The role of IL-6 and IL-1β in painful perineural inflammatory neuritis

Brain, Behavior, and Immunity

Volumn 23, Issue 4, 2009, Pages 474-484

  Eliav, Eli ^a   Benoliel, Rafael ^b   Herzberg, Uri ^c   Kalladka, Mythili ^d   Tal, Michael ^b  

^a RUTGERS SCHOOL OF DENTAL MEDICINE   (United States)

^b HADASSAH HEBREW UNIVERSITY MEDICAL CENTER   (Israel)

^c Center for Biomaterials and Advanced Technologies   (United States)

^d Research Center   (India)

Author keywords

Cytokines; IL 1 ; IL 6; Inflammation; Neuritis; Neuropathic pain

Indexed keywords

FREUND ADJUVANT; INTERLEUKIN 1BETA; INTERLEUKIN 6;

ACTION POTENTIAL; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE RELEASE; ELECTROPHYSIOLOGY; ENZYME LINKED IMMUNOSORBENT ASSAY; FORCE; HEAT; HYPERALGESIA; INFLAMMATION; MALE; MECHANICAL STIMULATION; MYELINATED NERVE; NEURITIS; NONHUMAN; PAIN; POSTOPERATIVE PERIOD; PRIORITY JOURNAL; PROTEIN FUNCTION; RAT; SAPHENOUS NERVE; SCIATIC NERVE; SKIN; SPINAL GANGLION; SPINAL ROOT;

ACTION POTENTIALS; ADJUVANTS, IMMUNOLOGIC; ANALYSIS OF VARIANCE; ANIMALS; ELECTRIC STIMULATION; ELECTROPHYSIOLOGY; ENZYME-LINKED IMMUNOSORBENT ASSAY; FREUND'S ADJUVANT; GANGLIA, SPINAL; HINDLIMB; HOT TEMPERATURE; HYPERALGESIA; INFLAMMATION; INTERLEUKIN-1BETA; INTERLEUKIN-6; MALE; NEURITIS; PAIN; PAIN MEASUREMENT; PAIN THRESHOLD; RATS; RATS, SPRAGUE-DAWLEY; SCIATIC NERVE; TIME FACTORS;

EID: 63549116683     PISSN: 08891591     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbi.2009.01.012     Document Type: Article

References (73)

