Pain hypersensitivity in rats with experimental autoimmune neuritis, an animal model of human inflammatory demyelinating neuropathy

Brain, Behavior, and Immunity

Volumn 21, Issue 5, 2007, Pages 699-710

  Moalem Taylor, Gila ^a   Allbutt, Haydn N ^a   Iordanova, Mihaela D ^a   Tracey, David J ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

Author keywords

Allodynia; Autoimmune neuropathy; EAN; GBS; Hyperalgesia; Inflammatory response; Neuropathic pain; Rat; Sciatic nerve

Indexed keywords

FREUND ADJUVANT; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; MYELIN BASIC PROTEIN;

ALLODYNIA; ANIMAL BEHAVIOR; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIGEN EXPRESSION; ARTICLE; AUTOIMMUNE DISEASE; CONTROLLED STUDY; DEMYELINATING DISEASE; DEMYELINATING NEUROPATHY; DEMYELINATION; GLIA CELL; GUILLAIN BARRE SYNDROME; HYPERALGESIA; HYPERSENSITIVITY; IMMUNIZATION; IMMUNOHISTOCHEMISTRY; INFLAMMATION; MACROPHAGE; MALE; NEURITIS; NEUROPATHIC PAIN; NONHUMAN; PERIPHERAL NERVOUS SYSTEM; POLYRADICULONEUROPATHY; PRIORITY JOURNAL; RAT; SCIATIC NERVE; STIMULUS RESPONSE; T LYMPHOCYTE;

ANIMALS; DISEASE MODELS, ANIMAL; GUILLAIN-BARRE SYNDROME; HYPERALGESIA; IMMUNIZATION; MALE; MYELIN P2 PROTEIN; NEURITIS, AUTOIMMUNE, EXPERIMENTAL; PAIN; PAIN THRESHOLD; PEPTIDE FRAGMENTS; RATS; RATS, INBRED LEW; SCIATIC NERVE; T-LYMPHOCYTES;

EID: 34249744464     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2006.07.007     Document Type: Article

References (90)

