Morphological evidence for the involvement of microglial p38 activation in CGRP-associated development of morphine antinociceptive tolerance

Peptides

Volumn 31, Issue 12, 2010, Pages 2179-2184

  Wang, Zhiyong ^a   Ma, Weiya ^a   Chabot, Jean Guy ^a   Quirion, Rémi ^a  

^a DOUGLAS MENTAL HEALTH UNIVERSITY INSTITUTE   (Canada)

Author keywords

Calcitonin gene related peptide; Glia; Morphine; Phosphorylation

Indexed keywords

CALCITONIN GENE RELATED PEPTIDE; MORPHINE; OLCEGEPANT; SYNAPTOPHYSIN;

ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CELL COUNT; CHRONIC DRUG ADMINISTRATION; CONTROLLED STUDY; DOSE RESPONSE; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; HYPERTROPHY; IMMUNOCOMPETENT CELL; MALE; MICROGLIA; MORPHINE TOLERANCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; SPINAL CORD DORSAL HORN;

ANALGESICS, OPIOID; ANIMALS; CALCITONIN GENE-RELATED PEPTIDE; DRUG TOLERANCE; MALE; MICROGLIA; MORPHINE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PIPERAZINES; QUINAZOLINES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 78049460574     PISSN: 01969781     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.peptides.2010.08.020     Document Type: Article

References (35)

