Home LiteratureArticle Details
PMID: 8947491 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Phosphorylation and activation of p42 and p44 mitogen-activated protein kinase are required for the P2 purinoceptor stimulation of endothelial prostacyclin production.

The Biochemical journal ·Vol. 320 ( Pt 1) ·1996-11-15 ·Pages 221-6

Patel V, Brown C, Goodwin A, Wilkie N, Boarder MR

Abstract

Extracellular ATP and ADP, released from platelets and other sites stimulate the endothelial production of prostacyclin (PGI2) by acting on G-protein-coupled P2Y2 and P2Y2 purinoceptors, contributing to the maintenance of a non-thrombogenic surface. The mechanism, widely described as being dependent on elevated cytosolic [Ca2+], also requires protein tyrosine phosphorylation. Here we show that activation of both these P2 receptor types leads to the tyrosine phosphorylation and activation of both the p42 and p44 forms of mitogen-activated protein kinase (MAPK). 2-Methylthio-ATP and UTP, selectively activating P2Y1 and P2Y2 purinoceptors respectively, and ATP, a non-selective agonist at these two receptors, stimulate the tyrosine phosphorylation of both p42mapk and p44mapk, as revealed by Western blots with an antiserum specific for the tyrosine-phosphorylated forms of the enzymes. By using separation on Resource Q columns, peptide kinase activity associated with the phosphorylated MAPK enzymes distributes into two peaks, one mainly p42mapk and one mainly p44mapk, both of which are stimulated by ATP with respect to kinase activity and phospho-MAPK immunoreactivity. Stimulation of P2Y1 or P2Y2 purinoceptors leads to a severalfold increase in PGI2 efflux; this was blocked in a dose-dependent manner by the selective MAPK kinase inhibitor PD98059. This drug also blocked the agonist-stimulated increase in phospho-MAPK immunoreactivity for both p42mapk and p44mapk but left the phospholipase C response to P2 agonists essentially unchanged. Olomoucine has been reported to inhibit p44mapk activity. Here we show that in the same concentration range olomoucine inhibits activity in both peaks from the Resource Q column and also the agonist stimulation of 6-keto-PGF1, but has no effect on agonist-stimulated phospho-MAPK immunoreactivity. These results provide direct evidence for the involvement of p42 and p44 MAPK in the PGI2 response of intact endothelial cells: we have shown that both the endothelial P2Y purinoceptors are linked to activation of MAPK, and that activation of this pathway is a requirement for the stimulation by ATP/ADP of endothelial PGI2 production.

