trisphosphate 3-kinase isoenzyme. Biochem. J., 278, 883-886.
47. Thomas, S., Brake, B., Luzio, J.P. Stanley, K. and Banting, G. (1994) Isolation and sequence of a full length cDNA encoding a novel rat inositol 1,4,5-trisphosphate 3-kinase. Biochim. Biophys. Acta, 1220, 219-222.
48. 2+ in agonist-stimulated pancreatic acini of the rat. Biochem. J., 242, 289-292.
49. Tsubokawa, H., Oguro, K., Robinson, H.P.C., Masuzawa, T., Rhee, T.S.G., Takenawa T. and Kawai, N. (1994) Inositol 1,3,4,5-tetrakisphosphate as a mediator of neuronal death in ischemic hippocampus. Neurosci., 59, 291-297.
50. 4. Nature, 371, 711-714.
51. 3 3-kinase isoenzymes. Biochem. J., 306, 429-435.
52. Woodring, P.J. and Garrison, J.C. (1996) Transformation of Rat-1 fibroblasts with the v-src oncogene induces inositol 1,4,5-trisphosphate 3-kinase expression. Biochem. J., 319, 73-80.
53. Yamaguchi, K., Hirata, M. and Kuriyama, H. (1987) Calmodulin activates inositol 1,4,5-trisphosphate 3-kinase activity in pig aortic smooth muscle. Biochem. J., 244, 787-791.
54. Yan, C., Zhao, A.Z., Bentley, J.K. and Beavo, J.A. (1996) The calmodulin-dependent phosphodiesterase gene PDE1C encodes several functionally different splice variants in a tissue-specific manner. J. Biol. Chem., 271, 25699-25706.
55. Zilberman, Y., Howe, L.R., Moore, J.P., Hesketh, T.R. and Metcalfe, J.C. (1987) Calcium regulates inositol 1,3,4,5-tetrakisphosphate production in lysed thymocytes and in intact cells stimulated with concanavalin A. EMBO J., 6, 957-962.