1. Aicher S.A., Silverman M.B., Winkler C.W., and Bebo Jr. B.F. Hyperalgesia in an animal model of multiple sclerosis. Pain 110 (2004) 560-570
2. Bai X.F., Zhu J., Zhang G.X., Kaponides G., Hojeberg B., van der Meide P.H., and Link H. IL-10 suppresses experimental autoimmune neuritis and down-regulates TH1-type immune responses. Clin. Immunol. Immunopathol. 83 (1997) 117-126
3. Beiter T., Artelt M.R., Trautmann K., and Schluesener H.J. Experimental autoimmune neuritis induces differential microglia activation in the rat spinal cord. J. Neuroimmunol. 160 (2005) 25-31
4. Brostoff S., Burnett P., Lampert P., and Eylar E.H. Isolation and characterization of a protein from sciatic nerve myelin responsible for experimental allergic neuritis. Nat. New Biol. 235 (1972) 210-212
5. Chacur M., Milligan E.D., Gazda L.S., Armstrong C., Wang H., Tracey K.J., Maier S.F., and Watkins L.R. A new model of sciatic inflammatory neuritis (SIN): induction of unilateral and bilateral mechanical allodynia following acute unilateral peri-sciatic immune activation in rats. Pain 94 (2001) 231-244
6. Colburn R.W., Rickman A.J., and DeLeo J.A. The effect of site and type of nerve injury on spinal glial activation and neuropathic pain behavior. Exp. Neurol. 157 (1999) 289-304
7. DeLeo J.A., and Yezierski R.P. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 90 (2001) 1-6
8. De Leo J.A., Tawfik V.L., and Lacroix-Fralish M.L. The tetrapartite synapse: Path to CNS sensitization and chronic pain. Pain 122 (2006) 17-21
9. Ekerfelt C., Dahle C., Weissert R., Kvarnstrom M., Olsson T., and Ernerudh J. Transfer of myelin-specific cells deviated in vitro towards IL-4 production ameliorates ongoing experimental allergic neuritis. Clin. Exp. Immunol. 123 (2001) 112-118
10. Eliav E., Herzberg U., Ruda M.A., and Bennett G.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain 83 (1999) 169-182
11. Eliav E., Benoliel R., and Tal M. Inflammation with no axonal damage of the rat saphenous nerve trunk induces ectopic discharge and mechanosensitivity in myelinated axons. Neurosci. Lett. 311 (2001) 49-52
12. Feasby T.E., Hahn A.F., Brown W.F., Bolton C.F., Gilbert J.J., and Koopman W.J. Severe axonal degeneration in acute Guillain-Barre syndrome: evidence of two different mechanisms?. J. Neurol. Sci. 116 (1993) 185-192
13. Friedl P., den Boer A.T., and Gunzer M. Tuning immune responses: diversity and adaptation of the immunological synapse. Nat. Rev. Immunol. 5 (2005) 532-545
14. Gabriel C.M., Hughes R.A., Moore S.E., Smith K.J., and Walsh F.S. Induction of experimental autoimmune neuritis with peripheral myelin protein-22. Brain 121 Pt. 10 (1998) 1895-1902
15. Gehrmann J., Gold R., Linington C., Lannes-Vieira J., Wekerle H., and Kreutzberg G.W. Microglial involvement in experimental autoimmune inflammation of the central and peripheral nervous system. Glia 7 (1993) 50-59
16. Hahn A.F. Experimental allergic neuritis (EAN) as a model for the immune-mediated demyelinating neuropathies. Rev. Neurol. (Paris) 152 (1996) 328-332
17. Hahn A.F., Feasby T.E., Steele A., Lovgren D.S., and Berry J. Demyelination and axonal degeneration in Lewis rat experimental allergic neuritis depend on the myelin dosage. Lab. Invest. 59 (1988) 115-125
18. Hahn A.F., Feasby T.E., Wilkie L., and Lovgren D. P2-peptide induced experimental allergic neuritis: a model to study axonal degeneration. Acta Neuropathol. (Berl) 82 (1991) 60-65
19. Hargreaves K., Dubner R., Brown F., Flores C., and Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 32 (1988) 77-88
20. Hartung H.P., and Toyka K.V. T-cell and macrophage activation in experimental autoimmune neuritis and Guillain-Barre syndrome. Ann. Neurol. 27 Suppl (1990) S57-S63
21. Heininger K., Stoll G., Linington C., Toyka K.V., and Wekerle H. Conduction failure and nerve conduction slowing in experimental allergic neuritis induced by P2-specific T-cell lines. Ann. Neurol. 19 (1986) 44-49
22. Herzberg U., Eliav E., Dorsey J.M., Gracely R.H., and Kopin I.J. NGF involvement in pain induced by chronic constriction injury of the rat sciatic nerve. Neuroreport 8 (1997) 1613-1618
