Platelet 12-lipoxygenase activation via glycoprotein VI: Involvement of multiple signaling pathways in agonist control of H(P)ETE synthesis

Circulation Research

Volumn 94, Issue 12, 2004, Pages 1598-1605

  Coffey, Marcus J ^a   Jarvis, Gavin E ^b   Gibbins, Jonathan M ^c   Coles, Barbara ^a   Barrett, Natasha E ^c   Wylie, Oliver R E ^a   O'Donnell, Valerie B ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

Collagen; Collagen receptor glycoprotein VI; Lipoxygenase; Platelets

Indexed keywords

12 HYDROPEROXYICOSATETRAENOIC ACID; 12 HYDROXYICOSATETRAENOIC ACID; 15 HYDROXY 11ALPHA,9ALPHA EPOXYMETHANOPROSTA 5,13 DIENOIC ACID; 4 AMINO 5 (CHLOROPHENYL) 7 (TERT BUTYL)PYRAZOLO[3,4 D]PYRIMIDINE; ADENOSINE DIPHOSPHATE; ALPHA PENTYL 4 (2 QUINOLYLMETHOXY)BENZYL ALCOHOL; ARACHIDONATE 12 LIPOXYGENASE; CD31 ANTIGEN; COLLAGEN; COLLAGEN RECEPTOR; COLLAGEN RELATED PEPTIDE; EGTAZIC ACID; ETHYLENE GLYCOL 1,2 BIS(2 AMINOPHENYL) ETHER N,N,N',N' TETRAACETIC ACID; FC RECEPTOR; GLYCOPROTEIN; GLYCOPROTEIN VI; LIPID; PEPTIDE DERIVATIVE; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN TYROSINE KINASE; PROTEIN TYROSINE KINASE INHIBITOR; STAUROSPORINE; THROMBIN; THROMBOCYTE ENZYME; UNCLASSIFIED DRUG; WORTMANNIN;

ARTICLE; CALCIUM MOBILIZATION; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME INHIBITION; ENZYME LOCALIZATION; HUMAN; HUMAN CELL; IMMUNORECEPTOR BASED ACTIVATORY MOTIF; INFLAMMATION; MAMMAL; PRIORITY JOURNAL; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SYNTHESIS; VASCULAR DISEASE;

12-HYDROXY-5,8,10,14-EICOSATETRAENOIC ACID; 15-HYDROXY-11 ALPHA,9 ALPHA-(EPOXYMETHANO)PROSTA-5,13-DIENOIC ACID; ADENOSINE DIPHOSPHATE; AMINO ACID MOTIFS; ANTIGENS, CD31; ARACHIDONATE 12-LIPOXYGENASE; ARACHIDONIC ACID; BLOOD PLATELETS; CALCIMYCIN; CALCIUM SIGNALING; CARRIER PROTEINS; COLLAGEN; CYCLOOXYGENASE 1; EGTAZIC ACID; ENZYME ACTIVATION; ENZYME INHIBITORS; HUMANS; INFLAMMATION; ISOENZYMES; LEUKOTRIENES; MEMBRANE PROTEINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PEPTIDES; PHOSPHORYLATION; PLATELET ACTIVATION; PLATELET MEMBRANE GLYCOPROTEINS; PROSTAGLANDIN-ENDOPEROXIDE SYNTHASES; PROTEIN KINASE C; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; QUINOLINES; RECEPTORS, IGG; THROMBIN;

EID: 3042823695     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000132281.78948.65     Document Type: Article

References (59)

