Mirror-image pain is mediated by nerve growth factor produced from tumor necrosis factor alpha-activated satellite glia after peripheral nerve injury

Pain

Volumn 155, Issue 5, 2014, Pages 906-920

  Cheng, Chau Fu ^a   Cheng, Jen Kun ^b   Chen, Chih Yang ^a   Lien, Cheng Chang ^a   Chu, Dachen ^c   Wang, Szu Yi ^a,b   Tsaur, Meei Ling ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b MACKAY MEMORIAL HOSPITAL   (Taiwan)

^c TAIPEI CITY HOSPITAL   (Taiwan)

Author keywords

Contralateral pain; Dorsal root ganglion; Glial inhibitor; Mechanical hypersensitivity; Neurotrophic factors; Nociceptor excitability; Spinal nerve ligation

Indexed keywords

FLUOROCITRIC ACID; NERVE GROWTH FACTOR; NEUROTROPHIN 3; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR ALPHA RECEPTOR;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CEREBROSPINAL FLUID; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; GLIA; HYPERALGESIA; IMMUNOREACTIVITY; MALE; MECHANICAL STRESS; MICROGLIA; MIRROR IMAGE PAIN; NERVE CELL EXCITABILITY; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; OLIGODENDROGLIA; PAIN; PAIN RECEPTOR; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SENSITIZATION; SPINAL CORD NERVE CELL; SPINAL GANGLION; ANIMAL; COMPLICATION; DRUG EFFECTS; METABOLISM; NEURALGIA; PAIN MEASUREMENT; PAIN THRESHOLD; PHYSIOLOGY; SENSORY NERVE CELL; SPRAGUE DAWLEY RAT;

ANIMALS; GANGLIA, SPINAL; HYPERALGESIA; MALE; NERVE GROWTH FACTOR; NEURALGIA; NEUROGLIA; NEURONS, AFFERENT; PAIN MEASUREMENT; PAIN THRESHOLD; PERIPHERAL NERVE INJURIES; RATS; RATS, SPRAGUE-DAWLEY; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84898596810     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2014.01.010     Document Type: Article

References (64)

