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Original Article

Differential regulation of oxidative stress and cytokine production by endothelin ETA and ETB receptors in superoxide anion-induced inflammation and pain in mice

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Pages 264-274 | Received 02 May 2016, Accepted 03 Oct 2016, Published online: 24 Oct 2016

References

  • Barton M, Yanagisawa M. Endothelin: 20 years from discovery to therapy. Can J Physiol Pharmacol 2008;86:485–98.
  • Sokolovsky M. Endothelins and sarafotoxins: physiological regulation, receptor subtypes and transmembrane signaling. Pharmacol Ther 1992;54:129–49.
  • Cunha TM, Verri WA Jr, Silva JS, et al. A cascade of cytokines mediates mechanical inflammatory hypernociception in mice. Proc Natl Acad Sci USA 2005;102:1755–60.
  • Jin X, Gereau RWT. Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-alpha. J Neurosci 2006;26:246–55.
  • Binshtok AM, Wang H, Zimmermann K, et al. Nociceptors are interleukin-1beta sensors. J Neurosci 2008;28:14062–73.
  • Verri WA Jr, Cunha TM, Parada CA, et al. Hypernociceptive role of cytokines and chemokines: targets for analgesic drug development? Pharmacol Ther 2006;112:116–38.
  • Zarpelon AC, Cunha TM, Alves-Filho JC, et al. IL-33/ST2 signalling contributes to carrageenin-induced innate inflammation and inflammatory pain: role of cytokines, endothelin-1 and prostaglandin E2. Br J Pharmacol 2013;169:90–101.
  • Verri WA Jr, Cunha TM, Parada CA, et al. IL-15 mediates immune inflammatory hypernociception by triggering a sequential release of IFN-gamma, endothelin, and prostaglandin. Proc Natl Acad Sci USA 2006;103:9721–5.
  • Verri WA Jr, Cunha TM, Parada CA, et al. Antigen-induced inflammatory mechanical hypernociception in mice is mediated by IL-18. Brain Behav Immun 2007;21:535–43.
  • Gokin AP, Fareed MU, Pan HL, et al. Local injection of endothelin-1 produces pain-like behavior and excitation of nociceptors in rats. J Neurosci 2001;21:5358–66.
  • Dahlof B, Gustafsson D, Hedner T, et al. Regional haemodynamic effects of endothelin-1 in rat and man: unexpected adverse reaction. J Hypertens 1990;8:811–17.
  • Ferreira SH, Romitelli M, De Nucci G. Endothelin-1 participation in overt and inflammatory pain. J Cardiovasc Pharmacol 1989;13:S220–S2.
  • Verri WA Jr, Cunha TM, Magro DA, et al. Targeting endothelin ETA and ETB receptors inhibits antigen-induced neutrophil migration and mechanical hypernociception in mice. Naunyn Schmiedebergs Arch Pharmacol 2009;379:271–9.
  • Ferrari LF, Bogen O, Green P, Levine JD. Contribution of Piezo2 to endothelium-dependent pain. Mol Pain 2015;11:65.
  • Hathaway CK, Grant R, Hagaman JR, et al. Endothelin-1 critically influences cardiac function via superoxide-MMP9 cascade. Proc Natl Acad Sci USA 2015;112:5141–6.
  • Lee I, Kim HK, Kim JH, et al. The role of reactive oxygen species in capsaicin-induced mechanical hyperalgesia and in the activities of dorsal horn neurons. Pain 2007;133:9–17.
  • Khattab MM. TEMPOL, a membrane-permeable radical scavenger, attenuates peroxynitrite- and superoxide anion-enhanced carrageenan-induced paw oedema and hyperalgesia: a key role for superoxide anion. Eur J Pharmacol 2006;548:167–73.
  • Fattori V, Pinho-Ribeiro FA, Borghi SM, et al. Curcumin inhibits superoxide anion-induced pain-like behaviour and leukocyte recruitment by increasing Nrf2 expression and reducing NF-kappaB activation. Inflamm Res 2015;64:993–1003.
