Spinal interleukin-17 promotes thermal hyperalgesia and NMDA NR1 phosphorylation in an inflammatory pain rat model

Pain

Volumn 154, Issue 2, 2013, Pages 294-305

  Meng, Xianze ^a,b   Zhang, Yu ^c   Lao, Lixing ^b   Saito, Rikka ^b   Li, Aihui ^b   Bäckman, Cristina M ^d   Berman, Brian M ^b   Ren, Ke ^e   Wei, Pin Kang ^a   Zhang, Rui Xin ^b  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^c SHANXI MEDICAL UNIVERSITY   (China)

^d NATIONAL INSTITUTE ON DRUG ABUSE   (United States)

^e UNIVERSITY OF MARYLAND DENTAL SCHOOL   (United States)

Author keywords

Glial cells; Hyperalgesia; Inflammation; Interleukin 17; Pain; Spinal cord

Indexed keywords

FREUND ADJUVANT; GLIAL FIBRILLARY ACIDIC PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17 ANTIBODY; INTERLEUKIN 17 RECEPTOR; INTERLEUKIN 17 RECEPTOR A; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; HYBRIDIZATION; HYPERALGESIA; IMMUNOREACTIVITY; INFLAMMATORY PAIN; MALE; MYCOBACTERIUM TUBERCULOSIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; REAL TIME POLYMERASE CHAIN REACTION; SPINAL CORD; UPREGULATION;

EID: 84872685685     PISSN: 03043959     EISSN: 18726623     Source Type: Journal    
DOI: 10.1016/j.pain.2012.10.022     Document Type: Article

References (46)

