Nitroglycerin-induced endothelial dysfunction and tolerance involve adverse phosphorylation and S-glutathionylation of endothelial nitric oxide synthase: Beneficial effects of therapy with the AT1 receptor blocker telmisartan

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 31, Issue 10, 2011, Pages 2223-2231

  Knorr, Maike ^a   Hausding, Michael ^a,b   Kröller Schuhmacher, Swenja ^a,b   Steven, Sebastian ^a   Oelze, Matthias ^a   Heeren, Tjebo ^a   Scholz, Alexander ^a   Gori, Tommaso ^a   Wenzel, Philip ^a,b   Schulz, Eberhard ^a   Daiber, Andreas ^a   Münzel, Thomas ^a  

^a Second Medical Clinic   (Germany)

^b UNIVERSITY MEDICAL CENTER MAINZ   (Germany)

Author keywords

endothelial function; nitric oxide synthase; nitroglycerin; superoxide

Indexed keywords

ALDEHYDE DEHYDROGENASE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUTATHIONE; GLYCERYL TRINITRATE; GUANOSINE TRIPHOSPHATE CYCLOHYDROLASE I; REACTIVE OXYGEN METABOLITE; TELMISARTAN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL REACTIVITY; CHEMOLUMINESCENCE; CONTROLLED STUDY; DRUG BLOOD LEVEL; DRUG EFFECT; DRUG TOLERANCE; ENDOTHELIAL DYSFUNCTION; ENZYME PHOSPHORYLATION; IN VIVO STUDY; LEUKOCYTE COUNT; MALE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; WESTERN BLOTTING;

ALDEHYDE DEHYDROGENASE; ANGIOTENSIN II TYPE 1 RECEPTOR BLOCKERS; ANIMALS; BENZIMIDAZOLES; BENZOATES; CELL LINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG TOLERANCE; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; ENZYME INHIBITORS; GLUTATHIONE; GTP CYCLOHYDROLASE; HUMANS; MALE; MITOCHONDRIA; NITRIC OXIDE SYNTHASE TYPE III; NITROGLYCERIN; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES; TETRAHYDROFOLATE DEHYDROGENASE; VASODILATION; VASODILATOR AGENTS;

EID: 80052968360     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.232058     Document Type: Article

References (37)

