Peri-sciatic administration of recombinant rat IL-1β induces mechanical allodynia by activation of src-family kinases in spinal microglia in rats

Experimental Neurology

Volumn 234, Issue 2, 2012, Pages 389-397

  Wei, Xu Hong ^a   Yang, Tao ^a,b   Wu, Qiang ^a   Xin, Wen Jun ^a   Wu, Jin Lang ^a   Wang, Ya Qiong ^a   Zang, Ying ^a   Wang, Jun ^a   Li, Yong Yong ^a   Liu, Xian Guo ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN MEMORIAL HOSPITAL OF SUN YAT SEN UNIVERSITY   (China)

Author keywords

IL 1 ; Microglia; Neuropathic pain; Spinal cord; Src family kinase

Indexed keywords

4 AMINO 7 TERT BUTYL 5 (4 CHLOROPHENYL)PYRAZOLO[3,4 D]PYRIMIDINE; BIOLOGICAL MARKER; CELL PROTEIN; MINOCYCLINE; PROTEIN IBA1; PROTEIN TYROSINE KINASE; RECOMBINANT INTERLEUKIN 1BETA; UNCLASSIFIED DRUG;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL BEHAVIOR; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CELL DAMAGE; CELL FUNCTION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DEMYELINATION; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MECHANICAL ALLODYNIA; MICROGLIA; MYELINATED NERVE; NOCICEPTION; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SCHWANN CELL; SCIATIC NERVE; SPINAL CORD DORSAL HORN; SPINAL MICROGLIA;

ANIMALS; HYPERALGESIA; INTERLEUKIN-1BETA; MALE; MICROGLIA; PAIN MEASUREMENT; PAIN THRESHOLD; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; SPINAL CORD; SRC-FAMILY KINASES;

EID: 84862815372     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2012.01.001     Document Type: Article

References (41)

