Role for peroxynitrite in sphingosine-1-phosphate-induced hyperalgesia in rats

Pain

Volumn 152, Issue 3, 2011, Pages 643-648

  Doyle, Tim ^a   Finley, Amanda ^a   Chen, Zhoumou ^a   Salvemini, Daniela ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Hyperalgesia; Nitric oxide; Peroxynitrite; Sphingosine kinase; Sphingosine 1 phosphate; Superoxide

Indexed keywords

5 (4 PHENYL 5 TRIFLUOROMETHYL 2 THIENYL) 3 (3 TRIFLUOROMETHYLPHENYL) 1,2,4 OXADIAZOLE; APOCYNIN; ARGININE METHYL ESTER; N(G) NITROARGININE METHYL ESTER; PEROXYNITRITE; SPHINGOSINE 1 PHOSPHATE; SPHINGOSINE 1 PHOSPHATE RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CATALYST; DECOMPOSITION; ENANTIOMER; HYPERALGESIA; MALE; NONHUMAN; PRIORITY JOURNAL; RAT; SENSITIZATION;

ACETOPHENONES; ANILIDES; ANIMALS; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME ACTIVATION; ENZYME INHIBITORS; HYPERALGESIA; LYSOPHOSPHOLIPIDS; MALE; METALLOPORPHYRINS; NG-NITROARGININE METHYL ESTER; OXADIAZOLES; PEROXYNITROUS ACID; PHOSPHONIC ACIDS; RATS; RATS, SPRAGUE-DAWLEY; REACTION TIME; RECEPTORS, LYSOSPHINGOLIPID; SPHINGOSINE; THIOPHENES; TIME FACTORS;

EID: 79851510995     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2010.12.011     Document Type: Article

References (70)

