Chronic administration of the HNO donor Angeli's salt does not lead to tolerance, cross-tolerance, or endothelial dysfunction: Comparison with GTN and DEA/NO

Antioxidants and Redox Signaling

Volumn 14, Issue 9, 2011, Pages 1615-1624

  Irvine, Jennifer C ^a,b   Kemp Harper, Barbara K ^a   Widdop, Robert E ^a  

^a MONASH UNIVERSITY   (Australia)

^b BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLCHOLINE; ACETYLCYSTEINE; ANGELI SALT; CYCLIC GMP; DIETHYLAMINE; GLYCERYL TRINITRATE; NITRIC OXIDE; NITROXYL; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTINUOUS INFUSION; DOSE RESPONSE; DRUG ACTIVITY; DRUG TOLERANCE; ENDOTHELIAL DYSFUNCTION; HEART RATE; MALE; MEAN ARTERIAL PRESSURE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY ANALYSIS; VASODILATATION;

ACETYLCHOLINE; ANIMALS; AORTA; CYCLIC GMP; DIETHYLAMINES; MALE; NITRIC OXIDE DONORS; NITRITES; NITROGEN OXIDES; NITROGLYCERIN; RATS;

RATTUS;

EID: 79953799131     PISSN: 15230864     EISSN: None     Source Type: Journal    
DOI: 10.1089/ars.2010.3269     Document Type: Article

References (48)

