Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats

Pain

Volumn 110, Issue 1-2, 2004, Pages 299-309

  Twining, Carin M ^a   Sloane, Evan M ^a   Milligan, Erin D ^a   Chacur, Marucia ^b   Martin, David ^c   Poole, Stephen ^d   Marsh, Henry ^e   Maier, Steven F ^a   Watkins, Linda R ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b INSTITUTO BUTANTAN   (Brazil)

^c AMGEN INC   (United States)

^d NATIONAL INSTITUTE FOR BIOLOGICAL STANDARDS AND CONTROL   (United Kingdom)

^e AVANT Immunotherapeutics Inc   (United States)

Author keywords

Allodynia; Complement; Interleukin 1; Interleukin 6; Reactive oxygen species; Sciatic nerve; Tumor necrosis factor

Indexed keywords

COMPLEMENT; CYTOKINE; INTERLEUKIN 1; INTERLEUKIN 6; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR; ZYMOSAN;

ALLODYNIA; ANIMAL EXPERIMENT; ARTICLE; CYTOKINE RELEASE; INFLAMMATION; MACROPHAGE; MALE; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; RAT; SCIATIC NERVE;

ANIMALS; ANTIBODIES; BEHAVIOR, ANIMAL; CARRIER PROTEINS; CATALASE; COMPLEMENT SYSTEM PROTEINS; CYTOKINES; DISEASE MODELS, ANIMAL; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; FUNCTIONAL LATERALITY; HYPERALGESIA; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-6; MALE; NEURALGIA; PAIN MEASUREMENT; PHYSICAL STIMULATION; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RECEPTORS, COMPLEMENT; RECEPTORS, TUMOR NECROSIS FACTOR; RECEPTORS, TUMOR NECROSIS FACTOR, TYPE I; SCIATIC NERVE; SCIATIC NEUROPATHY; SIALOGLYCOPROTEINS; SUPEROXIDE DISMUTASE; TUMOR NECROSIS FACTOR DECOY RECEPTORS; ZYMOSAN;

EID: 3242725996     PISSN: 03043959     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pain.2004.04.008     Document Type: Article

References (56)