1. Munzel T, Daiber A, Mulsch A. Explaining the phenomenon of nitrate tolerance. Circ Res. 2005;97:618-628. (Pubitemid 41416330)
2. Munzel T, Sayegh H, Freeman BA, Tarpey MM, Harrison DG. Evidence for enhanced vascular superoxide anion production in nitrate tolerance: a novel mechanism underlying tolerance and cross-tolerance. J Clin Invest. 1995;95:187-194.
3. Thomas GR, DiFabio JM, Gori T, Parker JD. Once daily therapy with isosorbide-5-mononitrate causes endothelial dysfunction in humans: evidence of a free-radical-mediated mechanism. J Am Coll Cardiol. 2007;49:1289-1295. (Pubitemid 46476841)
4. Munzel T, Kurz S, Rajagopalan S, Thoenes M, Berrington WR, Thompson JA, Freeman BA, Harrison DG. Hydralazine prevents nitro-glycerin tolerance by inhibiting activation of a membrane-bound NADH oxidase: a new action for an old drug. J Clin Invest. 1996;98:1465-1470. (Pubitemid 26322073)
5. Sydow K, Daiber A, Oelze M, Chen Z, August M, Wendt M, Ullrich V, Mulsch A, Schulz E, Keaney JF Jr, Stamler JS, Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest. 2004;113: 482-489. (Pubitemid 38544192)
6. Munzel T, Li H, Mollnau H, Hink U, Matheis E, Hartmann M, Oelze M, Skatchkov M, Warnholtz A, Duncker L, Meinertz T, Forstermann U. Effects of long-term nitroglycerin treatment on endothelial nitric oxide synthase (NOS III) gene expression, NOS III-mediated superoxide production, and vascular NO bioavailability. Circ Res. 2000;86:E7-E12.
7. Hirai N, Kawano H, Yasue H, Shimomura H, Miyamoto S, Soejima H, Kajiwara I, Sakamoto T, Yoshimura M, Nakamura H, Yodoi J, Ogawa H. Attenuation of nitrate tolerance and oxidative stress by an angiotensin II receptor blocker in patients with coronary spastic angina. Circulation. 2003;108:1446-1450. (Pubitemid 37176449)
8. Katz RJ, Levy WS, Buff L, Wasserman AG. Prevention of nitrate tolerance with angiotension converting enzyme inhibitors. Circulation. 1991;83:1271-1277.
9. Kurz S, Hink U, Nickenig G, Borthayre AB, Harrison DG, Munzel T. Evidence for a causal role of the renin-angiotensin system in nitrate tolerance. Circulation. 1999;99:3181-3187. (Pubitemid 29289085)
10. Milone SD, Azevedo ER, Forster C, Parker JD. The angiotensin II-receptor antagonist losartan does not prevent hemodynamic or vascular tolerance to nitroglycerin. J Cardiovasc Pharmacol. 1999;34:645-650. (Pubitemid 29491725)
11. Longobardi G, Ferrara N, Leosco D, Abete P, Furgi G, Cacciatore F, Corbi G, Pescatore R, Rengo F. Angiotensin II-receptor antagonist losartan does not prevent nitroglycerin tolerance in patients with coronary artery disease. Cardiovasc Drugs Ther. 2004;18:363-370. (Pubitemid 40558202)
12. Daiber A, Oelze M, Coldewey M, Bachschmid M, Wenzel P, Sydow K, Wendt M, Kleschyov AL, Stalleicken D, Ullrich V, Mulsch A, Munzel T. Oxidative stress and mitochondrial aldehyde dehydrogenase activity: a comparison of pentaerythritol tetranitrate with other organic nitrates. Mol Pharmacol. 2004;66:1372-1382. (Pubitemid 39564764)
13. Daiber A, Oelze M, Sulyok S, Coldewey M, Schulz E, Treiber N, Hink U, Mulsch A, Scharffetter-Kochanek K, Munzel T. Heterozygous deficiency of manganese superoxide dismutase in mice (Mn-SOD+/-): a novel approach to assess the role of oxidative stress for the development of nitrate tolerance. Mol Pharmacol. 2005;68:579-588. (Pubitemid 41206011)
14. Wenzel P, Mollnau H, Oelze M, Schulz E, Wickramanayake JM, Muller J, Schuhmacher S, Hortmann M, Baldus S, Gori T, Brandes RP, Munzel T, Daiber A. First evidence for a crosstalk between mitochondrial and NADPH oxidase-derived reactive oxygen species in nitroglycerin-triggered vascular dysfunction. Antioxid Redox Signal. 2008;10: 1435-1447.
15. Ma H, Guo R, Yu L, Zhang Y, Ren J. Aldehyde dehydrogenase 2 (ALDH2) rescues myocardial ischaemia/reperfusion injury: role of autophagy paradox and toxic aldehyde. Eur Heart J. 2011;32:1025-1038.
16. Chen CH, Budas GR, Churchill EN, Disatnik MH, Hurley TD, Mochly-Rosen D. Activation of aldehyde dehydrogenase-2 reduces is-chemic damage to the heart. Science. 2008;321:1493-1495.
17. Mount PF, Kemp BE, Power DA. Regulation of endothelial and myocardial NO synthesis by multi-site eNOS phosphorylation. J Mol Cell Cardiol. 2007;42:271-279. (Pubitemid 46135596)
18. Chen CA, Wang TY, Varadharaj S, Reyes LA, Hemann C, Talukder MA, Chen YR, Druhan LJ, Zweier JL. S-Glutathionylation uncouples eNOS and regulates its cellular and vascular function. Nature. 2010;468: 1115-1118.
19. Forstermann U, Munzel T. Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation. 2006;113:1708-1714.
20. Vasquez-Vivar J, Kalyanaraman B, Martasek P. The role of tetrahydro-biopterin in superoxide generation from eNOS: enzymology and physiological implications. Free Radic Res. 2003;37:121-127. (Pubitemid 36124338)
