IL-1 receptor antagonist improves morphine and buprenorphine efficacy in a rat neuropathic pain model

European Journal of Pharmacology

Volumn 764, Issue , 2015, Pages 240-248

  Pilat, Dominika ^a   Rojewska, Ewelina ^a   Jurga, Agnieszka M ^a   Piotrowska, Anna ^a   Makuch, Wioletta ^a   Przewlocka, Barbara ^a   Mika, Joanna ^a  

^a INSTITUTE OF PHARMACOLOGY   (Poland)

Author keywords

IL 1 receptor antagonist; IL 1 receptor type I; IL 1alpha; IL 1beta; Neuropathic pain

Indexed keywords

BUPRENORPHINE; INTERLEUKIN 1 RECEPTOR BLOCKING AGENT; INTERLEUKIN 1 RECEPTOR TYPE I; INTERLEUKIN 1ALPHA; INTERLEUKIN 1BETA; MESSENGER RNA; MORPHINE; NARCOTIC ANALGESIC AGENT;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; MALE; NEUROPATHIC PAIN; NONHUMAN; PHOTOTRANSDUCTION; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SINGLE DRUG DOSE; UPREGULATION; WESTERN BLOTTING; ANIMAL; DRUG EFFECTS; GENETICS; HYPERALGESIA; INJURIES; METABOLISM; NEURALGIA; SCIATIC NERVE; SPINAL CORD; TREATMENT OUTCOME; WISTAR RAT;

ANALGESICS, OPIOID; ANIMALS; BUPRENORPHINE; HYPERALGESIA; INTERLEUKIN 1 RECEPTOR ANTAGONIST PROTEIN; INTERLEUKIN-1ALPHA; INTERLEUKIN-1BETA; MALE; MORPHINE; NEURALGIA; RATS, WISTAR; RNA, MESSENGER; SCIATIC NERVE; SPINAL CORD; TREATMENT OUTCOME;

EID: 84937604946     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.05.058     Document Type: Article

References (65)