1. Anneroth G., Hansen L.S., and Silverman Jr. S. Malignancy grading in oral squamous cell carcinoma. I. Squamous cell carcinoma of the tongue and floor of mouth: histologic grading in the clinical evaluation. J. Oral Pathol. 15 3 (1986) 162-168
2. Arruda J.L., Colburn R.W., Rickman A.J., Rutkowski M.D., and DeLeo J.A. Increase of interleukin-6 mRNA in the spinal cord following peripheral nerve injury in the rat: potential role of IL-6 in neuropathic pain. Brain Res. Mol. Brain Res. 62 2 (1998) 228-235
3. Arruda J.L., Sweitzer S., Rutkowski M.D., and DeLeo J.A. Intrathecal anti-IL-6 antibody and IgG attenuates peripheral nerve injury-induced mechanical allodynia in the rat: possible immune modulation in neuropathic pain. Brain Res. 879 1-2 (2000) 216-225
4. Barron R.P., Benoliel R., Zeltser R., Eliav E., Nahlieli O., and Gracely R.H. Effect of dexamethasone and dipyrone on lingual and inferior alveolar nerve hypersensitivity following third molar extractions: preliminary report. J. Orofac. Pain 18 1 (2004) 62-68
5. Barton B.E. IL-6: insights into novel biological activities. Clin. Immunol. Immunopathol. 85 1 (1997) 16-20
6. Barton B.E., Shortall J., and Jackson J.V. Interleukins 6 and 11 protect mice from mortality in a staphylococcal enterotoxin-induced toxic shock model. Infect. Immun. 64 3 (1996) 714-718
7. Bennett G.J., and Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 33 1 (1988) 87-107
8. Benoliel R., Biron A., Quek S.Y., Nahlieli O., and Eliav E. Trigeminal neurosensory changes following acute and chronic paranasal sinusitis. Quintessence Int. 37 6 (2006) 437-443
9. Benoliel R., Wilensky A., Tal M., and Eliav E. Application of a pro-inflammatory agent to the orbital portion of the rat infraorbital nerve induces changes indicative of ongoing trigeminal pain. Pain 99 3 (2002) 567-578
10. Bessler H., Shavit Y., Mayburd E., Smirnov G., and Beilin B. Postoperative pain, morphine consumption, and genetic polymorphism of IL-1beta and IL-1 receptor antagonist. Neurosci. Lett. 404 1-2 (2006) 154-158
11. Boucher T.J., and McMahon S.B. Neurotrophic factors and neuropathic pain. Curr. Opin. Pharmacol. 1 1 (2001) 66-72
12. Boucher T.J., Okuse K., Bennett D.L., Munson J.B., Wood J.N., and McMahon S.B. Potent analgesic effects of GDNF in neuropathic pain states. Science 290 5489 (2000) 124-127
13. Bove G.M., Ransil B.J., Lin H.C., and Leem J.G. Inflammation induces ectopic mechanical sensitivity in axons of nociceptors innervating deep tissues. J. Neurophysiol. 90 3 (2003) 1949-1955
14. 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 3 (2001) 231-244
15. Cunha F.Q., Poole S., Lorenzetti B.B., Veiga F.H., and Ferreira S.H. Cytokine-mediated inflammatory hyperalgesia limited by interleukin-4. Br. J. Pharmacol. 126 1 (1999) 45-50
16. DeLeo J.A., Colburn R.W., Nichols M., and Malhotra A. Interleukin-6-mediated hyperalgesia/allodynia and increased spinal IL-6 expression in a rat mononeuropathy model. J. Interferon Cytokine Res. 16 9 (1996) 695-700
17. DeLeo J.A., Colburn R.W., and Rickman A.J. Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuropathy. Brain Res. 759 1 (1997) 50-57
18. Devor M., Janig W., and Michaelis M. Modulation of activity in dorsal root ganglion neurons by sympathetic activation in nerve-injured rats. J. Neurophysiol. 71 1 (1994) 38-47
19. Dilley A., and Bove G.M. Resolution of inflammation-induced axonal mechanical sensitivity and conduction slowing in C-fiber nociceptors. J. Pain 9 2 (2008) 185-192
20. Dilley A., Lynn B., and Pang S.J. Pressure and stretch mechanosensitivity of peripheral nerve fibres following local inflammation of the nerve trunk. Pain 117 3 (2005) 462-472
21. 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 1 (2001) 49-52
22. Eliav E., and Gracely R.H. Sensory changes in the territory of the lingual and inferior alveolar nerves following lower third molar extraction. Pain 77 2 (1998) 191-199
23. Eliav E., Herzberg U., Ruda M.A., and Bennett G.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain 83 2 (1999) 169-182
24. Eliav E., Tal M., and Benoliel R. Experimental malignancy in the rat induces early hypersensitivity indicative of neuritis. Pain 110 3 (2004) 727-737
25. Eliav E., Teich S., Benoliel R., Nahlieli O., Lewkowicz A.A., Baruchin A., and Gracely R. Large myelinated nerve fiber hypersensitivity in oral malignancy. Oral Surg. Oral Med. Oral Pathol. Oral Radiol. Endod. 94 1 (2002) 45-50