1. B. Almolda, M. Costa, M. Montoya, B. Gonzalez, and B. Castellano Increase in Th17 and Treg lymphocytes and decrease of IL22 correlate with the recovery phase of acute EAE in rat PLoS One 6 2011 e27473
2. M. Costigan, A. Moss, A. Latremoliere, C. Johnston, M. Verma-Gandhu, T.A. Herbert, L. Barrett, G.J. Brenner, D. Vardeh, C.J. Woolf, and M. Fitzgerald T-cell infiltration and signaling in the adult dorsal spinal cord is a major contributor to neuropathic pain-like hypersensitivity J Neurosci 29 2009 14415 14422
3. L. Daulhac, V. Maffre, C. Mallet, M. Etienne, A.M. Privat, A. Kowalski-Chauvel, C. Seva, J. Fialip, and A. Eschalier Phosphorylation of spinal N-methyl-d-aspartate receptor NR1 subunits by extracellular signal-regulated kinase in dorsal horn neurons and microglia contributes to diabetes-induced painful neuropathy Eur J Pain 15 2011 169.e161-169.e112
4. A.H. Dickenson, and A.F. Sullivan Differential effects of excitatory amino acid antagonists on dorsal horn nociceptive neurones in the rat Brain Res 506 1990 31 39
5. F. Fossiez, O. Djossou, P. Chomarat, L. Flores-Romo, S. Ait-Yahia, C. Maat, J.J. Pin, P. Garrone, E. Garcia, S. Saeland, D. Blanchard, C. Gaillard, B. Das Mahapatra, E. Rouvier, P. Golstein, J. Banchereau, and S. Lebecque T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines J Exp Med 183 1996 2593 2603
6. S.L. Gaffen, J.M. Kramer, J.J. Yu, and F. Shen The IL-17 cytokine family L. Gerald, Vitamins and hormones vol. 74 2006 Academic Press 255 282
7. X. Gao, H.K. Kim, J.M. Chung, and K. Chung Enhancement of NMDA receptor phosphorylation of the spinal dorsal horn and nucleus gracilis neurons in neuropathic rats PAIN® 116 2005 62 72
8. W. Guo, H. Wang, M. Watanabe, K. Shimizu, S. Zou, S.C. LaGraize, F. Wei, R. Dubner, and K. Ren Glial-cytokine-neuronal interactions underlying the mechanisms of persistent pain J Neurosci 27 2007 6006 6018
9. K. Hargreaves, R. Dubner, F. Brown, C. Flores, and J. Joris A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia PAIN® 32 1988 77 88
10. J. Hartupee, C. Liu, M. Novotny, X. Li, and T. Hamilton IL-17 enhances chemokine gene expression through mRNA stabilization J Immunol 179 2007 4135 4141
11. N.Y. Hemdan, G. Birkenmeier, G. Wichmann, A.M. Abu El-Saad, T. Krieger, K. Conrad, and U. Sack Interleukin-17-producing T helper cells in autoimmunity Autoimmun Rev 9 2010 785 792
12. S. Henness, C. Johnson, Q. Ge, C.L. Armour, J.M. Hughes, and A.J. Ammit IL-17 augments TNF-α-induced IL-6 expression in airway smooth muscle by enhancing mRNA stability J Allergy Clin Immunol 114 2004 958 964
13. C.F. Kim, and G. Moalem-Taylor Interleukin-17 contributes to neuroinflammation and neuropathic pain following peripheral nerve injury in mice J Pain 12 2011 370 383
14. H.K. Kim, J.H. Kim, X. Gao, J.L. Zhou, I. Lee, K. Chung, and J.M. Chung Analgesic effect of vitamin E is mediated by reducing central sensitization in neuropathic pain PAIN® 122 2006 53 62
15. C. Kleinschnitz, H.H. Hofstetter, S.G. Meuth, S. Braeuninger, C. Sommer, and G. Stoll T cell infiltration after chronic constriction injury of mouse sciatic nerve is associated with interleukin-17 expression Exp Neurol 200 2006 480 485
16. A. Li, Y. Zhang, L. Lao, J. Xin, K. Ren, B.M. Berman, and R.X. Zhang Serotonin receptor 2A/C is involved in electroacupuncture inhibition of pain in an osteoarthritis rat model Evid Based Complement Altern Med 2011 2011 619650
17. G.Z. Li, D. Zhong, L.M. Yang, B. Sun, Z.H. Zhong, Y.H. Yin, J. Cheng, B.B. Yan, and H.L. Li Expression of interleukin-17 in ischemic brain tissue Scand J Immunol 62 2005 481 486
18. E. Lubberts Th17 cytokines and arthritis Semin Immunopathol 32 2010 43 53
19. K.E. McNamee, S. Alzabin, J.P. Hughes, P. Anand, M. Feldmann, R.O. Williams, and J.J. Inglis IL-17 induces hyperalgesia via TNF-dependent neutrophil infiltration PAIN® 152 2011 1838 1845
20. E.D. Milligan, C. Twining, M. Chacur, J. Biedenkapp, K. O'Connor, S. Poole, K. Tracey, D. Martin, S.F. Maier, and L.R. Watkins Spinal glia and proinflammatory cytokines mediate mirror-image neuropathic pain in rats J Neurosci 23 2003 1026 1040
21. A.C. Murphy, S.J. Lalor, M.A. Lynch, and K.H. Mills Infiltration of Th1 and Th17 cells and activation of microglia in the CNS during the course of experimental autoimmune encephalomyelitis Brain Behav Immun 24 2010 641 651
22. N. Noma, J. Khan, I.F. Chen, S. Markman, R. Benoliel, E. Hadlaq, Y. Imamura, and E. Eliav Interleukin-17 levels in rat models of nerve damage and neuropathic pain Neurosci Lett 493 2011 86 91
23. L.G. Pinto, T.M. Cunha, S.M. Vieira, H.P. Lemos, W.A. Verri Jr, F.Q. Cunha, and S.H. Ferreira IL-17 mediates articular hypernociception in antigen-induced arthritis in mice PAIN® 148 2010 247 256
24. V. Raghavendra, F. Tanga, and J.A. DeLeo 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