21. Schuhmacher S, Wenzel P, Schulz E, Oelze M, Mang C, Kamuf J, Gori T, Jansen T, Knorr M, Karbach S, Hortmann M, Mathner F, Bhatnagar A, Forstermann U, Li H, Munzel T, Daiber A. Pentaerythritol tetranitrate improves angiotensin II-induced vascular dysfunction via induction of heme oxygenase-1. Hypertension. 2010;55:897-904.
22. Daiber A, August M, Baldus S, Wendt M, Oelze M, Sydow K, Kleschyov AL, Munzel T. Measurement of NAD(P)H oxidase-derived superoxide with the luminol analogue L-012. Free Radic Biol Med. 2004;36: 101-111. (Pubitemid 38068295)
23. Wenzel P, Schulz E, Oelze M, Muller J, Schuhmacher S, Alhamdani MS, Debrezion J, Hortmann M, Reifenberg K, Fleming I, Munzel T, Daiber A. AT1-receptor blockade by telmisartan upregulates GTP-cyclohydrolase I and protects eNOS in diabetic rats. Free Radic Biol Med. 2008;45: 619-626.
24. Oelze M, Mollnau H, Hoffmann N, Warnholtz A, Bodenschatz M, Smo-lenski A, Walter U, Skatchkov M, Meinertz T, Munzel T. Vasodilator-stimulated phosphoprotein serine 239 phosphorylation as a sensitive monitor of defective nitric oxide/cGMP signaling and endothelial dysfunction. Circ Res. 2000;87:999-1005.
25. Schuhmacher S, Schulz E, Oelze M, Konig A, Roegler C, Lange K, Sydow L, Kawamoto T, Wenzel P, Munzel T, Lehmann J, Daiber A. A new class of organic nitrates: investigations on bioactivation, tolerance and cross-tolerance phenomena. Br J Pharmacol. 2009;158:510-520.
26. Edgell CJ, McDonald CC, Graham JB. Permanent cell line expressing human factor VIII-related antigen established by hybridization. Proc Natl Acad Sci USA. 1983;80:3734-3737. (Pubitemid 13063134)
27. Jansen T, Hortmann M, Oelze M, Opitz B, Steven S, Schell R, Knorr M, Karbach S, Schuhmacher S, Wenzel P, Munzel T, Daiber A. Conversion of biliverdin to bilirubin by biliverdin reductase contributes to endothelial cell protection by heme oxygenase-1-evidence for direct and indirect antioxidant actions of bilirubin. J Mol Cell Cardiol. 2010;49:186-195.
28. Szocs K, Lassegue B, Wenzel P, Wendt M, Daiber A, Oelze M, Meinertz T, Munzel T, Baldus S. Increased superoxide production in nitrate tolerance is associated with NAD(P)H oxidase and aldehyde dehydrogenase 2 downregulation. J Mol Cell Cardiol. 2007;42:1111-1118. (Pubitemid 46829198)
29. Lin MI, Fulton D, Babbitt R, Fleming I, Busse R, Pritchard KA Jr, Sessa WC. Phosphorylation of threonine 497 in endothelial nitric-oxide synthase coordinates the coupling of L-arginine metabolism to efficient nitric oxide production. J Biol Chem. 2003;278:44719-44726. (Pubitemid 37377229)
30. Xu J, Wu Y, Song P, Zhang M, Wang S, Zou MH. Proteasome-dependent degradation of guanosine 5'-triphosphate cyclohydrolase I causes tetra-hydrobiopterin deficiency in diabetes mellitus. Circulation. 2007;116: 944-953. (Pubitemid 47300919)
31. Whitsett J, Picklo MJ, Sr., Vasquez-Vivar J. 4-Hydroxy-2-nonenal increases superoxide anion radical in endothelial cells via stimulated GTP cyclohydrolase proteasomal degradation. Arterioscler Thromb Vasc Biol. 2007;27:2340-2347. (Pubitemid 350203948)
32. Mulsch A, Oelze M, Kloss S, Mollnau H, Topfer A, Smolenski A, Walter U, Stasch JP, Warnholtz A, Hink U, Meinertz T, Munzel T. Effects of in vivo nitroglycerin treatment on activity and expression of the guanylyl cyclase and cGMP-dependent protein kinase and their downstream target vasodilator-stimulated phosphoprotein in aorta. Circulation. 2001;103: 2188-2194. (Pubitemid 32463296)
33. Hink U, Oelze M, Kolb P, Bachschmid M, Zou MH, Daiber A, Mollnau H, August M, Baldus S, Tsilimingas N, Walter U, Ullrich V, Munzel T. Role for peroxynitrite in the inhibition of prostacyclin synthase in nitrate tolerance. J Am Coll Cardiol. 2003;42:1826-1834. (Pubitemid 37433665)
34. Chen Z, Zhang J, Stamler JS. Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci USA. 2002;99: 8306-8311. (Pubitemid 34651048)
35. Mehta JL, Hu B, Chen J, Li D. Pioglitazone inhibits LOX-1 expression in human coronary artery endothelial cells by reducing intracellular superoxide radical generation. Arterioscler Thromb Vasc Biol. 2003;23: 2203-2208. (Pubitemid 37532321)
36. Warnholtz A, Mollnau H, Heitzer T, Kontush A, Moller-Bertram T, Lavall D, Giaid A, Beisiegel U, Marklund SL, Walter U, Meinertz T, Munzel T. Adverse effects of nitroglycerin treatment on endothelial function, vascular nitrotyrosine levels and cGMP-dependent protein kinase activity in hyperlipidemic Watanabe rabbits. J Am Coll Cardiol. 2002;40:1356-1363.
37. Andreassi MG, Botto N, Simi S, Casella M, Manfredi S, Lucarelli M, Venneri L, Biagini A, Picano E. Diabetes and chronic nitrate therapy as codeterminants of somatic DNA damage in patients with coronary artery disease. J Mol Med. 2005;83:279-286. (Pubitemid 40674954)