Generation of nitroxyl by heme protein-mediated peroxidation of hydroxylamine but not N-hydroxy-L-arginine

Free Radical Biology and Medicine

Volumn 45, Issue 5, 2008, Pages 578-584

  Donzelli, Sonia ^a   Espey, Michael Graham ^a   Flores Santana, Wilmarie ^a   Switzer, Christopher H ^a   Yeh, Grace C ^b   Huang, Jinming ^c   Stuehr, Dennis J ^d   King, S Bruce ^c   Miranda, Katrina M ^e   Wink, David A ^a  

^a NATIONAL CANCER INSTITUTE   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c WAKE FOREST UNIVERSITY   (United States)

^d LERNER RESEARCH INSTITUTE   (United States)

^e University of Arizona   (United States)

Author keywords

Heme; Hydroxylamine; N Hydroxy L arginine; Nitroxyl; Peroxidase; Sulfinamide

Indexed keywords

ARGININE DERIVATIVE; CATALASE; CYSTEINE; CYTOCHROME P450; GLUTATHIONE; HEMIN; HEMOGLOBIN; HEMOPROTEIN; HISTIDINE; HORSERADISH PEROXIDASE; HYDROXYLAMINE; LACTOPEROXIDASE; MYELOPEROXIDASE; MYOGLOBIN; NITRIC OXIDE; NITRIC OXIDE SYNTHASE; PEROXIDASE; SULFINAMIDE; TYROSINE;

ARTICLE; BIOSYNTHESIS; CELL STRAIN MCF 7; CHEMICAL REACTION; CHEMOLUMINESCENCE; ELECTRON SPIN RESONANCE; ENZYME ACTIVITY; FLUORESCENCE; GAS CHROMATOGRAPHY; HEART MUSCLE CELL; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HUMAN; HUMAN CELL; OXIDATION; PEROXIDATION; PRIORITY JOURNAL;

ARGININE; CELL LINE, TUMOR; ELECTRON SPIN RESONANCE SPECTROSCOPY; GLUTATHIONE; HEMEPROTEINS; HUMANS; HYDROXYLAMINE; NITROGEN OXIDES; PEROXIDES;

ARMORACIA RUSTICANA;

EID: 48649103143     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2008.04.036     Document Type: Article

References (69)

