Endogenous interleukin-6 contributes to hypersensitivity to cutaneous stimuli and changes in neuropeptides associated with chronic nerve constriction in mice

European Journal of Neuroscience

Volumn 11, Issue 7, 1999, Pages 2243-2253

  Murphy, P G ^a   Ramer, M S ^a   Borthwick, L ^a   Gauldie, J ^a   Richardson, P M ^a   Bisby, M A ^a  

^a MONTREAL GENERAL HOSPITAL   (Canada)

Author keywords

Galanin; Hypersensitivity; Interleukin 6; Nerve injury; Neuropathic pain; Substance P

Indexed keywords

GALANIN; INTERLEUKIN 6; MESSENGER RNA; NEUROPEPTIDE; SUBSTANCE P;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; FEMALE; HEAT; INTRATHECAL DRUG ADMINISTRATION; NERVE COMPRESSION; NEUROPATHY; NONHUMAN; PEPTIDE SYNTHESIS; PRESSURE; PRIORITY JOURNAL; RAT; SENSORY NERVE CELL; SKIN SENSITIZATION;

EID: 0032968705     PISSN: 0953816X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1460-9568.1999.00641.x     Document Type: Article

References (69)

1. Averill, S., McMahon, S.B., Clary, D.U., Reichardt, L.F., Priestley, J.V. 1995 Immunocytochemical localisation of trkA receptors in chemically identified subgroups of adult rat sensory neurons. Eur. J. Neurosci., 7, 1484 1494.
2. Banner, L.R., Patterson, P.H., Allchorne, A., Poole, S., Woolf, C.J. 1998 Leukemia inhibitory factor is an anti‐inflammatory and analgesic cytokine. J. Neurosci., 18, 5456 5462.
3. Basbaum, A.I., Gautron, M., Jazat, F., Mayes, M., Guilbaud, G. 1991 The spectrum of fibre loss in a model of neuropathic pain in the rat. Pain, 47, 359 367.
4. Bennett, G.J. & Xie, Y.K. 1988 A painful mononeuropathy in rat produces disorders of pain sensation like those seen in man. Pain, 33, 87 107.
5. Bessou, P. & Perl, E.R. 1969 Response of cutaneous sensory units with unmyelinated fibers to noxious stimuli. J. Neurophysiol., 32, 1025 1043.
6. Bolin, L.M., Verity, A.N., Silver, J.E., Shooter, E.M., Abrams, J.S. 1995 Interleukin‐6 production by Schwann cells and induction in sciatic nerve injury. J. Neurochem., 64, 850 858.
7. Braciak, T.A., Northemann, W., Chong, D.K., Schroeder, T.A., Gauldie, J. 1993 Vector derived expression of recombinant rat IL‐6. Protein Exp. Pur., 7, 269 274.
8. Campbell, J.N., Khan, A.A., Meyer, R.A., Raja, S.N. 1988 Response to heat of C‐fiber nociceptors in monkeys following a mechanical injury adjacent to and within the receptive field. Pain, 32, 327 332.
9. Cao, Y.Q., Mantyh, P.W., Carlson, E.J., Gillespie, A.‐M., Epstein, C.J., Basbaum, A.I. 1998 Primary afferent tachykinins are required to experience moderate to intense pain. Nature, 392, 390 394.
10. Chai, Z., Gatti, S., Poli, V., Bartfai, T. 1996 Interleukin (IL) ‐6 gene expression in the central nervous system is necessary for fever response to lipopolysaccharide or IL‐1β: a study on IL‐6‐deficient mice. J. Exp. Med., 183, 311 316.
11. Corness, J., Shi, T.J., Xu, Z.Q., Brulet, P., Hökfelt, T. 1996 Influence of leukemia inhibitory factor on galanin/GMAP and neuropeptide Y expression in mouse primary sensory neurons after axotomy. Exp. Brain Res., 112, 79 88.
12. Cressman, D.E., Greenbaum, L.E., DeAngelis, R.A., Ciliberto, G., Furth, E.E., Poli, V., Taub, R. 1996 Liver failure and defective hepatocyte regeneration in interleukin‐6‐deficient mice. Science, 274, 1379 1383.
13. Cridland, R.A. & Henry, J.L. 1988 Effects of intrathecal administration of neuropeptides on a spinal nociceptive reflex in the rat. Neuropeptides, 11, 23 32.
14. Dassan, P., Trevedi, P., McMahon, S.B., Jones, M., Swanson, G., Thompson, S.W.N. 1998 BDNF induces a prolonged increase in spinal reflex activity in vitro. Soc. Neurosci. Abstract., 24, 394.
