The nitroxyl donor, Angeli's salt, inhibits inflammatory hyperalgesia in rats

Neuropharmacology

Volumn 71, Issue , 2013, Pages 1-9

  Zarpelon, Ana C ^a   Souza, Guilherme R ^b   Cunha, Thiago M ^b   Schivo, Ieda R S ^b   Marchesi, Mario ^c   Casagrande, Rubia ^a   Pinge Filho, Phileno ^a   Cunha, Fernando Q ^b   Ferreira, Sergio H ^b   Miranda, Katrina M ^c   Verri, Waldiceu A ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c University of Arizona   (United States)

Author keywords

Angeli's salt; Cytokine; Nitric oxide; Nitroxyl; Nociception; Pain

Indexed keywords

ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; NITRIC ACID DERIVATIVE; NITROXYL; PROSTAGLANDIN E2; SODIUM TRIOXODINITRATE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOSE TIME EFFECT RELATION; ENZYME LINKED IMMUNOSORBENT ASSAY; HYPERALGESIA; IN VIVO STUDY; INFLAMMATION; MALE; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SIGNAL TRANSDUCTION; SPINAL GANGLION;

EID: 84878164869     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2013.03.009     Document Type: Article

References (59)

1. S. Adak, Q. Wang, and D.J. Stuehr Arginine conversion of nitroxide by tetrahydrobiopterin-free neuronal nitric-oxide synthase J. Biol. Chem. 275 2000 33554 33561
2. K.O. Aley, and J.D. Levine Role of protein kinase A in the maintenance of inflammatory pain J. Neurosci. 19 1999 2181 2186
3. K.L. Andrews, J.C. Irvine, M. Tare, J. Apostolopoulos, J.L. Favaloro, C.R. Triggle, and B.K. Kemp-Harper A role for nitroxyl (HNO) as an endothelium-derived relaxing and hyperpolarizing factor in resistance arteries Br. J. Pharmacol. 157 2009 540 550
4. - 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
5. C.F. Benjamim, S.H. Ferreira, and F.Q. Cunha Role of nitric oxide in the failure of neutrophil migration in sepsis J. Infect. Dis. 182 2000 214 223
6. F.T. Bonner, and B. Ravid Thermal decomposition of oxyhyponitrite (sodium trioxodinitrate(II)) in aqueous solution Inorg. Chem. 14 1975 558 563
7. F.Q. Cunha, M.M. Teixeira, and S.H. Ferreira Pharmacological modulation of secondary mediator systems-cyclic AMP and cyclic GMP-on inflammatory hyperalgesia Br. J. Pharmacol. 127 1999 671 678
8. T.M. Cunha, D. Roman-Campos, C.M. Lotufo, H.L. Duarte, G.R. Souza, W.A. Verri Jr., M.I. Funez, Q.M. Dias, I.R. Schivo, A.C. Domingues, D. Sachs, S. Chiavegatto, M.M. Teixeira, J.S. Hothersall, J.S. Cruz, F.Q. Cunha, and S.H. Ferreira Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway Proc. Natl. Acad. Sci. 107 2010 4442 4447
9. Y. Cury, G. Picolo, V.P. Gutierrez, and S.H. Ferreira Pain and analgesia: the dual effect of nitric oxide in the nociceptive system Nitric Oxide 25 2011 243 254
10. S. Donzelli, M.G. Espey, W. Flores-Santana, C.H. Switzer, G.C. Yeh, J. Huang, D.J. Stuehr, S.B. King, K.M. Miranda, and D.A. Wink Generation of nitroxyl by heme protein-mediated peroxidation of hydroxylamine but not N-hydroxy-L-arginine Free Radic. Biol. Med. 45 2008 578 584
11. M.G. Espey, K.M. Miranda, D.D. Thomas, and D.A. Wink Ingress and reactive chemistry of nitroxyl-derived species within human cells Free Radic. Biol. Med. 33 2002 827 834