MeSH Terms
Adenosine Triphosphate/pharmacology Animals Blotting, Western Calcium-Calmodulin-Dependent Protein Kinases/antagonists & inhibitors,metabolism Cattle Cells, Cultured Chromatography, Ion Exchange Endothelium, Vascular/cytology,drug effects,metabolism Enzyme Activation Enzyme Inhibitors/pharmacology Epoprostenol/biosynthesis Flavonoids/pharmacology Kinetin Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinase 3 Mitogen-Activated Protein Kinases Phosphorylation Protein-Tyrosine Kinases/antagonists & inhibitors,metabolism Purines/pharmacology Receptors, Purinergic P2/metabolism Type C Phospholipases/metabolism
Chemicals
Enzyme Inhibitors Flavonoids Purines Receptors, Purinergic P2 olomoucine Adenosine Triphosphate Epoprostenol Protein-Tyrosine Kinases Calcium-Calmodulin-Dependent Protein Kinases Mitogen-Activated Protein Kinase 1 Mitogen-Activated Protein Kinase 3 Mitogen-Activated Protein Kinases Type C Phospholipases Kinetin 2-(2-amino-3-methoxyphenyl)-4H-1-benzopyran-4-one
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Patel V
Department of Cell Physiology and Pharmacology, University of Leicester, U.K.
Brown C
Goodwin A
Wilkie N
Boarder M R
References (41)
41 references, click to expand
  1. Dual effect of beta-adrenergic receptors on mitogen-activated protein kinase. Evidence for a beta gamma-dependent activation and a G alpha s-cAMP-mediated inhibition.
    J Biol Chem. 1995 Oct 20;270(42):25259-65 PMID: 7559665
  2. Stimulation by the nucleotides, ATP and UTP of mitogen-activated protein kinase in EAhy 926 endothelial cells.
    Br J Pharmacol. 1996 Mar;117(6):1341-7 PMID: 8882634
  3. PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo.
    J Biol Chem. 1995 Nov 17;270(46):27489-94 PMID: 7499206
  4. Calcium-mediated translocation of cytosolic phospholipase A2 to the nuclear envelope and endoplasmic reticulum.
    J Biol Chem. 1995 Dec 22;270(51):30749-54 PMID: 8530515
  5. Maximal epidermal growth-factor-induced cytosolic phospholipase A2 activation in vivo requires phosphorylation followed by an increased intracellular calcium concentration.
    Biochem J. 1996 Jan 1;313 ( Pt 1):91-6 PMID: 8546715
  6. Evidence for requirement of tyrosine phosphorylation in endothelial P2Y- and P2U- purinoceptor stimulation of prostacyclin release.
    Br J Pharmacol. 1995 Nov;116(6):2563-8 PMID: 8590971
  7. Inhibition of MAP kinase kinase (MEK) blocks endothelial PGI2 release but has no effect on von Willebrand factor secretion or E-selectin expression.
    FEBS Lett. 1996 Jun 17;388(2-3):180-4 PMID: 8690082
  8. Culture of arterial endothelial cells: characterization and growth of bovine aortic cells.
    Thromb Diath Haemorrh. 1975 Dec 15;34(3):825-39 PMID: 174237
  9. Stimulation of prostaglandin production through purinoceptors on cultured porcine endothelial cells.
    Biochem J. 1983 Jul 15;214(1):273-6 PMID: 6311177
  10. Characteristics of the P2 purinoceptor that mediates prostacyclin production by pig aortic endothelial cells.
    Eur J Pharmacol. 1987 Feb 10;134(2):199-209 PMID: 3552706
  11. Ca2+-dependent and Ca2+-independent pathways for release of arachidonic acid from phosphatidylinositol in endothelial cells.
    J Biol Chem. 1987 Sep 25;262(27):13086-92 PMID: 3115976
  12. Regulation of P2y-purinoceptor-mediated prostacyclin release from human endothelial cells by cytoplasmic calcium concentration.
    Br J Pharmacol. 1988 Dec;95(4):1181-90 PMID: 3064854
  13. Protein kinase C activation alters the sensitivity of agonist-stimulated endothelial-cell prostacyclin production to intracellular Ca2+.
    Biochem J. 1989 Sep 1;262(2):431-7 PMID: 2508628
  14. Enhancement of thrombin- and ionomycin-stimulated prostacyclin and platelet-activating factor production in cultured endothelial cells by a tumor-promoting phorbol ester.
    J Cell Physiol. 1990 Jun;143(3):596-605 PMID: 2113537
  15. Endothelin, vasopressin, and angiotensin II enhance tyrosine phosphorylation by protein kinase C-dependent and -independent pathways in glomerular mesangial cells.
    J Biol Chem. 1991 Apr 5;266(10):6650-6 PMID: 1706722
  16. Definition of a consensus sequence for peptide substrate recognition by p44mpk, the meiosis-activated myelin basic protein kinase.
    J Biol Chem. 1991 Aug 15;266(23):15180-4 PMID: 1907971
  17. A nucleotide receptor in vascular endothelial cells is specifically activated by the fully ionized forms of ATP and UTP.
    Biochem J. 1992 Jun 15;284 ( Pt 3):733-9 PMID: 1320376
  18. Cytosolic phospholipase A2 is coupled to hormonally regulated release of arachidonic acid.