1. G.J. Bennett, and Y.K. Xie A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man Pain 33 1988 87 107
2. P. Chomczynski, and N. Sacchi Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction Anal. Biochem. 162 1987 156 159
3. D.E. Coyle Partial peripheral nerve injury leads to activation of astroglia and microglia which parallels the development of allodynic behavior Glia 23 1998 75 83
4. Y. Cui, Y. Chen, J.L. Zhi, R.X. Guo, J.Q. Feng, and P.X. Chen Activation of p38 mitogen- activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance Brain Res. 1069 2006 235 243
5. M. Dorazil-Dudzik, J. Mika, M.K. Schafer, Y. Li, I. Obara, J. Wordliczek, and B. Przewlocka The effects of local pentoxifylline and propentofylline treatment on formalin-induced pain and tumor necrosis factor-alpha messenger RNA levels in the inflamed tissue of the rat paw Anesth. Analg. 98 2004 1566 1573
6. D. Giulian, T.J. Baker, L.C. Shih, and L.B. Lachman Interleukin 1 of the central nervous system is produced by ameboid microglia J. Exp. Med. 164 1986 594 604
7. H. Gul, O. Yildiz, A. Dogrul, O. Yesilyurt, and A. Isimer The interaction between IL-1beta and morphine: possible mechanism of the deficiency of morphine-induced analgesia in diabetic mice Pain 89 2000 39 45
8. U.K. Hanisch Microglia as a source and target of cytokines Glia 40 2002 140 155
9. H. Hashizume, J.A. DeLeo, R.W. Colburn, and J.N. Weinstein Spinal glial activation and cytokine expression after lumbar root injury in the rat Spine 25 2000 1206 1217
10. M.A. Hook, G. Moreno, S. Woller, D. Puga, K. Hoy Jr., R. Balden, and J.W. Grau Intrathecal morphine attenuates recovery of function after a spinal cord injury J. Neurotrauma 26 2009 741 752
11. M.A. Hook, S.N. Washburn, G. Moreno, S.A. Woller, D. Puga, K.H. Lee, and J.W. Grau An IL-1 receptor antagonist blocks a morphine-induced attenuation of locomotor recovery after spinal cord injury Brain Behav. Immun. 25 2011 349 359
12. S.J. Hopkins, and N.J. Rothwell Cytokines and the nervous system. I: Expression and recognition Trends Neurosci. 18 1995 83 88
13. A. Inoue, K. Ikoma, N. Morioka, K. Kumagai, T. Hashimoto, I. Hide, and Y. Nakata Interleukin-1beta induces substance P release from primary afferent neurons through the cyclooxygenase-2 system J. Neurochem. 73 1999 2206 2213
14. I.N. Johnston, E.D. Milligan, J. Wieseler-Frank, M.G. Frank, V. Zapata, J. Campisi, S. Langer, D. Martin, P. Green, M. Fleshner, L. Leinwand, S.F. Maier, and L.R. Watkins A role for proinflammatory cytokines and fractalkine in analgesia, tolerance and subsequent pain facilitation induced by chronic intrathecal morphine J. Neurosci. 24 2004 7353 7565
15. Y. Kawasaki, L. Zhang, J.K. Cheng, and R.R. Ji Cytokine mechanisms of central sensitization: distinct and overlapping role of interleukin-1beta, interleukin-6, and tumor necrosis factor-alpha in regulating synaptic and neuronal activity in the superficial spinal cord J. Neurosci. 28 2008 5189 5194
16. A. Ledeboer, E.M. Sloane, E.D. Milligan, M.G. Frank, J.H. Mahony, S.F. Maier, and L.R. Watkins Minocycline attenuates mechanical allodynia and proinflammatory cytokine expression in rat models of pain facilitation Pain 115 2005 71 83
17. C.H. Lu, P.C. Chao, C.O. Borel, C.P. Yang, C.C. Yeh, C.S. Wong, and C.T. Wu Preincisional intravenous pentoxifylline attenuating Perioperative cytokine response, reducing morphine consumption, and improving recovery of bowel function in patients undergoing colorectal cancer surgery Anesth. Analg. 99 2004 1465 1471
18. R. Lundblad, P. Ekstrom, and K.E. Giercksky Pentoxifylline improves survival and reduces tumor necrosis factor,interleukin-6, and endothelin-1 in fulminantintra-abdominalsepsisin rats Shock 3 1995 210 215
19. M. Malcangio, N.G. Bowery, R.J. Flower, and M. Perretti Effect of interleukin-1beta on the release of substance P from rat isolated spinal cord Eur. J. Pharmacol. 299 1996 113 118
20. J. Mao, B. Sung, R.R. Ji, and G. Lim Chronic morphine induces downregulation of spinal glutamate transporters: implications in morphine tolerance and abnormal pain sensitivity J. Neurosci. 22 2002 8312 8323
21. J. Mao, D.D. Price, and D.J. Mayer Mechanisms of hyperalgesia and morphine tolerance: a current view of their possible interactions Pain 62 1995 259 274
