Peroxynitrite disrupts endothelial caveolae leading to eNOS uncoupling and diminished flow-mediated dilation in coronary arterioles of diabetic patients

Diabetes

Volumn 63, Issue 4, 2014, Pages 1381-1393

  Cassuto, James ^a   Dou, Huijuan ^a   Czikora, Istvan ^a   Szabo, Andras ^a   Patel, Vijay S ^a   Kamath, Vinayak ^a   De Chantemele, Eric Belin ^a   Feher, Attila ^a   Romero, Maritza J ^a   Bagi, Zsolt ^a  

^a MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

3 NITROTYROSINE; CAVEOLIN 1; ENDOTHELIAL NITRIC OXIDE SYNTHASE; METHYL BETA CYCLODEXTRIN; N(G) NITROARGININE METHYL ESTER; PEROXYNITRITE; SCAVENGER; SEPIAPTERIN; TETRAHYDROBIOPTERIN; URIC ACID;

AGED; ARTERIOLE; ARTICLE; CAVEOLA; CELL MEMBRANE; CELLULAR DISTRIBUTION; CLINICAL ARTICLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; CORONARY ARTERY DILATATION; CYTOSOL; DIABETIC PATIENT; ENDOTHELIUM CELL; FEMALE; FLOW MEDIATED DILATION; HEART SURGERY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOELECTRON MICROSCOPY; INSULIN DEPENDENT DIABETES MELLITUS; MALE; NON INSULIN DEPENDENT DIABETES MELLITUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

AGED; ANIMALS; ARTERIOLES; BETA-CYCLODEXTRINS; CAVEOLAE; CAVEOLIN 1; CELLS, CULTURED; DIABETES MELLITUS; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; FEMALE; HUMANS; MALE; MICE; MICE, KNOCKOUT; MIDDLE AGED; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PEROXYNITROUS ACID; PTERINS; REGIONAL BLOOD FLOW; TYROSINE; VASODILATION;

EID: 84897843508     PISSN: 00121797     EISSN: 1939327X     Source Type: Journal    
DOI: 10.2337/db13-0577     Document Type: Article

References (48)