26. Eliav E., Teich S., Nitzan D., El Raziq D.A., Nahlieli O., Tal M., Gracely R.H., and Benoliel R. Facial arthralgia and myalgia: can they be differentiated by trigeminal sensory assessment?. Pain 104 3 (2003) 481-490
27. Falchi M., Ferrara F., Gharib C., and Dib B. Hyperalgesic effect of intrathecally administered interleukin-1 in rats. Drugs Exp. Clin. Res. 27 3 (2001) 97-101
28. Farrell M., Gibson S., McMeeken J., and Helme R. Pain and hyperalgesia in osteoarthritis of the hands. J. Rheumatol. 27 2 (2000) 441-447
29. Farrell M.J., Gibson S.J., McMeeken J.M., and Helme R.D. Increased movement pain in osteoarthritis of the hands is associated with A beta-mediated cutaneous mechanical sensitivity. J. Pain 1 3 (2000) 229-242
30. Gazda L.S., Milligan E.D., Hansen M.K., Twining C.M., Poulos N.M., Chacur M., O'Connor K.A., Armstrong C., Maier S.F., Watkins L.R., and Myers R.R. Sciatic inflammatory neuritis (SIN): behavioral allodynia is paralleled by peri-sciatic proinflammatory cytokine and superoxide production. J. Peripher. Nerv. Syst. 6 3 (2001) 111-129
31. Govrin-Lippmann R., and Devor M. Ongoing activity in severed nerves: source and variation with time. Brain Res. 159 2 (1978) 406-410
32. Granados-Soto V., Alonso-Lopez R., Asomoza-Espinosa R., Rufino M.O., Gomes-Lopes L.D., and Ferreira S.H. Participation of COX, IL-1 beta and TNF alpha in formalin-induced inflammatory pain. Proc. West. Pharmacol. Soc. 44 (2001) 15-17
33. 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 1 (1988) 77-88
34. Hirano T. Cytokines and diseases. Abnormal expression of interleukin 6 and diseases. Nippon Naika Gakkai Zasshi 80 9 (1991) 1401-1408
35. Hirano T. Interleukin 6 (IL-6) and its receptor: their role in plasma cell neoplasias. Int. J. Cell Cloning 9 3 (1991) 166-184
36. Hoffmann T., Sauer S.K., Horch R.E., and Reeh P.W. Sensory transduction in peripheral nerve axons elicits ectopic action potentials. J. Neurosci. 28 24 (2008) 6281-6284
37. Hollins M., Sigurdsson A., Fillingim L., and Goble A.K. Vibrotactile threshold is elevated in temporomandibular disorders. Pain 67 1 (1996) 89-96
38. Hu S.J., and Xing J.L. An experimental model for chronic compression of dorsal root ganglion produced by intervertebral foramen stenosis in the rat. Pain 77 1 (1998) 15-23
39. Ignatowski T.A., Covey W.C., Knight P.R., Severin C.M., Nickola T.J., and Spengler R.N. Brain-derived TNFalpha mediates neuropathic pain. Brain Res. 841 1-2 (1999) 70-77
40. Junger H., and Sorkin L.S. Nociceptive and inflammatory effects of subcutaneous TNFalpha. Pain 85 1-2 (2000) 145-151
41. Kajander K.C., Wakisaka S., and Bennett G.J. Spontaneous discharge originates in the dorsal root ganglion at the onset of a painful peripheral neuropathy in the rat. Neurosci. Lett. 138 2 (1992) 225-228
42. Kleinschnitz C., Brinkhoff J., Sommer C., and Stoll G. Contralateral cytokine gene induction after peripheral nerve lesions: dependence on the mode of injury and NMDA receptor signaling. Brain Res. Mol. Brain Res. 136 1-2 (2005) 23-28
43. Lewin G.R., Rueff A., and Mendell L.M. Peripheral and central mechanisms of NGF-induced hyperalgesia. Eur. J. Neurosci. 6 12 (1994) 1903-1912
44. Liu C.N., Wall P.D., Ben-Dor E., Michaelis M., Amir R., and Devor M. Tactile allodynia in the absence of C-fiber activation: altered firing properties of DRG neurons following spinal nerve injury. Pain 85 3 (2000) 503-521
45. Ma W., and Quirion R. Targeting invading macrophage-derived PGE2, IL-6 and calcitonin gene-related peptide in injured nerve to treat neuropathic pain. Expert Opin. Ther. Targets 10 4 (2006) 533-546
46. 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
47. 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 3 (2003) 1026-1040
48. Murphy P.G., Ramer M.S., Borthwick L., Gauldie J., Richardson P.M., and Bisby M.A. Endogenous interleukin-6 contributes to hypersensitivity to cutaneous stimuli and changes in neuropeptides associated with chronic nerve constriction in mice. Eur. J. Neurosci. 11 7 (1999) 2243-2253
49. Poole S., Cunha F.Q., Selkirk S., Lorenzetti B.B., and Ferreira S.H. Cytokine-mediated inflammatory hyperalgesia limited by interleukin-10. Br. J. Pharmacol. 115 4 (1995) 684-688
50. Reichert F., Levitzky R., and Rotshenker S. Interleukin 6 in intact and injured mouse peripheral nerves. Eur. J. Neurosci. 8 3 (1996) 530-535