15. DeFelipe, C. & Hunt, S.P. 1994 The differential control of c‐jun expression in regenerating sensory neurons and their associated glial cells. J. Neurosci., 14, 2911 2923.
16. DeLeo, J.A., Colburn, R.W., Nichols, M., Malhotra, A. 1996 Interleukin‐6‐mediated hyperalgesia/allodynia and increased spinal IL‐6 expression in a rat mononeuropathy model. J. Interferon Cytokine Res., 16, 695 700.
17. Fattori, E., Cappelletti, M., Costa, P., Sellitto, C., Cantoni, L., Carelli, M., Faggioni, R., Fantuzzi, G., Ghezzi, P., Poli, V. 1994 Defective inflammatory response in interleukin‐6‐deficient mice. J. Exp. Med., 180, 1243 1250.
18. Fitzgerald, M., Wall, P.D., Goedert, M., Emson, P.C. 1985 Nerve growth factor counteracts the neurophysiological and neurochemical effects of chronic sciatic nerve section. Brain Res., 332, 131 141.
19. Frei, K., Malipiero, U.V., Leist, T.P., Zinkernagel, R.M., Schwab, M.E., Fontana, A. 1989 On the cellular source and function of interleukin 6 produced in the central nervous system in viral diseases. Eur. J. Immunol., 19, 689 694.
20. Gadient, R.A. & Otten, U. 1996 Postnatal expression of interleukin‐6 and IL‐6 receptor mRNAs in rat sympathetic and sensory ganglia. Brain Res., 724, 41 46.
21. Grenett, H.E., Danley, D.E., Strick, C.A., James, L.C., Otterness, I.G., Fuentes, N., Nesbitt, J.E., Fuller, G.M. 1991 Isolation and characterization of a biologically active murine IL‐6 produced in Escherichia coli. Gene, 109, 309 313.
22. Hargreaves, K., Dubner, R., Broun, F., Flores, C., Joris, J. 1988 A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain, 32, 77 78.
23. Hokfelt, T., Zhang, X., Wiesenfeld‐Hallin, Z. 1994 Messenger plasticity in primary sensory neurons following axotomy and its functional implications. Trends Neurosci., 17, 22 30.
24. Kajander, K.C. & Bennett, G.J. 1992 Onset of a painful peripheral neuropathy in rat: a partial and differential deafferentation and spontaneous discharge in A‐beta and A‐delta primary afferent neurons. J. Neurophysiol., 68, 734 744.
25. Kerekes, N., Landry, M., Rydh‐Rinder, M., Hokfelt, T. 1997 The effect of NGF, BDNF, and bFGF on expression of galanin in cultured rat dorsal root ganglia. Brain Res., 754, 131 141.
26. Kerr, B.J., Thompson, S.W.N., Wynick, D., McMahon, S.B. 1998 Galanin mutant mice are hypoalgesic in a partial nerve injury model. Soc. Neurosci. Abstract., 224, 1391.
27. Kiefer, R., Lindholm, D., Kreutzberg, G.W. 1993 Interleukin‐6 and transforming growth factor‐beta1 mRNAs are induced in rat facial nucleus following motoneuron axotomy. Eur. J. Neurosci., 5, 775 781.
28. Kishimoto, T., Taga, T., Akira, S. 1994 Cytokine signal transduction. Cell, 76, 253 262.
29. Klein, M.A., Moller, J.C., Jones, L.L., Bluethmann, H., Kreutzberg, G., Raivich, G. 1997 Impaired neuroglial activation in interleukin‐6 deficient mice. Glia, 19, 227 233.
30. Koltzenburg, M., Torebjork, H.E., Wahren, L.K. 1994 Nociceptor modulated central sensitization causes mechanical hyperalgesia in acute chemogenic and chronic neuropathic pain. Brain, 117, 579 591.
31. Kopf, M., Baumann, H., Freer, G., Freudenberg, M., Lamers, M., Kishimoto, T., Zinkernagel, R., Bluethmann, H., Köhler, G. 1994 Impaired immune and acute‐phase responses in interleukin‐6‐deficient mice. Nature, 368, 339 342.
32. Kuraishi, Y., Kawamura, M., Yamaguchi, T., Houtani, T., Kawabata, S., Futaki, S., Fujii, N., Satoh, M. 1991 Intrathecal injections of galanin and its antiserum affect nociceptive response of rat to mechanical but not thermal stimuli. Pain, 44, 321 324.
