Enhanced tyrosine nitration of prostacyclin synthase is associated with increased inflammation in atherosclerotic carotid arteries from type 2 diabetic patients

American Journal of Pathology

Volumn 176, Issue 5, 2010, Pages 2542-2549

  He, Chaoyong ^a   Choi, Hyoung Chul ^a   Xie, Zhonglin ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CELL ADHESION MOLECULE; GELATINASE A; GELATINASE B; INTRACELLULAR ADHESION MOLECULE 1; MYELOPEROXIDASE; NITRIC OXIDE SYNTHASE; OSTEOPONTIN; PROSTACYCLIN SYNTHASE; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG; VASCULAR ADHESION MOLECULE 1;

AGED; ARTERY OCCLUSION; ARTICLE; ATHEROSCLEROTIC CARDIOVASCULAR DISEASE; ATHEROSCLEROTIC PLAQUE; CAROTID ATHEROSCLEROSIS; CAROTID ENDARTERECTOMY; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; FEMALE; GENE EXPRESSION; HUMAN; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MALE; NITRATION; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; UPREGULATION; WESTERN BLOTTING;

EID: 77952073547     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.2353/ajpath.2010.090783     Document Type: Article

References (46)

1. Beckman JA, Creager MA, Libby P: Diabetes and atherosclerosis: epidemiology, pathophysiology, and management. JAMA 2002, 287: 2570-2581
2. Biondi-Zoccai GG, Abbate A, Liuzzo G, Biasucci LM: Atherothrombosis, inflammation, and diabetes. J Am Coll Cardiol 2003, 41:1071-1077
3. Libby P, Ridker PM, Maseri A: Inflammation and atherosclerosis. Circulation 2002, 105:1135-1143
4. Kobayashi T, Tahara Y, Matsumoto M, Iguchi M, Sano H, Murayama T, Arai H, Oida H, Yurugi-Kobayashi T, Yamashita JK, Katagiri H, Majima M, Yokode M, Kita T, Narumiya S: Roles of thromboxane A(2) and prostacyclin in the development of atherosclerosis in apo-Edeficient mice. J Clin Invest 2004, 114:784-794
5. Linton MF, Fazio S: Cyclooxygenase-2 and atherosclerosis. Curr Opin Lipidol 2002, 13:497-504
6. Zou MH, Shi C, Cohen RA: High glucose via peroxynitrite causes tyrosine nitration and inactivation of prostacyclin synthase that is associated with thromboxane/prostaglandin H(2) receptor-mediated apoptosis and adhesion molecule expression in cultured human aortic endothelial cells. Diabetes 2002, 51:198-203
7. Zuccollo A, Shi C, Mastroianni R, Maitland-Toolan KA, Weisbrod RM, Zang M, Xu S, Jiang B, Oliver-Krasinski JM, Cayatte AJ, Corda S, Lavielle G, Verbeuren TJ, Cohen RA: The thromboxane A2 receptor antagonist S18886 prevents enhanced atherogenesis caused by diabetes mellitus. Circulation 2005, 112:3001-3008
8. Ceriello A: New insights on oxidative stress and diabetic complications may lead to a "causal" antioxidant therapy. Diabetes Care 2003, 26:1589-1596
9. Bohlen HG, Lash JM: Topical hyperglycemia rapidly suppresses EDRF-mediated vasodilation of normal rat arterioles. Am J Physiol 1993, 265:H219-H225
10. Giugliano D, Marfella R, Coppola L, Verrazzo G, Acampora R, Giunta R, Nappo F, Lucarelli C, D'Onofrio F: Vascular effects of acute hyperglycemia in humans are reversed by L-arginine: evidence for reduced availability of nitric oxide during hyperglycemia. Circulation 1997, 95:1783-1790
11. Kawano H, Motoyama T, Hirashima O, Hirai N, Miyao Y, Sakamoto T, Kugiyama K, Ogawa H, Yasue H: Hyperglycemia rapidly suppresses flow-mediated endothelium-dependent vasodilation of brachial artery. J Am Coll Cardiol 1999, 34:146-154
