Antioxidant activity of sestrin 2 controls neuropathic pain after peripheral nerve injury

Antioxidants and Redox Signaling

Volumn 19, Issue 17, 2013, Pages 2013-2023

  Kallenborn Gerhardt, Wiebke ^a   Lu, Ruirui ^a,b   Syhr, Katharina M J ^a   Heidler, Juliana ^a   Von Melchner, Harald ^a   Geisslinger, Gerd ^a   Bangsow, Thorsten ^a   Schmidtko, Achim ^a  

^a GOETHE UNIVERSITY MEDICAL SCHOOL   (Germany)

^b UNIVERSITY OF WITTEN HERDECKE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ANTIOXIDANT; MESSENGER RNA; N TERT BUTYL ALPHA PHENYLNITRONE; REACTIVE OXYGEN METABOLITE; SCAVENGER; SESTRIN 2; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ARTICLE; CONTROLLED STUDY; FEMALE; GENOTYPE; HYPERSENSITIVITY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MOUSE; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVE; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; SENSORY NERVE CELL; SPINAL GANGLION; STEADY STATE; STRESS; UPREGULATION;

ACTIVATING TRANSCRIPTION FACTOR 3; ANIMALS; ANTIOXIDANTS; FEMALE; GANGLIA, SPINAL; HYPERALGESIA; INFLAMMATION; MALE; MICE; MICE, 129 STRAIN; MICE, INBRED C57BL; MICE, KNOCKOUT; NEURALGIA; NOCICEPTION; NUCLEAR PROTEINS; PERIPHERAL NERVE INJURIES; REACTIVE OXYGEN SPECIES; SENSORY RECEPTOR CELLS; UP-REGULATION; ZYMOSAN;

EID: 84889671864     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4958     Document Type: Article

References (43)