1. Mahgoub MA, Abd-Elfattah AS. Diabetes mellitus and cardiac function. Mol Cell Biochem 1998;180:59-64
2. Nitenberg A, Paycha F, Ledoux S, Sachs R, Attali JR, Valensi P. Coronary artery responses to physiological stimuli are improved by deferoxamine but not by L-arginine in non-insulin-dependent diabetic patients with angiographically normal coronary arteries and no other risk factors. Circulation 1998;97:736-743
3. Kaneda H, Taguchi J, Kuwada Y, et al. Coronary artery spasm and the polymorphisms of the endothelial nitric oxide synthase gene. Circ J 2006;70:409-413
4. Miura H, Wachtel RE, Loberiza FR Jr, et al. Diabetes mellitus impairs vasodilation to hypoxia in human coronary arterioles: reduced activity of ATP-sensitive potassium channels. Circ Res 2003;92:151-158
5. Beleznai T, Feher A, Spielvogel D, Lansman SL, Bagi Z. Arginase 1 contributes to diminished coronary arteriolar dilation in patients with diabetes. Am J Physiol Heart Circ Physiol 2011;300:H777-H783
6. Koller A, Sun D, Kaley G. Role of shear stress and endothelial prostaglandins in flow- and viscosity-induced dilation of arterioles in vitro. Circ Res 1993;72:1276-1284
7. Camici PG, Crea F. Coronary microvascular dysfunction. N Engl J Med 2007;356:830-840
8. Lambert J, Aarsen M, Donker AJ, Stehouwer CD. Endothelium-dependent and -independent vasodilation of large arteries in normoalbuminuric insulin-dependent diabetes mellitus. Arterioscler Thromb Vasc Biol 1996;16:705-711
9. Henry RM, Ferreira I, Kostense PJ, et al. Type 2 diabetes is associated with impaired endothelium-dependent, fl ow-mediated dilation, but impaired glucose metabolism is not; the Hoorn Study. Atherosclerosis 2004;174:49-56
10. Bagi Z, Koller A, Kaley G. PPARgamma activation, by reducing oxidative stress, increases NO bioavailability in coronary arterioles of mice with type 2 diabetes. Am J Physiol Heart Circ Physiol 2004;286:H742-H748
11. Bagi Z, Koller A, Kaley G. Superoxide-NO interaction decreases flow- and agonist-induced dilations of coronary arterioles in type 2 diabetes mellitus. Am J Physiol Heart Circ Physiol 2003;285:H1404-H1410
12. Forstermann U, Sessa WC. Nitric oxide synthases: regulation and function. Eur Heart J 2012;33:829-837, 837a-837d
13. Forbes JM, Cooper ME. Mechanisms of diabetic complications. Physiol Rev 2013;93:137-188
14. Sharma A, Bernatchez PN, de Haan JB. Targeting endothelial dysfunction in vascular complications associated with diabetes. Int J Vasc Med 2012;2012:750126
15. Pacher P, Beckman JS, Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007;87:315-424
16. Heijnen HF, van Donselaar E, Slot JW, et al. Subcellular localization of tyrosine-nitrated proteins is dictated by reactive oxygen species generating enzymes and by proximity to nitric oxide synthase. Free Radic Biol Med 2006;40:1903-1913
17. van der Loo B, Labugger R, Skepper JN, et al. Enhanced peroxynitrite formation is associated with vascular aging. J Exp Med 2000;192:1731-1744
18. Yu J, Bergaya S, Murata T, et al. Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest 2006;116:1284-1291
19. Szerafin T, Erdei N, Fülöp T, et al. Increased cyclooxygenase-2 expression and prostaglandin-mediated dilation in coronary arterioles of patients with diabetes mellitus. Circ Res 2006;99:e12-e17
20. Feher A, Rutkai I, Beleznai T, et al. Caveolin-1 limits the contribution of BK(Ca) channel to EDHF-mediated arteriolar dilation: implications in diet-induced obesity. Cardiovasc Res 2010;87:732-739
21. Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 2007;40:101-111
22. Sinha B, Köster D, Ruez R, et al. Cells respond to mechanical stress by rapid disassembly of caveolae. Cell 2011;144:402-413
23. Belin de Chantemèle EJ, Mintz JD, Rainey WE, Stepp DW. Impact of leptinmediated sympatho-activation on cardiovascular function in obese mice. Hypertension 2011;58:271-279
24. Woodman SE, Ashton AW, Schubert W, et al. Caveolin-1 knockout mice show an impaired angiogenic response to exogenous stimuli. Am J Pathol 2003;162:2059-2068
25. Szabó C, Ischiropoulos H, Radi R. Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 2007;6:662-680
26. Kooy NW, Lewis SJ, Royall JA, Ye YZ, Kelly DR, Beckman JS. Extensive tyrosine nitration in human myocardial inflammation: evidence for the presence of peroxynitrite. Crit Care Med 1997;25:812-819
27. Ravalli S, Albala A, Ming M, et al. Inducible nitric oxide synthase expression in smooth muscle cells and macrophages of human transplant coronary artery disease. Circulation 1998;97:2338-2345