22. F. Marchand, M. Perretti, and S.B. McMahon Role of the immune system in chronic pain Nat. Rev. Neurosci. 6 2005 521 532
23. D.J. Mayer, J. Mao, J. Holt, and D.D. Price Cellular mechanisms of neuropathic pain, morphine tolerance, and their interactions Proc. Natl. Acad. Sci. USA 96 1999 7731 7736
24. D.J. Mayer, J. Mao, and D.D. Price The association of neuropathic pain, morphine tolerance and dependence, and the translocation of protein kinase C NIDA Res. Monogr. 147 1995 269 298
25. X.P. Mei, L. Chen, W. Wang, D. Wu, L.Y. Wang, T. Zhang, H. Zhang, L.X. Xu, and Y.Q. Li Combination of tramadol with minocycline exerted synergistic effects on a rat model of nerve injury-induced neuropathic pain Neurosignals 21 2013 184 196
26. X.P. Mei, Y. Sakuma, C. Xie, D. Wu, I. Ho, J. Kotani, and L.X. Xu Depressing Interleukin-1β contributed to the synergistic effects of tramadol and minocycline on spinal nerve ligation-induced neuropathic pain Neurosignals 22 2013 30 42
27. J. Mika, M. Korostynski, D. Kaminska, A. Wawrzczak-Bargiela, M. Osikowicz, W. Makuch, R. Przewlocki, and B. Przewlocka Interleukin-1 alpha has antiallodynic and antihyperalgesic activities in a rat neuropathic pain model Pain 138 2008 587 597
28. J. Mika, M. Osikowicz, W. Makuch, and B. Przewlocka Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain Eur. J. Pharmacol. 560 2007 142 149
29. J. Mika, A. Wawrzczak-Bargiela, M. Osikowicz, W. Makuch, and B. Przewlocka J Attenuation of morphine tolerance by minocycline and pentoxifylline in naive and neuropathic mice Brain Behav Immun. 23 2009 75 84
30. S. Nadeau, M. Filali, J. Zhang, B.J. Kerr, S. Rivest, D. Soulet, Y. Iwakura, J.P. de Rivero Vaccari, R.W. Keane, and S. Lacroix Functional recovery after peripheral nerve injury is dependent on the pro-inflammatory cytokines IL-1β and TNF: implications for neuropathic pain J. Neurosci. 31 2011 12533 12542
31. P. Neuner, G. Klosner, E. Schauer, M. Pourmojib, W. Macheiner, C. Grunwald, R. Knobler, A. Schwarz, T.A. Luger, and T. Schwarz Pentoxifylline in vivo downregulates the release of IL-1b, IL-6, IL-8, and tumor necrosis factor-a by human peripheral blood mononuclear cells Immunology 83 1994 262 267
32. O. Obreja, P.K. Rathee, K.S. Lips, C. Distler, and M. Kress IL-1beta potentiates heat-activated currents in rat sensory neurons: involvement of IL-1RI, tyrosine kinase, and protein kinase C FASEB J. 16 2002 1497 1503
33. T. Oka, S. Aou, and T. Hori Intracerebroventricular injection of interleukin-1beta induces hyperalgesia in rats Brain Res. 624 1993 61 68
34. A. Opree, and M. Kress Involvement of the proinflammatory cytokines tumor necrosis factor-alpha, IL-1beta, and IL-6 but not IL-8 in the development of heat hyperalgesia: effects on heat-evoked calcitonin gene-related peptide release from rat skin J. Neurosci. 20 2000 6289 6293
35. Z.G. Piao, I.H. Cho, C.K. Park, J.P. Hong, S.Y. Choi, S.J. Lee, S. Lee, K. Park, J.S. Kim, and S.B. Oh Activation of glia and microglial p38 MAPK in medullary dorsal horn contributes to tactile hypersensitivity following trigeminal sensory nerve injury Pain 121 2006 219 231
36. V. Raghavendra, M.D. Rutkowski, and J.A. DeLeo The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and shamoperated rats J. Neurosci. 22 2002 9980 9989
37. 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
38. J.K. Relton, and N.J. Rothwell Interleukin-1 receptor antagonist inhibits ischaemic and excitotoxic neuronal damage in the rat Brain Res. Bull. 29 1992 243 246
39. K. Ren, and R. Torres Role of interleukin-1 β during pain and inflammation Brain Res Rev. 60 57 2009 64
40. E. Rojewska, K. Popiolek-Barczyk, A.M. Jurga, W. Makuch, B. Przewlocka, and J. Mika Involvement of pro- and antinociceptive factors in minocycline analgesia in rat neuropathic pain model J. Neuroimmunol. 277 2014 57 66
41. N.J. Rothwell Neuroimmune interactions: the role of cytokines Br. J. Pharmacol. 121 1997 841 847
42. S. Rotshenker, S. Aamar, and V. Barak Interleukin-1 activity in lesioned nerve J. Neuroimmunol. 39 1992 75 80
43. M. Schafers, J. Brinkhoff, S. Neukirchen, M. Marziniak, and C. Sommer Combined epineural therapy with neutralizing 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
44. M. Schäfers, and L. Sorkin Effect of cytokines on neuronal excitability Neurosci. Lett. 437 2008 188 193