1. B.M. Babior, R.S. Kipnes, and J.T. Curnutte Biological defense mechanisms. The production by leukocytes of superoxide, a potential bactericidal agent J Clin Invest 52 1973 741 744
2. B.M. Babior, J.D. Lambeth, and W. Nauseef The neutrophil NADPH oxidase Arch Biochem Biophys 397 2002 342 344 (Pubitemid 34852301)
3. I. Batinic-Haberle, I. Spasojevic, H.M. Tse, A. Tovmasyan, Z. Rajic, D.K. St. Clair, Z. Vujaskovic, M.W. Dewhirst, and J.D. Piganelli Design of Mn porphyrins for treating oxidative stress injuries and their redox-based regulation of cellular transcriptional activities Amino Acids 2010 [Epub ahead of print]
4. 2 · - dismutation J Chem Soc Dalton Trans 30 2002 2689 2696
5. C. Batthyany, F.J. Schopfer, P.R. Baker, R. Duran, L.M. Baker, Y. Huang, C. Cervenansky, B.P. Branchaud, and B.A. Freeman Reversible post-translational modification of proteins by nitrated fatty acids in vivo J Biol Chem 281 2006 20450 20463 (Pubitemid 44065818)
6. J.S. Beckman, T.W. Beckman, J. Chen, P.A. Marshall, and B.A. Freeman Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide Proc Natl Acad Sci USA 87 1990 1620 1624
7. D.S. Bredt, P.M. Hwang, and S.H. Snyder Localization of nitric oxide synthase indicating a neural role for nitric oxide Nature 347 1990 768 770
8. X. Cao, S.L. Demel, M.T. Quinn, J.J. Galligan, and D. Kreulen Localization of NADPH oxidase in sympathetic and sensory ganglion neurons and perivascular nerve fibers Auton Neurosci 151 2009 90 97
9. S. Catarzi, E. Giannoni, F. Favilli, E. Meacci, T. Iantomasi, and M.T. Vincenzini Sphingosine 1-phosphate stimulation of NADPH oxidase activity: relationship with platelet-derived growth factor receptor and c-Src kinase Biochim Biophys Acta 1770 2007 872 883 (Pubitemid 46617027)
10. J.K. Cheng, and R.R. Ji Intracellular signaling in primary sensory neurons and persistent pain Neurochem Res 33 2008 1970 1978
11. X.X. Chi, and G.D. Nicol The sphingosine 1-phosphate receptor, S1PR1, plays a prominent but not exclusive role in enhancing the excitability of sensory neurons J Neurophysiol 104 2010 2741 2748
12. O. Coste, C. Brenneis, B. Linke, S. Pierre, C. Maeurer, W. Becker, H. Schmidt, W. Gao, G. Geisslinger, and K. Scholich Sphingosine 1-phosphate modulates spinal nociceptive processing J Biol Chem 283 2008 32442 32451
13. U. Forstermann, J.S. Pollock, H.H. Schmidt, M. Heller, and F. Murad Calmodulin-dependent endothelium-derived relaxing factor/nitric oxide synthase activity is present in the particulate and cytosolic fractions of bovine aortic endothelial cells Proc Natl Acad Sci USA 88 1991 1788 1792 (Pubitemid 21916311)
14. D.M. Fries, E. Paxinou, M. Themistocleous, E. Swanberg, K.K. Griendling, D. Salvemini, J.W. Slot, H.F. Heijnen, S.L. Hazen, and H. Ischiropoulos Expression of inducible nitric-oxide synthase and intracellular protein tyrosine nitration in vascular smooth muscle cells: role of reactive oxygen species J Biol Chem 278 2003 22901 22907 (Pubitemid 36830354)
15. Y.A. Hannun, and L.M. Obeid Principles of bioactive lipid signalling: lessons from sphingolipids Nat Rev Mol Cell Biol 9 2008 139 150 (Pubitemid 351158911)
16. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia Pain 32 1988 77 88
17. H.F. Heijnen, E. van Donselaar, J.W. Slot, D.M. Fries, B. Blachard-Fillion, R. Hodara, R. Lightfoot, M. Polydoro, D. Spielberg, L. Thomson, E.A. Regan, J. Crapo, and H. Ischiropoulos Subcellular localization of tyrosine-nitrated proteins is dictated by reactive oxygen species generating enzymes and by proximity to nitric oxide synthase Free Radic Biol Med 40 2006 1903 1913 (Pubitemid 43728857)
18. M. Ibi, K. Matsuno, D. Shiba, M. Katsuyama, K. Iwata, T. Kakehi, T. Nakagawa, K. Sango, Y. Shirai, T. Yokoyama, S. Kaneko, N. Saito, and C. Yabe-Nishimura Reactive oxygen species derived from NOX1/NADPH oxidase enhance inflammatory pain J Neurosci 28 2008 9486 9494