1. Andrews KL, Irvine JC, Tare M, Apostolopoulos J, Favaloro JL, Triggle CR, and Kemp-Harper BK. A role for nitroxyl (HNO) as an endothelium-derived relaxing and hyperpolarizing factor in resistance arteries. Br J Pharmacol 157: 540-550, 2009.
2. Bermejo E, Saenz DA, Alberto F, Rosenstein RE, Bari SE, and Lazzari MA. Effect of nitroxyl on human platelets function. Thromb Haemost 94: 578-584, 2005. (Pubitemid 41300855)
3. Chen Z, Foster MW, Zhang J, Mao L, Rockman HA, Kawamoto T, Kitagawa K, Nakayama KI, Hess DT, and Stamler JS. An essential role for mitochondrial aldehyde dehydrogenase in nitroglycerin bioactivation. Proc Natl Acad Sci USA 102: 12159-12164, 2005. (Pubitemid 41291145)
4. Chen Z, Zhang J, and Stamler JS. Identification of the enzymatic mechanism of nitroglycerin bioactivation. Proc Natl Acad Sci USA 99: 8306-8311, 2002. (Pubitemid 34651048)
5. Dai T, Tian Y, Tocchetti CG, Katori T, Murphy AM, Kass DA, Paolocci N, and Gao WD. Nitroxyl increases force development in rat cardiac muscle. J Physiol 580: 951-960, 2007. (Pubitemid 46909044)
6. Daiber A, Wenzel P, Oelze M, and Münzel T. New insights into bioactivation of organic nitrates, nitrate tolerance and cross-tolerance. Clin Res Cardiol 97: 12-20, 2008.
7. De Witt BJ, Marrone JR, Kaye AD, Keefer LK, and Kadowitz PJ. Comparison of responses to novel nitric oxide donors in the feline pulmonary vascular bed. Eur J Pharmacol 430: 311-315, 2001. (Pubitemid 33050056)
8. DeMaster EG, Redfern B, and Nagasawa HT. Mechanisms of inhibition of aldehyde dehydrogenase by nitroxyl, the active metabolite of the alcohol deterrent agent cyanamide. Biochem Pharmacol 55: 2007-2015, 1998. (Pubitemid 28477471)
9. DeMaster EG, Refern B, Quast BJ, Dahlseid T, and Nagasawa HT. Mechanism for the inhibition of aldehyde dehydrogenase by nitric oxide. Alcohol 14: 181-189, 1997. (Pubitemid 27147337)
10. Dikalov S, Fink B, Skatchkov M, Stalleicken D, and Bassenge E. Formation of reactive oxygen species by pentaerithrity-ltetranitrate and glyceryl trinitrate in vivo and development of nitrate tolerance. J Pharmacol Exp Ther 286: 938-944, 1998. (Pubitemid 29003488)
11. Ellis A, Li CG, and Rand MJ. Differential actions of L-cysteine on responses to nitric oxide, nitroxyl anions and EDRF in the rat aorta. Br J Pharmacol 129: 315-322, 2000. (Pubitemid 30072652)
12. Favaloro JL and Kemp-Harper BK. The nitroxyl anion (HNO) is a potent dilator of rat coronary vasculature. Car-diovasc Res 73: 587-596, 2007. (Pubitemid 46073951)
13. Favaloro JL and Kemp-Harper BK. Redox variants of NO (NO and HNO) elicit vasorelaxation of resistance arteries via distinct mechanisms. Am J Physiol Heart Circ Physiol 296: H1274-1280, 2009.
14. Fukuto JM, Chiang K, Hszieh R, Wong PSY, and Chaudhurri G The pharmacological activity of nitroxyl: A potent vasodilator with activity similar to nitric oxide and/or endothelium-derived relaxing factor. J Pharmacol Exp Ther 263: 546-551, 1992.
15. Gori T, Mak SS, Kelly S, and Parker JD. Evidence supporting abnormalities in nitric oxide synthase function induced by nitroglycerin in humans. J Am Coll Cardiol 38: 1096-1101, 2001. (Pubitemid 32912717)
16. v channels to vasodilate resistance arteries. Hypertension 41: 1301-1307, 2003. (Pubitemid 36706081)
17. Irvine JC, Favaloro JL, Widdop RE, and Kemp-Harper BK. Nitroxyl anion donor, Angeli's salt, does not develop tolerance in rat isolated aortae. Hypertension 49: 885-892, 2007. (Pubitemid 351664199)
18. Irvine JC, Ritchie RH, Favaloro JL, Andrews KL, Widdop RE, and Kemp-Harper BK. Nitroxyl (HNO): The Cinderella of the nitric oxide story. Trends Pharmacol Sci 29: 601-608, 2008.