1. M.J. Arguis, J. Perez, G. Martinez, M. Ubre, and C. Gomar Contralateral neuropathic pain following a surgical model of unilateral nerve injury in rats Reg Anesth Pain Med 33 2008 211 216 (Pubitemid 351539078)
2. H. Bliddal Chronic widespread pain in the spectrum of rheumatological diseases Best Pract Res Clin Rheumatol 21 2007 391 402 (Pubitemid 46972008)
3. E. Bourinet, A. Alloui, A. Monteil, C. Barrere, B. Couette, O. Poirot, A. Pages, J. McRory, T.P. Snutch, A. Eschalier, and J. Nargeot Silencing of the Cav3.2 T-type calcium channel gene in sensory neurons demonstrates its major role in nociception EMBO J 24 2005 315 324 (Pubitemid 40216136)
4. S.R. Chaplan, F.W. Bach, J.W. Pogrel, J.M. Chung, and T.L. Yaksh Quantitative assessment of tactile allodynia in the rat paw J Neurosci Methods 53 1994 55 63 (Pubitemid 24238751)
5. L.Y. Chien, J.K. Cheng, D. Chu, C.F. Cheng, and M.L. Tsaur Reduced expression of A-type potassium channels in primary sensory neurons induces mechanical hypersensitivity J Neurosci 27 2007 9855 9865 (Pubitemid 47404010)
6. + currents J Physiol 587 2009 3233 3250
7. J.L. De la Calle, and C.L. Paino A procedure for direct lumbar puncture in rats Brain Res Bull 59 2002 245 250 (Pubitemid 35300461)
8. X. Fang, L. Djouhri, S. McMullan, C. Berry, K. Okuse, S.G. Waxman, and S.N. Lawson trkA is expressed in nociceptive neurons and influences electrophysiological properties via Nav1.8 expression in rapidly conducting nociceptor J Neurosci 25 2005 4868 4878 (Pubitemid 40664133)
9. Y.J. Gao, Z.Z. Xu, Y.C. Liu, Y.R. Wen, I. Decosterd, and R.R. Ji The c-Jun N-terminal kinase 1 (JNK1) in spinal astrocytes is required for the maintenance of bilateral mechanical allodynia under a persistent inflammatory pain condition PAIN® 148 2010 309 319
10. Y.J. Gao, L. Zhang, O.A. Samad, M.R. Suter, K. Yasuhiko, Z.Z. Xu, J.Y. Park, A.L. Lind, and R.R. Ji JNK-induced MCP-1 production in spinal cord astrocytes contributes to central sensitization and neuropathic pain J Neurosci 29 2009 4096 4108
11. M.S. Gold, S. Dastmalchi, and J.D. Levine Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro Neuroscience 71 1996 265 275 (Pubitemid 26041899)
12. H.J. Gould 3rd, T.N. Gould, J.D. England, D. Paul, Z.P. Liu, and S.R. Levinson A possible role for nerve growth factor in the augmentation of sodium channels in models of chronic pain Brain Res 854 2000 19 29 (Pubitemid 30067656)
13. 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
14. S. Hatashita, M. Sekiguchi, H. Kobayashi, S. Konno, and S. Kikuchi Contralateral neuropathic pain and neuropathology in dorsal root ganglion and spinal cord following hemilateral nerve injury in rats Spine 33 2008 1344 1351
15. M.M. He, A.S. Smith, J.D. Oslob, W.M. Flanagan, A.C. Braisted, A. Whitty, M.T. Cancilla, J. Wang, A.A. Lugovskoy, J.C. Yoburn, A.D. Fung, G. Farrington, J.K. Eldredge, E.S. Day, L.A. Cruz, T.G. Cachero, S.K. Miller, J.E. Friedman, I.C. Choong, and B.C. Cunningham Small-molecule inhibition of TNF-α Science 310 2005 1022 1025
16. R. Hebel, and M.W. Stromberg Anatomy of the laboratory rat 1976 Williams and Wilkins Baltimore
17. F.F. Hefti, A. Rosenthal, P.A. Walicke, S. Wyatt, G. Vergara, D.L. Shelton, and A.M. Davies Novel class of pain drugs based on antagonism of NGF Trends Pharmacol Sci 27 2006 85 91 (Pubitemid 43184029)
18. D. Huang, and B. Yu The mirror-image pain: an uncleared phenomenon and its possible mechanism Neurosci Biobehav Rev 34 2010 528 532
19. v1.8 by p38 mitogen-activated protein kinase increases current density in dorsal root ganglion neurons J Neurosci 28 2008 3190 3201 (Pubitemid 351442277)
20. W. Janig, and R. Baron Complex regional pain syndrome: mystery explained? Lancet Neurol 2 2003 687 697 (Pubitemid 37311322)
21. X. Jin, and R.W. Gereau IV Acute p38-mediated modulation of tetrodotoxin-resistant sodium channels in mouse sensory neurons by tumor necrosis factor-α J Neurosci 26 2008 246 255 (Pubitemid 43089538)
22. 2 receptors, in capsaicin-sensitive small neurons cultured from rat dorsal root ganglia Neurosci Res 32 1998 231 239 (Pubitemid 28559213)
23. M. Kasai, and K. Mizumura Increase in spontaneous action potentials and sensitivity in response to norepinephrine in dorsal root ganglion neurons of adjuvant inflamed rats Neurosci Res 39 2001 109 113 (Pubitemid 32042510)
