Detailed characterization of neuro-immune responses following neuropathic injury in mice

Brain Research

Volumn 1405, Issue , 2011, Pages 95-108

  Kim, Cristina Fabiola ^a   Moalem Taylor, Gila ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

DRG; Neuroinflammation; Neuropathic pain; Peripheral nerve injury; Sciatic nerve; Spinal cord

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; C57BL 6 MOUSE; CELL ACTIVATION; CELL INFILTRATION; COMPARATIVE STUDY; CONTROLLED STUDY; DENDRITIC CELL; FOREFOOT; HYPERALGESIA; IMMUNOCOMPETENT CELL; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; INFLAMMATORY CELL; LATENT PERIOD; LYMPHOCYTIC INFILTRATION; MACROPHAGE ACTIVATION; MALE; MECHANICAL ALLODYNIA; MICROGLIA; MOUSE; NERVE CELL LESION; NERVE ENDING; NEUROIMMUNOLOGY; NEUROPATHIC PAIN; NEUTROPHIL CHEMOTAXIS; NOCICEPTIVE RECEPTOR; NONHUMAN; PARTIAL SCIATIC NERVE INJURY; PERIKARYON; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; SCIATIC NERVE; SPINAL CORD DORSAL HORN; SPINAL CORD NERVE CELL; SPINAL CORD VENTRAL HORN; SPINAL GANGLION; THERMAL HYPERALGESIA; THERMAL STIMULATION; WITHDRAWAL REFLEX;

ANIMALS; GANGLIA, SPINAL; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; NEURALGIA; NEUROIMMUNOMODULATION; SCIATIC NERVE; SPINAL CORD;

MUS; RODENTIA;

EID: 79960727016     PISSN: 00068993     EISSN: 18726240     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.06.022     Document Type: Article

References (69)