1. L.M. Bohn, R.R. Gainetdinov, F.T. Lin, R.J. Lefkowitz, and M.G. Caron Mu-opioid receptor desensitization by beta-arrestin-2 determines morphine tolerance but not dependence Nature 408 2000 720 723
2. S.D. Brain, and A.D. Grant Vascular actions of calcitonin gene-related peptide and adrenomedullin Physiol Rev 84 2004 903 934
3. Y. Chen, C. Geis, and C. Sommer Activation of TRPV1 contributes to morphine tolerance: involvement of the mitogen-activated protein kinase signaling pathway J Neurosci 28 2008 5836 5845
4. K. Chung, W.T. Lee, and S.M. Carlton The effects of dorsal rhizotomy and spinal cord isolation on calcitonin gene-related peptide-labeled terminals in the rat lumbar dorsal horn Neurosci Lett 90 1988 27 32
5. 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
6. Y. Cui, X.X. Liao, W. Liu, R.X. Guo, Z.Z. Wu, and C.M. Zhao A novel role of minocycline: attenuating morphine antinociceptive tolerance by inhibition of p38 MAPK in the activated spinal microglia Brain Behav Immun 22 2008 114 123
7. S. De Biasi, and A. Rustioni Glutamate and substance P coexist in primary afferent terminals in the superficial laminae of spinal cord Proc Natl Acad Sci USA 85 1988 7820 7824
8. B.N. Evans, M.I. Rosenblatt, L.O. Mnayer, K.R. Oliver, and I.M. Dickerson CGRP-RCP, a novel protein required for signal transduction at calcitonin gene-related peptide and adrenomedullin receptors J Biol Chem 275 2000 31438 31443
9. L.R. Gardell, R. Wang, S.E. Burgess, M.H. Ossipov, T.W. Vanderah, and T.P. Malan Jr. Sustained morphine exposure induces a spinal dynorphin-dependent enhancement of excitatory transmitter release from primary afferent fibers J Neurosci 22 2002 6747 6755
10. T. Hokfelt, U. Arvidsson, S. Ceccatelli, R. Cortes, S. Cullheim, and A. Dagerlind Calcitonin gene-related peptide in the brain, spinal cord, and some peripheral systems Ann N Y Acad Sci 657 1992 119 134
11. I. Kangrga, J.S. Larew, and M. Randic The effects of substance P and calcitonin gene-related peptide on the efflux of endogenous glutamate and aspartate from the rat spinal dorsal horn in vitro Neurosci Lett 108 1990 155 160
12. T. King, M.H. Ossipov, T.W. Vanderah, F. Porreca, and J. Lai Is paradoxical pain induced by sustained opioid exposure an underlying mechanism of opioid antinociceptive tolerance? Neurosignals 14 2005 194 205
13. P. Le Greves, F. Nyberg, T. Hokfelt, and L. Terenius Calcitonin gene-related peptide is metabolized by an endopeptidase hydrolyzing substance P Regul Pept 25 1989 277 286
14. 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
15. J. Mao, D.D. Price, and D.J. Mayer Thermal hyperalgesia in association with the development of morphine tolerance in rats: roles of excitatory amino acid receptors and protein kinase C J Neurosci 14 1994 2301 2312
16. 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
17. D.P. Menard, D. van Rossum, S. Kar, S. St Pierre, M. Sutak, and K. Jhamandas A calcitonin gene-related peptide receptor antagonist prevents the development of tolerance to spinal morphine analgesia J Neurosci 16 1996 2342 2351
18. F. Nyberg, P. Le Greves, and L. Terenius Modulation of endopeptidase activity by calcitonin gene related peptide: a mechanism affecting substance P action? Biochimie 70 1988 65 68
19. N. Parameswaran, J. Disa, W.S. Spielman, D.P. Brooks, P. Nambi, and N. Aiyar Activation of multiple mitogen-activated protein kinases by recombinant calcitonin gene-related peptide receptor Eur J Pharmacol 389 2000 125 130
20. K.J. Powell, W. Ma, M. Sutak, H. Doods, R. Quirion, and K. Jhamandas Blockade and reversal of spinal morphine tolerance by peptide and non-peptide calcitonin gene-related peptide receptor antagonists Br J Pharmacol 131 2000 875 884
21. K.J. Powell, R. Quirion, and K. Jhamandas Inhibition of neurokinin-1-substance P receptor and prostanoid activity prevents and reverses the development of morphine tolerance in vivo and the morphine-induced increase in CGRP expression in cultured dorsal root ganglion neurons Eur J Neurosci 18 2003 1572 1583
22. J. Priller, C.A. Haas, M. Reddington, and G.W. Kreutzberg Calcitonin gene-related peptide and ATP induce immediate early gene expression in cultured rat microglial cells Glia 15 1995 447 457
23. 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
24. 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
25. M. Reddington, J. Priller, J. Treichel, C. Haas, and G.W. Kreutzberg Astrocytes and microglia as potential targets for calcitonin gene related peptide in the central nervous system Can J Physiol Pharmacol 73 1995 1047 1049
26. M.G. Rosenfeld, S.G. Amara, and R.M. Evans Alternative RNA processing: determining neuronal phenotype Science 225 1984 1315 1320
27. P. Song, and Z.Q. Zhao The involvement of glial cells in the development of morphine tolerance Neurosci Res 39 2001 281 286
28. R.Q. Sun, Y.J. Tu, N.B. Lawand, J.Y. Yan, Q. Lin, and W.D. Willis Calcitonin gene-related peptide receptor activation produces PKA- and PKC-dependent mechanical hyperalgesia and central sensitization J Neurophysiol 92 2004 2859 2866
29. Y.H. Tai, Y.H. Wang, R.Y. Tsai, J.J. Wang, P.L. Tao, and T.M. Liu Amitriptyline preserves morphine's antinociceptive effect by regulating the glutamate transporter GLAST and GLT-1 trafficking and excitatory amino acids concentration in morphine-tolerant rats Pain 129 2007 343 354
30. T. Trang, W. Ma, J.G. Chabot, R. Quirion, and K. Jhamandas Spinal modulation of calcitonin gene-related peptide by endocannabinoids in the development of opioid physical dependence Pain 126 2006 256 271
31. K.A. Trujillo, and H. Akil Inhibition of morphine tolerance and dependence by the NMDA receptor antagonist MK-801 Science 251 1991 85 87
32. Z. Wang, W. Ma, J.G. Chabot, and R. Quirion Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia FASEB J 23 2009 2576 2586
33. Z.Y. Wang, Y.Q. Zhang, and Z.Q. Zhao Inhibition of tetanically sciatic stimulation-induced LTP of spinal neurons and Fos expression by disrupting glutamate transporter GLT-1 Neuropharmacology 51 2006 764 772
34. L.R. Watkins, M.R. Hutchinson, I.N. Johnston, and S.F. Maier Glia: novel counter-regulators of opioid analgesia Trends Neurosci 28 2005 661 669
35. L.R. Watkins, M.R. Hutchinson, A. Ledeboer, J. Wieseler-Frank, E.D. Milligan, and S.F. Maier Norman Cousins Lecture. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids Brain Behav Immun 21 2007 131 146