19. J. Igarashi, S.G. Bernier, and T. Michel Sphingosine 1-phosphate and activation of endothelial nitric-oxide synthase. Differential regulation of Akt and MAP kinase pathways by EDG and bradykinin receptors in vascular endothelial cells J Biol Chem 276 2001 12420 12426
20. J. Igarashi, and T. Michel Agonist-modulated targeting of the EDG-1 receptor to plasmalemmal caveolae. eNOS activation by sphingosine 1-phosphate and the role of caveolin-1 in sphingolipid signal transduction J Biol Chem 275 2000 32363 32370
21. S.A. Jones, V.B. O'Donnell, J.D. Wood, J.P. Broughton, E.J. Hughes, and O.T. Jones Expression of phagocyte NADPH oxidase components in human endothelial cells Am J Physiol 271 1996 H1626 H1634
22. M.Y. Kochukov, T.A. McNearney, H. Yin, L. Zhang, F. Ma, L. Ponomareva, S. Abshire, and K.N. Westlund Tumor necrosis factor-alpha (TNF-alpha) enhances functional thermal and chemical responses of TRP cation channels in human synoviocytes Mol Pain 5 2009 49
23. J.W. Little, T. Doyle, and D. Salvemini Reactive nitroxidative species and nociceptive processing: determining the roles for nitric oxide, superoxide, and peroxynitrite in pain Amino Acids 2010 [Epub ahead of print]
24. F. Ma, L. Zhang, and K.N. Westlund Reactive oxygen species mediate TNFR1 increase after TRPV1 activation in mouse DRG neurons Mol Pain 5 2009 31
25. M.A. Marletta, P.S. Yoon, R. Iyengar, C.D. Leaf, and J.S. Wishnok Macrophage oxidation of l-arginine to nitrite and nitrate: nitric oxide is an intermediate Biochemistry 27 1988 8706 8711 (Pubitemid 19008186)
26. A.J. Melendez Sphingosine kinase signalling in immune cells: potential as novel therapeutic targets Biochim Biophys Acta 1784 2008 66 75
27. T.P. Misko, M.K. Highkin, A.W. Veenhuizen, P.T. Manning, M.K. Stern, M.G. Currie, and D. Salvemini Characterization of the cytoprotective action of peroxynitrite decomposition catalysts J Biol Chem 273 1998 15646 15653 (Pubitemid 28298180)
28. V. Mollace, C. Muscoli, E. Masini, S. Cuzzocrea, and D. Salvemini Modulation of prostaglandin biosynthesis by nitric oxide and nitric oxide donors Pharmacol Rev 57 2005 217 252 (Pubitemid 41043885)
29. S. Moncada, R.M. Palmer, and E.A. Higgs Nitric oxide: physiology, pathophysiology, and pharmacology Pharmacol Rev 43 1991 109 142
30. C. Muscoli, S. Cuzzocrea, M.M. Ndengele, V. Mollace, F. Porreca, F. Fabrizi, E. Esposito, E. Masini, G.M. Matuschak, and D. Salvemini Therapeutic manipulation of peroxynitrite attenuates the development of opiate-induced antinociceptive tolerance in mice J Clin Invest 117 2007 3530 3539 (Pubitemid 350097008)
31. C. Muscoli, S. Cuzzocrea, D.P. Riley, J.L. Zweier, C. Thiemermann, Z.Q. Wang, and D. Salvemini On the selectivity of superoxide dismutase mimetics and its importance in pharmacological studies Br J Pharmacol 140 2003 445 460 (Pubitemid 37330489)
32. C. Muscoli, T. Doyle, C. Dagostino, L. Bryant, Z. Chen, L.R. Watkins, J. Ryerse, E. Bieberich, W. Neumman, and D. Salvemini Counter-regulation of opioid analgesia by glial-derived bioactive sphingolipids J Neurosci 30 2010 15400 15408
33. S. Muzaffar, N. Shukla, G.D. Angelini, and J.Y. Jeremy Superoxide auto-augments superoxide formation and upregulates gp91(phox) expression in porcine pulmonary artery endothelial cells: inhibition by iloprost Eur J Pharmacol 538 2006 108 114
34. W.M. Nauseef The NADPH-dependent oxidase of phagocytes Proc Assoc Am Physicians 111 1999 373 382 (Pubitemid 29446878)
35. M.M. Ndengele, S. Cuzzocrea, E. Masini, M.C. Vinci, E. Esposito, C. Muscoli, D.N. Petrusca, V. Mollace, E. Mazzon, D. Li, I. Petrache, G.M. Matuschak, and D. Salvemini Spinal ceramide modulates the development of morphine antinociceptive tolerance via peroxynitrite-mediated nitroxidative stress and neuroimmune activation J Pharmacol Exp Ther 329 2009 64 75