12. A.R. Evans, M.R. Vasko, and G.D. Nicol The cAMP transduction cascade mediates the PGE2-induced inhibition of potassium currents in rat sensory neurones J. Physiol. 516 1999 163 178
13. J.L. Favaloro, and B.K. Kemp-Harper The nitroxyl anion (HNO) is a potent dilator of rat coronary vasculature Cardiovasc. Res. 73 2007 587 596
14. S.H. Ferreira Prostaglandins, aspirin-like drugs and analgesia Nat. New Biol. 240 1972 200 203
15. S.H. Ferreira, B.B. Lorenzetti, and F.M.A. Correa Central and peripheral antialgesic action of aspirin-like drugs Eur. J. Pharmacol. 53 1978 39 48
16. S.H. Ferreira, I.D. Duarte, and B.B. Lorenzetti The molecular mechanism of action of peripheral morphine analgesia: stimulation of the cGMP system via nitric oxide release Eur. J. Pharmacol. 201 1991 121 122
17. J.M. Fukuto, G.C. Wallace, R. Hszieh, and G. Chaudhuri 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
18. R.F. Furchgott, and J.V. Zawadzki The obligatory role of endothelial cells in the relaxation of arterial smooth muscle by acetylcholine Nature 288 1980 373 376
19. B. Furlong, A.H. Henderson, M.J. Lewis, and J.A. Smith Endothelium-derived relaxing factor inhibits in vitro platelet aggregation Br. J. Pharmacol. 90 1987 687 692
20. M.S. Gold, J.D. Levine, and A.M. Correa Modulation of TTX-R INa by PKC and PKA and their role in PGE2-induced sensitization of rat sensory neurons in vitro J. Neurosci. 18 1998 10345 10355
21. A.J. Gow, and J.S. Stamler Reactions between nitric oxide and haemoglobin under physiological conditions Nature 391 1998 169 173
22. C. Griffiths, V. Wykes, T.C. Bellamy, and J. Garthwaite A new and simple method for delivering clamped nitric oxide concentrations in the physiological range: application to activation of guanylyl cyclase-coupled nitric oxide receptors Mol. Pharmacol. 64 2003 1349 1356
23. A.J. Hobbs Soluble guanylate cyclase: the forgotten sibling Trends Pharmacol. Sci. 18 1997 484 491
24. A.J. Hobbs, J.M. Fukuto, and L.J. Ignarro 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. J.C. Irvine, J.L. Favaloro, and B.K. Kemp-Harper NO- activates soluble guanylate cyclase and Kv channels to vasodilate resistance arteries Hypertension 41 2003 1301 1307
26. J.C. Irvine, J.L. Favaloro, R.E. Widdop, and B.K. Kemp-Harper Nitroxyl anion donor, Angeli's salt, does not develop tolerance in rat isolated aortae Hypertension 49 2007 885 892
27. J.C. Irvine, R.H. Ritchie, J.L. Favaloro, K.L. Andrews, R.E. Widdop, and B.K. Kemp-Harper Nitroxyl (HNO): the Cinderella of the nitric oxide story Trends Pharmacol. Sci. 29 2008 601 608
28. X.G. Jin, S.R. Chen, X.H. Cao, L. Li, and H.L. Pan Nitric oxide inhibits nociceptive transmission by differentially regulating glutamate and glycine release to spinal dorsal horn neurons J. Biol. Chem. 286 2011 33190 33202
29. S.G. Khasar, Y.H. Lin, A. Martin, J. Dadgar, T. McMahon, D. Wang, B. Hundle, K.O. Aley, W. Isenberg, and G. McCarter A novel nociceptor signaling pathway revealed in protein kinase C epsilon mutant mice Neuron 24 1999 253 260
