Home LiteratureArticle Details
PMID: 2543370 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Activation of NADPH oxidase by purine and pyrimidine nucleotides involves G proteins and is potentiated by chemotactic peptides.

The Biochemical journal ·Vol. 259 ·No. 3 ·1989-05-01 ·Pages 813-9

Seifert R, Burde R, Schultz G

Abstract

Human neutrophils and HL-60 leukaemic cells possess an NADPH oxidase which catalyses superoxide (O2-) formation and is activated by the chemotactic peptide, N-formyl-L-methionyl-L-leucyl-L-phenylalanine (fMet-Leu-Phe). In dibutyryl cyclic AMP-differentiated HL-60 cells, ATP and UTP in the presence of cytochalasin B activated O2- formation with EC50 values of 5 microM and efficacies amounting to 30% of that of fMet-Leu-Phe. The potency order of purine nucleotides in activating O2- generation was ATP = adenosine 5'-O-(3-thiotriphosphate) greater than ITP greater than dATP = ADP. Pyrimidine nucleotides activated NADPH oxidase in the potency order UTP greater than dUTP greater than CTP = TTP = UDP. Pertussis toxin completely prevented activation of NADPH oxidase by fMet-Leu-Phe and UTP, whereas the effect of ATP was only partially inhibited. ATP and UTP enhanced O2- generation induced by fMet-Leu-Phe by up to 8-fold, and primed the cells to respond to non-stimulatory concentrations of fMet-Leu-Phe. Activation of NADPH oxidase by UTP but not by ATP was inhibited by various activators of adenylate cyclase. In dimethyl sulphoxide-differentiated HL-60 cells and in human neutrophils, ATP and UTP per se did not activate NADPH oxidase, but they potentiated the effect of fMet-Leu-Phe. Our results suggest that purine and pyrimidine nucleotides act via purino- and novel pyrimidinoceptors respectively, which are coupled to guanine nucleotide-binding proteins leading to the activation of NADPH oxidase. As ATP and UTP are released from cells under physiological and pathological conditions, these nucleotides may play roles as intercellular signal molecules in the activation of O2- formation.