  • Maioli NA, Zarpelon AC, Mizokami SS, et al. The superoxide anion donor, potassium superoxide, induces pain and inflammation in mice through production of reactive oxygen species and cyclooxygenase-2. Braz J Med Biol Res 2015;48:321–31.
  • Serafim KG, Navarro SA, Zarpelon AC, et al. Bosentan, a mixed endothelin receptor antagonist, inhibits superoxide anion-induced pain and inflammation in mice. Naunyn Schmiedebergs Arch Pharmacol 2015;388:1211–21.
  • Cunha TM, Verri WA Jr, Vivancos GG, et al. An electronic pressure-meter nociception paw test for mice. Braz J Med Biol Res 2004;37:401–7.
  • Victorino VJ, Panis C, Campos FC, et al. Decreased oxidant profile and increased antioxidant capacity in naturally postmenopausal women. Age (Dordr) 2013;35:1411–21.
  • Piovezan AP, D'orleans-Juste P, Souza GE, Rae GA. Endothelin-1-induced ET(A) receptor-mediated nociception, hyperalgesia and oedema in the mouse hind-paw: modulation by simultaneous ET(B) receptor activation. Br J Pharmacol 2000;129:961–8.
  • Ishimaru S, Shichiri M, Mineshita S, Hirata Y. Role of endothelin-1/endothelin receptor system in endotoxic shock rats. Hypertens Res 2001;24:119–26.
  • Khodorova A, Navarro B, Jouaville LS, et al. Endothelin-B receptor activation triggers an endogenous analgesic cascade at sites of peripheral injury. Nat Med 2003;9:1055–61.
  • Janosi T, Petak F, Fontao F, et al. Differential roles of endothelin-1 ETA and ETB receptors and vasoactive intestinal polypeptide in regulation of the airways and the pulmonary vasculature in isolated rat lung. Exp Physiol 2008;93:1210–19.
  • Davenport AP, Maguire JJ. Pharmacology of renal endothelin receptors. Contrib Nephrol 2011;172:1–17.
  • Piechota-Polanczyk A, Kleniewska P, Goraca A. The influence of ETA and ETB receptor blockers on LPS-induced oxidative stress and NF-kappaB signaling pathway in heart. Gen Physiol Biophys 2012;31:271–8.
  • Kim YO, Kim IJ, Yoon MH. Antiallodynic effect through spinal endothelin-B receptor antagonism in rat models of complex regional pain syndrome. Neurosci Lett 2015;584:45–9.
  • Forner S, Martini AC, De Andrade EL, Rae GA. Neuropathic pain induced by spinal cord injury: role of endothelin ETA and ETB receptors. Neurosci Lett 2016;617:14–21.
  • Kim HY, Lee I, Chun SW, Kim HK. Reactive oxygen species donors increase the responsiveness of dorsal horn neurons and induce mechanical hyperalgesia in rats. Neural Plast 2015;2015:293423.
  • Gloire G, Piette J. Redox regulation of nuclear post-translational modifications during NF-kappaB activation. Antioxid Redox Signal 2009;11:2209–22.
  • Jamaluddin M, Wang S, Boldogh I, et al. TNF-alpha-induced NF-kappaB/RelA Ser(276) phosphorylation and enhanceosome formation is mediated by an ROS-dependent PKAc pathway. Cell Signal 2007;19:1419–33.
  • Yamacita-Borin FY, Zarpelon AC, Pinho-Ribeiro FA, et al. Superoxide anion-induced pain and inflammation depends on TNFalpha/TNFR1 signaling in mice. Neurosci Lett 2015;605:53–8.
  • Pinho-Ribeiro FA, Fattori V, Zarpelon AC, et al. Pyrrolidine dithiocarbamate inhibits superoxide anion-induced pain and inflammation in the paw skin and spinal cord by targeting NF-kappaB and oxidative stress. Inflammopharmacology 2016;24:97–107.