30. T. Koch, and V. Höllt Role of receptor internalization in opioid tolerance and dependence Pharmacol. Ther. 117 2008 199 206
31. H. Kojima, N. Nakatsubo, K. Kikuchi, S. Kawahara, Y. Kirino, H. Nagoshi, Y. Hirata, and T. Nagano Detection and imaging of nitric oxide with novel fluorescent indicators: diaminofluoresceins Anal. Chem. 70 1998 2446 2454
32. B.B. Lorenzetti, and S.H. Ferreira Mode of analgesic action of dipyrone: direct antagonism of inflammatory hyperalgesia Eur. J. Pharmacol. 114 1985 375 381
33. C.M. Maragos, D. Morley, D.A. Wink, T.M. Dunams, J.E. Saavedra, A. Hoffman, A.A. Bove, L. Isaac, J.A. Hrabie, and L.K. Keefer Complexes of NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects J. Med. Chem. 34 1991 3242 3247
34. K.M. Miranda, N. Paolocci, T. Katori, D.D. Thomas, E. Ford, M.D. Bartberger, M.G. Espey, D.A. Kass, M. Feelisch, J.M. Fukuto, and D.A. Wink 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
35. K.M. Miranda, H.T. Nagasawa, and J.P. Toscano Donors of HNO Curr. Top. Med. Chem. 5 2005 649 664
36. + channels (BK(Ca)) in smooth muscle cells isolated from the rat mesenteric artery Br. J. Pharmacol. 124 1998 1131 1140
37. S.S. Mizokami, N.S. Arakawa, S.R. Ambrosio, A.C. Zarpelon, R. Casagrande, T.M. Cunha, S.H. Ferreira, and W.A. Verri Jr. Kaurenoic acid from Sphagneticola trilobata inhibits inflammatory pain: effect on cytokine production GMP-Protein kinase G-ATP-sensitive potassium channel signaling pathway and activation of the NO-cyclic J. Nat. Prod. 75 2012 896 904
38. M.H. Napimoga, G.R. Souza, T.M. Cunha, L.F. Ferrari, J.T. Clemente-Napimoga, C.A. Parada, W.A. Verri Jr., F.Q. Cunha, and S.H. Ferreira 15d-prostaglandin J2 inhibits inflammatory hyperalgesia: involvement of peripheral opioid receptor J. Pharmacol. Exp. Ther. 324 2008 313 321
39. N. Paolocci, M.I. Jackson, B.E. Lopez, K. Miranda, C.G. Tocchetti, D.A. Wink, A.J. Hobbs, and J.M. Fukuto The pharmacology of nitroxyl (HNO) and its therapeutic potential: not just the janus face of NO Pharmacol. Ther. 113 2007 442 458
40. R.Z. Pino, and M. Feelisch Bioassay discrimination between nitric oxide (NO.) and nitroxyl (NO-) using L-cysteine Biochem. Biophys. Res. Commun. 201 1994 54 62
41. R.A. Pufahl, J.S. Wishnok, and M.A. Marletta Hydrogen peroxide supported oxidation of NG-hydroxyl-L-arginine by nitric oxide synthase Biochemistry 34 1995 1930 1941
42. K.M. Rusche, M.M. Spiering, and M.A. Marletta Reactions catalyzed by tetrahydrobiopterin-free nitric oxide synthase Biochemistry 37 1998 15503 15512
43. + channel pathway Proc. Natl. Acad. Sci. 101 2004 3680 3685
44. M. Saleem, and H. Ohshima Xanthine oxidase converts nitric oxide to nitroxyl that inactivates the enzyme Biochem. Biophys. Res. Commun. 315 2004 455 462
45. L.J. Sampson, F. Plane, and C.J. Garland Involvement of cyclic GMP and potassium channels in relaxation evoked by the nitric oxide donor, diethylamine NONOate, in the rat small isolated mesenteric artery Naunyn. Schmiedebergs. Arch. Pharmacol. 364 2001 220 225