1. Taylor GW, Morris HR. Lipoxygenase pathways. Br Med Bull. 1983;39:219-222.
2. Kühn H, Belkner J, Zaiss S, Fährenklemper T, Wohfeil S, Involvement of 15-lipoxygenase in early stages of atherogenesis, J Exp Med. 1994;179:1903-1911,
3. Yla-Herttuala S, Rosenfeld ME, Parthasarathy S, Glass CK, Sigal E, Sarkioia T, Witztum, JT, Steinberg D. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. J Clin Invest. 1991;87:1146-1152.
4. Folcik VA, Nivar-Aristy RA, Krajewski LP, Cathcardt MK. Lipoxygenase contributes to the oxidation of lipids in human atherosclerotic plaques. J Clin Invest. 1995;96:504-510.
5. Belkner J, Stender H, Kühn H. The rabbit 15-lipoxygenase preferentially oxygenates LDL cholesterol esters, and this reaction does not require vitamin E. J Biol Chem. 1998;273:23225-23232.
6. Sendobry SM, Cornicelli JA, Welch K, Tait B, Trivedi BK, Colbry N, Dyer RD, Feinmark SJ, Daughtery A. Attenuation of diet-induced atherosclerosis in rabbits with a highly selective 15-lipoxygenase inhibitor lacking significant antioxidant properties. Br J Pharmacol. 1997;12: 1199-1206.
7. Bleich D, Chen S, Zipser B, Sun D, Funk CD, Nadler JL. Resistance to type 1 diabetes induction in 12-lipoxygenase knockout mice. J Clin Invest. 1999;103:1431-1436.
8. Cyrus T, Witztum JL, Rader DJ, Tangirala R, Fazio S, Linton MF, Funk CD. Disruption of the 12/15-lipoxygenase gene diminishes atherosclerosis in apo E-deficient mice. J Clin Invest. 1999;103:1597-1604.
9. Eynard AR, Tremoli E, Caruso D, Magni F, Sirtori CR, Galli G. Platelet formation of 12-hydroxyeicosatetraenoic acid and thromboxane B2 is increased in type IIA hypercholesterolemic subjects. Atherosclerosis. 1986;60:61-66.
10. Gonzalez-Nunez D, Claria J, Rivera F, Poch E. Increased levels of 12(S)-HETE in patients with essential hypertension. Hypertension. 2001; 37:334-338.
11. Kühn H, Thiele B. The diversity of the lipoxygenase family. Many sequence data but little information on biological significance. FEBS Lett. 1999;449:7-11.
12. Nie D, Hillman GG, Geddes T, Tang K, Pierson c, Grignon DJ, Honn KV. Platelet type 12-lipoxygenase regulates angiogenesis in human prostate carcinoma. Adv Exp Med Biol. 1999;469:623-630.
13. 5 integrin expression. Cancer Res. 2003;63:4258-4267.
14. Brinckmann R, Schnurr K, Heydeck D, Rosenbach T, Kolde G, Kühn H. Membrane translocation of 15-lipoxygenase in hematopoietic cells is calcium-dependent and activates the oxygenase activity of the enzyme. Blood. 1998;91:64-74.
15. Ozeki Y, Nagamura Y, Ito H, Unemi F, Kimura Y, Igawa T, Kambayashi J, Takahashi Y, Yoshimoto T. An anti-platelet agent, OPC-29030, inhibits translocation of 12-lipoxygenase and 12-hydroxyeicosatetraenoic acid production in human platelets. Br J Pharmacol. 1999;128:1699-16704.
16. Zhu H, Takahashi Y, Xu W, Kawajiri H, Murakami T, Yamamoto M, Iseki S, Iwasaki T, Hattori H, Yoshimoto T. Low density lipoprotein receptor-related protein-mediated membrane translocation of 12/15-lipoxygenase is required for oxidation of low density lipoprotein by macrophages. J Biol Chem. 2003;278:13350-13355.
17. Werz O, Burkert E, Samuelsson B, Radmark O, Steinhilber D. Activation of 5-lipoxygenase by cell stress is calcium independent in human polymorphonuclear leukocytes. Blood. 2002;99:1044-1052.
18. Brock TG, McNish RW, Bailie MB, Peters-Golden M. Rapid import of cytosolic 5-lipoxygenase into the nucleus of neutrophils after in vivo recruitment and in vitro adherence. J Biol Chem. 1997;272:8276-8280.
19. Werz O, Klemm J, Samuelsson B, Rådmark O. 5-lipoxygenase is phosphorylated by p38 kinase-dependent MAPKAP kinases. Proc Natl Acad Sci USA. 2000;97:5261-5266.
20. Lepley RA, Muskardin DT, Fitzpatrick FA. Tyrosine kinase activity modulates catalysis and translocation of cellular 5-lipoxygenase. J Biol Chem. 1996;271:6179-6184.
21. Miller YI, Chang MK, Funk CD, Feramisco JR, Witztum JL. 12/15-lipoxygenase translocation enhances site-specific actin polymerization in macrophages phagocytosing apoptotic cells. J Biol Chem. 2001;276: 19431-19439.