1. Aley K.O., Levine J.D. Different peripheral mechanisms mediate enhanced nociception in metobolic/toxic and traumatic painful peripheral neuropathies in the rat. Neuroscience. 111:2002;389-397
2. Baron R. Peripheral neuropathic pain: from mechanisms to symptoms. Clin J Pain. 16:(2 Suppl):2000;S12-S20
3. Chacur M., Milligan E.D., Gazda L.S., Armstrong C., Wang H., Tracey K.J., Maier S.F., 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
4. Chaplan S.R., Bach F.W., Pogrel J.W., Chung J.M., Yaksh T.L. Quantitative assessment of tactile allodynia in the rat paw. J Neurosci Methods. 53:1994;55-63
5. Colston J.T., Chandrasekar B., Freeman G.L. A novel peroxide-induced calcium transient regulates interleukin-6 expression in cardiac-derived fibroblasts. J Biol Chem. 277:2002;23477-23483
6. Dailey A.T., Avellino A.M., Benthem L., Silver J., Kliot M. Complement depletion reduces macrophage infiltration and activation during Wallerian degeneration and axonal regeneration. J Neurosci. 18:1998;6713-6722
7. Eliav E., Herzberg U., Ruda M.A., Bennett G.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain. 83:1999;169-182
8. Elsner J., Oppermann M., Czech W., Dobos G., Schopf E., Norgauer J., Kapp A. C3a activates reactive oxygen radical species production and intracellular calcium transients in human eosinophils. Eur J Immunol. 24:1994;518-522
9. Ezekowitz R.A., Sim R.B., MacPherson G.G., Gordon S. Interaction of human monocytes, macrophages, and polymorphonuclear leukocytes with zymosan in vitro. Role of type 3 complement receptors and macrophage-derived complement. J Clin Invest. 76:1985;2368-2376
10. Feng L., Xia Y., Garcia G.E., Hwang D., Wilson C.B. Involvement of reactive oxygen intermediates in cyclooxygenase-2 expression induced by interleukin-1, tumor necrosis factor-alpha, and lipopolysaccharide. J Clin Invest. 95:1995;1669-1675
11. Gazda L.S., Milligan E.D., Hansen M.K., Twining C.M., Paulos N., Chacur M., O'Connor K.A., Armstrong C., Maier S.F. Sciatic inflammatory neuritis (SIN): behavioral allodynia is paralleled by peri-sciatic proinflammatory cytokine and superoxide production. J Peripheral Nerv Syst. 6:2001;111-129
12. Ginsburg I., Misgav R., Pinson A., Varani J., Ward P.A., Kohen R. Synergism among oxidants, proteinases, phospholipases, microbial hemolysins, cationic proteins, and cytokines. Inflammation. 16:1992;519-538
13. Harvey L.O. Efficient estimation of sensory thresholds. Behav Res Methods, Instrum Comput. 18:1986;623-632
14. Jung S., Toyka K.V., Hartung H.P. Soluble complement receptor type 1 inhibits experimental autoimmune neuritis in Lewis rats. Neurosci Lett. 200:1995;167-170
15. Khalil Z., Khodr B. A role for free radicals and nitric oxide in delayed recovery in aged rats with chronic constriction nerve injury. Free Radic Biol Med. 31:2001;430-439
16. Lindenlaub T., Teuteberg P., Hartung T., Sommer C. Effects of neutralizing antibodies to TNF-alpha on pain-related behavior and nerve regeneration in mice with chronic constriction injury. Brain Res. 866:2000;15-22
17. Liu T., Knight K.R., Racey D.J. Hyperalgesia due to nerve injury - role of peroxynitrite. Neuroscience. 97:2000;125-131
18. Maleki J., LeBel A.A., Bennett G.J., Schwartzman R.J. Patterns of spread in complex regional pain syndrome, type I (reflex sympathetic dystrophy). Pain. 88:2000;259-266
19. Matsumo R., Aramaki Y., Arima H., Adachi Y., Ohno N., Yadomae T., Tsuchiya S. Contribution of CR3 to nitric oxide production from macrophages stimulated with high-dose of LPSA. Biochem Biophys Res Commun. 244:1998;115-119
20. Mendes A.F., Caramona M.M., Carvalho A.P., Lopes M.C. Differential roles of hydrogen peroxide and superoxide in mediating IL-1-induced NF-kappa B activation and iNOS expression in bovine articular chondrocytes. J Cell Biochem. 88:2003;783-793
21. Milligan E.D., Mehmert K.K., Hinde J.L., Harvey L.O., Martin D., Tracey K.J., Maier S.F., Watkins L.R. Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120. Brain Res. 861:2000;105-116
22. Milligan E.D., O'Connor K.A., Nguyen K.T., Armstrong C.B., Twining C., Gaykema R.P., Holguin A., Martin D., Maier S.F., Watkins L.R. Intrathecal HIV-1 envelope glycoprotein gp120 induces enhanced pain states mediated by spinal cord proinflammatory cytokines. J Neurosci. 21:2001;2808-2819
23. Milligan E.D., Twining C., Chacur M., Biedenkapp J., O'Connor K.A., Poole S., Tracey K.J., Martin D., Maier S.F., Watkins L.R. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain. J Neurosci. 23:2003;1026-1040
24. Milligan E.D., Maier S.F., Watkins L.R. Sciatic inflammatory neuropathy: a new model for studying neuropathic pain of inflammatory origin. Luo D. Pain research: methods and protocols; methods of molecular medicine. 2004;Humana Press, New York. p. 67-89
25. Monaco S., Ferrari S., Bonetti B., Moretto G., Kirshfink M., Nardelli E., Nobile-Orazio E., Zanusso G., Rizzuot N., Tedesco F. Experimental induction of myelin changes by anti-MAG antibodies and terminal complement complex. J Neuropathol Exp Neurol. 54:1995;96-104
26. Morgan B.P. Regulation of the complement membrane attack pathway. Crit Rev Immunol. 19:1999;173-198