1. Paolocci N., Saavedra W.F., Miranda K.M., Martignani C., Isoda T., Hare J.M., Espey M.G., Fukuto J.M., Feelisch M., Wink D.A., and Kass D.A. Nitroxyl anion exerts redox-sensitive positive cardiac inotropy in vivo by calcitonin gene-related peptide signaling. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10463-10468
2. Paolocci N., Katori T., Champion H.C., St. John M.E., Miranda K.M., Fukuto J.M., Wink D.A., and Kass D.A. Positive inotropic and lusitropic effects of HNO/NO- in failing hearts: independence from b-adrenergic signaling. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 5537-5542
3. Pagliaro P., Mancardi D., Rastaldo R., Penna C., Gattullo D., Miranda K.M., Feelisch M., Wink D.A., Kass D.A., and Paolocci N. Nitroxyl affords thiol-sensitive myocardial protective effects akin to early preconditioning. Free Radic. Biol. Med. 34 (2003) 33-43
4. Ma X.L., Gao F., Liu G.L., Lopez B.L., Christopher T.A., Fukuto J.M., Wink D.A., and Feelisch M. Opposite effects of nitric oxide and nitroxyl on postischemic myocardial injury. Proc. Natl. Acad. Sci. U. S. A. 96 (1999) 14617-14622
5. + channels to vasodilate resistance arteries. Hypertension 41 (2003) 1301-1307
6. 2+ release from skeletal and cardiac sarcoplasmic reticulum by oxidizing ryanodine receptors. Cell Calcium 37 (2005) 87-96
7. Kim W.K., Choi Y.B., Rayudu P.V., Das P., Asaad W., Arnelle D.R., Stamler J.S., and Lipton S.A. Attenuation of NMDA receptor activity and neurotoxicity by nitroxyl anion, NO-. Neuron 24 (1999) 461-469
8. Colton C.A., Gbadegesin M., Wink D.A., Miranda K.M., Espey M.G., and Vicini S. Nitroxyl anion regulation of the NMDA receptor. J. Neurochem. 78 (2001) 1126-1134
9. Hewett S.J., Espey M.G., Uliasz T.F., and Wink D.A. Neurotoxicity of nitroxyl: insights into HNO and NO biochemical imbalance. Free Radic. Biol. Med. 39 (2005) 1478-1488
10. 2+ cycling. Circ. Res. 100 (2007) 96-104
11. Miranda K.M., Paolocci N., Katori T., Thomas D.D., Ford E., Bartberger M.D., Espey M.G., Kass D.A., Feelisch M., Fukuto J.M., and Wink D.A. A biochemical rationale for the discrete behavior of nitroxyl and nitric oxide in the cardiovascular system. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 9196-9201
12. Wink D.A., Miranda K.M., Katori T., Mancardi D., Thomas D.D., Ridnour L.A., Espey M.G., Feelisch M., Colton C.A., Fukuto J.M., Pagliaro P., Kass D.A., and Paolocci N. Orthogonal properties of the redox siblings nitroxyl and nitric oxide in the cardiovascular system: a novel redox paradigm. Am. J. Physiol. Heart Circ. Physiol. 285 (2003) H2264-H2276
13. Miranda K.M. The chemistry of nitroxyl (HNO) and implications in biology. Coordin. Chem. Rev. 249 (2005) 433-455
14. Feelisch M. Nitroxyl gets to the heart of the matter. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 4978-4980
15. Ferguson J.K.W. A new drug for alcoholism treatment. Can. Med. Assoc. J. 74 (1956) 793-795
16. Nagasawa H.T., DeMaster E.G., Redfern B., Shirota F.N., and Goon D.J. Evidence for nitroxyl in the catalase-mediated bioactivation of the alcohol deterrent agent cyanamide. J. Med. Chem. 33 (1990) 3120-3122
17. Kim-Shapiro D.B., King S.B., Bonifant C.L., Kolibash C.P., and Ballas S.K. Time resolved absorption study of the reaction of hydroxyurea with sickle cell hemoglobin. Biochim. Biophys. Acta 1380 (1998) 64-74
18. King S.B. The nitric oxide producing reactions of hydroxyurea. Curr. Med. Chem. 10 (2003) 437-452
