Nitroxyl inhibits overt pain-like behavior in mice: Role of cGMP/PKG/ATP-sensitive potassium channel signaling pathway

Pharmacological Reports

Volumn 66, Issue 4, 2014, Pages 691-698

  Staurengo Ferrari, Larissa ^a   Zarpelon, Ana C ^a   Longhi Balbinot, Daniela T ^a   Marchesi, Mario ^b   Cunha, Thiago M ^c   Alves Filho, José C ^c   Cunha, Fernando Q ^c   Ferreira, Sergio H ^c   Casagrande, Rubia ^a   Miranda, Katrina M ^b   Verri, Waldiceu A ^a  

^a STATE UNIVERSITY OF LONDRINA   (Brazil)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF SÃO PAULO   (Brazil)

Author keywords

Angeli's salt; Formalin; Nitroxyl; Nociception; Pain

Indexed keywords

1H 1,2,4 OXADIAZOLO[4,3 A]QUINOXALIN 1 ONE; ACETIC ACID; ADENOSINE TRIPHOSPHATE SENSITIVE POTASSIUM CHANNEL; ANGELI SALT; ANTINOCICEPTIVE AGENT; CYCLIC GMP; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYSTEINE; GLIBENCLAMIDE; GUANYLATE CYCLASE; KT 5823; PHENYLQUINONE; UNCLASSIFIED DRUG; ANALGESIC AGENT; NITROGEN OXIDE; NITROXYL;

ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; FORMALIN TEST; INHIBITION KINETICS; MALE; MOUSE; NONHUMAN; PAIN; PAIN ASSESSMENT; SCORING SYSTEM; SIGNAL TRANSDUCTION; WRITHING TEST; ANIMAL; DRUG EFFECTS; ENZYMOLOGY; METABOLISM; PAIN MEASUREMENT;

ANALGESICS; ANIMALS; BEHAVIOR, ANIMAL; CYCLIC GMP; CYCLIC GMP-DEPENDENT PROTEIN KINASES; KATP CHANNELS; MALE; MICE; NITROGEN OXIDES; PAIN; PAIN MEASUREMENT; SIGNAL TRANSDUCTION;

EID: 84902485137     PISSN: 22995684     EISSN: 22995684     Source Type: Journal    
DOI: 10.1016/j.pharep.2014.04.003     Document Type: Article

References (52)