1. C. Abbadie, J.A. Lindia, A.M. Cumiskey, L.B. Peterson, J.S. Mudgett, E.K. Bayne, J.A. DeMartino, D.E. MacIntyre, and M.J. Forrest Impaired neuropathic pain responses in mice lacking the chemokine receptor CCR2 Proc. Natl. Acad. Sci. U. S. A. 100 2003 7947 7952 (Pubitemid 36760075)
2. P.J. Austin, and G. Moalem-Taylor The neuro-immune balance in neuropathic pain: involvement of inflammatory immune cells, immune-like glial cells and cytokines J. Neuroimmunol. 229 2010 26 50
3. S. Averill, G.J. Michael, P.J. Shortland, R.C. Leavesley, V.R. King, E.J. Bradbury, S.B. McMahon, and J.V. Priestley NGF and GDNF ameliorate the increase in ATF3 expression which occurs in dorsal root ganglion cells in response to peripheral nerve injury Eur. J. Neurosci. 19 2004 1437 1445 (Pubitemid 38437906)
4. A.L. Bailey, and A. Ribeiro-da-Silva Transient loss of terminals from non-peptidergic nociceptive fibers in the substantia gelatinosa of spinal cord following chronic constriction injury of the sciatic nerve Neuroscience 138 2006 675 690 (Pubitemid 43255575)
5. J. Barclay, A.K. Clark, P. Ganju, C. Gentry, S. Patel, G. Wotherspoon, F. Buxton, C. Song, J. Ullah, J. Winter, A. Fox, S. Bevan, and M. Malcangio Role of the cysteine protease cathepsin S in neuropathic hyperalgesia Pain 130 2007 225 234 (Pubitemid 46977115)
6. A. Brack, H.L. Rittner, H. Machelska, K. Leder, S.A. Mousa, M. Schafer, and C. Stein Control of inflammatory pain by chemokine-mediated recruitment of opioid-containing polymorphonuclear cells Pain 112 2004 229 238 (Pubitemid 39550722)
7. W.M. Campana Schwann cells: activated peripheral glia and their role in neuropathic pain Brain Behav. Immun. 21 2007 522 527 (Pubitemid 46829780)
8. W.M. Campana, X. Li, V.I. Shubayev, M. Angert, K. Cai, and R.R. Myers Erythropoietin reduces Schwann cell TNF-alpha, Wallerian degeneration and pain-related behaviors after peripheral nerve injury Eur. J. Neurosci. 23 2006 617 626
9. L. Cao, and J.A. DeLeo CNS-infiltrating CD4+ T lymphocytes contribute to murine spinal nerve transection-induced neuropathic pain Eur. J. Immunol. 38 2008 448 458
10. A.K. Clark, C. Gentry, E.J. Bradbury, S.B. McMahon, and M. Malcangio Role of spinal microglia in rat models of peripheral nerve injury and inflammation Eur. J. Pain 11 2007 223 230 (Pubitemid 44829964)
11. M. Costigan, A. Moss, A. Latremoliere, C. Johnston, M. Verma-Gandhu, T.A. Herbert, L. Barrett, G.J. Brenner, D. Vardeh, C.J. Woolf, and M. Fitzgerald T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity J. Neurosci. 29 2009 14415 14422
12. D.E. Coyle Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior Glia 23 1998 75 83 (Pubitemid 28174047)
13. J.G. Cui, S. Holmin, T. Mathiesen, B.A. Meyerson, and B. Linderoth Possible role of inflammatory mediators in tactile hypersensitivity in rat models of mononeuropathy Pain 88 2000 239 248
14. J.C. Fleming, F. Bao, Y. Chen, E.F. Hamilton, L.E. Gonzalez-Lara, P.J. Foster, and L.C. Weaver Timing and duration of anti-alpha4beta1 integrin treatment after spinal cord injury: effect on therapeutic efficacy J. Neurosurg. Spine 11 2009 575 587
15. J. Frisen, M. Risling, and K. Fried Distribution and axonal relations of macrophages in a neuroma Neuroscience 55 1993 1003 1013 (Pubitemid 23231910)
16. X. Gao, H.K. Kim, J.M. Chung, and K. Chung Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats Pain 116 2005 62 72 (Pubitemid 40828501)
17. Y.J. Gao, L. Zhang, O.A. Samad, M.R. Suter, K. Yasuhiko, Z.Z. Xu, J.Y. Park, A.L. Lind, Q. Ma, 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
18. M. Hanani, T.Y. Huang, P.S. Cherkas, M. Ledda, and E. Pannese Glial cell plasticity in sensory ganglia induced by nerve damage Neuroscience 114 2002 279 283 (Pubitemid 35245408)
19. P. Hu, and E.M. McLachlan Macrophage and lymphocyte invasion of dorsal root ganglia after peripheral nerve lesions in the rat Neuroscience 112 2002 23 38 (Pubitemid 34603495)
20. P. Hu, A.L. Bembrick, K.A. Keay, and E.M. McLachlan Immune cell involvement in dorsal root ganglia and spinal cord after chronic constriction or transection of the rat sciatic nerve Brain Behav. Immun. 21 2007 599 616 (Pubitemid 46830961)
21. L. Jasmin, J.P. Vit, A. Bhargava, and P.T. Ohara Can satellite glial cells be therapeutic targets for pain control? Neuron Glia Biol. 6 2010 63 71
22. C.F. Kim, and G. Moalem-Taylor Interleukin-17 contributes to neuroinflammation and neuropathic pain following peripheral nerve injury in mice J. Pain 12 2011 370 383