19. Pufahl R.A., Wishnok J.S., and Marletta M.A. Hydrogen peroxide-supported oxidation of N-G-hydroxy-L-arginine by nitric oxide synthase. Biochemistry 34 (1995) 1930-1941
20. Schmidt H.H.H.W., Hofmann H., Schindler U., Shutenko Z.S., Cunningham D.D., and Feelisch M. No NO from NO synthase. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 14492-14497
21. Clague M.J., Wishnok J.S., and Marletta M.A. Formation of N-delta-cyanoornithine from NG-hydroxy-L-arginine and hydrogen peroxide by neuronal nitric oxide synthase: implications for mechanism. Biochemistry 36 (1997) 14465-14473
22. Rusche K.M., Spiering M.M., and Marletta M.A. Reactions catalyzed by tetrahydrobiopterin-free nitric oxide synthase. Biochemistry 37 (1998) 15503-15512
23. Adak S., Wang Q., and Stuehr D.J. Arginine conversion to nitroxide by tetrahydrobiopterin-free neuronal nitric-oxide synthase-implications for mechanism. J. Biol. Chem. 275 (2000) 33554-33561
24. Hobbs A.J., Fukuto J.M., and Ignarro L.J. Formation of free nitric oxide from L-arginine by nitric oxide synthase-direct enhancement of generation by superoxide dismutase. Proc. Natl. Acad. Sci. U. S. A. 91 (1994) 10992-10996
25. Oae S., Kim Y.H., Fukushima D., and Shinhama K. New syntheses of thionitrites and their chemical reactivities. J. Chem. Soc., Perkin Trans. 1 (1978) 913-917
26. Schulz U., and McCalla D.R. Reactions of cysteine with N-methyl-N-nitroso-P-toluenesulfonamide and N-methyl-N′-nitro-N-nitrosoguanidine. Can. J. Chem. 47 (1969) 2021-2027
27. Arnelle D.R., and Stamler J.S. NO+, NO, and NO- donation by S-nitrosothiols- implications for regulation of physiological functions by S- nitrosylation and acceleration of disulfide formation. Arch. Biochem. Biophys. 318 (1995) 279-285
28. Hogg N., Singh R.J., and Kalyanaraman B. The role of glutathione in the transport and catabolism of nitric oxide. FEBS Lett. 382 (1996) 223-228
29. Reeder B.J., and Wilson M.T. Hemoglobin and myoglobin associated oxidative stress: from molecular mechanisms to disease states. Curr. Med. Chem. 12 (2005) 2741-2751
30. Osawa Y., and Williams M.S. Covalent crosslinking of the heme prosthetic group to myoglobin by H2O2: toxicological implications. Free Radic. Biol. Med. 21 (1996) 35-41
31. Buga G.M., Singh R., Pervin S., Rogers N.E., Schmitz D.A., Jenkinson C.P., Cederbaum S.D., and Ignarro L.J. Arginase activity in endothelial cells: inhibition by NG-hydroxy-L-arginine during high-output NO production. Am. J. Physiol. 271 (1996) H1988-H1998
32. Gwilt P.R., and Tracewell W.G. Pharmacokinetics and pharmacodynamics of hydroxyurea. Clin. Pharmacokinet. 34 (1998) 347-358
33. Donzelli S., Espey M.G., Thomas D.D., Mancardi D., Tocchetti C.G., Ridnour L.A., Paolocci N., King S.B., Miranda K.M., Lazzarino G., Fukuto J.M., and Wink D.A. Discriminating HNO formation from that of other reactive nitrogen oxide species. Free Radic. Biol. Med. 40 (2006) 1056-1066
34. Paulus W.J., Vantrimpont P.J., and Shah A.M. Acute effects of nitric oxide on left ventricular relaxation and diastolic distensibility in humans. Assessment by bicoronary sodium nitroprusside infusion. Circulation 89 (1994) 2070-2078
35. Wong P.S.Y., Hyun J., Fukuto J.M., Shirota F.N., DeMaster E.G., Shoeman D.W., and Nagasawa H.T. Reaction between S-nitrosothiols and thiols: generation of nitroxyl (HNO) and subsequent chemistry. Biochemistry 37 (1998) 5362-5371
36. Espey M.G., Miranda K.M., Thomas D.D., and Wink D.A. Ingress and reactive chemistry of nitroxyl-derived species within human cells. Free Radic. Biol. Med. 33 (2002) 827-834