19. Kim D, Rybalkin SD, Pi X, Wang Y, Zhang C, Munzel T, Beavo JA, Berk BC, and Yan C. Upregulation of phospho-diesterase 1A1 expression is associated with the development of nitrate tolerance. Circulation 104: 2338-2343, 2001. (Pubitemid 33049518)
20. Kollau A, Hofer A, Russwurm M, Koesling D, Keung WM, Schmidt K, Brunner F, and Mayer B. Contribution of aldehyde dehydrogenase to mitochondrial bioactivation of ni-troglycerin: Evidence for the activation of purified soluble guanylate cyclase through direct formation of nitric oxide. Biochem J 385: 769-777, 2005. (Pubitemid 40208838)
21. Lancel S, Zhang J, Evangelista A, Trucillo MP, Tong X, Siwik DA, Cohen RA, and Colucci WS. Nitroxyl activates SERCA in cardiac myocytes via glutathiolation of cysteine 674. Circ Res 104: 720-723, 2009.
22. Laursen JB, Boesgaard S, Poulsen HE, and Aldershvile J. Nitrate tolerance impairs nitric oxide-mediated vasodilation in vivo. Cardiovasc Res 31: 814-819, 1996.
23. Ma XL, Gao F, Liu G-L, Lopez BL, Christopher TA, Fukuto JM, Wink DA, and Feelisch M. Opposite effects of nitric oxide and nitroxyl on postischemic myocardial injury. Proc Natl Acad Sci USA 96: 14617-14622, 1999. (Pubitemid 30000699)
24. MacPherson JD, Gillespie TD, Dunkerley HA, Maurice DH, and Bennett BM. Inhibition of phosphodiesterase 5 selectively reverses nitrate tolerance in the venous circulation. J Pharmacol Exp Ther 317: 188-195, 2006.
25. Mergia E, Friebe A, Dangel O, Russwurm M, and Koesling D. Spare guanylyl cyclase NO receptors ensure high NO sensitivity in the vascular system. J Clin Invest 116: 1731-1737, 2006.
26. Miranda KM, Katori T, Torres de Holding CL, Thomas L, Ridnour LA, McLendon WJ, Cologna SM, Dutton AS, Champion HC, Mancardi D, Tocchetti CG, Saavedra JE, Keefer LK, Houk KN, Fukuto JM, Kass DA, Paolocci N, and Wink DA. Comparison of the NO and HNO donating properties of diazeniumdiolates: Primary amine adducts release HNO in vivo. J Med Chem 48: 8220-8228, 2005. (Pubitemid 43032530)
27. Miranda KM, Nims RW, Thomas DD, Espey MG, Citrin D, Bartberger MD, Paolocci N, Fukuto JM, Feelisch M, and Wink DA. Comparison of the reactivity of nitric oxide and nitroxyl with heme proteins. A chemical discussion of the differential biological effects of these redox related products of NOS. J Inorg Biochem 93: 52-60, 2003. (Pubitemid 36132133)
28. Miranda KM, Paolocci N, Katori T, Thomas DD, Ford E, Bartberger MD, Espey MG, Kass DA, Feelisch M, Fukuto JM, and Wink DA. A biochemical rationale for the discrete behavior of nitroxyl and nitric oxide in the cardiovascular system. Proc Natl Acad Sci USA 100: 9196-9201, 2003. (Pubitemid 37033906)
29. Miranda KM, Yamada K, Espey MG, Thomas DD, DeGraff WG, Mitchell JB, Krishna MC, Colton CA, and Wink DA. Further evidence for distinct reactive intermediates from nitroxyl and peroxynitrite: Effects of buffer composition on the chemistry of Angeli's salt and synthetic peroxynitrite. Arch Biochem Biophys 401: 134-144, 2002. (Pubitemid 34848615)
30. Mullershausen F, Lange A, Mergia E, Friebe A, and Koesling D. Desensitization of NO=cGMP signaling in smooth muscle: Blood vessels versus airways. Mol Pharmacol 69: 1969- 1974, 2006. (Pubitemid 43894315)
31. Mulsch A, Oelze M, Kloss S, Mollnau H, Topfer A, Smo-lenski A, Walter U, Stasch JP, Warnholtz A, Hink U, Mei-nertz T, and 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 103: 2188-2194, 2001. (Pubitemid 32463296)
32. Munzel T, Hink U, Yigit H, Macharzina R, Harrison DG, and Mulsch A. Role of superoxide dismutase in in vivo and in vitro nitrate tolerance. Br J Pharmacol 127: 1224-1230, 1999. (Pubitemid 29326646)
33. Munzel T, Li H, Mollnau H, Hink U, Matheis E, Hartmann M, Oelze M, Skatchkov M, Warnholtz A, Duncker L, Mei-nertz T and 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 86: e7-e12, 2000.