24. S.H. Kim, and J.M. Chung An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat PAIN® 50 1992 355 363
25. M. Koltzenburg, P.D. Wall, and S.B. McMahon Does the right side know what the left is doing? Trends Neurosci 22 1999 122 127 (Pubitemid 29151805)
26. K.H. Konopka, M. Harbers, A. Houghton, R. Kortekaas, A. van Vliet, W. Timmerman, J.A. den Boer, M.M.R.F. Struys, and M. van Wijhe Bilateral sensory abnormalities in patients with unilateral neuropathic pain; a quantitative sensory testing (QST) study PLoS One 7 2012 e37524
27. R. Kuno, Y. Yoshida, A. Nitta, T. Nabeshima, J. Wang, Y. Sonobe, J. Kawanokuchi, H. Takeuchi, T. Mizuno, and A. Suzumura The role of TNF-alpha and its receptors in the production of NGF and BDNF by astrocytes Brain Res 1116 2006 12 18 (Pubitemid 44485022)
28. G.R. Lewin, A.M. Ritter, and L.M. Mendell Nerve growth factor-induced hyperalgesia in the neonatal and adult rat J Neurosci 13 1993 2136 2148 (Pubitemid 23113422)
29. C.C. Lien, and P. Jonas Kv3 potassium conductance is necessary and kinetically optimized for high-frequency action potential generation in hippocampal interneurons J Neurosci 23 2003 2058 2068 (Pubitemid 36368893)
30. F.Y. Liu, Y.N. Sun, F.T. Wang, Q. Li, L. Su, Z.F. Zhao, X.L. Meng, H. Zhao, X. Wu, Q. Sun, G.G. Xing, and Y. Wan Activation of satellite glial cells in lumbar dorsal root ganglia contributes to neuropathic pain after spinal nerve ligation Brain Res 1427 2012 65 77
31. S.A. Malin, D.C. Molliver, H.R. Koerber, P. Cornuet, R. Frye, K.M. Albers, and B.M. Davis Glial cell line-derived neuropathic factor family members sensitize nociceptors in vitro and produce thermal hyperalgesia in vivo J Neurosci 26 2006 8588 8599 (Pubitemid 44316188)
32. C.S. McCabe, R.C. Haigh, N.G. Shenker, J. Lewis, and D.R. Blake Phantoms in rheumatology Novartis Found Symp 260 2004 154 174
33. S.B. McMahon, and W.B.J. Caffetty Neurotrophic influences on neuropathic pain D.J. Chadwick, J. Goode, Pathological pain: from molecular to clinical aspects 2004 John Wiley & Sons Chichester, UK 68 102 (Pubitemid 41329072)
34. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkaapp, K. O'Connor, S. Poole, K. Tracey, D. Martin, S.F. Maier, and L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats J Neurosci 23 2003 1026 1040 (Pubitemid 36206195)
35. K. Obata, H. Katsura, J. Sakurai, K. Kobayashi, H. Yamanaka, Y. Dai, T. Fukuoka, and K. Noguchi Suppression of the p75 neurotrophin receptor in uninjured sensory neurons reduces neuropathic pain after nerve injury J Neurosci 26 2006 11974 11986 (Pubitemid 44772108)
36. H. Obata, S. Sakurazawa, M. Kimura, and S. Saito Activation of astrocytes in the spinal cord contributes to the development of bilateral allodynia after peripheral nerve injury in rats Brain Res 1363 2010 72 80
37. S. Ohtori, K. Takahashi, H. Moriya, and R.R. Myers TNF-alpha and TNF-alpha receptor type 1 upregulation in glia and neurons after peripheral nerve injury: studies in murine DRG and spinal cord Spine 29 2004 1082 1088 (Pubitemid 38649821)
38. D. Papir-Kricheli, J. Frey, R. Laufer, C. Gilon, M. Chorev, Z. Selinger, and M. Devor Behavioural effects of receptor-specific substance P agonists PAIN® 31 1987 263 276
39. A. Parent Carpenter's human neuroanatomy 1996 Williams and Wilkins Baltimore
40. S. Pezet, and S.B. McMahon Neurotrophins: mediators and modulators of pain Annu Rev Neurosci 29 2006 507 538 (Pubitemid 44476854)
41. W.J. Ren, Y. Liu, L.J. Zhou, W. Li, Y. Zhong, R.P. Pang, W.J. Xin, X.H. Wei, J. Wang, H.Q. Zhu, C.Y. Wu, Z.H. Qin, G. Liu, and X.G. Liu Peripheral nerve injury leads to working memory deficits and dysfunction of the hippocampus by upregulation of TNF-α in rodents Neuropsychopharmacology 36 2011 979 992
42. D. Sapunar, S. Kostic, A. Banozic, and L. Puljak Dorsal root ganglion - a potential new therapeutic target for neuropathic pain J Pain Res 5 2012 31 38
43. 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-α after spinal nerve ligation J Neurosci 23 2003 3028 3038 (Pubitemid 36418639)
44. M. Schafers, C.I. Svensson, C. Sommer, and L.S. Sorkin Tumor necrosis factor-alpha induces mechanical allodynia after spinal nerve ligation by activation of p38 MAPK in primary sensory neurons J Neurosci 23 2003 2517 2521 (Pubitemid 36418584)
