Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance

Brain Research

Volumn 1069, Issue 1, 2006, Pages 235-243

  Cui, Yu ^a   Chen, Yu ^b   Zhi, Jun Li ^a   Guo, Rui Xian ^a   Feng, Jian Qiang ^a   Chen, Pei Xi ^a  

^a SUN YAT SEN UNIVERSITY   (China)

^b SUN YAT SEN UNIVERSITY   (China)

Author keywords

Microglia; Morphine; p38 MAPK; Spinal cord; Tolerance

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; MITOGEN ACTIVATED PROTEIN KINASE P38; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MORPHINE;

ANALGESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; ASTROCYTE; CONTROLLED STUDY; DRUG TOLERANCE; ENZYME ACTIVATION; IMMUNOCOMPETENT CELL; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MALE; MICROGLIA; NERVE CELL; NONHUMAN; PRIORITY JOURNAL; RAT; SPINAL CORD;

ANALGESICS, OPIOID; ANALYSIS OF VARIANCE; ANIMALS; ANTIGENS, CD11B; BEHAVIOR, ANIMAL; CELL COUNT; DRUG ADMINISTRATION SCHEDULE; DRUG INTERACTIONS; ENZYME ACTIVATION; ENZYME INHIBITORS; GLIAL FIBRILLARY ACIDIC PROTEIN; IMIDAZOLES; IMMUNOHISTOCHEMISTRY; MALE; MICROGLIA; MORPHINE; MORPHINE DEPENDENCE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHOPYRUVATE HYDRATASE; PYRIDINES; RATS; RATS, SPRAGUE-DAWLEY; SPINAL CORD; TIME FACTORS;

ANIMALIA;

EID: 31344448048     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2005.11.066     Document Type: Article

References (50)