23. Heumann R., Korsching S., Bandtlow C., and Thoenen H. Changes of nerve growth factor synthesis in nonneuronal cells in response to sciatic nerve transection. J. Cell Biol. 104 (1987) 1623-1631
24. Hoffman P.M., Powers J.M., Weise M.J., and Brostoff S.W. Experimental allergic neuritis. I. Rat strain differences in the response to bovine myelin antigens. Brain Res. 195 (1980) 355-362
25. Howarth A.L. Pain management for multiple sclerosis patients. Prof. Nurse 16 (2000) 824-826
26. Hughes R.A., and Cornblath D.R. Guillain-Barre syndrome. Lancet 366 (2005) 1653-1666
27. Hughes R., Atkinson P., Coates P., Hall S., and Leibowitz S. Sural nerve biopsies in Guillain-Barre syndrome: axonal degeneration and macrophage-associated demyelination and absence of cytomegalovirus genome. Muscle Nerve 15 (1992) 568-575
28. Hughes R.A., Hadden R.D., Gregson N.A., and Smith K.J. Pathogenesis of Guillain-Barre syndrome. J. Neuroimmunol. 100 (1999) 74-97
29. Jander S., and Stoll G. Interleukin-18 is induced in acute inflammatory demyelinating polyneuropathy. J. Neuroimmunol. 114 (2001) 253-258
30. Kadlubowski M., and Hughes R.A. Identification of the neuritogen for experimental allergic neuritis. Nature 277 (1979) 140-141
31. Kleinschnitz C., Hofstetter H.H., Meuth S.G., Braeuninger S., Sommer C., and Stoll G. T cell infiltration after chronic constriction injury of mouse sciatic nerve is associated with interleukin-17 expression. Exp. Neurol. 200 (2006) 480-485
32. Ledeboer A., Sloane E.M., Milligan E.D., Frank M.G., Mahony J.H., Maier S.F., and Watkins L.R. Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation. Pain 115 (2005) 71-83
33. Li L., Xian C.J., Zhong J.H., and Zhou X.F. Effect of lumbar 5 ventral root transection on pain behaviors: a novel rat model for neuropathic pain without axotomy of primary sensory neurons. Exp. Neurol. 175 (2002) 23-34
34. Lilje O. The processing and presentation of endogenous and exogenous antigen by Schwann cells in vitro. Cell Mol. Life Sci. 59 (2002) 2191-2198
35. Linington C., Izumo S., Suzuki M., Uyemura K., Meyermann R., and Wekerle H. A permanent rat T cell line that mediates experimental allergic neuritis in the Lewis rat in vivo. J. Immunol. 133 (1984) 1946-1950
36. Linington C., Lassmann H., Ozawa K., Kosin S., and Mongan L. Cell adhesion molecules of the immunoglobulin supergene family as tissue-specific autoantigens: induction of experimental allergic neuritis (EAN) by P0 protein-specific T cell lines. Eur. J. Immunol. 22 (1992) 1813-1817
37. Liu T., van Rooijen N., and Tracey D.J. Depletion of macrophages reduces axonal degeneration and hyperalgesia following nerve injury. Pain 86 (2000) 25-32
38. Marchand F., Perretti M., and McMahon S.B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 6 (2005) 521-532
39. Milligan E.D., Twining C., Chacur M., Biedenkapp J., O'Connor K., Poole S., Tracey K., Martin D., Maier S.F., and Watkins L.R. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci. 23 (2003) 1026-1040
40. Milligan E.D., Maier S.F., and Watkins L.R. Sciatic inflammatory neuropathy in the rat: surgical procedures, induction of inflammation, and behavioral testing. Methods Mol. Med. 99 (2004) 67-89
41. Milligan E.D., Langer S.J., Sloane E.M., He L., Wieseler-Frank J., O'Connor K., Martin D., Forsayeth J.R., Maier S.F., Johnson K., Chavez R.A., Leinwand L.A., and Watkins L.R. Controlling pathological pain by adenovirally driven spinal production of the anti-inflammatory cytokine, interleukin-10. Eur. J. Neurosci. 21 (2005) 2136-2148
42. Milligan E.D., Sloane E.M., Langer S.J., Cruz P.E., Chacur M., Spataro L., Wieseler-Frank J., Hammack S.E., Maier S.F., Flotte T.R., Forsayeth J.R., Leinwand L.A., Chavez R., and Watkins L.R. Controlling neuropathic pain by adeno-associated virus driven production of the anti-inflammatory cytokine, interleukin-10. Mol. Pain 1 (2005) 9
43. Milner P., Lovelidge C.A., Taylor W.A., and Hughes R.A. P0 myelin protein produces experimental allergic neuritis in Lewis rats. J. Neurol. Sci. 79 (1987) 275-285
44. Moalem G., and Tracey D.J. Immune and inflammatory mechanisms in neuropathic pain. Brain Res. Brain Res. Rev. 51 (2006) 240-264