22. Pouliot M, McDonald PP, Krump E, Mancini JA, McColl SR, Weech PK, Borgeat P. Colocalization of cytosolic phospholipase A2, 5-lipoxygenase, and 5-lipoxygenase-activating protein at the nuclear membrane of A23187-stimulated human neutrophils. Eur J Biochem. 1996;238: 250-258.
23. Wijkander J, O'Flaherty JT, Nixon AB, Wykle RL. 5-Lipoxygenase products modulate the activity of the 85-kDa phospholipase A2 in human neutrophils. J Biol Chem. 1995;270;26543-26549.
24. Marleau S, Fruteau de Laclos B, Sanchez AB, Poubelle PE, Borgeat P. Role of 5-lipoxygenase products in the local accumulation of neutrophils in dermal inflammation in the rabbit. J Immunol. 1999;163:3449-3458.
25. Malle E, Nimpf J, Leis HJ, Wurm H, Gleispach H, Kostner GM. Cyclooxygenase and lipoxygenase metabolites during platelet aggregation: quantitative measurement by negative ion chemical ionization-gas chromatography/mass spectrometry. Prostaglandins Leukot Med. 1987;27: 53-70.
26. Hwang DH. Characteristics of the formation of the platelet lipoxygenase product from endogenous arachidonic acid. Lipids. 1982;17:845-847.
27. Sekiya F, Takagi J, Usui T, Kawajiri K, Kobayashi Y, Sato F, Saito Y. 12S-hydroxyeicosatetraenoic acid plays a central role in the regulation of platelet activation. Biochem Biophys Res Comm. 1991;179:345-351.
28. McNichol A. Platelet preparation and estimation of functional responses. In: Watson SP, Authi KS, eds. Platelets, a Practical Approach. IRL Press;1996:1-6.
29. Kehrel B, Wierwille S, Clemetson KJ, Anders O, Steiner M, Knight CG, Farndale RW, Okuma M, Barnes MJ. Glycoprotein VI is a major collagen receptor for platelet activation: it recognizes the platelet-activating quaternary structure of collagen, whereas CD36, glycoprotein IIb/IIIa, and von Willebrand factor do not. Blood. 1998;91:491-499.
30. Yanaga F, Poole A, Asselin J, Blake R, Schieven GL, Clark EA, Law CL, Watson SP. Syk interacts with tyrosine-phosphorylated proteins in human platelets activated by collagen and cross-linking of the Fc gamma-IIA receptor. Biochem J. 1995;311:471-478.
31. Briddon SJ, Watson SP. Evidence for the involvement of p59fyn and p53/56lyn in collagen receptor signalling in human platelets. Biochem J. 1999;338:203-209.
32. Falet H, Barkalow KL, Pivniouk VI, Barnes MJ, Geha RS, Hartwig JH. Roles of SLP-76, phosphoinositide 3-kinase, and gelsolin in the platelet shape changes initiated by the collagen receptor GPVI/FcRγ,-chain complex. Blood. 2000;96:3786-3792.
33. Quinton TM, Kim S, Dangalmaier C, Dorsam RT, Jin J, Daniel JL, Kunapuli SP. Protein kinase C- and calcium-regulated pathways independently synergize with Gi pathways in agonist-induced fibrinogen receptor activation. Biochem J. 2002;368:535-543.
34. Börsch-Haubold AG, Kramer RM, Watson SP. Phosphorylation and activation of cytosolic phospholipase A2 by 38-kDa mitogen-activated protein kinase in collagen-stimulated human platelets. Eur J Biochem. 1997;245:751-759.
35. Vezza R, Mezzasoma AM, Venditti G, Gresele P. Prostaglandin endoperoxides and thromboxane A2 activate the same receptor isoforms in human platelets. Thromb Haemost. 2002;87:114-121.
36. 3 integrin receptor activation, and aspirin-insensitive mechanisms of thrombin-stimulated human platelets. Circulation. 2000;102:1924-1930.
37. Cicmil M, Thomas JM, Leduc M, Bon C, Gibbins JM. Platelet endothelial cell adhesion molecule-1 signaling inhibits the activation of human platelets. Blood. 2002;99:137-144.
38. Shrimpton CN, Borthakur G, Larrucea S, Cruz MA, Lopez J. Localization of the adhesion receptor glycoprotein Ib-IX-V complex to lipid rafts is required for platelet adhesion and activation. J Exp Med. 2002;196: 1057-1066.
39. Kunicki TJ. The influence of platelet collagen receptor polymorphisms in hemostasis and thrombotic disease. Arterioscler Thromb Vasc Biol. 2002; 22:14-20.
40. Kunicki TJ, Ruggeri ZM. Platelet collagen receptors and risk prediction in stroke and coronary artery disease. Circulation. 2001;104:1451-1453.