1. N.R. Bhat, P. Zhang, J.C. Lee, and E.L. Hogan Extracellular signal-regulated kinase and p38 subgroups of mitogen-activated protein kinases regulate inducible nitric oxide synthase and tumor necrosis factor-alpha gene expression in endotoxin-stimulated primary glial cultures J. Neurosci. 18 1998 1633 1641
2. J. Da Silva, B. Pierrat, J.L. Mary, and W. Lesslauer Blockade of p38 mitogen-activated protein kinase pathway inhibits inducible nitric-oxide synthase expression in mouse astrocytes J. Biol. Chem. 272 1997 28373 28380
3. J.A. DeLeo, R.W. Colburn, and A.J. Rickman Cytokine and growth factor immunohistochemical spinal profiles in two animal models of mononeuropathy Brain Res. 759 1997 50 57
4. G.H. Fan, L.Z. Wang, H.C. Qiu, L. Ma, and G. Pei Inhibition of calcium/calmodulin-dependent protein kinase II in rat hippocampus attenuates morphine tolerance and dependence Mol. Pharmacol. 56 1999 39 45
5. V. Granados-Soto, I. Kalcheva, X. Hua, A. Newton, and T.L. Yaksh Spinal PKC activity and expression: role in tolerance produced by continuous spinal morphine infusion Pain 85 2000 395 404
6. Z. Guan, S.Y. Buckman, A.P. Pentland, D.J. Templeton, and A.R. Morrison Induction of cyclooxygenase-2 by the activated MEKK1→SEK1/MKK4→p38 mitogen-activated protein kinase pathway J. Biol. Chem. 273 1998 12901 12908
7. U.K. Hanisch Microglia as a source and target of cytokines Glia 40 2002 140 155
8. R.R. Ji, T.A. Samad, S.X. Jin, R. Schmoll, and C.J. Woolf p38 MAPK activation by NGF in primary sensory neurons after inflammation increases TRPV1 levels and maintains heat hyperalgesia Neuron 36 2002 57 68
9. S.X. Jin, Z.Y. Zhuang, C.J. Woolf, and R.R. Ji 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. 23 2003 4017 4022
10. 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 7365
11. S.Y. Kim, J.C. Bae, J.Y. Kim, H.L. Lee, K.M. Lee, D.S. Kim, and H.J. Cho Activation of p38 MAP kinase in the rat dorsal root ganglia and spinal cord following peripheral inflammation and nerve injury NeuroReport 13 2002 2483 2486
12. J.C. Lee, J.T. Laydon, P.C. McDonnell, T.F. Gallagher, S. Kumar, D. Green, D. McNulty, M.J. Blumenthal, J.R. Heys, and S.W. Landvatter A protein kinase involved in the regulation of inflammatory cytokine biosynthesis Nature 372 1994 739 746
13. G. Lim, S. Wang, Q. Zeng, B. Sung, and J. Mao Evidence for a long-term influence on morphine tolerance after previous morphine exposure: role of neuronal glucocorticoid receptors Pain 114 2005 81 92
14. G. Lim, S. Wang, Q. Zeng, B. Sung, and J. Mao Spinal glucocorticoid receptors contribute to the development of morphine tolerance in rats Anesthesiology 102 2005 832 837
15. W. Ma, W.H. Zheng, K. Powell, K. Jhamandas, and R. Quirion Chronic morphine exposure increases the phosphorylation of MAP kinases and the transcription factor CREB in dorsal root ganglion neurons: an in vitro and in vivo study Eur. J. Neurosci. 14 2001 1091 1104
16. J. Mao NMDA and opioid receptors: their interactions in antinociception, tolerance and neuroplasticity Brain Res. Brain Res. Rev. 30 1999 289 304
17. 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, U. S. A. 96 1999 7731 7736
18. S.T. Meller, C. Dykstra, D. Grzybycki, S. Murphy, and G.F. Gebhart The possible role of glia in nociceptive processing and hyperalgesia in the spinal cord of the rat Neuropharmacology 33 1994 1471 1478
19. 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
20. E.D. Milligan, S.J. Langer, E.M. Sloane, L. He, J. Wieseler-Frank, K. O'Connor, D. Martin, J.R. Forsayeth, S.F. Maier, K. Johnson, R.A. Chavez, L.A. Leinwand, and L.R. Watkins Controlling pathological pain by adenovirally driven spinal production of the anti-inflammatory cytokine, interleukin-10 Eur. J. Neurosci. 21 2005 2136 2148
21. E.D. Milligan, E.M. Sloane, S.J. Langer, P.E. Cruz, M. Chacur, L. Spataro, J. Wieseler-Frank, S.E. Hammack, S.F. Maier, T.R. Flotte, J.R. Forsayeth, L.A. Leinwand, R. Chavez, and L.R. Watkins Controlling neuropathic pain by adeno-associated virus driven production of the anti-inflammatory cytokine, interleukin-10 Mol. Pain 1 2005 9
22. T. Mizushima, K. Obata, H. Yamanaka, Y. Dai, T. Fukuoka, A. Tokunaga, T. Mashimo, and K. Noguchi Activation of p38 MAPK in primary afferent neurons by noxious stimulation and its involvement in the development of thermal hyperalgesia Pain 113 2005 51 60
23. E.J. Nestler, and G.K. Aghajanian Molecular and cellular basis of addiction Science 278 1997 58 63
24. K. Ono, and J. Han The p38 signal transduction pathway: activation and function Cell Signalling 12 2000 1 13
25. K.J. Powell, A. Hosokawa, A. Bell, M. Sutak, B. Milne, R. Quirion, and K. Jhamandas Comparative effects of cyclo-oxygenase and nitric oxide synthase inhibition on the development and reversal of spinal opioid tolerance Br. J. Pharmacol. 127 1999 631 644
