Activation of ERK signalling by Src family kinases (SFKs) in DRG neurons contributes to hydrogen peroxide (H₂O₂)-induced thermal hyperalgesia

References

• Wang ZQ, Porreca F, Cuzzocrea S, Galen K, Lightfoot R, Masini E, et al. A newly identified role for superoxide in inflammatory pain. J Pharmacol Exp Ther 2004;309:869–878.
   PubMed Web of Science ®Google Scholar
• Khattab MM. Tempol, a membrane-permeable radical scavenger, attenuates peroxynitrite and superoxide anion enhanced carrageenan induced paw edema and hyperalgesia: a key role for superoxide anion. Eur J Pharmacol 2006;548:167–173.
   PubMed Web of Science ®Google Scholar
• Keeble JE, Bodkin JV, Liang L, Wodarski R, Davies M, Fernandes ES, et al. Hydrogen peroxide is a novel mediator of inflammatory hyperalgesia, acting via transient receptor potential vanilloid 1-dependent and independent mechanisms. Pain 2009;141:135–142.
   PubMed Web of Science ®Google Scholar
• Mittal N, Joshi R, Hota D, Chakrabarti A. Evaluation of antihyperalgesic effect of curcumin on formalin-induced orofacial pain in rat. Phytother Res 2009;23:507–512.
   PubMed Web of Science ®Google Scholar
• Singh AK, Vinayak M. Curcumin attenuates CFA induced thermal hyperalgesia by modulation of antioxidant enzymes and down regulation of TNF-α, IL-1β and IL-6. Neurochem Res 2015;40:463–472.
   PubMed Web of Science ®Google Scholar
• Singh AK, Vinayak M. Anti-nociceptive effect of resveratrol during inflammatory hyperalgesia via differential regulation of pro-inflammatory mediators. Phytother Res 2016;30:1164–1171.
   PubMed Web of Science ®Google Scholar
• Naik AK, Tandan SK, Dudhgaonkar SP, Jadhav SH, Kataria M, Prakash VR, Kumar D. Role of oxidative stress in pathophysiology of peripheral neuropathy and modulation by N-acetyl-L-cysteine in rats. Eur J Pain 2006;10: 573–579.
   PubMed Web of Science ®Google Scholar
• Mikuls TR, O’Dell JR, Ertl R, et al. Examining the exhaled levels of hydrogen peroxide in rheumatoid arthritis: a pilot study. Ann Rheum Dis 2006;65:1252–1253.
   PubMed Web of Science ®Google Scholar
• Gao YJ, Ji RR. c-Fos and pERK, which is a better marker for neuronal activation and central sensitization after noxious stimulation and tissue injury? Open Pain J 2009;2:11–17.
   PubMedGoogle Scholar
• Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, et al. Oxidative stress activates extracellular signal–regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest 1997;100:1813–1821.
   PubMed Web of Science ®Google Scholar
• Zhuang S, Yan Y, Daubert RA, Han J, Schnellmann RG. ERK promotes hydrogen peroxide-induced apoptosis through caspase-3 activation and inhibition of Akt in renal epithelial cells. Am J Physiol Renal Physiol 2007;292:F440–FF447.
   PubMed Web of Science ®Google Scholar
• Rosseland CM, Wierød L, Oksvold MP, Werner H, Ostvold AC, Thoresen GH, et al. Cytoplasmic retention of peroxide-activated ERK provides survival in primary cultures of rat hepatocytes. Hepatology 2005;42:200–207.
   PubMed Web of Science ®Google Scholar
• Bhat NR, Zhang P. Hydrogen peroxide activation of multiple mitogen-activated protein kinases in an oligodendrocyte cell line: role of extracellular signal-regulated kinase in hydrogen peroxide-induced cell death. J Neurochem 1999;72:112–119.