1. S. Moncada, R.M.J. Palmer, and E.A. Higgs Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol Rev 43 2 1991 109 142
2. D.S. Bredt, and S.H. Snyder Nitric oxide: a novel neuronal messenger Neuron 8 1 1992 3 11
3. S.R. Vincent, and B.T. Hope Neurons that say NO Trends Neurosci 15 3 1992 108 113
4. S. Moncada, and E.A. Higgs The discovery of nitric oxide and its role in vascular biology Br J Pharmacol 147 Suppl. 1 2006 S193 S201
5. Y. Cury, G. Picolo, V.P. Gutierrez, and Ferreira S.H. Pain and analgesia: the dual effect of nitric oxide in the nociceptive system Nitric Oxide 25 3 2011 243 254
6. J.V. Esplugues NO as a signalling molecule in the nervous system Br J Pharmacol 135 2002 1079 1095 (Pubitemid 34259107)
7. N. Olson, and A. van der Vliet Interactions between nitric oxide and hypoxia inducible factor signaling pathways in inflammatory disease Nitric Oxide 25 2 2011 125 137
8. W.A. Paradise, B.J. Vesper, A. Goel, J.D. Waltonen, K.W. Altman, and G.K. Haines et al. Nitric oxide: perspectives and emerging studies of a well known cytotoxin Int J Mol Sci 11 2010 2715 2745
9. T.M. Cunha, D. Roman-Campos, C.M. Lotufo, H.L. Duarte, G.R. Souza, and W.A. Verri Jr. et al. Morphine peripheral analgesia depends on activation of the PI3Kgamma/AKT/nNOS/NO/KATP signaling pathway Proc Natl Acad Sci USA 107 2010 4442 4447
10. A.M. Sousa, and W.A. Prado The dual effect of a nitric oxide donor in nociception Brain Res 897 2001 9 19 (Pubitemid 32244347)
11. A. Kawabata, Y. Fukuzumi, Y. Fukushima, and H. Takagi Antinociceptive effect of L-arginine on the carrageenin-induced hyperalgesia of the rat: possible involvement of central opioidergic systems Eur J Pharmacol 218 1992 153 158
12. J. Rocha, M.E. Peixoto, S. Jancar, F.Q. Cunha, R.A. Ribeiro, and F.A. Rocha Dual effect of nitric oxide in articular inflammatory pain in zymosan-induced arthritis in rats Br J Pharmacol 136 2002 588 596 (Pubitemid 34717703)
13. I.D. Duarte, I.R. Dos Santos, B.B. Lorenzetti, and S.H. Ferreira Analgesia by direct antagonism of nociceptor sensitization involves the arginine nitric oxide cGMP pathway Eur J Pharmacol 217 1992 225 227
14. R. Ventura-Martinez, M. Deciga-Campos, M.I. Diaz-Reval, M.E. Gonzalez-Trujano, and F.J. Lopez-Munoz Peripheral involvement of the nitric oxide-cGMP pathway in the indomethacin-induced antinociception in rat Eur J Pharmacol 503 2004 43 48 (Pubitemid 39445939)
15. D. Sachs, F.Q. Cunha, and S.H. Ferreira Peripheral analgesic blockade of hypernociception: activation of arginine/NO/cGMP/protein kinase G/ATPsensitive K+ channel pathway Proc Natl Acad Sci USA 101 2004 3680 3685 (Pubitemid 38338254)
16. S.S. Mizokami, N.S. Arakawa, S.R. Ambrosio, A.C. Zarpelon, R. Casagrande, and T.M. Cunha et al. Kaurenoic acid from Sphagneticola trilobata inhibits inflammatory pain: effect on cytokine production and activation of the NO-cyclic GMP-protein kinase G-ATP-sensitive potassium channel signaling pathway J Nat Prod 75 5 2012 896 904
17. T. Santodomingo-Garzon, T.M. Cunha, W.A. Verri Jr., D.A. Valério, C.A. Parada, and S. Poole et al. Atorvastatin inhibits inflammatory hypernociception Br J Pharmacol 149 1 2006 14 22 (Pubitemid 44299064)
18. M.L. Vale, D.E. Rolim, I.F. Cavalcante, R.A. Ribeiro, and M.H. Sousa Role of NO/cGMP/KATP pathway in antinociceptive effect of sildenafil in zymosan writhing response in mice Inflamm Res 56 2 2007 83 88 (Pubitemid 46412014)
19. 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 12 2008 601 608
20. 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
21. J.M. Fukuto, C.H. Switzer, K.M. Miranda, and D.A. Wink Nitroxyl (HNO): chemistry, biochemistry, and pharmacology Annu Rev Pharmacol Toxicol 45 2005 335 355 (Pubitemid 40261809)
22. S. Donzelli, M.G. Espey, D.D. Thomas, D. Mancardi, C.G. Tocchetti, and L.A. Ridnour et al. Discriminating formation of HNO from other reactive nitrogen oxide species Free Radic Biol Med 40 6 2006 1056 1066 (Pubitemid 43376015)
23. S. Donzelli, M.G. Espey, W. Flores-Santana, C.H. Switzer, G.C. Yeh, and J. Huang et al. Generation of nitroxyl by heme protein-mediated peroxidation of hydroxylamine but not N-hydroxy-L-arginin Free Radic Biol Med 45 5 2008 578 584
24. P. Pagliaro, D. Mancardi, R. Rastaldo, C. Penna, D. Gattullo, and K.M. Miranda et al. Nitroxyl affords thiol-sensitive myocardial protective effects akin to early preconditioning Free Radic Bio Med 34 2003 33 43 (Pubitemid 36043884)
25. - activates soluble guanylate cyclase and Kv channels to vasodilate resistance arteries Hypertension 41 2003 1301 1307 (Pubitemid 36706081)
26. K.L. Andrews, J.C. Irvine, M. Tare, J. Apostolopoulos, J.L. Favaloro, and C.R. Triggle et al. A role for nitroxyl (HNO) as an endothelium-derived relaxing and hyperpolarizing factor in resistance arteries Br J Pharmacol 157 4 2009 540 550
27. F.T. Bonner, and B. Ravid Thermal decomposition of oxyhyponitrite (sodium trioxodinitrate (II) in aqueous solution Inorg Chem 14 1975 558 563