1. Braz JM and Basbaum AI. Differential ATF3 expression in dorsal root ganglion neurons reveals the profile of primary afferents engaged by diverse noxious chemical stimuli. Pain 150: 290-301, 2010.
2. Budanov AV, Lee JH, and Karin M. Stressin' Sestrins take an aging fight. EMBO Mol Med 2: 388-400, 2010.
3. Decosterd I and Woolf CJ. Spared nerve injury: an animal model of persistent peripheral neuropathic pain. Pain 87: 149-158, 2000.
4. Essler S, Dehne N, and Brune B. Role of sestrin2 in peroxide signaling in macrophages. FEBS Lett 583: 3531-3535, 2009.
5. Ferreira J, Campos MM, Pesquero JB, Araujo RC, Bader M, and Calixto JB. Evidence for the participation of kinins in Freund's adjuvant-induced inflammatory and nociceptive responses in kinin B1 and B2 receptor knockout mice. Neuropharmacology 41: 1006-1012, 2001.
6. Forman HJ, Maiorino M, and Ursini F. Signaling functions of reactive oxygen species. Biochemistry 49: 835-842, 2010.
7. Greenspan JD, Craft RM, LeResche L, Arendt-Nielsen L, Berkley KJ, Fillingim RB, Gold MS, Holdcroft A, Lautenbacher S, Mayer EA, Mogil JS, Murphy AZ, and Traub RJ. Studying sex and gender differences in pain and analgesia: a consensus report. Pain 132 Suppl 1: S26-S45, 2007.
8. Heine S, Michalakis S, Kallenborn-Gerhardt W, Lu R, Lim HY, Weiland J, Del Turco D, Deller T, Tegeder I, Biel M, Geisslinger G, and Schmidtko A. CNGA3: a target of spinal nitric oxide/cGMP signaling and modulator of inflammatory pain hypersensitivity. J Neurosci 31: 11184-11192, 2011.
9. Hoetzenecker W, Echtenacher B, Guenova E, Hoetzenecker K, Woelbing F, Bruck J, Teske A, Valtcheva N, Fuchs K, Kneilling M, Park JH, Kim KH, Kim KW, Hoffmann P, Krenn C, Hai T, Ghoreschi K, Biedermann T, and Rocken M. ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat Med 18: 128-134, 2012.
10. Ibi M, Matsuno K, Shiba D, Katsuyama M, Iwata K, Kakehi T, Nakagawa T, Sango K, Shirai Y, Yokoyama T, Kaneko S, Saito N, and Yabe-Nishimura C. Reactive oxygen species derived from NOX1/NADPH oxidase enhance inflammatory pain. J Neurosci 28: 9486-9494, 2008.
11. Jonsson TJ and Lowther WT. The peroxiredoxin repair proteins. Subcell Biochem 44: 115-141, 2007.
12. Kim D, You B, Jo EK, Han SK, Simon MI, and Lee SJ. NADPH oxidase 2-derived reactive oxygen species in spinal cord microglia contribute to peripheral nerve injury-induced neuropathic pain. Proc Natl Acad Sci U S A 107: 14851-14856, 2010.
13. Kim HK, Kim JH, Gao X, Zhou JL, Lee I, Chung K, and Chung JM. Analgesic effect of vitamin E is mediated by reducing central sensitization in neuropathic pain. Pain 122: 53-62, 2006.
14. Kim HK, Park SK, Zhou JL, Taglialatela G, Chung K, Coggeshall RE, and Chung JM. Reactive oxygen species (ROS) play an important role in a rat model of neuropathic pain. Pain 111: 116-124, 2004.
15. Kiryu-Seo S, Kato R, Ogawa T, Nakagomi S, Nagata K, and Kiyama H. Neuronal injury-inducible gene is synergistically regulated by ATF3, c-Jun, and STAT3 through the interaction with Sp1 in damaged neurons. J Biol Chem 283: 6988-6996, 2008.
16. Kwan KY, Allchorne AJ, Vollrath MA, Christensen AP, Zhang DS, Woolf CJ, and Corey DP. TRPA1 contributes to cold, mechanical, and chemical nociception but is not essential for hair-cell transduction. Neuron 50: 277-289, 2006.
17. Lee WY, Orestes P, Latham J, Naik AK, Nelson MT, Vitko I, Perez-Reyes E, Jevtovic-Todorovic V, and Todorovic SM. Molecular mechanisms of lipoic acid modulation of T-type calcium channels in pain pathway. J Neurosci 29: 9500-9509, 2009.
18. Lu R, Kallenborn-Gerhardt W, Geisslinger G, and Schmidtko A. Additive antinociceptive effects of a combination of vitamin C and vitamin E after peripheral nerve injury. PLoS One 6: e29240, 2011.
19. Mao YF, Yan N, Xu H, Sun JH, Xiong YC, and Deng XM. Edaravone, a free radical scavenger, is effective on neuropathic pain in rats. Brain Res 1248: 68-75, 2009.
20. Meller ST and Gebhart GF. Intraplantar zymosan as a reliable, quantifiable model of thermal and mechanical hyperalgesia in the rat. Eur J Pain 1: 43-52, 1997.
21. Melnikova I. Pain market. Nat Rev Drug Discov 9: 589-590, 2010.
22. Moalem G and Tracey DJ. Immune and inflammatory mechanisms in neuropathic pain. Brain Res Rev 51: 240-264, 2006.