34. Munzel TT, Daiber AA and Mulsch AA. Explaining the phenomenon of nitrate tolerance. Circ Res 97: 618-628, 2005.
35. Pagliaro P, Mancardi D, Rastaldo R, Penna C, Gattullo D, Miranda KM, Feelisch M, Wink DA, Kass DA and Paolocci N. Nitroxyl affords thiol-sensitive myocardial protective effects akin to early preconditioning. Free Radic Biol Med 34: 33-43, 2003. (Pubitemid 36043884)
36. Paolocci N, Jackson MI, Lopez BE, Miranda K, Tocchetti CG, Wink DA, Hobbs AJ and Fukuto JM. The pharmacology of nitroxyl (HNO) and its therapeutic potential: not just the Janus face of NO. Pharmacol Ther 113: 442-458, 2007.
37. Paolocci N, Katori T, Champion HC, St. John ME, Miranda KM, Fukuto JM, Wink DA, and Kass DA. Positive inotropic and lusitropic effects of HNO/NO∼ in failing hearts: Independence from ß-adrenergic signaling. Proc Natl Acad Sci USA 100: 5537-5542, 2003. (Pubitemid 36542740)
38. Paolocci N, Saavedra WF, Miranda KM, Martignani C, Isoda T, Hare JM, Espey MG, Fukuto JM, Feelisch M, Wink DA, and Kass DA. Nitroxyl anion exerts redox-sensitive positive cardiac inotropy in vivo by calcitonin gene-related peptide signaling. Proc Natl Acad Sci USA 98: 10463-10468, 2001. (Pubitemid 32803042)
39. Plane F, Sampson LJ, Smith JJ, and Garland CJ. Relaxation to authentic nitric oxide and SIN-1 in rat isolated mesenteric arteries: Variable role for smooth muscle hyperpolarization. Br J Pharmacol 133: 665-672, 2001. (Pubitemid 32642872)
40. Ritchie RH, Irvine JC, Rosenkranz AC, Patel R, Wendt IR, Horowitz JD, and Kemp-Harper BK. Exploiting cGMP-based therapies for the prevention of left ventricular hypertrophy: NO" and beyond. Pharmacol Ther 124: 279-300, 2009.
41. Sydow K, Daiber A, Oelze M, Cheng Z, August M, Wendt M, Ullrich V, Mulsch A, Schulz E, Keaney JF, Stamler JS, and Munzel T. Central role of mitochondrial aldehyde dehydrogenase and reactive oxygen species in nitroglycerin tolerance and cross-tolerance. J Clin Invest 113: 482-489, 2004. (Pubitemid 38544192)
42. Tocchetti CG, Wang W, Froehlich JP, Huke S, Aon MA, Wilson GM, Di Benedetto G, O'Rourke B, Gao WD, Wink DA, Toscano JP, Zaccolo M, Bers DM, Valdivia HH, Cheng H, Kass DA, and Paolocci N. Nitroxyl improves cellular heart function by directly enhancing cardiac sarcoplasmic reticulum Ca2+ cycling. Circ Res 100: 96-104, 2007. (Pubitemid 46066777)
43. Vleeming W, van de Kuil A, te Biesebeek JD, Meulenbelt J, and Boink AB. Effect of nitrite on blood pressure in anaesthetized and free-moving rats. Food Chem Toxicol 35: 615-619, 1997. (Pubitemid 27273783)
44. Wang EQ, Lee WI, and Fung HL. Lack of critical involvement of endothelial nitric oxide synthase in vascular nitrate tolerance in mice. Br J Pharmacol 135: 299-302, 2002. (Pubitemid 34151161)
45. Wanstall JC, Jeffery TK, Gambino A, Lovren F, and Triggle CR. Vascular smooth muscle relaxation mediated by nitric oxide donors: A comparison with acetylcholine, nitric oxide and nitroxyl ion. Br J Pharmacol 134: 463-472, 2001. (Pubitemid 32977891)
46. Wenzel P, Oelze M, Coldewey M, Hortmann M, Seeling A, Hink U, Mollnau H, Stalleicken D, Weiner H, Lehmann J, Li H, Forstermann U, Munzel T, and Daiber A. Heme oxyge-nase-1: A novel key player in the development of tolerance in response to organic nitrates. Arterioscler Thromb Vasc Biol 27: 1729-1735, 2007. (Pubitemid 47207167)
47. Wiley KE and Davenport AP. Comparison of the effects of atherosclerosis and nitrate therapy on responses to nitric oxide and endothelin-1 in human arteries in vitro. Clin Sci 103: 124S-127S, 2002. (Pubitemid 35007135)
48. Zamora Pino R and Feelisch M. Bioassay discrimination between nitric oxide and nitroxyl using L-cysteine. Biochem Biophys Res Commun 201: 54-62, 1994. (Pubitemid 24213693)