  • Hattori H, Subramanian KK, Sakai J, et al. Small-molecule screen identifies reactive oxygen species as key regulators of neutrophil chemotaxis. Proc Natl Acad Sci USA 2010;107:3546–51.
  • Sakai J, Li J, Subramanian KK, et al. Reactive oxygen species-induced actin glutathionylation controls actin dynamics in neutrophils. Immunity 2012;37:1037–49.
  • Alhawaj R, Patel D, Kelly MR, et al. Heme biosynthesis modulation via delta-aminolevulinic acid administration attenuates chronic hypoxia-induced pulmonary hypertension. Am J Physiol Lung Cell Mol Physiol 2015;308:L719–28.
  • Lee JJ, Hung CC, Tsai JC, Chen HC. Endothelin-1 enhances superoxide and prostaglandin E2 production of isolated diabetic glomeruli. Kaohsiung J Med Sci 2010;26:350–6.
  • Zeng Q, Zhou Q, Yao F, et al. Endothelin-1 regulates cardiac L-type calcium channels via NAD(P)H oxidase-derived superoxide. J Pharmacol Exp Ther 2008;326:732–8.
  • Rancourt ME, Rodrigue ME, Agharazii M, et al. Role of oxidative stress in erythropoietin-induced hypertension in uremic rats. Am J Hypertens 2010;23:314–20.
  • Kim HY, Chung JM, Chung K. Increased production of mitochondrial superoxide in the spinal cord induces pain behaviors in mice: the effect of mitochondrial electron transport complex inhibitors. Neurosci Lett 2008;447:87–91.
  • Fernandes ES, Vong CT, Quek S, et al. Superoxide generation and leukocyte accumulation: key elements in the mediation of leukotriene B(4)-induced itch by transient receptor potential ankyrin 1 and transient receptor potential vanilloid 1. FASEB J 2013;27:1664–73.
  • Verri WA Jr, Guerrero AT, Fukada SY, et al. IL-33 mediates antigen-induced cutaneous and articular hypernociception in mice. Proc Natl Acad Sci USA 2008;105:2723–8.
  • Magro DA, Hohmann MS, Mizokami SS, et al. An interleukin-33/ST2 signaling deficiency reduces overt pain-like behaviors in mice. Braz J Med Biol Res 2013;46:601–6.
  • Joseph EK, Green PG, Bogen O, et al. Vascular endothelial cells mediate mechanical stimulation-induced enhancement of endothelin hyperalgesia via activation of P2X2/3 receptors on nociceptors. J Neurosci 2013;33:2849–59.
  • Joseph EK, Green PG, Levine JD. ATP release mechanisms of endothelial cell-mediated stimulus-dependent hyperalgesia. J Pain 2014;15:771.
  • Baamonde A, Lastra A, Villazon M, et al. Involvement of endogenous endothelins in thermal and mechanical inflammatory hyperalgesia in mice. Naunyn Schmiedebergs Arch Pharmacol 2004;369:245–51.
  • Conte Fde P, Barja-Fidalgo C, Verri WA, Jr, et al. Endothelins modulate inflammatory reaction in zymosan-induced arthritis: participation of LTB4, TNF-alpha, and CXCL-1. J Leukoc Biol 2008;84:652–60.
  • Zarpelon AC, Pinto LG, Cunha TM, et al. Endothelin-1 induces neutrophil recruitment in adaptive inflammation via TNFalpha and CXCL1/CXCR2 in mice. Can J Physiol Pharmacol 2012;90:187–99.
  • Cuzzocrea S, Pisano B, Dugo L, et al. Superoxide-related signaling cascade mediates nuclear factor-kappaB activation in acute inflammation. Antioxid Redox Signal 2004;6:699–704.
  • Mitra S, Abraham E. Participation of superoxide in neutrophil activation and cytokine production. Biochim Biophys Acta 2006;1762:732–41.