45. H.M. Schrijver, J.B. Crusius, B.M. Uitdehaag, M.A. Garcia, Gonzalez, P.J. Kostense, C.H. Polman, and A.S. Pena Association of interleukin-1beta and interleukin-1 receptor antagonist genes with disease severity in MS Neurology 5 1999 595 599
46. Y. Shavit, G. Wolf, I. Goshen, D. Livshits, and R. Yirmiya Interleukin-1 antagonizes morphine analgesia and underlies morphine tolerance Pain 115 2005 50 59
47. C. Sommer, S. Petrausch, T. Lindenlaub, and K.V. Toyka Neutralizing antibodies to interleukin-1 receptor reduce pain associated behavior in mice with experimental neuropathy Neurosci. Lett. 270 1999 25 28
48. P. Song, and Z.Q. Zhao The involvement of glial cells in the development of morphine tolerance Neurosci. Res. 39 2001 281 286
49. D. Stellwagen, E.C. Beattie, J.Y. Seo, and R.C. Malenka Differential regulation of AMPA receptor and GABA receptor trafficking by tumor necrosis factor-alpha J. Neurosci. 25 2005 3219 3228
50. B. Sung, G. Lim, and J. Mao Altered expression and uptake activity of spinal glutamate transporters after nerve injury contribute to the pathogenesis of neuropathic pain in rats J. Neurosci. 23 2003 2899 2910
51. C.S. Sung, Z.H. Wen, W.K. Chang, S.T. Ho, S.K. Tsai, Y.C. Chang, and C.S. Wong Intrathecal interleukin-1beta administration induces thermal hyperalgesia by activating inducible nitric oxide synthase expression in the rat spinal cord Brain Res. 1015 2004 145 153
52. 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
53. I. Szabo, X.H. Chen, L. Xin, M.W. Adler, O.M. Howard, J.J. Oppenheim, and T.J. Rogers Heterologous desensitization of opioid Receptors by chemokines inhibits chemotaxis and enhances the perception of pain Proc. Natl. Acad. Sci. USA 99 2002 10276 10281
54. A.M. Szczepanik, J. Wordliczek, W. Serednicki, M. Siedlar, and A. Czupryna Pentoxifylline does not affect nociception if administered postoperatively Pol. J. Pharmacol. 56 2004 611 616
55. O. Touzani, H. Boutin, J. Chuquet, and N. Rothwell Potential mechanisms of interleukin-1 involvement in cerebral ischaemia J. Neuroimmunol. 100 1999 203 215
56. A. Vezzani, M. Conti, A. De Luigi, T. Ravizza, D. Moneta, F. Marchesi, and M.G. De Simoni Interleukin-1beta immunoreactivity and microglia are enhanced in the rat hippocampus by focal kainate application: functional evidence for enhancement of electrographic seizures J. Neurosci. 19 1999 5054 5065
57. B. Viviani, S. Bartesaghi, F. Gardoni, A. Vezzani, M.M. Behrens, T. Bartfai, M. Binaglia, E. Corsini, M. Di Luca, C.L. Galli, and M. Marinovich Interleukin-1beta enhances NMDA receptor-mediated intracellular calcium increase through activation of the Src family of kinases J. Neurosci. 23 2003 8692 8700
58. L.R. Watkins, M.R. Hutchinson, I.N. Johnston, and S.F. Maier Glia: novel counterregulators of opioid analgesia Trends Neurosci. 28 2005 661 669
59. L.R. Watkins, M.R. Hutchinson, A. Ledeboer, J. Wieseler-Frank, E.D. Milligan, and S.F. Maier Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids Brain Behav. Immun. 21 2007 131 146
60. B.A. Winkelstein, M.D. Rutkowski, S.M. Sweitzer, J.L. Pahl, and J.A. DeLeo Nerve injury proximal or distal to the DRG induces similar spinal glial activation and selective cytokine expression but differential behavioral responses to pharmacologic treatment J. Comp. Neurol. 439 2001 127 139
61. W.J. Xin, H.R. Weng, and P.M. Dougherty Plasticity in expression of the glutamate transporters GLT-1 and GLAST in spinal dorsal horn glial cells following partial sciatic nerve ligation Mol. Pain 26 2009 5 15
62. T.L. Yaksh, and T.A. Rudy Chronic catheterization of the spinal subarachnoid space Physiol. Behav. 17 1976 1031 1036
63. L.P. Yan, Y.G. Liu, X.T. Wu, S.D. Li, and C. Ma Effect of electroacupuncture intervention on N-methyl-d-aspartic acid receptor expression in spinal cord in rats with chronic constrictive injury of the sciatic nerve Zhen Ci Yan Jiu 38 2013 380 385
64. T.M. Zanjani, M. Sabetkasaei, N. Mosaffa, H. Manaheji, F. Labibi, and B. Farokhi Suppression of interleukin- 6 by minocycline in a rat model of neuropathic pain Eur. J. Pharmacol. 538 2006 66 72
65. M. Zimmermann Ethical guidelines for investigations of experimental pain in conscious animals Pain 16 1983 109 110