23. Mogil JS. Animal models of pain: progress and challenges. Nat Rev Neurosci 10: 283-294, 2009.
24. Mogil JS and Chanda ML. The case for the inclusion of female subjects in basic science studies of pain. Pain 117: 1-5, 2005.
25. Moore DL and Goldberg JL. Multiple transcription factor families regulate axon growth and regeneration. Dev Neurobiol 71: 1186-1211, 2011.
26. Papadia S, Soriano FX, Leveille F, Martel MA, Dakin KA, Hansen HH, Kaindl A, Sifringer M, Fowler J, Stefovska V, McKenzie G, Craigon M, Corriveau R, Ghazal P, Horsburgh K, Yankner BA, Wyllie DJ, Ikonomidou C, and Hardingham GE. Synaptic NMDA receptor activity boosts intrinsic antioxidant defenses. Nat Neurosci 11: 476-487, 2008.
27. Schmidtko A, Del Turco D, Coste O, Ehnert C, Niederberger E, Ruth P, Deller T, Geisslinger G, and Tegeder I. Essential role of the synaptic vesicle protein synapsin II in formalininduced hyperalgesia and glutamate release in the spinal cord. Pain 115: 171-181, 2005.
28. Schmidtko A, Gao W, Konig P, Heine S, Motterlini R, Ruth P, Schlossmann J, Koesling D, Niederberger E, Tegeder I, Friebe A, and Geisslinger G. cGMP produced by NO-sensitive guanylyl cyclase essentially contributes to inflammatory and neuropathic pain by using targets different from cGMPdependent protein kinase I. J Neurosci 28: 8568-8576, 2008.
29. Schnell SA, Staines WA, and Wessendorf MW. Reduction of lipofuscin-like autofluorescence in fluorescently labeled tissue. J Histochem Cytochem 47: 719-730, 1999.
30. Scholz J and Woolf CJ. The neuropathic pain triad: neurons, immune cells and glia. Nat Neurosci 10: 1361-1368, 2007.
31. Seijffers R, Mills CD, and Woolf CJ. ATF3 increases the intrinsic growth state of DRG neurons to enhance peripheral nerve regeneration. J Neurosci 27: 7911-7920, 2007.
32. Shao D, Oka S, Brady CD, Haendeler J, Eaton P, and Sadoshima J. Redox modification of cell signaling in the cardiovascular system. J Mol Cell Cardiol 52: 550-558, 2012.
33. Siniscalco D, Fuccio C, Giordano C, Ferraraccio F, Palazzo E, Luongo L, Rossi F, Roth KA, Maione S, and de Novellis V. Role of reactive oxygen species and spinal cord apoptotic genes in the development of neuropathic pain. Pharmacol Res 55: 158-166, 2007.
34. Takeda M, Kato H, Takamiya A, Yoshida A, and Kiyama H. Injury-specific expression of activating transcription factor-3 in retinal ganglion cells and its colocalized expression with phosphorylated c-Jun. Invest Ophthalmol Vis Sci 41: 2412-2421, 2000.
35. Thacker MA, Clark AK, Marchand F, and McMahon SB. Pathophysiology of peripheral neuropathic pain: immune cells and molecules. Anesth Analg 105: 838-847, 2007.
36. Thompson MR, Xu D, and Williams BR. ATF3 transcription factor and its emerging roles in immunity and cancer. J Mol Med (Berl) 87: 1053-1060, 2009.
37. Todorovic SM, Jevtovic-Todorovic V, Meyenburg A, Mennerick S, Perez-Reyes E, Romano C, Olney JW, and Zorumski CF. Redox modulation of T-type calcium channels in rat peripheral nociceptors. Neuron 31: 75-85, 2001.
38. Todorovic SM, Meyenburg A, and Jevtovic-Todorovic V. Redox modulation of peripheral T-type Ca2 + channels in vivo: alteration of nerve injury-induced thermal hyperalgesia. Pain 109: 328-339, 2004.
39. Tsujino H, Kondo E, Fukuoka T, Dai Y, Tokunaga A, Miki K, Yonenobu K, Ochi T, and Noguchi K. Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury. Mol Cell Neurosci 15: 170-182, 2000.
40. Vincent AM, Kato K, McLean LL, Soules ME, and Feldman EL. Sensory neurons and schwann cells respond to oxidative stress by increasing antioxidant defense mechanisms. Antioxid Redox Signal 11: 425-438, 2009.
41. von Hehn CA, Baron R, and Woolf CJ. Deconstructing the neuropathic pain phenotype to reveal neural mechanisms. Neuron 73: 638-652, 2012.
42. Wempe F, De-Zolt S, Koli K, Bangsow T, Parajuli N, Dumitrascu R, Sterner-Kock A, Weissmann N, Keski-Oja J, and von Melchner H. Inactivation of sestrin 2 induces TGF-beta signaling and partially rescues pulmonary emphysema in a mouse model of COPD. Dis Model Mech 3: 246-253, 2010.
43. Yowtak J, Lee KY, Kim HY, Wang J, Kim HK, Chung K, and Chung JM. Reactive oxygen species contribute to neuropathic pain by reducing spinal GABA release. Pain 152: 844-852, 2011.