   PubMed Web of Science ®Google Scholar
• Ruffels J, Griffin M, Dickenson JM. Activation of ERK1/2, JNK and PKB by hydrogen peroxide in human SH-SY5Y neuroblastoma cells: role of ERK1/2 in H2O2-induced cell death. Eur J Pharmacol 2004;483:163–173.
   PubMed Web of Science ®Google Scholar
• Lee K, Esselman WJ. Inhibition of PTPs by H2O2 regulates the activation of distinct MAPK pathways. Free Radic Biol Med 2002;33:1121–1132.
   PubMed Web of Science ®Google Scholar
• Meng TC, Fukada T, Tonks NK. Reversible oxidation and inactivation of protein tyrosine phosphatases in vivo. Mol Cell 2002;9:387–399.
   PubMed Web of Science ®Google Scholar
• Giannoni E, Buricchi F, Raugei G, Ramponi G, Chiarugi P. Intracellular reactive oxygen species activate Src tyrosine kinase during cell adhesion and anchorage-dependent cell growth. Mol Cell Biol 2005;25:6391–6403.
   PubMed Web of Science ®Google Scholar
• Suo ZW, Yang X, Li L, Liu YN, Shi L, Hu XD. Inhibition of protein tyrosine phosphatases in spinal dorsal horn attenuated inflammatory pain by repressing Src signaling. Neuropharmacology 2013;70:122–130.
   PubMed Web of Science ®Google Scholar
• Azkona G, Saavedra A, Aira Z, Aluja D, Xifró X, Baguley T, et al. Striatal-enriched protein tyrosine phosphatase modulates nociception: evidence from genetic deletion and pharmacological inhibition. Pain 2016;157:377–386.
   PubMed Web of Science ®Google Scholar
• Hensellek S, Brell P, Schaible HG, Bräuer R, Segond von Banchet G. The cytokine TNF-α increases the proportion of DRG neurons expressing the TRPV1 receptor via the TNFR1 receptor and ERK activation. Mol Cell Neurosci 2007;36:381–391.
   PubMed Web of Science ®Google Scholar
• Gordon JA. Use of vanadate as protein-phosphotyrosine phosphatase inhibitor. Methods Enzymol 1991;201:477–482.
   PubMed Web of Science ®Google Scholar
• Kawasaki Y, Kohno T, Zhuang ZY, Brenner GJ, Wang H, Van Der Meer C, et al. Ionotropic and metabotropic receptors, protein kinase A, protein kinase C, and Src contribute to C-fiber-induced ERK activation and cAMP response element-binding protein phosphorylation in dorsal horn neurons, leading to central sensitization. J Neurosci 2004;24:8310–8321.
   PubMed Web of Science ®Google Scholar
• Zhang G, Chen W, Marvizón JC. Src family kinases mediate the inhibition of substance P release in the rat spinal cord by μ-opioid receptors and GABA(B) receptors, but not α2 adrenergic receptors. Eur J Neurosci 2010;32:963–973.
   PubMed Web of Science ®Google Scholar
• Mestre C, Pélissier T, Fialip J, Wilcox G, Eschalier A. A method to perform direct transcutaneous intrathecal injection in rats. J Pharmacol Toxicol Methods 1994;32:197–200.
   PubMed Web of Science ®Google Scholar
• Dubey R, Singh P, Singh AK, Yadav MK, Swati D, Vinayak M, et al. Polymorphic signature of the anti-inflammatory activity of 2,2’-{[1,2-Phenylenebis(methy-lene)]bis(sulfanediyl)}bis(4,6-dimethylnicotinonitrile). Cryst Growth Des 2014;14:1347–1356.
   Web of Science ®Google Scholar
• Ohkawa H, Ohishi N, Yagi K. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 1979;95:351–358.
   PubMed Web of Science ®Google Scholar
• Harris JA. Using c-Fos as a neural marker of pain. Brain Res Bull 1998;45:1–8.