MeSH Terms
Adenosine Triphosphate/pharmacology Bucladesine Enzyme Activation/drug effects GTP-Binding Proteins/physiology Humans N-Formylmethionine Leucyl-Phenylalanine/pharmacology NADH, NADPH Oxidoreductases/metabolism NADPH Oxidases Neutrophils/drug effects,enzymology Superoxides/metabolism Tumor Cells, Cultured/drug effects,enzymology Uracil Nucleotides/pharmacology Uridine Triphosphate/pharmacology
Chemicals
Uracil Nucleotides Superoxides N-Formylmethionine Leucyl-Phenylalanine Bucladesine Adenosine Triphosphate NADH, NADPH Oxidoreductases NADPH Oxidases GTP-Binding Proteins Uridine Triphosphate
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Seifert R
Institut für Pharmakologie, Freie Universität Berlin, Federal Republic of Germany.
Burde R
Schultz G
References (35)
35 references, click to expand
  1. Intracellular Ca2+ mobilization activated by extracellular ATP in Ehrlich ascites tumor cells.
    J Biol Chem. 1985 Sep 5;260(19):10653-61 PMID: 4030763
  2. Receptor-specific threshold effects of cyclic AMP are involved in the regulation of enzyme release and superoxide production from human neutrophils.
    Biochim Biophys Acta. 1985 Aug 30;846(2):286-95 PMID: 2411298
  3. Factors influencing platelet function: adhesion, release, and aggregation.
    Pharmacol Rev. 1970 Jun;22(2):97-187 PMID: 4192958
  4. Adenine-, guanine- and uridine-5'-phosphonucleotides in blood platelets and storage organelles of various species.
    J Pharmacol Exp Ther. 1971 Jul;178(1):210-5 PMID: 5087398
  5. Inhibition by islet-activating protein of a chemotactic peptide-induced early breakdown of inositol phospholipids and Ca2+ mobilization in guinea pig neutrophils.
    J Biol Chem. 1985 Dec 15;260(29):15771-80 PMID: 2999136
  6. A pertussis toxin-sensitive GTP-binding protein in the human neutrophil regulates multiple receptors, calcium mobilization, and lectin-induced capping.
    Proc Natl Acad Sci U S A. 1985 Dec;82(24):8643-7 PMID: 3001714
  7. Extracellular ATP: effects, sources and fate.
    Biochem J. 1986 Jan 15;233(2):309-19 PMID: 3006665
  8. Guanine nucleotides stimulate NADPH oxidase in membranes of human neutrophils.
    FEBS Lett. 1986 Sep 1;205(1):161-5 PMID: 3017756
  9. Receptor-cytoskeleton interactions and membrane traffic may regulate chemoattractant-induced superoxide production in human granulocytes.
    J Biol Chem. 1986 Oct 15;261(29):13662-9 PMID: 3020040
  10. The O2- -forming NADPH oxidase of the phagocytes: nature, mechanisms of activation and function.
    Biochim Biophys Acta. 1986 Nov 4;853(1):65-89 PMID: 3021215
  11. Regulation of neutrophil NADPH oxidase activation in a cell-free system by guanine nucleotides and fluoride. Evidence for participation of a pertussis and cholera toxin-insensitive G protein.
    J Biol Chem. 1987 Feb 5;262(4):1685-90 PMID: 3027097
  12. Fatty-acid-induced activation of NADPH oxidase in plasma membranes of human neutrophils depends on neutrophil cytosol and is potentiated by stable guanine nucleotides.
    Eur J Biochem. 1987 Feb 2;162(3):563-9 PMID: 3549290
  13. Purification and immunochemical characterization of the major pertussis-toxin-sensitive guanine-nucleotide-binding protein of bovine-neutrophil membranes.
    Eur J Biochem. 1987 May 15;165(1):185-94 PMID: 3106040
  14. Role of a guanine nucleotide regulatory protein in the activation of phospholipase C by different chemoattractants.
    J Immunol. 1987 Jun 15;138(12):4374-80 PMID: 3108387
  15. Endothelium-dependent relaxation by uridine tri- and diphosphate in isolated human pial vessels.
    Blood Vessels. 1987;24(3):150-5 PMID: 3593977
  16. Adenosine triphosphate stimulates inositol phospholipid metabolism and prostacyclin formation in adrenal medullary endothelial cells by means of P2-purinergic receptors.
    Proc Natl Acad Sci U S A. 1987 Aug;84(16):5630-4 PMID: 3039498
  17. G proteins: transducers of receptor-generated signals.
    Annu Rev Biochem. 1987;56:615-49 PMID: 3113327
  18. Reversible activation of NADPH oxidase in membranes of HL-60 human leukemic cells.
    Biochem Biophys Res Commun. 1987 Aug 14;146(3):1296-302 PMID: 3113431
  19. Actions of extracellular UTP and ATP in perfused rat liver. A comparative study.
    Eur J Biochem. 1987 Aug 17;167(1):65-71 PMID: 3622510
  20. P2-purinergic receptors are coupled to two signal transduction systems leading to inhibition of cAMP generation and to production of inositol trisphosphate in rat hepatocytes.
    J Biol Chem. 1987 Oct 5;262(28):13483-90 PMID: 2443492
  21. P2Y-purinoceptor regulation of surfactant secretion from rat isolated alveolar type II cells is associated with mobilization of intracellular calcium.
    Br J Pharmacol. 1987 Aug;91(4):833-8 PMID: 3664080
  22. The effect of six prostaglandins, prostacyclin and iloprost on generation of superoxide anions by human polymorphonuclear leukocytes stimulated by zymosan or formyl-methionyl-leucyl-phenylalanine.
    Biochem Pharmacol. 1987 Dec 15;36(24):4209-13 PMID: 2446631
  23. Evidence for a vasoconstriction-mediating receptor for UTP, distinct from the P2 purinoceptor, in rabbit ear artery.
    Naunyn Schmiedebergs Arch Pharmacol. 1987 Nov;336(5):556-60 PMID: 3437923
  24. ATP induces transient elevations of [Ca2+]i in human neutrophils and primes these cells for enhanced O2- generation.
    Lab Invest. 1988 Apr;58(4):448-53 PMID: 2833660
  25. Studies with protein kinase C inhibitors presently available cannot elucidate the role of protein kinase C in the activation of NADPH oxidase.
    Biochem Biophys Res Commun. 1988 Apr 29;152(2):585-92 PMID: 2835037
  26. Different sensitivities of the responses of human neutrophils stimulated with immune complex and C5a anaphylatoxin to pertussis toxin.
    FEBS Lett. 1988 Jul 4;234(1):231-4 PMID: 2839363
  27. The role of nucleoside-diphosphate kinase reactions in G protein activation of NADPH oxidase by guanine and adenine nucleotides.
    Eur J Biochem. 1988 Jul 15;175(1):51-5 PMID: 2841126
  28. Cyclic nucleotide-induced maturation of human promyelocytic leukemia cells.
    J Clin Invest. 1982 Nov;70(5):953-64 PMID: 6290539
  29. Mechanisms of the contractile effect induced by uridine 5-triphosphate in canine cerebral arteries.
    Stroke. 1983 May-Jun;14(3):347-55 PMID: 6658902
  30. Activation of the human neutrophil respiratory burst with zymosan-activated serum.
    Biochem Biophys Res Commun. 1984 Jun 15;121(2):695-701 PMID: 6329209
  31. Stimulus response coupling in the human neutrophil. Differential requirements for receptor occupancy in neutrophil responses to a chemoattractant.
    J Biol Chem. 1984 Jun 25;259(12):7439-45 PMID: 6330057
  32. Mechanisms of regulating the respiratory burst in leukocytes.
    Contemp Top Immunobiol. 1984;14:247-81 PMID: 6088173
  33. Inhibition of receptor-mediated release of arachidonic acid by pertussis toxin.
    Cell. 1984 Dec;39(2 Pt 1):301-8 PMID: 6094010
  34. Adenosine; a physiologic modulator of superoxide anion generation by human neutrophils. Adenosine acts via an A2 receptor on human neutrophils.
    J Immunol. 1985 Aug;135(2):1366-71 PMID: 2989364
  35. Is there a basis for distinguishing two types of P2-purinoceptor?
    Gen Pharmacol. 1985;16(5):433-40 PMID: 2996968
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1989-05-01
Pages
813-9
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1138590
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com