23. D.S. Kim, K.W. Figueroa, K.W. Li, A. Boroujerdi, T. Yolo, and Z. David Luo Profiling of dynamically changed gene expression in dorsal root ganglia post peripheral nerve injury and a critical role of injury-induced glial fibrillary acidic protein in maintenance of pain behaviors [corrected] Pain 143 2009 114 122
24. T.R. Lavich, A. Siqueira Rde, F.A. Farias-Filho, R.S. Cordeiro, P.M. Rodrigues e Silva, and M.A. Martins Neutrophil infiltration is implicated in the sustained thermal hyperalgesic response evoked by allergen provocation in actively sensitized rats Pain 125 2006 180 187 (Pubitemid 44498978)
25. A. Ledeboer, E.M. Sloane, E.D. Milligan, M.G. Frank, J.H. Mahony, S.F. Maier, and L.R. Watkins Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation Pain 115 2005 71 83
26. T. Liu, N. van Rooijen, and D.J. Tracey Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury Pain 86 2000 25 32 (Pubitemid 30211699)
27. A.B. Malmberg, and A.I. Basbaum Partial sciatic nerve injury in the mouse as a model of neuropathic pain: behavioral and neuroanatomical correlates Pain 76 1998 215 222 (Pubitemid 28304959)
28. F. Marchand, C. Tsantoulas, D. Singh, J. Grist, A.K. Clark, E.J. Bradbury, and S.B. McMahon Effects of Etanercept and Minocycline in a rat model of spinal cord injury Eur. J. Pain 13 2009 673 681
29. E. McLachlan, P. Hu, and C. Geczy Neutrophils rarely invade dorsal root ganglia after peripheral nerve lesions J. Neuroimmunol. 187 212-3 2007 214 215 author reply
30. E.D. Milligan, and L.R. Watkins Pathological and protective roles of glia in chronic pain Nat. Rev. Neurosci. 10 2009 23 36
31. G. Moalem, and D.J. Tracey Immune and inflammatory mechanisms in neuropathic pain Brain Res. Rev. 51 2006 240 264 (Pubitemid 43902971)
32. G. Moalem, A. Monsonego, Y. Shani, I.R. Cohen, and M. Schwartz Differential T cell response in central and peripheral nerve injury: connection with immune privilege FASEB J. 13 1999 1207 1217 (Pubitemid 29300366)
33. G. Moalem, K. Xu, and L. Yu T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats Neuroscience 129 2004 767 777 (Pubitemid 39487128)
34. G. Moalem-Taylor, H.N. Allbutt, M.D. Iordanova, and D.J. Tracey Pain hypersensitivity in rats with experimental autoimmune neuritis, an animal model of human inflammatory demyelinating neuropathy Brain Behav. Immun. 21 2007 699 710 (Pubitemid 46829765)
35. N. Morin, S.A. Owolabi, M.W. Harty, E.F. Papa, T.F. Tracy Jr., S.K. Shaw, M. Kim, and C.Y. Saab Neutrophils invade lumbar dorsal root ganglia after chronic constriction injury of the sciatic nerve J. Neuroimmunol. 184 2007 164 171 (Pubitemid 46365998)
36. R. Munglani, A. Bond, G.D. Smith, S.M. Harrison, P.J. Elliot, P.J. Birch, and S.P. Hunt Changes in neuronal markers in a mononeuropathic rat model relationship between neuropeptide Y, pre-emptive drug treatment and long-term mechanical hyperalgesia Pain 63 1995 21 31
37. R.R. Myers, H.M. Heckman, and M. Rodriguez Reduced hyperalgesia in nerve-injured WLD mice: relationship to nerve fiber phagocytosis, axonal degeneration, and regeneration in normal mice Exp. Neurol. 141 1996 94 101 (Pubitemid 26317185)
38. K. Obata, H. Yamanaka, T. Fukuoka, D. Yi, A. Tokunaga, N. Hashimoto, H. Yoshikawa, and K. Noguchi Contribution of injured and uninjured dorsal root ganglion neurons to pain behavior and the changes in gene expression following chronic constriction injury of the sciatic nerve in rats Pain 101 2003 65 77 (Pubitemid 36050112)
39. K. Obata, H. Katsura, T. Mizushima, J. Sakurai, K. Kobayashi, H. Yamanaka, Y. Dai, T. Fukuoka, and K. Noguchi Roles of extracellular signal-regulated protein kinases 5 in spinal microglia and primary sensory neurons for neuropathic pain J. Neurochem. 102 2007 1569 1584 (Pubitemid 47256198)
40. P.T. Ohara, J.P. Vit, A. Bhargava, and L. Jasmin Evidence for a role of connexin 43 in trigeminal pain using RNA interference in vivo J. Neurophysiol. 100 2008 3064 3073
41. M.C. Oliveira, A. Pelegrini-da-Silva, C.A. Parada, and C.H. Tambeli 5-HT acts on nociceptive primary afferents through an indirect mechanism to induce hyperalgesia in the subcutaneous tissue Neuroscience 145 2007 708 714 (Pubitemid 46357522)
42. N.M. Perkins, and D.J. Tracey Hyperalgesia due to nerve injury: role of neutrophils Neuroscience 101 2000 745 757
43. V.H. Perry, M.C. Brown, and S. Gordon The macrophage response to central and peripheral nerve injury. A possible role for macrophages in regeneration J. Exp. Med. 165 1987 1218 1223 (Pubitemid 17064518)
44. R. Press, I. Nennesmo, M. Kouwenhoven, Y.M. Huang, H. Link, and M. Pashenkov Dendritic cells in the cerebrospinal fluid and peripheral nerves in Guillain-Barre syndrome and chronic inflammatory demyelinating polyradiculoneuropathy J. Neuroimmunol. 159 2005 165 176 (Pubitemid 40126189)