37. Archer S. Measurement of nitric oxide in biological models. FASEB J. 7 (1993) 349-360
38. Miranda K.M., Katori T., Torres de Holding C.L., Thomas L., Ridnour L.A., McLendon W.J., Dutton A.S., Champion H.C., Mancardi D., Tocchetti C.G., Saavedra J.E., Keefer L.K., Houk K.N., Fukuto J.M., Kass D.A., Paolocci N., and Wink D.A. Comparison of the NO and HNO donating properties of diazeniumdiolates: primary amine adducts release HNO in vivo. J. Med. Chem. 48 (2005) 8220-8228
39. Smith P.A.S., and Hein G.E. The alleged role of nitroxyl in certain reactions of aldehydes and alkyl halides. J. Am. Chem. Soc. 82 (1960) 5731-5740
40. Kohout F.C., and Lampe F.W. On the role of the nitroxyl molecule in the reaction of hydrogen atoms with nitric oxide. J. Am. Chem. Soc. 87 (1965) 5795-5796
41. Miranda K.M., Espey M.G., Yamada K., Krishna M., Ludwick N., Kim S., Jourd'heuil D., Grisham M.B., Feelisch M., Fukuto J.M., and Wink D.A. Unique oxidative mechanisms for the reactive nitrogen oxide species, nitroxyl anion. J. Biol. Chem. 276 (2001) 1720-1727
42. Miranda K.M., Yamada K., Espey M.G., Thomas D.D., DeGraff W., Mitchell J.B., Krishna M.C., Colton C.A., and Wink D.A. 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 (2002) 134-144
43. Miranda K.M., Dutton A.S., Ridnour L.A., Foreman C.A., Ford E., Paolocci N., Katori T., Tocchetti C.G., Mancardi D., Thomas D.D., Espey M.G., Houk K.N., Fukuto J.M., and Wink D.A. Mechanism of aerobic decomposition of Angeli's salt (sodium trioxodinitrate) at physiological pH. J. Am. Chem. Soc. 127 (2005) 722-731
44. Katori T., Hoover D.B., Ardell J.L., Helm R.H., Belardi D.F., Tocchetti C.G., Forfia P.R., Kass D.A., and Paolocci N. Calcitonin gene-related peptide in vivo positive inotropy is attributable to regional sympatho-stimulation and is blunted in congestive heart failure. Circ. Res. 96 (2005) 234-243
45. Katori T., Donzelli S., Tocchetti C.G., Miranda K.M., Cormaci G., Thomas D.D., Ketner E.A., Lee M.J., Mancardi D., Wink D.A., Kass D.A., and Paolocci N. Peroxynitrite and myocardial contractility: in vivo versus in vitro effects. Free Radic. Biol. Med. 41 (2006) 1606-1618
46. Espey M.G., Miranda K.M., Thomas D.D., and Wink D.A. Distinction between nitrosating mechanisms within human cells and aqueous solution. J. Biol. Chem. 276 (2001) 30085-30091
47. Saavedra J.E., Southan G.J., Davies K.M., Lundell A., Markou C., Hanson S.R., Adrie C., Hurford W.E., Zapol W.M., and Keefer L.K. Localizing antithrombotic and vasodilatory activity with a novel, ultrafast nitric oxide donor. J. Med. Chem. 39 (1996) 4361-4365
48. King S.B. N-hydroxyurea and acyl nitroso compounds as nitroxyl (HNO) and nitric oxide (NO) donors. Curr. Top. Med. Chem. 5 (2005) 665-673
49. Fukuto J.M., Wallace G.C., Hszieh R., and Chaudhuri G. Chemical oxidation of N-hydroxyguanidine compounds: release of nitric oxide, nitroxyl and possible relationship to the mechanism of biological nitric oxide generation. Biochem. Pharmacol. 43 (1992) 607-613
50. Fukuto J.M., Stuehr D.J., Feldman P.L., Bova M.P., and Wong P. Peracid oxidation of an N-hydroxyguanidine compound-a chemical model for the oxidation of N-omega-hydroxy-L-arginine by nitric oxide synthase. J. Med. Chem. 36 (1993) 2666-2670
51. Fukuto J.M., Switzer C.H., Miranda K.M., and Wink D.A. Nitroxyl (HNO): chemistry, biochemistry, and pharmacology. Annu. Rev. Pharmacol. Toxicol. 45 (2005) 335-355