51. Ruzek M.C., Miller A.H., Opal S.M., Pearce B.D., and Biron C.A. Characterization of early cytokine responses and an interleukin (IL)-6-dependent pathway of endogenous glucocorticoid induction during murine cytomegalovirus infection. J. Exp. Med. 185 7 (1997) 1185-1192
52. Sachs D., Cunha F.Q., Poole S., and Ferreira S.H. Tumour necrosis factor-alpha, interleukin-1beta and interleukin-8 induce persistent mechanical nociceptor hypersensitivity. Pain 96 1-2 (2002) 89-97
53. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., and Woolf C.J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmacol. 115 7 (1995) 1265-1275
54. Samad T.A., Moore K.A., Sapirstein A., Billet S., Allchorne A., Poole S., Bonventre J.V., and Woolf C.J. Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity. Nature 410 6827 (2001) 471-475
55. Schwartz M., Sivron T., Eitan S., Hirschberg D.L., Lotan M., and Elman-Faber A. Cytokines and cytokine-related substances regulating glial cell response to injury of the central nervous system. Prog. Brain Res. 103 (1994) 331-341
56. Shamash S., Reichert F., and Rotshenker S. The cytokine network of Wallerian degeneration: tumor necrosis factor-alpha, interleukin-1alpha, and interleukin-1beta. J. Neurosci. 22 8 (2002) 3052-3060
57. Sommer C., Petrausch S., Lindenlaub T., and Toyka K.V. Neutralizing antibodies to interleukin 1-receptor reduce pain associated behavior in mice with experimental neuropathy. Neurosci. Lett. 270 1 (1999) 25-28
58. Song M., and Kellum J.A. Interleukin-6. Crit. Care Med. 33 12 Suppl. (2005) S463-S465
59. 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 1 (1997) 255-262
60. Stohler C.S., Kowalski C.J., and Lund J.P. Muscle pain inhibits cutaneous touch perception. Pain 92 3 (2001) 327-333
61. Sweitzer S.M., Hickey W.F., Rutkowski M.D., Pahl J.L., and DeLeo J.A. Focal peripheral nerve injury induces leukocyte trafficking into the central nervous system: potential relationship to neuropathic pain. Pain 100 1-2 (2002) 163-170
62. Tadano T., Namioka M., Nakagawasai O., Tan-No K., Matsushima K., Endo Y., and Kisara K. Induction of nociceptive responses by intrathecal injection of interleukin-1 in mice. Life Sci. 65 3 (1999) 255-261
63. Tal M., and Bennett G.J. Extra-territorial pain in rats with a peripheral mononeuropathy: mechano-hyperalgesia and mechano-allodynia in the territory of an uninjured nerve. Pain 57 3 (1994) 375-382
64. Tal M., and Eliav E. Abnormal discharge originates at the site of nerve injury in experimental constriction neuropathy (CCI) in the rat. Pain 64 3 (1996) 511-518
65. Tilg H., Trehu E., Atkins M.B., Dinarello C.A., and Mier J.W. Interleukin-6 (IL-6) as an anti-inflammatory cytokine: induction of circulating IL-1 receptor antagonist and soluble tumor necrosis factor receptor p55. Blood 83 1 (1994) 113-118
66. Wagner R., and Myers R.R. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. Neuroreport 7 18 (1996) 2897-2901
67. Watkins L.R., Wiertelak E.P., Goehler L.E., Smith K.P., Martin D., and Maier S.F. Characterization of cytokine-induced hyperalgesia. Brain Res. 654 1 (1994) 15-26
68. Wewers M.D., Dare H.A., Winnard A.V., Parker J.M., and Miller D.K. IL-1 beta-converting enzyme (ICE) is present and functional in human alveolar macrophages: macrophage IL-1 beta release limitation is ICE independent. J. Immunol. 159 12 (1997) 5964-5972
69. Wieseler-Frank J., Jekich B.M., Mahoney J.H., Bland S.T., Maier S.F., and Watkins L.R. A novel immune-to-CNS communication pathway: cells of the meninges surrounding the spinal cord CSF space produce proinflammatory cytokines in response to an inflammatory stimulus. Brain Behav. Immun. 21 5 (2007) 711-718
70. Wolf G., Yirmiya R., Goshen I., Iverfeldt K., Holmlund L., Takeda K., and Shavit Y. Impairment of interleukin-1 (IL-1) signaling reduces basal pain sensitivity in mice: genetic, pharmacological and developmental aspects. Pain 104 3 (2003) 471-480
71. Woolf C.J., Allchorne A., Safieh-Garabedian B., and Poole S. Cytokines, nerve growth factor and inflammatory hyperalgesia: the contribution of tumour necrosis factor alpha. Br. J. Pharmacol. 121 3 (1997) 417-424
72. 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 3 (2005) 257-263
73. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 16 2 (1983) 109-110