    Proc Natl Acad Sci U S A. 1992 Jul 1;89(13):6147-51 PMID: 1631101
  19. Xenopus MAP kinase activator is a serine/threonine/tyrosine kinase activated by threonine phosphorylation.
    EMBO J. 1992 Aug;11(8):2903-8 PMID: 1322292
  20. The primary structure of MEK, a protein kinase that phosphorylates the ERK gene product.
    Science. 1992 Oct 16;258(5081):478-80 PMID: 1411546
  21. Phosphorylation and activation of a high molecular weight form of phospholipase A2 by p42 microtubule-associated protein 2 kinase and protein kinase C.
    J Biol Chem. 1993 Jan 25;268(3):1960-4 PMID: 8380583
  22. cPLA2 is phosphorylated and activated by MAP kinase.
    Cell. 1993 Jan 29;72(2):269-78 PMID: 8381049
  23. Heterogeneity of ATP receptors in aortic endothelial cells. Involvement of P2y and P2u receptors in inositol phosphate response.
    Circ Res. 1993 Mar;72(3):504-10 PMID: 8431980
  24. The regulation of aortic endothelial cells by purines and pyrimidines involves co-existing P2y-purinoceptors and nucleotide receptors linked to phospholipase C.
    Br J Pharmacol. 1993 Mar;108(3):689-93 PMID: 8467357
  25. Expression of a mutant Gi2 alpha subunit inhibits ATP and thrombin stimulation of cytoplasmic phospholipase A2-mediated arachidonic acid release independent of Ca2+ and mitogen-activated protein kinase regulation.
    J Biol Chem. 1994 Jan 21;269(3):1889-95 PMID: 8294438
  26. P2Y purinoceptor and nucleotide receptor-induced relaxation of precontracted bovine aortic collateral artery rings: differential sensitivity to suramin and indomethacin.
    J Pharmacol Exp Ther. 1994 Feb;268(2):881-7 PMID: 8114001
  27. Differential heterologous and homologous desensitization of two receptors for ATP (P2y purinoceptors and nucleotide receptors) coexisting on endothelial cells.
    Mol Pharmacol. 1994 Apr;45(4):731-6 PMID: 8183253
  28. Ras-dependent activation of MAP kinase pathway mediated by G-protein beta gamma subunits.
    Nature. 1994 Jun 2;369(6479):418-20 PMID: 8196770
  29. Differential regulation of inositol 1,4,5-trisphosphate by co-existing P2Y-purinoceptors and nucleotide receptors on bovine aortic endothelial cells.
    Br J Pharmacol. 1994 Mar;111(3):723-8 PMID: 8019751
  30. Inhibition of cyclin-dependent kinases by purine analogues.
    Eur J Biochem. 1994 Sep 1;224(2):771-86 PMID: 7925396
  31. Activation of cytosolic phospholipase A2 by basic fibroblast growth factor via a p42 mitogen-activated protein kinase-dependent phosphorylation pathway in endothelial cells.
    J Biol Chem. 1995 Feb 3;270(5):2360-6 PMID: 7836470
  32. Stimulation by extracellular ATP and UTP of the mitogen-activated protein kinase cascade and proliferation of rat renal mesangial cells.
    Br J Pharmacol. 1994 Dec;113(4):1455-63 PMID: 7889302
  33. Direct stimulation of Jak/STAT pathway by the angiotensin II AT1 receptor.
    Nature. 1995 May 18;375(6528):247-50 PMID: 7746328
  34. Inhibition of MAP kinase kinase blocks the differentiation of PC-12 cells induced by nerve growth factor.
    J Biol Chem. 1995 Jun 9;270(23):13585-8 PMID: 7775407
  35. G protein-coupled P2 purinoceptors: from molecular biology to functional responses.
    Trends Pharmacol Sci. 1995 Apr;16(4):133-9 PMID: 7610499
  36. G beta gamma subunits mediate mitogen-activated protein kinase activation by the tyrosine kinase insulin-like growth factor 1 receptor.
    J Biol Chem. 1995 Jul 14;270(28):16495-8 PMID: 7622449
  37. Signal transduction. Team blue sees red.
    Nature. 1995 Aug 31;376(6543):727-9 PMID: 7651531
  38. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions.
    Nature. 1995 Aug 31;376(6543):737-45 PMID: 7544443
  39. Receptor-tyrosine-kinase- and G beta gamma-mediated MAP kinase activation by a common signalling pathway.
    Nature. 1995 Aug 31;376(6543):781-4 PMID: 7651538
  40. Protein kinase C isoforms in bovine aortic endothelial cells: role in regulation of P2Y- and P2U-purinoceptor-stimulated prostacyclin release.
    Br J Pharmacol. 1996 May;118(1):123-30 PMID: 8733584
  41. The activation of distinct mitogen-activated protein kinase cascades is required for the stimulation of 2-deoxyglucose uptake by interleukin-1 and insulin-like growth factor-1 in KB cells.
    Biochem J. 1995 Nov 1;311 ( Pt 3):735-8 PMID: 7487926
Article Info
Journal
The Biochemical journal
Abbr.
Biochem J
ISSN
0264-6021
Published
1996-11-15
Pages
221-6
Language
English
Region
England
NLM ID
2984726R
PMCID
PMC1217921
Subset
IM
Grants
Wellcome Trust · United Kingdom
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: [email protected]