36. G.D. Nicol Nerve growth factor, sphingomyelins, and sensitization in sensory neurons Sheng Li Xue Bao 60 2008 603 604
37. J.H. Paik, S. Chae, M.J. Lee, S. Thangada, and T. Hla Sphingosine 1-phosphate-induced endothelial cell migration requires the expression of EDG-1 and EDG-3 receptors and Rho-dependent activation of alpha vbeta3- and beta1-containing integrins J Biol Chem 276 2001 11830 11837
38. P. Puntambekar, D. Mukherjea, S. Jajoo, and V. Ramkumar Essential role of Rac1/NADPH oxidase in nerve growth factor induction of TRPV1 expression J Neurochem 95 2005 1689 1703 (Pubitemid 41804065)
39. R. Reinehr, S. Becker, A. Eberle, S. Grether-Beck, and D. Haussinger Involvement of NADPH oxidase isoforms and Src family kinases in CD95-dependent hepatocyte apoptosis J Biol Chem 280 2005 27179 27194 (Pubitemid 41040757)
40. H. Rosen, P. Gonzalez-Cabrera, D. Marsolais, S. Cahalan, A.S. Don, and M.G. Sanna Modulating tone: the overture of S1P receptor immunotherapeutics Immunol Rev 223 2008 221 235 (Pubitemid 351986190)
41. H. Rosen, P.J. Gonzalez-Cabrera, M.G. Sanna, and S. Brown Sphingosine 1-phosphate receptor signaling Annu Rev Biochem 78 2009 743 768
42. F. Roviezzo, M. Bucci, C. Delisle, V. Brancaleone, A. Di Lorenzo, I.P. Mayo, S. Fiorucci, A. Fontana, J.P. Gratton, and G. Cirino Essential requirement for sphingosine kinase activity in eNOS-dependent NO release and vasorelaxation FASEB J 20 2006 340 342 (Pubitemid 46671164)
43. F.A. Russell, E.S. Fernandes, J.P. Courade, J.E. Keeble, and S.D. Brain Tumour necrosis factor alpha mediates transient receptor potential vanilloid 1-dependent bilateral thermal hyperalgesia with distinct peripheral roles of interleukin-1beta, protein kinase C and cyclooxygenase-2 signalling Pain 142 2009 264 274
44. D. Salvemini, M.P. Jensen, D.P. Riley, and T.P. Misko Therapeutic manipulations of peroxynitrite Drug News Perspect 11 1998 204 214
45. D. Salvemini, and J.L. Masferrer Interactions of nitric oxide with cyclooxygenase: in vitro, ex vivo, and in vivo studies Methods Enzymol 269 1996 12 25 (Pubitemid 26295692)
46. D. Salvemini, E. Mazzon, L. Dugo, D.P. Riley, I. Serraino, A.P. Caputi, and S. Cuzzocrea Pharmacological manipulation of the inflammatory cascade by the superoxide dismutase mimetic, M40403 Br J Pharmacol 132 2001 815 827 (Pubitemid 32193638)
47. D. Salvemini, and W. Neumann Targeting peroxynitrite driven nitroxidative stress with synzymes: a novel therapeutic approach in chronic pain management Life Sci 86 2010 604 614
48. D. Salvemini, and W.L. Neumann Peroxynitrite: a strategic linchpin of opioid analgesic tolerance Trends Pharmacol Sci 30 2009 194 202
49. D. Salvemini, D.P. Riley, and S. Cuzzocrea SOD mimetics are coming of age Nat Rev Drug Discov 1 2002 367 374 (Pubitemid 37361466)
50. D. Salvemini, Z.Q. Wang, M.K. Stern, M.G. Currie, and T.P. Misko Peroxynitrite decomposition catalysts: therapeutics for peroxynitrite-mediated pathology Proc Natl Acad Sci USA 95 1998 2659 2663
51. M.G. Sanna, S.K. Wang, P.J. Gonzalez-Cabrera, A. Don, D. Marsolais, M.P. Matheu, S.H. Wei, I. Parker, E. Jo, W.C. Cheng, M.D. Cahalan, C.H. Wong, and H. Rosen Enhancement of capillary leakage and restoration of lymphocyte egress by a chiral S1P1 antagonist in vivo Nat Chem Biol 2 2006 434 441 (Pubitemid 44114922)
52. M. Schafers, D.H. Lee, D. Brors, T.L. Yaksh, and L.S. Sorkin Increased sensitivity of injured and adjacent uninjured rat primary sensory neurons to exogenous tumor necrosis factor-alpha after spinal nerve ligation J Neurosci 23 2003 3028 3038 (Pubitemid 36418639)