45. J. Scholz, and C.J. Woolf The neuropathic pain triad: neurons, immune cells and glia Nat Neurosci 10 2007 1361 1368 (Pubitemid 350014681)
46. K.L. Schreiber, A.J. Beitz, and G.L. Wilcox Activation of spinal microglia in a murine model of peripheral inflammation-induced, long-lasting contralateral allodynia Neurosci Lett 440 2008 63 67
47. C. Sommer, C. Schmidt, and A. George Hyperalgesia in experimental neuropathy is dependent on the TNF receptor 1 Exp Neurol 151 1998 138 142 (Pubitemid 28223862)
48. G.R. Souza, J. Talbot, C.M. Lotufo, F.Q. Cunha, T.M. Cunha, and S.H. Ferreira Fractalkine mediates inflammatory pain through activation of satellite glial cells Proc Natl Acad Sci USA 110 2013 11193 11198
49. L.E. Spataro, E.M. Sloane, E.D. Milligan, J. Wieseler-Frank, D. Schoeniger, B.M. Jekich, R.M. Barrientos, S.F. Maier, and L.R. Watkins Spinal gap junctions: potential involvement in pain facilitation J Pain 5 2004 392 405 (Pubitemid 39410108)
50. v1.7 and alters its gating properties J Neurosci 30 2010 1637 1647
51. C.S. Sung, C.H. Cherng, Z.H. Wen, W.K. Chang, S.Y. Huang, S.L. Lin, K.H. Chan, and C.S. Wong Minocycline and fluorocitrate suppress spinal nociceptive signaling in intrathecal IL-1β-induced thermal hyperalgesic rats Glia 60 2012 2004 2017
52. M. Takeda, M. Takahashi, and S. Matsumoto Contribution of the activation of satellite glia in sensory ganglia to pathological pain Neurosci Biobehav Rev 33 2009 784 792
53. Y. Takei, and R. Laskey Interpreting crosstalk between TNF-α and NGF: potential implications for diseases Trends Mol Med 14 2008 381 388
54. C.M. Twining, E.M. Sloane, E.D. Milligan, M. Chacur, D. Martin, S. Poole, H. Marsh, S.F. Maier, and L.R. Watkins Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats PAIN® 110 2004 299 309 (Pubitemid 38953295)
55. B. Wang, J.R. Jenkins, and P. Trayhurn Expression and secretion of inflammation-related adipokines by human adipocytes differentiated in culture: integrated response to TNF-α Am J Physiol Endocrinol Metab 288 2005 E731 E740
56. X.H. Wei, Y. Zang, C.Y. Wu, J.T. Xu, W.J. Xin, W.J. Xin, and X.G. Liu Peri-sciatic administration of recombinant rat TNF-α induces mechanical allodynia via upregulation of TNF-α in dorsal root ganglia and in spinal dorsal horn: the role of NF-kappa B pathway Exp Neurol 205 2007 471 484 (Pubitemid 46755768)
57. T.D. Wilson-Gerwing, M.V. Dmyterko, D.W. Zochodne, J.M. Johnston, and V.M.K. Verge Neurotriphin-3 suppresses thermal hyperalgesia associated with neuropathic pain and attenuates transient receptor potential vanilloid receptor-1 expression in adult sensory neurons J Neurosci 25 2005 758 767
58. C.J. Woolf, A. Allchorne, B. Safieh-Garabedian, and S. Poole Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumor necrosis factor α Br J Pharmcol 121 1997 417 424 (Pubitemid 27226293)
59. W.R. Xie, H. Deng, H. Li, T.L. Brown, J.A. Strong, and J.M. Zhang Robust increase of cutaneous sensitivity, cytokine production and sympathetic sprouting in rats with localized inflammatory irritation of the spinal ganglia Neuroscience 142 2006 809 822 (Pubitemid 44485910)
60. J.T. Xu, W.J. Xin, Y. Zang, C.Y. Wu, and X.G. Liu The role of tumor necrosis factor-alpha in the neuropathic pain induced by lumbar 5 ventral root transection in rat PAIN® 123 2006 306 321
61. Y.H. Zhang, and G.D. Nicol NGF-mediated sensitization of excitability of rat sensory neurons is prevented by blocking antibody to the p75 neurotrophin receptor Neurosci Lett 366 2004 187 192 (Pubitemid 38970153)
62. X.F. Zhou, R. Rush, and E.M. McLachlan Differential expression of the p75 nerve growth factor receptor in glia and neurons of the rat dorsal root ganglia after peripheral nerve transection J Neurosci 16 1996 2901 2911 (Pubitemid 26121834)
63. X.F. Zhou, Y.S. Deng, E. Chie, Q. Xue, J.H. Zhong, E.M. McLachlan, R.A. Rush, and C.J. Xian Satellite-cell-derived nerve growth factor and neurotrophin-3 are involved in noradrenergic sprouting in the dorsal root ganglia following peripheral nerve injury in the rat Eur J Neurosci 11 1999 1711 1722
64. X.F. Zhou, Y.S. Deng, C.J. Xian, and J.H. Zhong Neurotrophins from dorsal root ganglia trigger allodynia after spinal nerve injury in rats Eur J Neurosci 12 2000 100 105 (Pubitemid 30068415)