   PubMed Web of Science ®Google Scholar
• Munglani R, Hunt SP. Molecular biology of pain. Br J Anaesth 1995;75:186–192.
   PubMed Web of Science ®Google Scholar
• Rittner HL, Machelska H, Stein C. Leukocytes in the regulation of pain and analgesia. J Leukoc Biol 2005;78:1215–1222.
   PubMed Web of Science ®Google Scholar
• Perlson E, Hanz S, Ben-Yaakov KB, Segal-Ruder Y, Seger R, Fainzilber M. Vimentin-dependent spatial translocation of an activated MAP kinase in injured nerve. Neuron 2005;45:715–726.
   PubMed Web of Science ®Google Scholar
• Ruscheweyh R, Forsthuber L, Schoffnegger D, Sandkühler J. Modification of classical neurochemical markers in identified primary afferent neurons with Abeta-, Adelta-, and C-fibers after chronic constriction injury in mice. J Comp Neurol 2007;502:325–336.
   PubMed Web of Science ®Google Scholar
• Basbaum AI, Bautista DM, Scherrer G, Julius D,. Cellular and molecular mechanisms of pain. Cell 2009;139:267–284.
   PubMed Web of Science ®Google Scholar
• Sies H. Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem 2014;289:8735–8741.
   PubMed Web of Science ®Google Scholar
• Gough DR, Cotter TG. Hydrogen peroxide: a Jekyll and Hyde signalling molecule. Cell Death Dis 2011;2:e213.
   PubMed Web of Science ®Google Scholar
• Katsura H, Obata K, Mizushima T, Sakurai J, Kobayashi K, Yamanaka H, et al. Activation of Src-family kinases in spinal microglia contributes to mechanical hypersensitivity after nerve injury. J Neurosci 2006;26:8680–8690.
   PubMed Web of Science ®Google Scholar
• Tan YH, Li K, Chen XY, et al. Activation of Src family kinases in spinal microglia contributes to formalin-induced persistent pain state through p38 pathway. J Pain 2012;13:1008–1015.
   PubMed Web of Science ®Google Scholar
• Stoker AW. Protein tyrosine phosphatases and signalling. J Endocrinol 2005;185:19–33.
   PubMed Web of Science ®Google Scholar
• Tabernero L, Aricescu AR, Jones EY, Szedlacsek SE. Protein tyrosine phosphatases: structure-function relationships. FEBS J 2008;275:867–882.
   PubMed Web of Science ®Google Scholar
• Tonks NK. Protein tyrosine phosphatases: from genes, to function, to disease. Nat Rev Mol Cell Biol 2006;7:833–846.
   PubMed Web of Science ®Google Scholar
• Rhee SG, Chang TS, Bae YS, Lee SR, Kang SW. Cellular regulation by hydrogen peroxide. Am Soc Nephrol J 2003;14:S211–S215.
   PubMed Web of Science ®Google Scholar
• Zhou HY, Chen SR, Pan HL. Targeting N-methyl-D-aspartate receptors for treatment of neuropathic pain. Expert Rev Clin Pharmacol 2011;4:379–388.
   PubMedGoogle Scholar
• Guo W, Zou S, Guan Y, et al. Tyrosine phosphorylation of the NR2B subunit of the NMDA receptor in the spinal cord during the development and maintenance of inflammatory hyperalgesia. J Neurosci 2002;22:6208–6217.
   PubMed Web of Science ®Google Scholar
• Ma F, Zhang L, Westlund KN. Reactive oxygen species mediate TNFR1 increase after TRPV1 activation in mouse DRG neurons. Mol Pain 2009;5:31.
   PubMed Web of Science ®Google Scholar
• Toh ML, Aeberli D, Lacey D, Yang Y, Santos LL, Clarkson M, et al. Regulation of IL-1 and TNF receptor expression and function by endogenous macrophage migration inhibitory factor. J Immunol 2006;177:4818–4825.
   PubMed Web of Science ®Google Scholar