52. Stuehr D.J., Kwon N.S., Nathan C.F., Griffith O.W., Feldman P.L., and Wiseman J. N-omega-hydroxy-L-arginine is an intermediate in the biosynthesis of nitric oxide from L-arginine. J. Biol. Chem. 266 (1991) 6259-6263
53. Wallace G.C., Gulati P., and Fukuto J.M. N-omega-Hydroxy-L-arginine: a novel arginine analog capable of causing vasorelaxation in bovine intrapulmonary artery. Biochem. Biophys. Res. Commun. 176 (1991) 528-534
54. Katsuki S., Arnold W., Mittal C.K., and Murad F. Stimulation of guanylate cyclase by sodium nitroprusside, nitroglycerin and nitric oxide in various tissue preparations and comparison to the effects of sodium azide and hydroxylamine. J. Cyclic. Nucleotide Res. 3 (1977) 23-35
55. Shafirovich V., and Lymar S.V. Nitroxyl and its anion in aqueous solutions: spin states, protic equilibria, and reactivities toward oxygen and nitric oxide. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 7340-7345
56. Liochev S.I., and Fridovich I. The mode of decomposition of Angeli's salt (Na2N2O3) and the effects thereon of oxygen, nitrite, superoxide dismutase, and glutathione. Free Radic. Biol. Med. 34 (2003) 1399-1404
57. Ford P.C., and Lorkovic I.M. Mechanistic aspects of the reactions of nitric oxide with transition-metal complexes. Chem. Rev. 102 (2002) 993-1018
58. Liebmann J.E., Hahn S.M., Cook J.A., Lipschultz C., Mitchell J.B., and Kaufman D.C. Glutathione depletion by L-buthionine sulfoximine antagonizes taxol cytotoxicity. Cancer Res. 53 (1993) 2066-2070
59. DeMaster E.G., Shirota F.N., and Nagasawa H.T. The metabolic activation of cyanamide to an inhibitor of aldehyde dehydrogenase is catalyzed by catalase. Biochem. Biophys. Res. Commun. 122 (1984) 358-365
60. Fukuto J.M., Chiang K., Hszieh R., Wong P., and Chaudhuri 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 (1992) 546-551
61. De Witt B.J., Marrone J.R., Kaye A.D., Keefer L.K., and Kadowitz P.J. Comparison of responses to novel nitric oxide donors in the feline pulmonary vascular bed. Eur. J. Pharmacol. 430 (2001) 311-315
62. Cook N.M., Shinyashiki M., Jackson M.I., Leal F.A., and Fukuto J.M. Nitroxyl-mediated disruption of thiol proteins: inhibition of the yeast transcription factor Ace1. Arch. Biochem. Biophys. 410 (2003) 89-95
63. Aniruddha S., Vidwans T.F.U., Hewett J.A., and Hewett S.J. Differential modulation of prostaglandin H synthase-2 by nitric oxide-related species in intact cells. Biochemistry 40 (2001) 11533-11542
64. Naughton P., Foresti R., Bains S.K., Hoque M., Green C.J., and Motterlini R. Induction of heme oxygenase 1 by nitrosative stress. J. Biol. Chem. 277 (2002) 40666-40674
65. Costa G., Labadia A., Triguero D., Jimenez E., and Garcia-Pascual A. Nitrergic relaxation in urethral smooth muscle: involvement of potassium channels and alternative redox forms of NO. Naunyn-Schmiedebergs Arch. Pharmacol. 364 (2001) 516-523
66. DeMaster E.G., Redfern B., and Nagasawa H.T. Mechanisms of inhibition of aldehyde dehydrogenase by nitroxyl, the active metabolite of the alcohol deterrent agent cyanamide. Biochem. Pharmacol. 55 (1998) 2007-2015
67. Huang Y. Hydroxylamine-induced relaxation inhibited by K+ channel blockers in rat aortic rings. Eur. J. Biochem. 349 (1998) 53-60
68. Booth B.P., Tabrizi-Fard M.A., and Fung H.L. Calcitonin gene-related peptide-dependent vascular relaxation of rat aorta-an additional mechanism for nitroglycerin. Biochem. Pharmacol. 59 (2000) 1603-1609
69. Zhang R., Pinson A., and Samuni A. Both hydroxylamine and nitroxide protect cardiomyocytes from oxidative stress. Free Radic. Biol. Med. 24 (1998) 66-75