28. Li H, Gutterman DD, Rusch NJ, Bubolz A, Liu Y. Nitration and functional loss of voltage-gated K+ channels in rat coronary microvessels exposed to high glucose. Diabetes 2004;53:2436-2442
29. Liu Y, Zhao H, Li H, Kalyanaraman B, Nicolosi AC, Gutterman DD. Mitochondrial sources of H2O2 generation play a key role in flow-mediated dilation in human coronary resistance arteries. Circ Res 2003;93:573-580
30. Bagi Z, Frangos JA, Yeh JC, White CR, Kaley G, Koller A. PECAM-1 mediates NO-dependent dilation of arterioles to high temporal gradients of shear stress. Arterioscler Thromb Vasc Biol 2005;25:1590-1595
31. Liu Y, Bubolz AH, Shi Y, Newman PJ, Newman DK, Gutterman DD. Peroxynitrite reduces the endothelium-derived hyperpolarizing factor component of coronary flow-mediated dilation in PECAM-1-knockout mice. Am J Physiol Regul Integr Comp Physiol 2006;290:R57-R65
32. Kloner RA, Ganote CE, Jennings RB. The "no-reflow" phenomenon after temporary coronary occlusion in the dog. J Clin Invest 1974;54:1496-1508
33. Peterson TE, Poppa V, Ueba H, Wu A, Yan C, Berk BC. Opposing effects of reactive oxygen species and cholesterol on endothelial nitric oxide synthase and endothelial cell caveolae. Circ Res 1999;85:29-37
34. Peterson TE, d'Uscio LV, Cao S, Wang XL, Katusic ZS. Guanosine triphosphate cyclohydrolase I expression and enzymatic activity are present in caveolae of endothelial cells. Hypertension 2009;53:189-195
35. Cohen AW, Hnasko R, Schubert W, Lisanti MP. Role of caveolae and caveolins in health and disease. Physiol Rev 2004;84:1341-1379
36. García-Cardeña G, Martasek P, Masters BS, et al. Dissecting the interaction between nitric oxide synthase (NOS) and caveolin. Functional significance of the nos caveolin binding domain in vivo. J Biol Chem 1997;272:25437-25440
37. Michel JB, Feron O, Sacks D, Michel T. Reciprocal regulation of endothelial nitric-oxide synthase by Ca2+-calmodulin and caveolin. J Biol Chem 1997;272:15583- 15586
38. Ju H, Zou R, Venema VJ, Venema RC. Direct interaction of endothelial nitric-oxide synthase and caveolin-1 inhibits synthase activity. J Biol Chem 1997;272:18522-18525
39. Lungu AO, Jin ZG, Yamawaki H, Tanimoto T, Wong C, Berk BC. Cyclosporin A inhibits flow-mediated activation of endothelial nitric-oxide synthase by altering cholesterol content in caveolae. J Biol Chem 2004;279:48794-48800
40. Blair A, Shaul PW, Yuhanna IS, Conrad PA, Smart EJ. Oxidized low density lipoprotein displaces endothelial nitric-oxide synthase (eNOS) from plasmalemmal caveolae and impairs eNOS activation. J Biol Chem 1999;274:32512-32519
41. Maniatis NA, Brovkovych V, Allen SE, et al. Novel mechanism of endothelial nitric oxide synthase activation mediated by caveolae internalization in endothelial cells. Circ Res 2006;99:870-877
42. Zhang Q, Church JE, Jagnandan D, Catravas JD, Sessa WC, Fulton D. Functional relevance of Golgi- and plasma membrane-localized endothelial NO synthase in reconstituted endothelial cells. Arterioscler Thromb Vasc Biol 2006;26:1015-1021
43. Bernatchez P, Sharma A, Bauer PM, Marin E, Sessa WC. A noninhibitory mutant of the caveolin-1 scaffolding domain enhances eNOS-derived NO synthesis and vasodilation in mice. J Clin Invest 2011;121:3747-3755
44. Vásquez-Vivar J, Martásek P, Whitsett J, Joseph J, Kalyanaraman B. The ratio between tetrahydrobiopterin and oxidized tetrahydrobiopterin analogues controls superoxide release from endothelial nitric oxide synthase: an EPR spin trapping study. Biochem J 2002;362:733-739
45. Alp NJ, Channon KM. Regulation of endothelial nitric oxide synthase by tetrahydrobiopterin in vascular disease. Arterioscler Thromb Vasc Biol 2004;24:413-420
46. Wunderlich C, Schober K, Schmeisser A, et al. The adverse cardiopulmonary phenotype of caveolin-1 deficient mice is mediated by a dysfunctional endothelium. J Mol Cell Cardiol 2008;44:938-947
47. Kuzkaya N, Weissmann N, Harrison DG, Dikalov S. Interactions of peroxynitrite, tetrahydrobiopterin, ascorbic acid, and thiols: implications for uncoupling endothelial nitric-oxide synthase. J Biol Chem 2003;278:22546-22554
48. Chen W, Druhan LJ, Chen CA, et al. Peroxynitrite induces destruction of the tetrahydrobiopterin and heme in endothelial nitric oxide synthase: transition from reversible to irreversible enzyme inhibition. Biochemistry 2010; 49:3129-3137