27. Moriwaki K., Yuge O. Topographical features of cutaneous tactile hypoesthetic and hyperesthetic abnormalities in chronic pain. Pain. 81:1999;1-6
28. Murphy P.G., Ramer M.S., Borthwick L., Gauldie J., Richardson P.M., 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. 11:1999;2243-2253
29. Myers R.R., Heckman H.M., Rodriguez M. 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
30. Nakahara H., Song J., Sugimoto M., Hagihara K., Kishimoto T., Yoshizaki K., Nishimoto N. Anti-interleukin-6 receptor antibody therapy reduces vascular endothelial growth factor production in rheumatoid arthritis. Arthritis Rheum. 48:2003;1521-1529
31. Nicholson-Weller A., Halperin J.A. Membrane signaling by complement C5b-9, the membrane attack complex. Immunol Res. 12:1993;244-257
32. Ohta Y., Nishida K. Protective effect of coadministered superoxide dismutase and catalase against stress-induced gastric mucosal lesions. Clin Exp Pharmacol Physiol. 30:2003;545-550
33. Schafers M., Brinkhoff J., Neukirchen S., Marziniak M., Sommer C. Combined epineurial therapy with neutrlizing 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
34. 2-mediated complement activation and cytokines-mediated fibroblasts superoxide generation on skin inflammation. Dermatologica. 179:(Suppl 1):1989;107-112
35. Shingu M., Nonaka S., Nishimukai H., Nobunaga M., Kitamura H., Tomo-Oka K. Activation of complement in normal serum by hydrogen peroxide and hydrogen peroxide-related oxygen radicals produced by activated neutrophils. Clin Exp Immunol. 90:1992;72-78
36. Shir Y., Seltzer Z. Effects of sympathectomy in a model of causalgiform pain produced by partial sciatic nerve injury in rats. Pain. 45:1991;309-320
37. Slart R., Yu A.L., Yaksh T.L., Sorkin L.S. An animal model of pain produced by systemic administration of an immunotherapeutic anti-ganglioside antibody. Pain. 69:1997;119-125
38. Sommer C., Marziniak M., Myers R.R. The effect of thalidomide treatment on vascular pathology and hyperalgesia caused by chronic constriction injury of rat nerve. Pain. 74:1998;83-91
39. Sommer C., Petrausch S., Lindenlaub T., Toyka K.V. Neutralizing antibodies to interleukin-1 receptor reduce pain associated behavior in mice with experimental neuropathy. Neurosci Lett. 270:1999;25-28
40. Sommer C., Schafers M., Marziniak M., Toyka K.V. Etanercept reduces hyperalgesia in experimental painful neuropathy. J Peripheral Nerv Syst. 6:2001;67-72
41. Sredni-Kenigsbuch D., Kambayashi T., Strassmann G. Neutrophils augment the release of TNFalpha from LPS-stimulated macrophages via hydrogen peroxide. Immunol Lett. 71:2000;97-102
42. Syriatowicz J.P., Hu D., alker J.S., Trtacey D.J. Hyperalgesia due to nerve injury: role of prostaglandins. Neuroscience. 1999;94
43. Takao S., Smith E.H., Wang D., Chan C.K., Bulkley G.B., Klein A.S. Role of reactive oxygen metabolites in murine peritoneal macrophage phagocytosis and phagocytic killing. Am J Physiol. 271:1996;C1278-C1284
44. Tal M. A novel antioxidant alleviates heat hyperalgesia in rats with an experimental painful peripheral neuropathy. Neuroreport. 31:1996;1382-1384
45. Theodosiou M., Rush R.A., Zhou X.F., Hu D., Walker J.S., Tracey D.J. Hyperalgesia due to nerve damage: role of nerve growth factor. Pain. 81:1999;245-255
46. Thomas D.A., Ren K., Besse D., Ruda M.A., Dubner R. Application of nitric oxide synthase ihibitor, N-omega-nitro-L-arginine methyl ester, on injured nerve attenuates neuropathy-induced thermal hyperalgesia in rats. Neurosci Lett. 210:1996;124-126
47. Treutwein B., Strasburger H. Fitting the psychometric function. Percept Psychophys. 61:1999;87-106
48. Vanguri P., Koski C.L., Silverman B., Shin M.L. Complement activation by isolated myein: activation of the classical pathway in the absence of myelin-specific antibodies. Proc Natl Acad Sci. 79:1982;3290-3294
49. Wagner R., Myers R.R. Endoneurial injection of TNF-alpha produces neuropathic pain behaviors. NeuroResport. 7:1996;2897-2901
50. Wang T., Qin L., Liu B., Liu Y., Wilson B., Eling T.E., Langenbach R., Taniura S., Hong J.S. Role of reactive oxygen species in LPS-induced production of prostaglandin E2 in microglia. J Neurochem. 88:2004;939-947
51. Watkins L.R., Maier S.F. Beyond neurons: evidence that immune and glial cells contribute to pathological pain states. Physiol Rev. 82:2002;981-1011
52. Woda A., Pionchon P. A unified concept of idiopathic orofacial pain: pathophysiologic features. J Orofacial Pain. 14:2000;196-212
53. Woolf C.J., Salter M.W. Neuronal plasticity: increasing the gain in pain. Science. 288:2000;1765-1769
54. Yabe Y., Kobayashi N., Nishihashi T., Takahashi R., Nishikawa M., Takakura Y., Hashida M. Prevention of neutrophil-mediated hepatic ischemia/reperfusion injury by superoxide dismutase and catalase derivatives. J Pharmacol Exp Ther. 298:2001;894-899
55. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain. 16:1983;109-110
56. Zuo Y., Perkins N.M., Tracey D.J., Geczy C.L. Inflammation and hyperalgesia induced by nerve injury in the rat: a key role of mast cells. Pain. 105:2003;467-479