45. V. Raghavendra, F. Tanga, and J.A. DeLeo Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy J. Pharmacol. Exp. Ther. 306 2003 624 630 (Pubitemid 36886161)
46. M. Rigaud, G. Gemes, M.E. Barabas, D.I. Chernoff, S.E. Abram, C.L. Stucky, and Q.H. Hogan Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain Pain 136 2008 188 201
47. F. Sallusto, and A. Lanzavecchia Mobilizing dendritic cells for tolerance, priming, and chronic inflammation J. Exp. Med. 189 1999 611 614 (Pubitemid 29193361)
48. B. Salomon, L. Rhee, H. Bour-Jordan, H. Hsin, A. Montag, B. Soliven, J. Arcella, A.M. Girvin, J. Padilla, S.D. Miller, and J.A. Bluestone Development of spontaneous autoimmune peripheral polyneuropathy in B7-2-deficient NOD mice J. Exp. Med. 194 2001 677 684 (Pubitemid 32844777)
49. J. Scholz, and C.J. Woolf The neuropathic pain triad: neurons, immune cells and glia Nat. Neurosci. 10 2007 1361 1368 (Pubitemid 350014681)
50. Z. Seltzer, R. Dubner, and Y. Shir A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury Pain 43 1990 205 218 (Pubitemid 20385185)
51. S.A. Shehab, R.C. Spike, and A.J. Todd Do central terminals of intact myelinated primary afferents sprout into the superficial dorsal horn of rat spinal cord after injury to a neighboring peripheral nerve? J. Comp. Neurol. 474 2004 427 437 (Pubitemid 38720436)
52. P.J. Shortland, B. Baytug, A. Krzyzanowska, S.B. McMahon, J.V. Priestley, and S. Averill ATF3 expression in L4 dorsal root ganglion neurons after L5 spinal nerve transection Eur. J. Neurosci. 23 2006 365 373
53. C. Sommer, and M. Kress Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia Neurosci. Lett. 361 2004 184 187 (Pubitemid 38609247)
54. C. Sommer, and M. Schafers Painful mononeuropathy in C57BL/Wld mice with delayed wallerian degeneration: differential effects of cytokine production and nerve regeneration on thermal and mechanical hypersensitivity Brain Res. 784 1998 154 162 (Pubitemid 28137859)
55. J.E. Swett, and C.J. Woolf The somatotopic organization of primary afferent terminals in the superficial laminae of the dorsal horn of the rat spinal cord J. Comp. Neurol. 231 1985 66 77 (Pubitemid 15199486)
56. F.Y. Tanga, N. Nutile-McMenemy, and J.A. DeLeo The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy Proc. Natl. Acad. Sci. U. S. A. 102 2005 5856 5861 (Pubitemid 40559649)
57. M.A. Thacker, A.K. Clark, T. Bishop, J. Grist, P.K. Yip, L.D. Moon, S.W. Thompson, F. Marchand, and S.B. McMahon CCL2 is a key mediator of microglia activation in neuropathic pain states Eur. J. Pain 13 2009 263 272
58. M. Tsuda, Y. Shigemoto-Mogami, S. Koizumi, A. Mizokoshi, S. Kohsaka, M.W. Salter, and K. Inoue P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury Nature 424 2003 778 783 (Pubitemid 37021707)
59. M. Tsuda, K. Kuboyama, T. Inoue, K. Nagata, H. Tozaki-Saitoh, and K. Inoue Behavioral phenotypes of mice lacking purinergic P2X4 receptors in acute and chronic pain assays Mol. Pain 5 2009 28
60. H. Tsujino, E. Kondo, T. Fukuoka, Y. Dai, A. Tokunaga, K. Miki, K. Yonenobu, T. Ochi, and K. Noguchi Activating transcription factor 3 (ATF3) induction by axotomy in sensory and motoneurons: a novel neuronal marker of nerve injury Mol. Cell. Neurosci. 15 2000 170 182 (Pubitemid 30109120)
61. C. Ultenius, B. Linderoth, B.A. Meyerson, and J. Wallin Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat Neurosci. Lett. 399 2006 85 90
62. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial activation: a driving force for pathological pain Trends Neurosci. 24 2001 450 455 (Pubitemid 32695356)
63. L.R. Watkins, E.D. Milligan, and S.F. Maier Spinal cord glia: new players in pain Pain 93 2001 201 205 (Pubitemid 32763176)
64. C.J. Woolf, and R.J. Mannion Neuropathic pain: aetiology, symptoms, mechanisms, and management Lancet 353 1999 1959 1964
65. J. Zhang, and Y. De Koninck Spatial and temporal relationship between monocyte chemoattractant protein-1 expression and spinal glial activation following peripheral nerve injury J. Neurochem. 97 2006 772 783
66. 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
67. X. Zou, Q. Lin, and W.D. Willis Enhanced phosphorylation of NMDA receptor 1 subunits in spinal cord dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats J. Neurosci. 20 2000 6989 6997
68. X. Zou, Q. Lin, and W.D. Willis Role of protein kinase A in phosphorylation of NMDA receptor 1 subunits in dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats Neuroscience 115 2002 775 786 (Pubitemid 35336020)
69. Y. Zuo, N.M. Perkins, D.J. Tracey, and C.L. Geczy Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells Pain 105 2003 467 479 (Pubitemid 37186908)