45. Moalem G., Gdalyahu A., Shani Y., Otten U., Lazarovici P., Cohen I.R., and Schwartz M. Production of neurotrophins by activated T cells: implications for neuroprotective autoimmunity. J. Autoimmun. 15 (2000) 331-345
46. Moalem G., Xu K., and Yu L. T lymphocytes play a role in neuropathic pain following peripheral nerve injury in rats. Neuroscience 129 (2004) 767-777
47. Moulin D.E., Hagen N., Feasby T.E., Amireh R., and Hahn A. Pain in Guillain-Barre syndrome. Neurology 48 (1997) 328-331
48. Myers R.R., Campana W.M., and Shubayev V.I. The role of neuroinflammation in neuropathic pain: mechanisms and therapeutic targets. Drug Discov. Today 11 (2006) 8-20
49. Nguyen D.K., Agenarioti-Belanger S., and Vanasse M. Pain and the Guillain-Barre syndrome in children under 6 years old. J. Pediatr. 134 (1999) 773-776
50. Olsson T., Holmdahl R., Klareskog L., and Forsum U. Ia-expressing cells and T lymphocytes of different subsets in peripheral nerve tissue during experimental allergic neuritis in Lewis rats. Scand. J. Immunol. 18 (1983) 339-343
51. Olsson T., Holmdahl R., Klareskog L., Forsum U., and Kristensson K. Dynamics of Ia-expressing cells and T lymphocytes of different subsets during experimental allergic neuritis in Lewis rats. J. Neurol. Sci. 66 (1984) 141-149
52. Pentland B., and Donald S.M. Pain in the Guillain-Barre syndrome: a clinical review. Pain 59 (1994) 159-164
53. Perkins N.M., and Tracey D.J. Hyperalgesia due to nerve injury: role of neutrophils. Neuroscience 101 (2000) 745-757
54. Raghavendra V., Tanga F., and DeLeo J.A. 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
55. Raghavendra V., Tanga F.Y., and DeLeo J.A. Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS. Eur. J. Neurosci. 20 (2004) 467-473
56. Ramer M.S., French G.D., and Bisby M.A. Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 72 (1997) 71-78
57. Rostami A., Burns J.B., Brown M.J., Rosen J., Zweiman B., Lisak R.P., and Pleasure D.E. Transfer of experimental allergic neuritis with P2-reactive T-cell lines. Cell. Immunol. 91 (1985) 354-361
58. Ruiz G., Ceballos D., and Banos J.E. Behavioral and histological effects of endoneurial administration of nerve growth factor: possible implications in neuropathic pain. Brain Res. 1011 (2004) 1-6
59. Schafers M., Brinkhoff J., Neukirchen S., Marziniak M., and Sommer C. Combined epineurial therapy with neutralizing antibodies to tumor necrosis factor-alpha and interleukin-1 receptor has an additive effect in reducing neuropathic pain in mice. Neurosci. Lett. 310 (2001) 113-116
60. Schafers M., Svensson C.I., Sommer C., and Sorkin L.S. 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
61. Schmidt B., Stoll G., Hartung H.P., Heininger K., Schafer B., and Toyka K.V. Macrophages but not Schwann cells express Ia antigen in experimental autoimmune neuritis. Ann. Neurol. 28 (1990) 70-77
62. Schott K., Jenner A., Wietholter H., Schabet M., and Stevens A. Demyelination of sciatic nerve in acute experimental allergic neuritis of the rat. A gel electrophoresis investigation. J. Neuroimmunol. 20 (1988) 53-61
63. Sheth R.N., Dorsi M.J., Li Y., Murinson B.B., Belzberg A.J., Griffin J.W., and Meyer R.A. Mechanical hyperalgesia after an L5 ventral rhizotomy or an L5 ganglionectomy in the rat. Pain 96 (2002) 63-72
64. Shin H.C., McFarlane E.F., Pollard J.D., and Watson E.G. Induction of experimental allergic neuritis with synthetic peptides from myelin P2 protein. Neurosci. Lett. 102 (1989) 309-312
65. Slart R., Yu A.L., Yaksh T.L., and Sorkin L.S. An animal model of pain produced by systemic administration of an immunotherapeutic anti-ganglioside antibody. Pain 69 (1997) 119-125
66. Sommer C., and Kress M. Recent findings on how proinflammatory cytokines cause pain: peripheral mechanisms in inflammatory and neuropathic hyperalgesia. Neurosci. Lett. 361 (2004) 184-187
67. Sorkin L.S., Xiao W.H., Wagner R., and Myers R.R. Tumour necrosis factor-alpha induces ectopic activity in nociceptive primary afferent fibres. Neuroscience 81 (1997) 255-262
68. Stoll G., Wessig C., Gold R., and Bendszus M. Assessment of lesion evolution in experimental autoimmune neuritis by gadofluorine M-enhanced MR neurography. Exp. Neurol. 197 (2006) 150-156
