Inhibition of Inositol 1,4,5-trisphosphate-induced Ca2+ Release by CAMP-dependent Protein Kinase in a Living Cell

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 1998 Mar 21

PMID 9465064

Citations 26

Authors

S Tertyshnikova

A Fein

Affiliations

Soon will be listed here.

Abstract

Interaction of intracellular free calcium ([Ca2+]i) and cAMP signaling mechanisms was examined in intact single megakaryocytes by using a combination of single-cell fluorescence microscopy to measure [Ca2+]i and flash photolysis of caged Ca2+, inositol 1,4, 5-trisphosphate (IP3), or cAMP to elevate rapidly the concentration of these compounds inside the cell. Photolysis of caged IP3 stimulated Ca2+ release from an IP3-sensitive store. The cAMP-elevating agent carbacyclin inhibited this IP3-induced rise in [Ca2+]i but did not affect the rate of Ca2+ removal from the cytoplasm after photolysis of caged Ca2+. Photolysis of caged cAMP during ADP-induced [Ca2+]i oscillations caused the [Ca2+]i oscillation to transiently cease without affecting the rate of Ca2+ uptake and/or extrusion. We conclude that the principal mechanism of cAMP-dependent inhibition of Ca2+ mobilization in megakaryocytes appears to be by inhibition of IP3-induced Ca2+ release and not by stimulation of Ca2+ removal from the cytoplasm. Two inhibitors of cAMP-dependent protein kinase, a specific peptide inhibitor of the catalytic subunit of cAMP protein kinase and KT5720, blocked the inhibitory effect of carbacyclin, indicating that the inhibition of IP3-induced Ca2+-release by carbacyclin is mediated by cAMP-dependent protein kinase.

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References

Ferris C, Cameron A, Bredt D, Huganir R, Snyder S . Inositol 1,4,5-trisphosphate receptor is phosphorylated by cyclic AMP-dependent protein kinase at serines 1755 and 1589. Biochem Biophys Res Commun. 1991; 175(1):192-8. DOI: 10.1016/s0006-291x(05)81219-7. View

Sudhof T, Newton C, Archer 3rd B, Ushkaryov Y, Mignery G . Structure of a novel InsP3 receptor. EMBO J. 1991; 10(11):3199-206. PMC: 453043. DOI: 10.1002/j.1460-2075.1991.tb04882.x. View

Nakade S, Rhee S, Hamanaka H, Mikoshiba K . Cyclic AMP-dependent phosphorylation of an immunoaffinity-purified homotetrameric inositol 1,4,5-trisphosphate receptor (type I) increases Ca2+ flux in reconstituted lipid vesicles. J Biol Chem. 1994; 269(9):6735-42. View

Kase H, Iwahashi K, Nakanishi S, Matsuda Y, Yamada K, Takahashi M . K-252 compounds, novel and potent inhibitors of protein kinase C and cyclic nucleotide-dependent protein kinases. Biochem Biophys Res Commun. 1987; 142(2):436-40. DOI: 10.1016/0006-291x(87)90293-2. View

Feinstein M, Egan J, Shaafi R, White J . The cytoplasmic concentration of free calcium in platelets is controlled by stimulators of cyclic AMP production (PGD2, PGE1, forskolin). Biochem Biophys Res Commun. 1983; 113(2):598-604. DOI: 10.1016/0006-291x(83)91768-0. View

Ferris C, Cameron A, Huganir R, Snyder S . Quantal calcium release by purified reconstituted inositol 1,4,5-trisphosphate receptors. Nature. 1992; 356(6367):350-2. DOI: 10.1038/356350a0. View

Whittle B, Moncada S, Whiting F, Vane J . Carbacyclin--a potent stable prostacyclin analogue for the inhibition of platelet aggregation. Prostaglandins. 1980; 19(4):605-27. DOI: 10.1016/s0090-6980(80)80010-4. View

Marrero I, Cobbold P . Different modulatory effects of elevated cyclic AMP on cytosolic Ca2+ spikes induced by phenylephrine or vasopressin in single rat hepatocytes. Biochem J. 1993; 291 ( Pt 1):163-8. PMC: 1132496. DOI: 10.1042/bj2910163. View

Fischer T, White 2nd G . cAMP-dependent protein kinase substrates in platelets. Evidence that thrombolamban, a 22,000 dalton substrate, and the Ca++-ATPase are not associated proteins. Biochem Biophys Res Commun. 1989; 159(2):644-50. DOI: 10.1016/0006-291x(89)90043-0. View

10.

Supattapone S, Danoff S, Theibert A, Joseph S, Steiner J, Snyder S . Cyclic AMP-dependent phosphorylation of a brain inositol trisphosphate receptor decreases its release of calcium. Proc Natl Acad Sci U S A. 1988; 85(22):8747-50. PMC: 282538. DOI: 10.1073/pnas.85.22.8747. View

11.

Enouf J, Bredoux R, Papp B, Djaffar I, Lompre A, Kieffer N . Human platelets express the SERCA2-b isoform of Ca(2+)-transport ATPase. Biochem J. 1992; 286 ( Pt 1):135-40. PMC: 1133029. DOI: 10.1042/bj2860135. View

12.

Quinton T, Brown K, Dean W . Inositol 1,4,5-trisphosphate-mediated Ca2+ release from platelet internal membranes is regulated by differential phosphorylation. Biochemistry. 1996; 35(21):6865-71. DOI: 10.1021/bi960128m. View

13.

Joseph S, Ryan S . Phosphorylation of the inositol trisphosphate receptor in isolated rat hepatocytes. J Biol Chem. 1993; 268(31):23059-65. View

14.

Tertyshnikova S, Fein A . [Ca2+]i oscillations and [Ca2+]i waves in rat megakaryocytes. Cell Calcium. 1997; 21(5):331-44. DOI: 10.1016/s0143-4160(97)90026-9. View

15.

DAndrea P, Paschini V, Vittur F . Dual mechanism for cAMP-dependent modulation of Ca2+ signalling in articular chondrocytes. Biochem J. 1996; 318 ( Pt 2):569-73. PMC: 1217658. DOI: 10.1042/bj3180569. View

16.

Kapural L, Fein A . Changes in the expression of voltage-gated K+ currents during development of human megakaryocytic cells. Biochim Biophys Acta. 1997; 1326(2):319-28. DOI: 10.1016/s0005-2736(97)00035-7. View

17.

KASER-GLANZMANN R, Jakabova M, George J, LUSCHER E . Stimulation of calcium uptake in platelet membrane vesicles by adenosine 3',5'-cyclic monophosphate and protein kinase. Biochim Biophys Acta. 1977; 466(3):429-40. DOI: 10.1016/0005-2736(77)90336-4. View

18.

Sage S, Rink T . The kinetics of changes in intracellular calcium concentration in fura-2-loaded human platelets. J Biol Chem. 1987; 262(34):16364-9. View

19.

Uneyama H, Uneyama C, Akaike N . Intracellular mechanisms of cytoplasmic Ca2+ oscillation in rat megakaryocyte. J Biol Chem. 1993; 268(1):168-74. View

20.

Teixeira M, Gristwood R, Cooper N, Hellewell P . Phosphodiesterase (PDE)4 inhibitors: anti-inflammatory drugs of the future?. Trends Pharmacol Sci. 1997; 18(5):164-71. DOI: 10.1016/s0165-6147(97)01049-3. View