26. V. Raghavendra, M.D. Rutkowski, and J.A. DeLeo The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats J. Neurosci. 22 2002 9980 9989
27. 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
28. V. Raghavendra, F. Tanga, M.D. Rutkowski, and J.A. DeLeo Anti-hyperalgesic and morphine-sparing actions of propentofylline following peripheral nerve injury in rats: mechanistic implications of spinal glia and proinflammatory cytokines Pain 104 2003 655 664
29. V. Raghavendra, F.Y. Tanga, and J.A. DeLeo Attenuation of morphine tolerance, withdrawal-induced hyperalgesia, and associated spinal inflammatory immune responses by propentofylline in rats Neuropsychopharmacology 29 2004 327 334
30. J. Raingeaud, S. Gupta, J.S. Rogers, M. Dickens, J. Han, R.J. Ulevitch, and R.J. Davis Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine J. Biol. Chem. 270 1995 7420 7426
31. S.H. Ridley, J.L. Dean, S.J. Sarsfield, M. Brook, A.R. Clark, and J. Saklatvala A p38 MAP kinase inhibitor regulates stability of interleukin-1-induced cyclooxygenase-2 mRNA FEBS Lett. 439 1998 75 80
32. M.T. Santamarta, I. Ulibarri, and J. Pineda Inhibition of neuronal nitric oxide synthase attenuates the development of morphine tolerance in rats Synapse 57 2005 38 46
33. H. Schmidt, S. Schulz, M. Klutzny, T. Koch, M. Handel, and V. Hollt Involvement of mitogen-activated protein kinase in agonist-induced phosphorylation of the mu-opioid receptor in HEK 293 cells J. Neurochem. 74 2000 414 422
34. 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
35. P. Song, and Z.Q. Zhao The involvement of glial cells in the development of morphine tolerance Neurosci. Res. 39 2001 281 286
36. C.S. Sung, Z.H. Wen, W.K. Chang, K.H. Chan, S.T. Ho, S.H. Tsai, Y.C. Chang, and C.S. Wong Inhibition of p38 mitogen-activated protein kinase attenuates interleukin-1β-induced thermal hyperalgesia and inducible nitric oxide synthase expression in the spinal cord J. Neurochem. 94 2005 742 752
37. C.I. Svensson, X.Y. Hua, A.A. Protter, H.C. Powell, and T.L. Yaksh Spinal p38 MAP kinase is necessary for NMDA-induced spinal PGE(2) release and thermal hyperalgesia NeuroReport 14 2003 1153 1157
38. C.I. Svensson, M. Marsala, A. Westerlund, N.A. Calcutt, W.M. Campana, J.D. Freshwater, R. Catalano, Y. Feng, A.A. Protter, B. Scott, and T.L. Yaksh Activation of p38 mitogen-activated protein kinase in spinal microglia is a critical link in inflammation-induced spinal pain processing J. Neurochem. 86 2003 1534 1544
39. S.M. Sweitzer, M.C. Peters, J.Y. Ma, I. Kerr, R. Mangadu, S. Chakravarty, S. Dugar, S. Medicherla, A.A. Protter, and D.C. Yeomans Peripheral and central p38 MAPK mediates capsaicin-induced hyperalgesia Pain 111 2004 278 285
40. T. Tikka, B.L. Fiebich, G. Goldsteins, R. Keinanen, and J. Koistinaho Minocycline, a tetracycline derivative, is neuroprotective against excitotoxicity by inhibiting activation and proliferation of microglia J. Neurosci. 21 2001 2580 2588
41. L. Tong, S. Pav, D.M. White, S. Rogers, K.M. Crane, C.L. Cywin, M.L. Brown, and C.A. Pargellis A highly specific inhibitor of human p38 MAP kinase binds in the ATP pocket Nat. Struct. Biol. 4 1997 311 316
42. K.A. Trujillo, and H. Akil Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801 Science 251 1991 85 87
43. M. Tsuda, A. Mizokoshi, Y. Shigemoto-Mogami, S. Koizumi, and K. Inoue Activation of p38 mitogen-activated protein kinase in spinal hyperactive microglia contributes to pain hypersensitivity following peripheral nerve injury Glia 45 2004 89 95
44. V. Waetzig, K. Czeloth, U. Hidding, K. Mielke, M. Kanzow, S. Brecht, M. Goetz, R. Lucius, T. Herdegen, and U.K. Hanisch c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia Glia 30 2005 455 461
45. C. Watanabe, T. Sakurada, K. Okuda, C. Sakurada, R. Ando, and S. Sakurada The role of spinal nitric oxide and glutamate in nociceptive behaviour evoked by high-dose intrathecal morphine in rats Pain 106 2003 269 283
46. L.R. Watkins, and S.F. Maier Beyond neurons: evidence that immune and glial cells contribute to pathological pain states Physiol. Rev. 82 2002 981 1011
47. L.R. Watkins, E.D. Milligan, and S.F. Maier Glial activation: a driving force for pathological pain Trends Neurosci. 24 2001 450 455
48. L.R. Watkins, E.D. Milligan, and S.F. Maier Spinal cord glia: new players in pain Pain 93 2001 201 205
49. C. Widmann, S. Gibson, M.B. Jarpe, and G.L. Johnson Mitogen-activated protein kinase: conservation of a three-kinase module from yeast to human Physiol. Rev. 79 1999 143 180
50. Z.Y. Zhuang, P. Gerner, C.J. Woolf, and R.R. Ji ERK is sequentially activated in neurons, microglia, and astrocytes by spinal nerve ligation and contributes to mechanical allodynia in this neuropathic pain model Pain 114 2005 149 159