69. Sweitzer S.M., Colburn R.W., Rutkowski M., and DeLeo J.A. Acute peripheral inflammation induces moderate glial activation and spinal IL-1beta expression that correlates with pain behavior in the rat. Brain Res. 829 (1999) 209-221
70. Tanga F.Y., Raghavendra V., and DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 45 (2004) 397-407
71. Theodosiou M., Rush R.A., Zhou X.F., Hu D., Walker J.S., and Tracey D.J. Hyperalgesia due to nerve damage: role of nerve growth factor. Pain 81 (1999) 245-255
72. Tsuda M., Inoue K., and Salter M.W. Neuropathic pain and spinal microglia: a big problem from molecules in "small" glia. Trends Neurosci. 28 (2005) 101-107
73. Vikman K.S., Siddall P.J., and Duggan A.W. Increased responsiveness of rat dorsal horn neurons in vivo following prolonged intrathecal exposure to interferon-gamma. Neuroscience 135 (2005) 969-977
74. Wagner R., and Myers R.R. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. Neuroreport 7 (1996) 2897-2901
75. Wagner R., Janjigian M., and Myers R.R. Anti-inflammatory interleukin-10 therapy in CCI neuropathy decreases thermal hyperalgesia, macrophage recruitment, and endoneurial TNF-alpha expression. Pain 74 (1998) 35-42
76. Waksman B.H., and Adams R.D. Allergic neuritis: an experimental disease of rabbits induced by the injection of peripheral nervous tissue and adjuvants. J. Exp. Med. 102 (1955) 213-236
77. Wallace V.C., Cottrell D.F., Brophy P.J., and Fleetwood-Walker S.M. Focal lysolecithin-induced demyelination of peripheral afferents results in neuropathic pain behavior that is attenuated by cannabinoids. J. Neurosci. 23 (2003) 3221-3233
78. Watkins L.R., and Maier S.F. Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol. Rev. 82 (2002) 981-1011
79. Weskamp G., and Otten U. An enzyme-linked immunoassay for nerve growth factor (NGF): a tool for studying regulatory mechanisms involved in NGF production in brain and in peripheral tissues. J. Neurochem. 48 (1987) 1779-1786
80. White F.A., Bhangoo S.K., and Miller R.J. Chemokines: integrators of pain and inflammation. Nat. Rev. Drug Discov. 4 (2005) 834-844
81. Winer J.B. Guillain Barre syndrome. Mol. Pathol. 54 (2001) 381-385
82. Wolf G., Gabay E., Tal M., Yirmiya R., and Shavit Y. Genetic impairment of interleukin-1 signaling attenuates neuropathic pain, autotomy, and spontaneous ectopic neuronal activity, following nerve injury in mice. Pain 120 (2006) 315-324
83. Wu G., Ringkamp M., Murinson B.B., Pogatzki E.M., Hartke T.V., Weerahandi H.M., Campbell J.N., Griffin J.W., and Meyer R.A. Degeneration of myelinated efferent fibers induces spontaneous activity in uninjured C-fiber afferents. J. Neurosci. 22 (2002) 7746-7753
84. Xiao W.H., Yu A.L., and Sorkin L.S. Electrophysiological characteristics of primary afferent fibers after systemic administration of anti-GD2 ganglioside antibody. Pain 69 (1997) 145-151
85. Yu S., Chen Z., Mix E., Zhu S.W., Winblad B., Ljunggren H.G., and Zhu J. Neutralizing antibodies to IL-18 ameliorate experimental autoimmune neuritis by counter-regulation of autoreactive Th1 responses to peripheral myelin antigen. J. Neuropathol. Exp. Neurol. 61 (2002) 614-622
86. Zelenka M., Schafers M., and Sommer C. Intraneural injection of interleukin-1beta and tumor necrosis factor-alpha into rat sciatic nerve at physiological doses induces signs of neuropathic pain. Pain 116 (2005) 257-263
87. Zhu J., Link H., Mix E., Olsson T., and Huang W.X. Th1-like cell responses to peripheral nerve myelin components over the course of experimental allergic neuritis in Lewis rats. Acta. Neurol. Scand. 90 (1994) 19-25
88. Zhu J., Mix E., and Link H. Cytokine production and the pathogenesis of experimental autoimmune neuritis and Guillain-Barre syndrome. J. Neuroimmunol. 84 (1998) 40-52
89. Zhu Y., Ljunggren H.G., Mix E., Li H.L., van der Meide P., Elhassan A.M., Winblad B., and Zhu J. Suppression of autoimmune neuritis in IFN-gamma receptor-deficient mice. Exp. Neurol. 169 (2001) 472-478
90. Zuo Y., Perkins N.M., Tracey D.J., and Geczy C.L. Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain 105 (2003) 467-479