53. M. Schafers, C. Sommer, C. Geis, T. Hagenacker, P. Vandenabeele, and L.S. Sorkin Selective stimulation of either tumor necrosis factor receptor differentially induces pain behavior in vivo and ectopic activity in sensory neurons in vitro Neuroscience 157 2008 414 423
54. A. Sculptoreanu, F.A. Kullmann, D.E. Artim, F.A. Bazley, F. Schopfer, S. Woodcock, B.A. Freeman, and W.C. de Groat Nitro-oleic acid inhibits firing and activates TRPV1- and TRPA1-mediated inward currents in dorsal root ganglion neurons from adult male rats J Pharmacol Exp Ther 333 2010 883 895
55. L.J. Sim-Selley, P.B. Goforth, M.U. Mba, T.L. Macdonald, K.R. Lynch, S. Milstien, S. Spiegel, L.S. Satin, S.P. Welch, and D.E. Selley Sphingosine-1-phosphate receptors mediate neuromodulatory functions in the CNS J Neurochem 110 2009 1191 1202
56. J.M. Simons, B.A. Hart, T.R. Ip Vai Ching, H. Van Dijk, and R.P. Labadie Metabolic activation of natural phenols into selective oxidative burst agonists by activated human neutrophils Free Radic Biol Med 8 1990 251 258
57. A.J. Snider, K.A. Orr Gandy, and L.M. Obeid Sphingosine kinase: role in regulation of bioactive sphingolipid mediators in inflammation Biochimie 92 2010 707 715
58. S. Spiegel, and S. Milstien Sphingosine-1-phosphate: an enigmatic signalling lipid Nat Rev Mol Cell Biol 4 2003 397 407 (Pubitemid 36565571)
59. S. Spiegel, and S. Milstien Functions of the multifaceted family of sphingosine kinases and some close relatives J Biol Chem 282 2007 2125 2129 (Pubitemid 47076736)
60. J. Stolk, T.J. Hiltermann, J.H. Dijkman, and A.J. Verhoeven Characteristics of the inhibition of NADPH oxidase activation in neutrophils by apocynin, a methoxy-substituted catechol Am J Respir Cell Mol Biol 11 1994 95 102
61. A.C. Straub, L.R. Klei, D.B. Stolz, and A. Barchowsky Arsenic requires sphingosine-1-phosphate type 1 receptors to induce angiogenic genes and endothelial cell remodeling Am J Pathol 174 2009 1949 1958
62. C. Szabo, H. Ischiropoulos, and R. Radi Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat Rev Drug Discov 6 2007 662 680 (Pubitemid 47207751)
63. T.A. Taha, K.M. Argraves, and L.M. Obeid Sphingosine-1-phosphate receptors: receptor specificity versus functional redundancy Biochim Biophys Acta 1682 2004 48 55 (Pubitemid 38670534)
64. K. Takabe, S.W. Paugh, S. Milstien, and S. Spiegel "Inside-out" signaling of sphingosine-1-phosphate: therapeutic targets Pharmacol Rev 60 2008 181 195 (Pubitemid 351962008)
65. J.S. Won, and I. Singh Sphingolipid signaling and redox regulation Free Radic Biol Med 40 2006 1875 1888 (Pubitemid 43728861)
66. F. Yi, A.Y. Zhang, N. Li, R.W. Muh, M. Fillet, A.F. Renert, and P.L. Li Inhibition of ceramide-redox signaling pathway blocks glomerular injury in hyperhomocysteinemic rats Kidney Int 70 2006 88 96 (Pubitemid 44000124)
67. T. Yoshida, R. Inoue, T. Morii, N. Takahashi, S. Yamamoto, Y. Hara, M. Tominaga, S. Shimizu, Y. Sato, and Y. Mori Nitric oxide activates TRP channels by cysteine S-nitrosylation Nat Chem Biol 2 2006 596 607 (Pubitemid 44610344)
68. Y.H. Zhang, J.C. Fehrenbacher, M.R. Vasko, and G.D. Nicol Sphingosine-1-phosphate via activation of a G-protein-coupled receptor(s) enhances the excitability of rat sensory neurons J Neurophysiol 96 2006 1042 1052 (Pubitemid 44371500)
69. Y.H. Zhang, M.R. Vasko, and G.D. Nicol Ceramide, a putative second messenger for nerve growth factor, modulates the TTX-resistant Na(+) current and delayed rectifier K(+) current in rat sensory neurons J Physiol 544 2002 385 402 (Pubitemid 35244257)
70. Y.H. Zhang, M.R. Vasko, and G.D. Nicol Intracellular sphingosine 1-phosphate mediates the increased excitability produced by nerve growth factor in rat sensory neurons J Physiol 575 2006 101 113 (Pubitemid 44178131)