33. Kurek, J.B., Austin, L., Cheema, S.S., Bartlett, P.F., Murphy, M. 1996 Up‐regulation of leukemia inhibitory factor and interleukin‐6 in transected sciatic nerve and muscle following denervation. Neuromusc. Disord., 6, 105 114.
34. Lamotte, R.H., Thalhammer, J.G., Robinson, C.J. 1983 Peripheral neural correlates of magnitude of cutaneous pain and hyperalgesia: a comparison of neural events in the monkey with sensory judgements in human. J. Neurophysiol., 50, 1 26.
35. Lewin, G.R. & Mendell, L.M. 1994 Peripheral and central mechanisms of NGF‐induced hyperalgesia. Eur. J. Neurosci., 6, 1903–12.
36. Ma, W. & Bisby, M.A. 1997 Differential expression of galanin immunoreactivities in the primary sensory neurons following partial and complete sciatic nerve injuries. Neuroscience, 79, 1183 1195.
37. Ma, Q.‐P. & Woolf, C.J. 1995 Involvement of neurokinin receptors in the induction but not the maintenance of mechanical allodynia in rat flexor motoneurons. J. Physiol., 486, 769 777.
38. Mantyh, P.W., Rogers, S.D., Honore, P., Allen, B.J., Ghilardi, J.R., Li, J., Daughters, R.S., Lappi, D.A.,. Wiley, R.G., Simone, D.A. 1997 Inhibition of hyperalgesia by ablation of lamina 1 spinal neurons expressing the substance P receptor. Science, 278, 275 279.
39. McMahon, S.B., Bennett, D.L.H., Priestley, J.V., Shelton, D.L. 1995 The biological effect of endogenous nerve growth factor on adult sensory neurons revealed by a trkA‐IgG fusion molecule. Nature Med., 1, 774 780.
40. McMahon, S.B., Lewin, G.R., Wall, P.D. 1993 Central hyperexcitability triggered by noxious inputs. Curr. Opin. Neurobiol., 3, 602 610.
41. Murphy, P.G., Grondin, J., Altares, M., Richardson, P.M. 1995 Induction of interleukin‐6 in axotomized sensory neurons. J. Neurosci., 15, 5130 5138.
42. Nahin, R.L., Ren, K., DeLeon, M., Ruda, M. 1994 Primary sensory neurons exhibit altered gene expression in a rat model of neuropathic pain. Pain, 58, 95 108.
43. Neugebauer, V., Lucke, T., Schaible, H.‐G. 1993 N ‐methyl‐ d‐aspartate and non‐NMDA receptor antagonists block the hyperexcitability of dorsal horn neurons during development of acute arthritis in rat’s knee joint. J. Neurophysiol., 70, 1365 1377.
44. Neumann, S., Doubell, T.P., Leslie, T., Woolf, C.J. 1996 Inflammatory pain hypersensitivity mediated by phenotypic switch in myelinated primary sensory neurons. Nature, 384, 360 364.
45. Noguchi, K., Kawai, Y., Fukoka, T., Senba, E., Miki, K. 1995 Substance P induced by peripheral nerve injury in primary afferent sensory neurons and its effect on dorsal column nucleus neurons. J. Neurosci., 15, 7633 7643.
46. Oka, T., Oka, K., Hosoi, M., Hori, T. 1995 Intracerebroventricular injection of interleukin‐6 induces thermal hyperalgesia in rats. Brain Res., 692, 123 128.
47. Ramer, M.S., French, G.D., Bisby, M.A. 1997 Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain, 72, 71 78.
48. Ramer, M.S., Murphy, P.G., Richardson, P.M., Bisby, M.A. 1998 Spinal nerve lesion‐induced allodynia and adrenergic sprouting in sensory ganglia are attenuated in interleukin‐6 knockout mice. Pain, 78, 115 121.
49. Ramsay, A.J., Husband, A.J., Ramshaw, I.A., Bao, S., Matthaei, K.I., Koehler, G., Kopf, M. 1994 The role of interleukin‐6 in mucosal IgA antibody responses in vivo. Science, 264, 561 563.
50. Rao, M.S., Sun, Y., Escary, J.L., Perreau, J., Tresser, S., Patterson, P.H., Zigmond, R.E., Brulet, P., Landis, S.C. 1993 Leukemia inhibitory factor mediates an injury response but not a target‐directed developmental transmitter switch in sympathetic neurons. Neuron, 11, 1175 1185.
51. Reichert, F., Levitsky, R., Rotshenker, S. 1996 Interleukin‐6 in intact and injured mouse peripheral nerve. Eur. J.Neurosci., 8, 530 535.