46. T. Santodomingo-Garzón, T.M. Cunha, W.A. Verri Jr., D.A. Valério, C.A. Parada, S. Poole, S.H. Ferreira, and F.Q. Cunha Atorvastatin inhibits inflammatory hyperalgesia Br. J. Pharmacol. 149 2006 14 22
47. H.H.W. Schmidt, H. Hofmann, U. Schindler, Z.S. Shutenko, D.D. Cunningham, and M. Feelisch NO from NO synthase Proc. Natl. Acad. Sci. 93 1996 14492 14497
48. M.A. Sharpe, and C.E. Cooper Reactions of nitric oxide with mitochondrial cytochrome c: a novel mechanism for the formation of nitroxyl anion and peroxynitrite Biochem. J. 332 1998 9 19
49. P.A.S. Smith, and G.E. Hein The alleged role of nitroxyl in certain reactions of aldehydes and alkyl halides J. Am. Chem. Soc. 82 1960 5731 5746
50. C.R. Tonussi, and S.H. Ferreira Rat knee-joint carrageenin incapacitation test: an objective screen for central and peripheral analgesics Pain 48 1992 421 427
51. C.R. Tonussi, and S.H. Ferreira Mechanism of diclofenac analgesia: direct blockade of inflammatory sensitization Eur. J. Pharmacol. 251 1994 173 179
52. D.A. Valério, F.I. Ferreira, T.M. Cunha, J.C. Alves-Filho, F.O. Lima, J.R. De Oliveira, S.H. Ferreira, F.Q. Cunha, R.H. Queiroz, and W.A. Verri Jr. Fructose-1,6-bisphosphate reduces inflammatory pain-like behaviour in mice: role of adenosine acting on A1 receptors Br. J. Pharmacol. 158 2009 558 568
53. W.A. Verri Jr., T.M. Cunha, C.A. Parada, S. Poole, F.Q. Cunha, and S.H. Ferreira Hyperalgesic role of cytokines and chemokines: targets for analgesic drug development? Pharmacol. Ther. 112 2006 116 138
54. W.A. Verri Jr., F.O. Souto, S.M. Vieira, S.C. Almeida, S.Y. Fukada, D. Xu, J.C. Alves-Filho, T.M. Cunha, A.T. Guerrero, R.B. Mattos-Guimaraes, F.R. Oliveira, M.M. Teixeira, J.S. Silva, I.B. McInnes, S.H. Ferreira, P. Louzada-Junior, F.Y. Liew, and F.Q. Cunha IL-33 induces neutrophil migration in rheumatoid arthritis and is a target of anti-TNF therapy Ann. Rheum. Dis. 69 2010 1697 1703
55. Z.Q. Wang, F. Porreca, S. Cuzzocrea, K. Galen, R. Lightfoot, E. Masini, C. Muscoli, V. Mollace, M. Ndengele, H. Ischiropoulos, and D. Salvemini A newly identified role for superoxide in inflammatory pain J. Pharmacol. Exp. Ther. 309 2004 869 878
56. J.C. Wanstall, T.K. Jeffery, A. Gambino, F. Lovren, and C.R. Triggle Vascular smooth muscle relaxation mediated by nitric oxide donors: a comparison with acetylcholine, nitric oxide and nitroxyl ion Br. J. Pharmacol. 134 2001 463 472
57. D.A. Wink, M. Feelisch, J. Fukuto, D. Chistodoulou, D. Jourd'heuil, M.B. Grisham, Y. Vodovotz, J.A. Cook, M. Krishna, W.G. DeGraff, S. Kim, J. Gamson, and J.B. Mitchell The cytotoxicity of nitroxyl: possible implications for the pathophysiological role of NO Arch. Biochem. Biophys. 351 1998 66 74
58. P.S.Y. Wong, J. Hyun, J.M. Fukuto, F.N. Shirota, E.G. DeMaster, and D.W. Shoeman Reaction between S-nitrosothiols and thiols: generation of nitroxyl (HNO) and subsequent chemistry Biochemistry 37 1998 5362 5371
59. A. Zeller, M.V. Wenzl, M. Beretta, H. Stessel, M. Russwurm, D. Koesling, K. Schmidt, and B. Mayer Mechanisms underlying activation of soluble guanylate cyclase by the nitroxyl donor Angeli's salt Mol. Pharmacol. 76 2009 1115 1122