1. Binshtok A.M., Wang H., Zimmermann K., Amaya F., Vardeh D., Shi L., Brenner G.J., Ji R.R., Bean B.P., Woolf C.J., Samad T.A. Nociceptors are interleukin-1beta sensors. J. Neurosci. 2008, 28:14062-14073.
2. 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 2001, 94:231-244.
3. 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. Meth. 1994, 53:55-63.
4. Chang Y.W., Tan A., Saab C., Waxman S. Unilateral focal burn injury is followed by long-lasting bilateral allodynia and neuronal hyperexcitability in spinal cord dorsal horn. J. Pain 2010, 11:119-130.
5. Cunha J.M., Cunha F.Q., Poole S., Ferreira S.H. Cytokine-mediated inflammatory hyperalgesia limited by interleukin-1 receptor antagonist. Br. J. Pharmacol. 2000, 130:1418-1424.
6. DeLeo J.A., Coombs D.W., Willenbring S., Colburn R.W., Fromm C., Wagner R., Twitchell B.B. Characterization of a neuropathic pain model: sciatic cryoneurolysis in the rat. Pain 1994, 56:9-16.
7. DeLeo J.A., Yezierski R.P. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 2001, 90:1-6.
8. Eliav E., Herzberg U., Ruda M.A., Bennett G,.J. Neuropathic pain from an experimental neuritis of the rat sciatic nerve. Pain 1999, 83:169-182.
9. Ferreira S.H., Lorenzetti B.B., Bristow A.F., Poole S. Interleukin-1 beta as a potent hyperalgesic agent antagonized by a tripeptide analogue. Nature 1988, 334:698-700.
10. Freudenburg W., Buller R.M., Corbett J.A. Src family kinases participate in the regulation of encephalomyocarditis virus-induced cyclooxygenase-2 expression by macrophages. J. Gen. Virol. 2010, 91:2278-2285.
11. Fukuoka H., Kawatani M., Hisamitsu T., Takeshige C. Cutaneous hyperalgesia induced by peripheral injection of interleukin-1 beta in the rat. Brain Res. 1994, 657:133-140.
12. He X.H., Zang Y., Chen X., Pang R.P., Xu J.T., Zhou X., Wei X.H., Li Y.Y., Xin W.J., Qin Z.H., Liu X.G. TNF-alpha contributes to up-regulation of Nav1.3 and Nav1.8 in DRG neurons following motor fiber injury. Pain 2010, 151:266-279.
13. Jin S.X., Zhuang Z.Y., Woolf C.J., Ji R.R. p38 mitogen-activated protein kinase is activated after a spinal nerve ligation in spinal cord microglia and dorsal root ganglion neurons and contributes to the generation of neuropathic pain. J. Neurosci. 2003, 23:4017-4022.
14. Katsura H., Obata K., Mizushima T., Sakurai J., Kobayashi K., Yamanaka H., Dai Y., Fukuoka T., Sakagami M., Noguchi K. Activation of Src-family kinases in spinal microglia contributes to mechanical hypersensitivity after nerve injury. J. Neurosci. 2006, 26:8680-8690.
15. Kim S.H., Chung J.M. An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. Pain 1992, 50(3):355-363.
16. Liu Y.L., Zhou L.J., Hu N.W., Xu J.T., Wu C.Y., Zhang T., Li Y.Y., Liu X.G. Tumor necrosis factor-alpha induces long-term potentiation of C-fiber evoked field potentials in spinal dorsal horn in rats with nerve injury: the role of NF-kappa B, JNK and p38 MAPK. Neuropharmacology 2007, 52:708-715.
17. Marchand F., Perretti M., McMahon S.B. Role of the immune system in chronic pain. Nat. Rev. Neurosci. 2005, 6:521-532.
18. Milligan E.D., Twining C., Chacur M., Biedenkapp J., O'Connor K., Poole S., Tracey K., Martin D., Maier S.F., Watkins L.R. Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats. J. Neurosci. 2003, 23:1026-1040.
19. Ozaktay A.C., Kallakuri S., Takebayashi T., Cavanaugh J.M., Asik I., DeLeo J.A., Weinstein J.N. Effects of interleukin-1 beta, interleukin-6, and tumor necrosis factor on sensitivity of dorsal root ganglion and peripheral receptive fields in rats. Eur. Spine J. 2006, 15:1529-1537.
20. Poole S., Cunha F.Q., Ferreira S.H. Hyperalgesia from subcutaneous cytokines. Birkhar̈user, Basel: Cytokines and pain 1999, 59-87. S.F. Maier (Ed.).
21. Reeve A.J., Patel S., Fox A., Walker K., Urban L. Intrathecally administered endotoxin or cytokines produce allodynia, hyperalgesia and changes in spinal cord neuronal responses to nociceptive stimuli in the rat. Eur. J. Pain 2000, 4:247-257.
22. Safieh-Garabedian B., Poole S., Allchorne A., Winter J., Woolf C.J. Contribution of interleukin-1 beta to the inflammation-induced increase in nerve growth factor levels and inflammatory hyperalgesia. Br. J. Pharmacol. 1995, 115:1265-1275.
23. Seltzer Z., Dubner R., Shir Y. A novel behavioral model of neuropathic pain disorders produced in rats by partial sciatic nerve injury. Pain 1990, 43:205-218.
24. Skubitz K.M., Campbell K.D., Skubitz A.P. CD50 monoclonal antibodies inhibit neutrophil activation. J. Immunol. 1997, 159:820-828.
25. Spataro L.E., Sloane E.M., Milligan E.D., Wieseler-Frank J., Schoeniger D., Jekich B.M., Barrientos R.M., Maier S.F., Watkins L.R. Spinal gap junctions: potential involvement in pain facilitation. J. Pain 2004, 5:392-405.
26. Tal M., 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 1994, 57:375-382.
27. Twining C.M., Sloane E.M., Milligan E.D., Chacur M., Martin D., Poole S., Marsh H., Maier S.F., Watkins L.R. Peri-sciatic proinflammatory cytokines, reactive oxygen species, and complement induce mirror-image neuropathic pain in rats. Pain 2004, 110:299-309.
28. Wang H., Bloom O., Zhang M., Vishnubhakat J.M., Ombrellino M., Che J., Frazier A., Yang H., Ivanova S., Borovikova L., Manogues K.R., Faist E., Abraham E., Andersson J., Andesson U., Molina P.E., Abumrad N.N., Sama A., Tracey K.J. HMG-1 as a later mediator of endotoxin lethality in mice. Science 1999, 285:248-251.
29. Watkins L.R., Maier S.F. Glia: a novel drug discovery target for clinical xpain. Nat. Rev. Drug Discov. 2003, 2:973-985.
30. Watkins L.R., Milligan E.D., Maier S.F. Spinal cord glia: new players in pain. Pain 2001, 93:201-205.
31. Wei X.H., Zang Y., Wu C.Y., Xu J.T., Xin W.J., Liu X.G. Peri-sciatic administration of recombinant rat TNF-alpha induces mechanical allodynia via upregulation of TNF-alpha in dorsal root ganglia and in spinal dorsal horn: the role of NF-kappa B pathway. Exp. Neurol. 2007, 205:471-484.
32. Wen Y.R., Tan P.H., Cheng J.K., Liu Y.C., Ji R.R. Microglia: a promising target for treating neuropathic and postoperative pain, and morphine tolerance. J. Formos. Med. Assoc. 2011, 110:487-494.
33. Willis W.D. Long-term potentiation in spinothalamic neurons. Brain Res. Brain Res. Rev. 2002, 40:202-214.
34. Xu J.T., Xin W.J., Zang Y., Wu C.Y., Liu X.G. The role of tumor necrosis factor-alpha in the neuropathic pain induced by lumbar 5 ventral root transection in rat. Pain 2006, 123:306-321.
35. Zang Y., He X.H., Xin W.J., Pang R.P., Wei X.H., Zhou L.J., Li Y.Y., Liu X.G. Inhibition of NF-kappaB prevents mechanical allodynia induced by spinal ventral root transection and suppresses the re-expression of Nav1.3 in DRG neurons in vivo and in vitro. Brain Res. 2010, 1363:151-158.
36. Zhou L.J., Yang T., Wei X., Liu Y., Xin W.J., Chen Y., Pang R.P., Zang Y., Li Y.Y., Liu X.G. Brain-derived neurotrophic factor contributes to spinal long-term potentiation and mechanical hypersensitivity by activation of spinal microglia in rat. Brain Behav. Immun. 2010, 25:322-334.
37. Zhuang Z.Y., Gerner P., Woolf C.J., Ji R.R. ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model. Pain 2005, 114:149-159.
38. Zelenka M., Schäfers M., 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 2005, 116:257-263.
39. Zhong Y., Zhou L.J., Ren W.J., Xin W.J., Li Y.Y., Zhang T., Liu X.G. Interleukin-1b induces long-term potentiation of C-fiber evoked field potentials in spinal dorsal horn in rats with neuropathic pain. Open Pain J. 2009, 2:18-23.
40. Zhong Y., Zhou L.J., Ren W.J., Xin W.J., Li Y.Y., Zhang T., Liu X.G. The direction of synaptic plasticity mediated by C-fibers in spinal dorsal horn is decided by Src-family kinases in microglia: the role of tumor necrosis factor-alpha. Brain Behav. Immun. 2010, 24:874-880.
41. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.