12. Tesfamariam B, Cohen RA: Free radicals mediate endothelial cell dysfunction caused by elevated glucose. Am J Physiol 1992, 263: H321-H326
13. Marfella R, Verrazzo G, Acampora R, La MC, Giunta R, Lucarelli C, Paolisso G, Ceriello A, Giugliano D: Glutathione reverses systemic hemodynamic changes induced by acute hyperglycemia in healthy subjects. Am J Physiol 1995, 268:E1167-E1173
14. Ting HH, Timimi FK, Boles KS, Creager SJ, Ganz P, Creager MA: Vitamin C improves endothelium-dependent vasodilation in patients with non-insulin-dependent diabetes mellitus. J Clin Invest 1996, 97:22-28
15. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA: Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990, 87:1620-1624
16. Beckman JS, Koppenol WH: Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 1996, 271:C1424-C1437
17. Beckman JS, Chen J, Ischiropoulos H, Crow JP: Oxidative chemistry of peroxynitrite. Methods Enzymol 1994, 233:229-240
18. Zou MH, Ullrich V: Peroxynitrite formed by simultaneous generation of nitric oxide and superoxide selectively inhibits bovine aortic prostacyclin synthase. FEBS Lett 1996, 382:101-104
19. Tesfamariam B, Jakubowski JA, Cohen RA: Contraction of diabetic rabbit aorta caused by endothelium-derived PGH2-TxA2. Am J Physiol 1989, 257:H1327-H1333
20. Dai FX, Diederich A, Skopec J, Diederich D: Diabetes-induced endothelial dysfunction in streptozotocin-treated rats: role of prostaglandin endoperoxides and free radicals. J Am Soc Nephrol 1993, 4:1327-1336
21. Shimizu K, Muramatsu M, Kakegawa Y, Asano H, Toki Y, Miyazaki Y, Okumura K, Hashimoto H, Ito T: Role of prostaglandin H2 as an endothelium-derived contracting factor in diabetic state. Diabetes 1993, 42:1246-1252
22. Zou MH, Leist M, Ullrich V: Selective nitration of prostacyclin synthase and defective vasorelaxation in atherosclerotic bovine coronary arteries. Am J Pathol 1999, 154:1359-1365
23. Young B, Moore WS, Robertson JT, Toole JF, Ernst CB, Cohen SN, Broderick JP, Dempsey RJ, Hosking JD: An analysis of perioperative surgical mortality and morbidity in the asymptomatic carotid atherosclerosis study. ACAS Investigators. Asymptomatic Carotid Artheriosclerosis Study. Stroke 1996, 27:2216-2224
24. Report of the expert committee on the diagnosis and classification of diabetes mellitus: Diabetes Care 2003, 26(Suppl 1):S5-S20
25. Xie Z, Dong Y, Scholz R, Neumann D, Zou MH: Phosphorylation of LKB1 at serine 428 by protein kinase C-zeta is required for metformin-enhanced activation of the AMP-activated protein kinase in endothelial cells. Circulation 2008, 117:952-962
26. Xie Z, Zhang J, Wu J, Viollet B, Zou MH: Upregulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes 2008, 57:3222-3230
27. Xie Z, Dong Y, Zhang M, Cui MZ, Cohen RA, Riek U, Neumann D, Schlattner U, Zou MH: Activation of protein kinase C zeta by peroxynitrite regulates LKB1-dependent AMP-activated protein kinase in cultured endothelial cells. J Biol Chem 2006, 281:6366-6375
28. Xie Z, Dong Y, Zhang J, Scholz R, Neumann D, Zou MH: Identification of the serine 307 of LKB1 as a novel phosphorylation site essential for its nucleocytoplasmic transport and endothelial cell angiogenesis. Mol Cell Biol 2009, 29:3582-3596