25. V. Raghavendra, F.Y. Tanga, and J.A. DeLeo Complete Freunds adjuvant-induced peripheral inflammation evokes glial activation and proinflammatory cytokine expression in the CNS Eur J Neurosci 20 2004 467 473
26. K. Ren, J.L.K. Hylden, G.M. Williams, M.A. Ruda, and R. Dubner The effects of a noncompetitiveNMDA receptor antagonist, MK-801, on behavioral hyperalgesia and dorsal horn neuronal activity in rats with unilateral inflammation PAIN® 50 1992 331 344
27. D.H. Roh, H.S. Seo, S.Y. Yoon, S. Song, H.J. Han, A.J. Beitz, and J.H. Lee Activation of spinal alpha-2 adrenoceptors, but not mu-opioid receptors, reduces the intrathecal N-methyl-d-aspartate-induced increase in spinal NR1 subunit phosphorylation and nociceptive behaviors in the rat Anesth Analg 110 2010 622 629
28. T.A. Samad, K.A. Moore, A. Sapirstein, S. Billet, A. Allchorne, S. Poole, J.V. Bonventre, and C.J. Woolf Interleukin-1beta-mediated induction of Cox-2 in the CNS contributes to inflammatory pain hypersensitivity Nature 410 2001 471 475
29. 4- lymphocytes during infection with Salmonella enterica serovar Enteritidis and has a mild effect in bacterial clearance Int Immunol 20 2008 1129 1138
30. T.P. Singh, B. Huettner, H. Koefeler, G. Mayer, I. Bambach, K. Wallbrecht, M.P. Schön, and P. Wolf Platelet-activating factor blockade inhibits the T-helper type 17 cell pathway and suppresses psoriasis-like skin disease in K5.hTGF-β1 transgenic mice Am J Pathol 178 2011 699 708
31. S. Sweitzer, D. Martin, and J.A. DeLeo Intrathecal interleukin-1 receptor antagonist in combination with soluble tumor necrosis factor receptor exhibits an anti-allodynic action in a rat model of neuropathic pain Neuroscience 103 2001 529 539
32. S.M. Sweitzer, R.W. Colburn, M. Rutkowski, and J.A. DeLeo 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
33. J.S. Tzartos, M.A. Friese, M.J. Craner, J. Palace, J. Newcombe, M.M. Esiri, and L. Fugger Interleukin-17 production in central nervous system-infiltrating T cells and glial cells is associated with active disease in multiple sclerosis Am J Pathol 172 2008 146 155
34. C. Ultenius, B. Linderoth, B.A. Meyerson, and J. Wallin Spinal NMDA receptor phosphorylation correlates with the presence of neuropathic signs following peripheral nerve injury in the rat Neurosci Lett 399 2006 85 90
35. D.D. Wang, Y.F. Zhao, G.Y. Wang, B. Sun, Q.F. Kong, K. Zhao, Y. Zhang, J.H. Wang, Y.M. Liu, L.L. Mu, D.S. Wang, and H.L. Li IL-17 potentiates neuronal injury induced by oxygen-glucose deprivation and affects neuronal IL-17 receptor expression J Neuroimmunol 212 2009 17 25
36. F. Wang, J. Flanagan, N. Su, L.C. Wang, S. Bui, A. Nielson, X. Wu, H.T. Vo, X.J. Ma, and Y. Luo RNAscope: a novel in situ RNA analysis platform for formalin-fixed, paraffin-embedded tissues J Mol Diagn 14 2012 22 29
37. L.R. Watkins, D. Martin, P. Ulrich, K.J. Tracey, and S.F. Maier Evidence for the involvement of spinal cord glia in subcutaneous formalin induced hyperalgesia in the rat PAIN® 71 1997 225 235
38. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial proinflammatory cytokines mediate exaggerated pain states: implications for clinical pain Adv Exp Med Biol 521 2003 1 21
39. Z. Yao, W.C. Fanslow, M.F. Seldin, A.M. Rousseau, S.L. Painter, M.R. Comeau, J.I. Cohen, and M.K. Spriggs Herpesvirus saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor Immunity 3 1995 811 821
40. Q.H. You, G.Y. Sun, N. Wang, J.L. Shen, and Y. Wang Interleukin-17F- induced pulmonary microvascular endothelial monolayer hyperpermeability via the protein kinase C pathway J Surg Res 162 2010 110 121
41. R.X. Zhang, L. Lao, L. Wang, B. Liu, X. Wang, K. Ren, and B.M. Berman Involvement of opioid receptors in electroacupuncture-produced anti-hyperalgesia in rats with peripheral inflammation Brain Res 1020 2004 12 17
42. R.X. Zhang, A. Li, B. Liu, L. Wang, K. Ren, H. Zhang, B.M. Berman, and L. Lao IL-1ra alleviates inflammatory hyperalgesia through preventing phosphorylation of NMDA receptor NR-1 subunit in rats PAIN® 135 2008 232 239
43. R.X. Zhang, H. Wang, M. Ruda, M.J. Iadarola, and J.T. Qiao C-Fos expression in NMDA receptor-contained neurons in spinal cord in a rat model of inflammation: a double immunocytochemical study Brain Res 795 1998 282 286
44. X. Zhang, J. Wu, Y. Lei, L. Fang, and W.D. Willis Protein phosphatase modulates the phosphorylation of spinal cord NMDA receptors in rats following intradermal injection of capsaicin Mol Brain Res 138 2005 264 272
45. X. Zou, Q. Lin, and W.D. Willis Enhanced phosphorylation of NMDA receptor 1 subunits in spinal cord dorsal horn and spinothalamic tract neurons after intradermal injection of capsaicin in rats J Neurosci 20 2000 6989 6997
46. X. Zou, Q. Lin, and W.D. Willis Effect of protein kinase C blockade on phosphorylation of NR1 in dorsal horn and spinothalamic tract cells caused by intradermal capsaicin injection in rats Brain Res 1020 2004 95 105