52. Robertson, B., Xu, X.‐J., Hao, J.‐X., Wiesenfeld‐Hallin, Z., Mhlanga, J., Grant, G., Kristensson, K. 1997 Interferon‐gamma receptors in nociceptive pathways: role in neuropathic pain‐related behaviour. Neuroreport, 8, 1311 1316.
53. Sambrook, J., Fritsch, E.F., Maniatis, T. 1989 Molecular Cloning. A Laboratory Manual. 2nd edn. Cold Spring Harbour Laboratory Press, Cold Spring Harbour, New York.
54. Schalling, M., Dagerlind, A., Brene, S., Hallman, H., Djurfeldt, M., Persson, H., Terenius, L., Goldstein, M., Schlesinger, D., Hokfelt, T. 1988 Coexistence and gene expression of phenylethanolamine N ‐methyltranferase, tyrosine hydroxylase, and neuropeptide tyrosine in the rat and bovine adrenal gland: effects of reserpine. Proc. Natl Acad. Sci. USA, 85, 8306 8310.
55. Shortland, P., Kinnman, E., Molander, C. 1997 Sprouting of A‐fibre primary afferents into lamina II in two rat models of neuropathic pain. Eur. J. Pain, 1, 215 227.
56. Study, R.E. & Kral, M.G. 1996 Spontaneous action potential activity in isolated dorsal root ganglion neurons from rats with a painful neuropathy. Pain, 65, 235 242.
57. Sun, Y. & Zigmond, R. 1996 Leukaemia inhibitory factor induced in the sciatic nerve after axotomy is involved in the induction of galanin in sensory neurons. Eur. J. Neurosci., 8, 2213 2220.
58. Taga, T. & Kishimoto, T. 1997 Gp130 and the interleukin‐6 family of cytokines. Annu. Rev. Immunol., 15, 797 819.
59. Thompson, S.W.N., Dray, A., Urban, L. 1996 Leukemia inhibitory factor induces mechanical allodynia but not thermal hyperalgesia in the juvenile rat. Neuroscience, 71, 1091 1094.
60. Thompson, S.W.N. & Majithia, A.A. 1998a Leukemia inhibitory factor induces sympathetic sprouting in intact dorsal root ganglia in the adult rat in vivo. J. Physiol., 506, 809 816.
61. Thompson, S.W.N., Priestley, J.V., Southall, A. 1998b GP130 cytokines, leukemia inhibitory factor and interleukin‐6, induce neuropeptide expression in intact adult rat sensory neurons in vivo. Neuroscience, 84, 1247 1255.
62. Verge, V.M.K., Richardson, P.M., Benoit, R., Riopelle, R.J. 1989 Histochemical characterization of sensory neurons with high‐affinity receptors for nerve growth factor. J. Neurocytol., 18, 583 591.
63. Verge, V.M.K., Richardson, P.M., Wiesenfeld‐Hallin, Z., Hökfelt, T. 1995 Differential influence of nerve growth factor on neuropeptide expression in vivo. J. Neurosci., 15, 2081 2096.
64. Verge, V.M.K., Tetzlaff, W., Bisby, M.A., Richardson, P.M. 1990a Influence of nerve growth factor on neurofilament gene expression in mature primary sensory neurons. J. Neurosci., 10, 2018 2025.
65. Verge, V.M.K., Tetzlaff, W., Richardson, P.M., Bisby, M.A. 1990b Correlation between GAP43 and nerve growth factor receptors in rat sensory neurons. J. Neurosci., 10, 926 934.
66. Wiesenfeld‐Hallin, Z., Villar, M., Hokfelt, T. 1988 Intrathecal galanin at low doses increases spinal reflex excitability in rats more to thermal than mechanical stimuli. Exp. Brain Res., 71, 663 666.
67. Woolf, C.J. & King, A.E. 1987 Physiology and morphology of multireceptive neurons with C‐afferent fibre inputs in the deep dorsal horn of the rat lumbar spinal cord. J. Neurophysiol., 58, 460 479.
68. Woolf, C.J., Shortland, P., Sivilotti, L.G. 1994 Sensitization of high mechanothreshold superficial dorsal horn and flexor motor neurones following chemosensitive primary afferent activation. Pain, 58, 141 155.
69. Xu, X.‐J., Hao, J.‐X., Andell‐Jonsson, P., Poli, V., Bartfai, T., Wiesenfeld‐Hallin, Z. 1997 Nociceptive responses in interleukin‐6 deficient mice to peripheral inflammation and peripheral nerve section. Cytokine, 9, 1028 1033.