Abstract
The susceptibility of purified protein kinase C to oxidative inactivation by H2O2 was found to be increased by Ca2+ either alone at a high (5 mM) concentration or at a low (approximately 50 microM) concentration along with phosphatidylserine and diacylglycerol and by tumor-promoting phorbol esters even in the absence of Ca2+. This suggested that the membrane-bound and/or catalytically active form of protein kinase C is relatively more susceptible to oxidative inactivation. Although both the regulatory and catalytic domains of protein kinase C were susceptible to oxidative inactivation, a selective modification of the regulatory domain was obtained under mild oxidative conditions by protecting the catalytic site with ATP/Mg2+. Under these conditions there was a loss of both phorbol ester binding and Ca2+/phospholipid-stimulated kinase activity. However, this modified form of enzyme exhibited an increase in Ca2+/phospholipid-independent kinase activity. This suggests that selective oxidative modification of the regulatory domain may negate the requirement for Ca2+ and lipids for activation. Treatment of intact C6 glioma or B16 melanoma cells with H2O2 resulted in a time- and temperature-dependent decrease in Ca2+/phospholipid-dependent protein kinase C activity along with a concomitant transient increase in an oxidatively modified isoform of protein kinase C that exhibited activity in the absence of Ca2+ and phospholipids. Since protein kinase C can initially be activated by mild oxidative modification and subsequently inactivated by further oxidation, this dual activation-inactivation of protein kinase C in response to H2O2 suggests an effective on/off signal mechanism to influence cellular events.
MeSH Terms
Animals
Brain/enzymology
Calcium/pharmacology
Cattle
Cell Line
Egtazic Acid/pharmacology
Enzyme Activation
Glioma
Hydrogen Peroxide/pharmacology
Kinetics
Phorbol 12,13-Dibutyrate/pharmacology
Phosphatidylserines/pharmacology
Protein Kinase C/isolation & purification,metabolism
Signal Transduction
Tetradecanoylphorbol Acetate/pharmacology
Chemicals
Phosphatidylserines
Phorbol 12,13-Dibutyrate
Egtazic Acid
Hydrogen Peroxide
Protein Kinase C
Tetradecanoylphorbol Acetate
Calcium
Authors & Affiliations
2 authors, click to expand affiliations / ORCID
Gopalakrishna R
Department of Pathology, School of Medicine, University of California, Los Angeles 90024-1732.
Anderson W B
References (26)
26 references, click to expand
-
Binding to erythrocyte membrane is the physiological mechanism for activation of Ca2+-dependent neutral proteinase.
Biochem Biophys Res Commun. 1985 Apr 16;128(1):331-8
PMID: 2985077
-
The effects of chemical modification of calmodulin on Ca2+-induced exposure of a hydrophobic region. Separation of active and inactive forms of calmodulin.
Biochim Biophys Acta. 1985 Feb 21;844(2):265-9
PMID: 3918583
-
Fate of immunoprecipitable protein kinase C in GH3 cells treated with phorbol 12-myristate 13-acetate.
J Biol Chem. 1985 Dec 5;260(28):15194-9
PMID: 3905792
-
Studies and perspectives of protein kinase C.
Science. 1986 Jul 18;233(4761):305-12
PMID: 3014651
-
Stimulation of tyrosine-specific protein phosphorylation in the rat liver plasma membrane by oxygen radicals.
Biochem Biophys Res Commun. 1986 Sep 14;139(2):439-45
PMID: 3767971
-
Factors influencing chelator-stable, detergent-extractable, phorbol diester-induced membrane association of protein kinase C. Differences between Ca2+-induced and phorbol ester-stabilized membrane bindings of protein kinase C.
J Biol Chem. 1986 Dec 15;261(35):16438-45
PMID: 3465725
-
Differential expression of multiple protein kinase C subspecies in rat central nervous tissue.
Biochem Biophys Res Commun. 1987 Sep 30;147(3):911-9
PMID: 3311046
-
Differential distribution of protein kinase C isozymes in the various regions of brain.
J Biol Chem. 1987 Nov 15;262(32):15714-20
PMID: 3119580
-
Role of insulin receptor phosphorylation in the insulinomimetic effects of hydrogen peroxide.
Proc Natl Acad Sci U S A. 1987 Nov;84(22):8115-9
PMID: 3317401
-
Susceptibility of protein kinase C to oxidative inactivation: loss of both phosphotransferase activity and phorbol diester binding.
FEBS Lett. 1987 Dec 10;225(1-2):233-7
PMID: 2826240
-
Tumor promoter-induced membrane-bound protein kinase C regulates hematogenous metastasis.
Proc Natl Acad Sci U S A. 1988 Jan;85(2):612-6
PMID: 3422445
-
Formation of hydroxyl radicals from hydrogen peroxide in the presence of iron. Is haemoglobin a biological Fenton reagent?
Biochem J. 1988 Jan 1;249(1):185-90
PMID: 3342006
-
Hydrogen peroxide stimulates tyrosine phosphorylation of the insulin receptor and its tyrosine kinase activity in intact cells.
Biochem J. 1988 Feb 15;250(1):95-101
PMID: 2833239
-
Protein kinases 1988: a current perspective.
FASEB J. 1988 Nov;2(14):2957-69
PMID: 2972578
-
Evidence for the involvement of sulfhydryl oxidation in the regulation of fat cell hexose transport by insulin.
Proc Natl Acad Sci U S A. 1974 Oct;71(10):4173-7
PMID: 4372610
-
Activation of soluble guanylate cyclase from rat lung by incubation or by hydrogen peroxide.
J Biol Chem. 1976 Dec 10;251(23):7304-12
PMID: 12160
-
Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues. II. Proenzyme and its activation by calcium-dependent protease from rat brain.
J Biol Chem. 1977 Nov 10;252(21):7610-6
PMID: 199594
-
Cell division in normal and transformed cells: the possible role of superoxide and hydrogen peroxide.
Med Hypotheses. 1981 Jan;7(1):21-42
PMID: 6259499
-
Turnover of bacterial glutamine synthetase: oxidative inactivation precedes proteolysis.
Proc Natl Acad Sci U S A. 1981 Apr;78(4):2120-4
PMID: 6113590
-
Stimulation of human polymorphonuclear leukocyte superoxide anion radical production by tumor promoters.
Cancer Lett. 1981 Jan;11(3):257-62
PMID: 6265062
-
Diminution of mouse epidermal superoxide dismutase and catalase activities by tumor promoters.
Carcinogenesis. 1981;2(11):1141-6
PMID: 7318151
-
Phorbol diester receptor copurifies with protein kinase C.
Proc Natl Acad Sci U S A. 1983 Jan;80(1):36-40
PMID: 6296873
-
Competitive inhibition by diacylglycerol of specific phorbol ester binding.
Proc Natl Acad Sci U S A. 1984 Jan;81(2):607-10
PMID: 6320198
-
A potential second messenger role for unsaturated fatty acids: activation of Ca2+-dependent protein kinase.
Science. 1984 May 11;224(4649):622-5
PMID: 6231726
-
Modulation of Ca2+-activated, phospholipid-dependent protein kinase in platelets treated with a tumor-promoting phorbol ester.
Biochem Biophys Res Commun. 1984 Jul 18;122(1):158-64
PMID: 6234894
-
Rapid purification of calcium-activated protease by calcium-dependent hydrophobic-interaction chromatography.
FEBS Lett. 1985 Jul 8;186(2):246-50
PMID: 2989008