29. Xie Z, Singh M, Siwik DA, Joyner WL, Singh K: Osteopontin inhibits interleukin-1beta-stimulated increases in matrix metalloproteinase activity in adult rat cardiac fibroblasts: role of protein kinase C-zeta. J Biol Chem 2003, 278:48546-48552
30. Zou MH, Klein T, Pasquet JP, Ullrich V: Interleukin 1beta decreases prostacyclin synthase activity in rat mesangial cells via endogenous peroxynitrite formation. Biochem J 1998, 336(Pt 2):507-512
31. Cho HJ, Cho HJ, Kim HS: Osteopontin: a multifunctional protein at the crossroads of inflammation, atherosclerosis, and vascular calcification. Curr Atheroscler Rep 2009, 11:206-213
32. Calles-Escandon J, Cipolla M: Diabetes and endothelial dysfunction: a clinical perspective. Endocr Rev 2001, 22:36-52
33. Cosentino F, Hishikawa K, Katusic ZS, Luscher TF: High glucose increases nitric oxide synthase expression and superoxide anion generation in human aortic endothelial cells. Circulation 1997, 96:25-28
34. Brownlee M: Biochemistry and molecular cell biology of diabetic complications. Nature 2001, 414:813-820
35. Ding Y, Vaziri ND, Coulson R, Kamanna VS, Roh DD: Effects of simulated hyperglycemia, insulin, and glucagon on endothelial nitric oxide synthase expression. Am J Physiol Endocrinol Metab 2000, 279:E11-E17
36. Cromheeke KM, Kockx MM, De Meyer GR, Bosmans JM, Bult H, Beelaerts WJ, Vrints CJ, Herman AG: Inducible nitric oxide synthase colocalizes with signs of lipid oxidation/peroxidation in human atherosclerotic plaques. Cardiovasc Res 1999, 43:744-754
37. White CR, Brock TA, Chang LY, Crapo J, Briscoe P, Ku D, Bradley WA, Gianturco SH, Gore J, Freeman BA: Superoxide and peroxynitrite in atherosclerosis. Proc Natl Acad Sci USA 1994, 91:1044-1048
38. Daugherty A, Dunn JL, Rateri DL, Heinecke JW: Myeloperoxidase, a catalyst for lipoprotein oxidation, is expressed in human atherosclerotic lesions. J Clin Invest 1994, 94:437-444
39. Xu J, Xie Z, Reece R, Pimental D, Zou MH: Uncoupling of endothelial nitric oxidase synthase by hypochlorous acid: role of NAD(P)H oxidase- derived superoxide and peroxynitrite. Arterioscler Thromb Vasc Biol 2006, 26:2688-2695
40. Bult H: Nitric oxide and atherosclerosis: possible implications for therapy. Mol Med Today 1996, 2:510-518
41. Zou M, Jendral M, Ullrich V: Prostaglandin endoperoxide-dependent vasospasm in bovine coronary arteries after nitration of prostacyclin synthase. Br J Pharmacol 1999, 126:1283-1292 (Pubitemid 29142057)
42. Galis ZS, Khatri JJ: Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ Res 2002, 90:251-262
43. Galis ZS, Sukhova GK, Lark MW, Libby P: Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest 1994, 94: 2493-2503
44. Kadoglou NP, Daskalopoulou SS, Perrea D, Liapis CD: Matrix metalloproteinases and diabetic vascular complications. Angiology 2005, 56:173-189
45. Death AK, Fisher EJ, McGrath KC, Yue DK: High glucose alters matrix metalloproteinase expression in two key vascular cells: potential impact on atherosclerosis in diabetes. Atherosclerosis 2003, 168:263-269
46. Viles-Gonzalez JF, Fuster V, Corti R, Valdiviezo C, Hutter R, Corda S, Anand SX, Badimon JJ: Atherosclerosis regression and TP receptor inhibition: effect of S18886 on plaque size and composition: a magnetic resonance imaging study. Eur Heart J 2005, 26:1557-1561