41. Croft SA, Samani NJ, Teare MD, Hampton KK, Steeds RP, Channer KS, Daly ME. Novel platelet membrane glycoprotein VI dimorphism is a risk factor for myocardial infarction. Circulation. 2001;104:459-1463.
42. Berlanga O, Tulasne D, Bori T, Snell DC, Miura Y, Jung S, Moroi M, Frampton J, Watson SP. The Fc receptor gamma-chain is necessary and sufficient to initiate signalling through glycoprotein VI in transfected cells by the snake C-type lectin, convulxin. Eur J Biochem. 2002;269: 2951-2960.
43. Polanowska-Grabowska R, Geanacopolous M, Gear ARL. Platelet adhesion to collagen via the α2β1 integrin under arterial flow conditions causes rapid tyrosine phosphorylation of ppI25FAK. Biochem J. 1993; 296:543-547.
44. Watson SP, Asazuma A, Atkinson B, Berlanga O, Best D, Bobe R, Jarvis GE, Marshall S, Snell D, Stafford M, Tulasne D, Wilde J, Wonerow P, Frampton J. The role of ITAM- and ITIM-coupled receptors in platelet activation by collagen. Thromb Haemost. 2001;86:276-288.
45. Pasquet JM, Bobe R, Gross B, Gratacap MP, Tomlinson MG, Payrastre B, Watson SP. A collagen-related peptide regulates phospholipase Cγ2 via phosphatidylinositol 3-kinase in human platelets. Biochem J. 1999; 342:171-177.
46. Bobe R, Wilde JI, Mascberger P, Venkateswarlu K, Cullen PJ, Siess W, Watson SP. Phosphatidylinositol 3-kinase-dependent translocation of phospholipase Cgamma2 in mouse megakaryocytes is independent of Bruton tyrosine kinase translocation. Blood. 2001;97:678-684.
47. Madani S, Hichami A, Legrand A, Belleville J, Khan NA. Implication of acyl chain of diacylglycerol in activation of different isoforms of protein kinase C. FASEB J. 2001;15:2595-25601.
48. 2+ store, with functional properties distinct from those of the endoplasmic reticulum. EMBO J. 1998;17: 5298-52308.
49. Sundaresan P, Farndale RW. P38 mitogen-activated protein kinase dephosphorylation is regulated by protein phosphatase 2A in human platelets activated by collagen. FEBS Lett. 2002;528:139-144.
50. Baba A, Sakuma S, Okamoto H, Inoue T, Iwata H. Calcium induces membrane translocation of 12-lipoxygenase in rat platelets. J Biol Chem. 1989;264:15790-15795.
51. Hagmann W, Gao X, Zacharek A, Wojciechowski LA, Honn KV. 12-Lipoxygenase in Lewis lung carcinoma cells: molecular identity, intracellular distribution of activity and protein, and Ca(2+)-dependent translocation from cytosol to membranes. Prostaglandins. 1995;49:49-62.
52. Remijn JA, Wu YP, Jeninga EH, Ijsseldijk MJ, van Willigen G, de Groot PG, Sixma JJ, Nurden AT, Nurden P. Role of ADP receptor P2Y(12) in platelet adhesion and thrombus formation in flowing blood. Arterioscler Thromb Vasc Biol. 2002;22:686-691.
53. Paul BZ, Jin J, Kinapuli SP. Molecular mechanism of thromboxane A(2)-induced platelet aggregation. Essential role for p2t(ac) and α2a receptors. J Biol Chem. 1999;274:29108-29114.
54. Andrews DA, Yang L, Low PS. Phorbol ester stimulates a protein kinase C-mediated agatoxin-TK-sensitive calcium permeability pathway in human red blood cells. Blood. 2002;100:3392-3399.
55. Crosby D, Poole AW. Interaction of Bruton's tyrosine kinase and protein kinase Cθ in platelets. Cross-talk between tyrosine and serine/threonine kinases. J Biol Chem. 2002;277:9958-9965.
56. Crosby D, Poole AW. Physical and functional interaction between protein kinase C delta and Fyn tyrosine kinase in human platelets. J Biol Chem. 2003;278:24533-24541.
57. Billadeau DD, Leibson PJ. ITAMs versus ITIMs: striking a balance during cell regulation. J Clin Invest. 2002;109:161-168.
58. Jones KL, Hughan SC, Dopheide SM, Farndale RW, Jackson SP, Jackson DE. Platelet endothelial cell adhesion molecule-I is a negative regulator of platelet-collagen interactions. Blood. 2001;98:1456-1463.
59. Cicmil M, Thomas JM, Sage T, Barry FA, Leduc M, Bon C, Gibbins JM. Collagen, convulxin, and thrombin stimulate aggregation-independent tyrosine phosphorylation of CD31 in platelets. Evidence for the involvement of Src family kinases. J Biol Chem. 2000;275:27339-27347.