Turkey Erythrocytes Possess a Membrane-associated Inositol 1,4,5-trisphosphate 3-kinase That is Activated by Ca2+ in the Presence of Calmodulin

Overview

Journal Biochem J

Specialty Biochemistry

Date 1987 Dec 1

PMID 2829830

Citations 21

Authors

A J Morris

C P Downes

T K Harden

R H Michell

Affiliations

Soon will be listed here.

Abstract

Turkey erythrocytes contain soluble and particulate kinase activities which catalyse the ATP-dependent phosphorylation of inositol 1,4,5-trisphosphate [Ins(1,4,5)P3]. The particle-bound activity accounts for approximately one-quarter of the total cellular Ins(1,4,5)P3 kinase, when assayed at a [Ca2+] of 10 nM. The particle-bound Ins(1,4,5)P3 kinase is not washed from the membrane by 0.6 M-KCl, yet may be solubilized by a variety of detergents. This suggests that it is an intrinsic membrane protein. The product of the membrane-bound Ins(1,4,5)P3 kinase is inositol 1,3,4,5-tetrakisphosphate [Ins(1,3,4,5)P4], identifying the enzyme as an Ins(1,4,5)P3 3-kinase. In the presence of calmodulin, the membrane-associated Ins(1,4,5)P3 3-kinase is activated as [Ca2+] is increased over the range 0.2-1.0 microM. Under these conditions, the rates of dephosphorylation of Ins(1,3,4,5)P4 and Ins(1,4,5)P3 by phosphatases in the membrane fraction are unchanged.

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References

Beam K, Alper S, Palade G, Greengard P . Hormonally regulated phosphoprotein of turkey erythrocytes: localization to plasma membrane. J Cell Biol. 1979; 83(1):1-15. PMC: 2110436. DOI: 10.1083/jcb.83.1.1. View

Bradford M . A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976; 72:248-54. DOI: 10.1016/0003-2697(76)90527-3. View

Downes C, Mussat M, Michell R . The inositol trisphosphate phosphomonoesterase of the human erythrocyte membrane. Biochem J. 1982; 203(1):169-77. PMC: 1158207. DOI: 10.1042/bj2030169. View

Tsien R, Pozzan T, Rink T . Calcium homeostasis in intact lymphocytes: cytoplasmic free calcium monitored with a new, intracellularly trapped fluorescent indicator. J Cell Biol. 1982; 94(2):325-34. PMC: 2112871. DOI: 10.1083/jcb.94.2.325. View

Sharps E, MCCARL R . A high-performance liquid chromatographic method to measure 32P incorporation into phosphorylated metabolites in cultured cells. Anal Biochem. 1982; 124(2):421-4. DOI: 10.1016/0003-2697(82)90059-8. View

NISHIZUKA Y . The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature. 1984; 308(5961):693-8. DOI: 10.1038/308693a0. View

Berridge M, Irvine R . Inositol trisphosphate, a novel second messenger in cellular signal transduction. Nature. 1984; 312(5992):315-21. DOI: 10.1038/312315a0. View

Storey D, Shears S, Kirk C, Michell R . Stepwise enzymatic dephosphorylation of inositol 1,4,5-trisphosphate to inositol in liver. Nature. 1984; 312(5992):374-6. DOI: 10.1038/312374a0. View

Batty I, Nahorski S, Irvine R . Rapid formation of inositol 1,3,4,5-tetrakisphosphate following muscarinic receptor stimulation of rat cerebral cortical slices. Biochem J. 1985; 232(1):211-5. PMC: 1152860. DOI: 10.1042/bj2320211. View

10.

Irvine R, Letcher A, Heslop J, Berridge M . The inositol tris/tetrakisphosphate pathway--demonstration of Ins(1,4,5)P3 3-kinase activity in animal tissues. Nature. 1986; 320(6063):631-4. DOI: 10.1038/320631a0. View

11.

Hansen C, Mah S, Williamson J . Formation and metabolism of inositol 1,3,4,5-tetrakisphosphate in liver. J Biol Chem. 1986; 261(18):8100-3. View

12.

Biden T, Wollheim C . Ca2+ regulates the inositol tris/tetrakisphosphate pathway in intact and broken preparations of insulin-secreting RINm5F cells. J Biol Chem. 1986; 261(26):11931-4. View

13.

Cerdan S, Hansen C, JOHANSON R, Inubushi T, Williamson J . Nuclear magnetic resonance spectroscopic analysis of myo-inositol phosphates including inositol 1,3,4,5-tetrakisphosphate. J Biol Chem. 1986; 261(31):14676-80. View

14.

Downes C, Hawkins P, Irvine R . Inositol 1,3,4,5-tetrakisphosphate and not phosphatidylinositol 3,4-bisphosphate is the probable precursor of inositol 1,3,4-trisphosphate in agonist-stimulated parotid gland. Biochem J. 1986; 238(2):501-6. PMC: 1147162. DOI: 10.1042/bj2380501. View

15.

Hawkins P, Stephens L, Downes C . Rapid formation of inositol 1,3,4,5-tetrakisphosphate and inositol 1,3,4-trisphosphate in rat parotid glands may both result indirectly from receptor-stimulated release of inositol 1,4,5-trisphosphate from phosphatidylinositol 4,5-bisphosphate. Biochem J. 1986; 238(2):507-16. PMC: 1147163. DOI: 10.1042/bj2380507. View

16.

Connolly T, Bansal V, Bross T, Irvine R, MAJERUS P . The metabolism of tris- and tetraphosphates of inositol by 5-phosphomonoesterase and 3-kinase enzymes. J Biol Chem. 1987; 262(5):2146-9. View

17.

Irvine R, Moor R . Micro-injection of inositol 1,3,4,5-tetrakisphosphate activates sea urchin eggs by a mechanism dependent on external Ca2+. Biochem J. 1986; 240(3):917-20. PMC: 1147508. DOI: 10.1042/bj2400917. View

18.

Harden T, Stephens L, Hawkins P, Downes C . Turkey erythrocyte membranes as a model for regulation of phospholipase C by guanine nucleotides. J Biol Chem. 1987; 262(19):9057-61. View

19.

Biden T, Comte M, Cox J, Wollheim C . Calcium-calmodulin stimulates inositol 1,4,5-trisphosphate kinase activity from insulin-secreting RINm5F cells. J Biol Chem. 1987; 262(20):9437-40. View

20.

Shears S, PARRY J, Tang E, Irvine R, Michell R, Kirk C . Metabolism of D-myo-inositol 1,3,4,5-tetrakisphosphate by rat liver, including the synthesis of a novel isomer of myo-inositol tetrakisphosphate. Biochem J. 1987; 246(1):139-47. PMC: 1148250. DOI: 10.1042/bj2460139. View