28. A.C. Zarpelon, G.R. Souza, T.M. Cunha, I.R. Schivo, M. Marchesi, and R. Casagrande et al. The nitroxyl donor, Angeli's salt, inhibits inflammatory hyperalgesia in rats Neuropharmacology 71 2013 1 9
29. H.O. Collier, L.C. Dinneen, C.A. Johnson, and C. Schneider The abdominal constriction response and its suppression by analgesic drugs in the mouse Br J Pharmacol Chemother 32 2 1968 295 310
30. D. Dubuisson, and S.G. Dennis The formalin test: a quantitative study of the analgesic effects of morphine, meperidine, and brain stem stimulation in rats and cats Pain 4 2 1977 161 174 (Pubitemid 8234766)
31. W.A. Verri Jr., T.M. Cunha, C.A. Parada, S. Poole, F.Q. Cunha, and S.H. Ferreira Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 112 1 2006 116 138 (Pubitemid 44301486)
32. 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
33. C.M. Maragos, D. Morley, D.A. Wink, T.M. Dunams, J.E. Saavedra, and A. Hoffman et al. Complexes of NO with nucleophiles as agents for the controlled biological release of nitric oxide. Vasorelaxant effects J Med Chem 34 11 1991 3242 3247
34. W.A. Verri Jr., T.M. Cunha, D.A. Magro, A.C. Domingues, S.M. Vieira, and G.R. Sousa et al. Role of IL-18 in overt pain-like behaviour in mice Eur J Pharmacol 2-3 2008 207 212
35. G.F. Pavao-de-Souza, A.C. Zarpelon, G.C. Tedeschi, S.S. Mizokami, J.S. Sanson, and T.M. Cunha et al. Acetic acid and phenyl-p-benzoquinone-induced overt pain-like behavior depends on spinal activation of MAP kinases: PI(3)K and microglia in mice Pharmacol Biochem Behav 101 3 2012 320 328
36. C.R. Tonussi, and S.H. Ferreira Mechanism of diclofenac analgesia: direct blockade of inflammatory sensitization Eur J Pharmacol 251 2-3 1994 173 179 (Pubitemid 24061092)
37. D.A. Valerio, S.R. Georgetti, D.A. Magro, R. Casagrande, T.M. Cunha, and F.T. Vicentini et al. Quercetin reduces inflammatory pain: inhibition of oxidative stress and cytokine production J Nat Prod 72 11 2009 1975 1979
38. J.F. Emele, and J.E. Shanaman Analgesic activity of namoxyrate (2-[4-biphenylylbutyric acid 2-dimethylaminoethanol salt) Arch Int Pharmacodyn Ther 170 1 1967 99 107
39. 6), inhibits inflammatory pain: involvement of TRPV1 and cGMP/PKG/ATP-sensitive potassium channel signaling pathway Pharmacol Biochem Behav 105C 2013 157 165
40. N. Paolocci, M.I. Jackson, B.E. Lopez, K. Miranda, C.G. Tocchetti, and D.A. Wink et al. The pharmacology of nitroxyl (HNO) and its therapeutic potential: not just the janus face of NO Pharmacol Ther 113 2007 442 458
41. R.A. Ribeiro, M.V. Vale, S.M. Thomazzi, A.B.P. Paschoalato, S. Poole, and S.H. Ferreira et al. Involvement of resident macrophages and mast cells in the writhing nociceptive response induced by zymosan and acetic acid in mice Eur J Pharmacol 387 2000 111 118 (Pubitemid 30035382)
42. H. Zeashan, G. Amresh, C.V. Rao, and S. Singh Antinociceptive activity of Amaranthus spinosus in experimental animals J Ethnopharmacol 122 2009 492 496
43. C.A. Parada, C.H. Tambeli, F.Q. Cunha, and S.H. Ferreira The major role of peripheral release of histamine and 5-hydroxytryptamine in formalin-induced nociception Neuroscience 102 2001 937 944 (Pubitemid 32155888)
44. J.G. Chichorro, B.B. Lorenzetti, and A.R. Zampronio Involvement of bradykinin, cytokines, sympathetic amines and prostaglandins in formalin-induced orofacial nociception in rats Br J Pharmacol 141 7 2004 1175 1184 (Pubitemid 38582255)
45. J.L. Favaloro, and B.K. Kemp-Harper The nitroxyl anion (HNO) is a potent dilator of rat coronary vasculature Cardiovasc Res 73 3 2007 587 596 (Pubitemid 46073951)
46. 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 4 2007 885 892 (Pubitemid 351664199)
47. T.W. Miller, M.M. Cherney, A.J. Lee, N.E. Francoleon, P.J. Farmer, and S.B. King et al. The effects of nitroxyl (HNO) on soluble guanylate cyclase activity: interactions at ferrous heme and cysteine thiols J Biol Chem 284 33 2009 21788 21796
48. A. Zeller, M.V. Wenzl, M. Beretta, H. Stessel, M. Russwurm, and D. Koesling et al. Mechanisms underlying activation of soluble guanylate cyclase by the nitroxyl donor Angeli's salt Mol Pharmacol 76 5 2009 1115 1122
49. Z.Q. Wang, F. Porreca, S. Cuzzocrea, K. Galen, R. Lightfoot, and E. Masini et al. A newly identified role for superoxide in inflammatory pain J Pharmacol Exp Ther 309 3 2004 869 878 (Pubitemid 38669673)
50. + channels (BK(Ca)) in smooth muscle cells isolated from the rat mesenteric artery Br J Pharmacol 124 6 1998 1131 1140 (Pubitemid 28333935)
51. S.H. Ferreira, I.D. Duarte, and B.B. Lorenzetti Molecular base of acetylcholine and morphine analgesia Agents Actions Suppl 32 1991 101 106
52. A. Hervera, S. Leánez, and O. Pol The inhibition of the nitric oxide-cGMP-PKG-JNK signaling pathway avoids the development of tolerance to the local antiallodynic effects produced by morphine during neuropathic pain Eur J Pharmacol 685 1-3 2012 42 51