  • Cunha TM, Verri WA Jr, Schivo IR, et al. Crucial role of neutrophils in the development of mechanical inflammatory hypernociception. J Leukoc Biol 2008;83:824–32.
  • Fattori V, Amaral FA, Verri WA Jr. Neutrophils and arthritis: role in disease and pharmacological perspectives. Pharmacol Res 2016;112:84–98.
  • Gonon AT, Gourine AV, Middelveld RJ, et al. Limitation of infarct size and attenuation of myeloperoxidase activity by an endothelin A receptor antagonist following ischaemia and reperfusion. Basic Res Cardiol 2001;96:454–62.
  • Guo J, Li Y, He Z, et al. Targeting endothelin receptors A and B attenuates the inflammatory response and improves locomotor function following spinal cord injury in mice. Int J Mol Med 2014;34:74–82.
  • Saito S, Aikawa R, Shiojima I, et al. Endothelin-1 induces expression of fetal genes through the interleukin-6 family of cytokines in cardiac myocytes. FEBS Lett 1999;456:103–7.
  • Zhong X, Wang H, Huang S. Endothelin-1 induces interleukin-18 expression in human osteoblasts. Arch Oral Biol 2014;59:289–96.
  • Verri WA Jr, Schivo IR, Cunha TM, et al. Interleukin-18 induces mechanical hypernociception in rats via endothelin acting on ETB receptors in a morphine-sensitive manner. J Pharmacol Exp Ther 2004;310:710–17.
  • Piovezan AP, D'orleans-Juste P, Tonussi CR, Rae GA. Endothelins potentiate formalin-induced nociception and paw edema in mice. Can J Physiol Pharmacol 1997;75:596–600.
  • Khodorova A, Fareed MU, Gokin A, et al. Local injection of a selective endothelin-B receptor agonist inhibits endothelin-1-induced pain-like behavior and excitation of nociceptors in a naloxone-sensitive manner. J Neurosci 2002;22:7788–96.
  • Pomonis JD, Rogers SD, Peters CM, et al. Expression and localization of endothelin receptors: implications for the involvement of peripheral glia in nociception. J Neurosci 2001;21:999–1006.
  • Vellani V, Prandini M, Giacomoni C, et al. Functional endothelin receptors are selectively expressed in isolectin B4-negative sensory neurons and are upregulated in isolectin B4-positive neurons by neurturin and glia-derived neurotropic factor. Brain Res 2011;1381:31–7.
  • Koyama Y, Mizobata T, Yamamoto N, et al. Endothelins stimulate expression of cyclooxygenase 2 in rat cultured astrocytes. J Neurochem 1999;73:1004–11.
  • Chichorro JG, Fiuza CR, Bressan E, et al. Endothelins as pronociceptive mediators of the rat trigeminal system: role of ETA and ETB receptors. Brain Res 2010;1345:73–83.
  • Laziz I, Larbi A, Grebert D, et al. Endothelin as a neuroprotective factor in the olfactory epithelium. Neuroscience 2011;172:20–9.
  • Da Cunha JM, Rae GA, Ferreira SH, Cunha Fde Q. Endothelins induce ETB receptor-mediated mechanical hypernociception in rat hindpaw: roles of cAMP and protein kinase C. Eur J Pharmacol 2004;501:87–94.
  • Hucho T, Levine JD. Signaling pathways in sensitization: toward a nociceptor cell biology. Neuron 2007;55:365–76.
  • Verri WA Jr, Molina RO, Schivo IR, et al. Nociceptive effect of subcutaneously injected interleukin-12 is mediated by endothelin (ET) acting on ETB receptors in rats. J Pharmacol Exp Ther 2005;315:609–15.
  • National Center for Biotechnology Information. PubChem Compound Database; CID = 6433095. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/6433095 [last accessed 11 Jun 2016].
  • National Center for Biotechnology Information. PubChem Compound Database; CID = 16759603. Available from: https://pubchem.ncbi.nlm.nih.gov/compound/16759603 [last accessed 11 Jun 2016].

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