Repeated morphine treatment-mediated hyperalgesia, allodynia and spinal glial activation are blocked by co-administration of a selective cannabinoid receptor type-2 agonist

Journal of Neuroimmunology

Volumn 244, Issue 1-2, 2012, Pages 23-31

  Tumati, Suneeta ^a   Largent Milnes, Tally M ^a   Keresztes, Attila ^a   Ren, Jiyang ^a   Roeske, William R ^a,c   Vanderah, Todd W ^a,b   Varga, Eva V ^a,b,c  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

Author keywords

Allodynia; CB2 agonist; Hyperalgesia; Morphine; Pain sensitization; Spinal glia

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 3 (2 IODO 5 NITROBENZOYL) 1 (1 METHYL 2 PIPERIDINYLMETHYL)INDOLE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; INTERLEUKIN 1BETA; MORPHINE SULFATE; TUMOR NECROSIS FACTOR ALPHA;

ADULT ANIMAL; ALLODYNIA; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; CONTROLLED STUDY; FEMALE; GLIA; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; NONHUMAN; PHARMACOLOGICAL BLOCKING; PRIORITY JOURNAL; RAT; SPINAL CORD; SPINAL GLIA;

ANALGESICS; ANALGESICS, OPIOID; ANIMALS; CANNABINOIDS; HYPERALGESIA; INDOLES; INFLAMMATION; INTERLEUKIN-1BETA; MALE; MORPHINE; NEUROGLIA; PAIN; PIPERIDINES; PYRAZOLES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB2; SPINAL CORD; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84857919068     PISSN: 01655728     EISSN: 18728421     Source Type: Journal    
DOI: 10.1016/j.jneuroim.2011.12.021     Document Type: Article

References (47)

1. Arner S., Rawal N., Gustafsson L.L. Clinical experience of long-term treatment with epidural and intrathecal opioids - a nationwide survey. Acta Anaesthesiol. Scand. 1988, 32:253-259.
2. Beltramo M. Cannabinoid type 2 receptor as a target for chronic pain. Mini Rev. Med. Chem. 2009, 9:11-25.
3. Chang S.L., Sharp B.M., Madden J.J. Cellular mechanisms involved in the modulation of the immune system by drugs of abuse. Adv. Exp. Med. Biol. 1998, 437:1-12.
4. 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. Methods 1994, 53:55-63.
5. Cichewicz D.L., Welch S.P. Modulation of oral morphine antinociceptive tolerance and naloxone-precipitated withdrawal signs by oral Delta 9-tetrahydrocannabinol. J. Pharmacol. Exp. Ther. 2003, 305:812-817.
6. Cui Y., Y, Zhi J.L., Guo R.X., Feng J.Q., Chen P.X. Activation of p38 mitogen-activated protein kinase in spinal microglia mediates morphine antinociceptive tolerance. Brain Res. 2006, 1069:235-243.
7. DeLeo J.A., Yezierski R.P. The role of neuroinflammation and neuroimmune activation in persistent pain. Pain 2001, 90:1-6.
8. Dixon W.J. Efficient analysis of experimental observations. Annu. Rev. Pharmacol. Toxicol. 1980, 20:441-462.
9. Ehrhart J., Obregon D., Mori T., Hou H., Sun N., Bai Y., Klein T., Fernandez F., Tan J., Shytle R.D. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J. Neuroinflammation 2005, 2:29-35.
10. Eljaschewitsch E., Witting A., Mawrin C., Lee T., Schmidt P.M., Wolf S., Hoertnagl H., Raine C.S., Schneider-Stock R., Nitsch R., Ullrich O. The endocannabinoid anandamide protects neurons during CNS inflammation by induction of MKP-1 in microglial cells. Neuron 2006, 49:67-79.
11. Fernández-Ruiz J., Romero J., Velasco G., Tolón R.M., Ramos J.A., Guzmán M. Cannabinoid CB2 receptor: a new target for controlling neural cell survival?. Trends Pharmacol. Sci. 2007, 28:39-45.
12. Gardell L.R., Wang R., Burgess S.E., Ossipov M.H., Vanderah T.W., Malan T.P., Lai J., Porreca F. Sustained morphine exposure induces a spinal dynorphin-dependent enhancement of excitatory transmitter release from primary afferent fibers. J. Neurosci. 2002, 22:6747-6755.
13. Hargreaves K., Dubner R., Brown F., Flores C., Joris J. A new and sensitive method for measuring thermal nociception in cutaneous hyperalgesia. Pain 1988, 32:77-88.
14. Hou L., Li W., Wang X. Mechanism of IL-1β-induced CGRP peptide production from DRG neurons of neonatal rats. J. Neurosci. Res. 2003, 73:188-197.
15. Hulsebosch C.E. Gliopathy ensures persistent inflammation and chronic pain after spinal cord injury. Exp. Neurol. 2008, 214:6-9.
16. Hutchinson M.R., Bland S.T., Johnson K.W., Rice K.C., Maier S.F., Watkins L.R. Opioid-induced glial activation: mechanisms of activation and implications for opioid analgesia, dependence, and reward. Sci. World J. 2007, 7:98-111.
17. Ibrahim M.M., Deng H., Zvonok A., Cockayne D.A., Kwan J., Mata H.P., Vanderah T.W., Lai J., Porreca F., Makriyannis A., Malan T.P. Activation of CB2 cannabinoid receptors by AM 1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. Proc. Natl. Acad. Sci. U S A 2003, 100:10529-10533.
18. Ibrahim M.M., Rude M.L., Stagg N.J., Mata H.P., Lai J., Vanderah T.W., Porreca F., Buckley N.E., Makriyannis A., Malan T.P. CB2 cannabinoid receptor mediation of antinociception. Pain 2006, 122:36-42.
19. Ji R.R., Strichartz G. Cell signaling and the genesis of neuropathic pain. Sci. STKE 2004, 21:E14.
20. Johnston I.N., Milligan E.D., Wieseler-Frank J., Frank M.G., Zapata V., Campisi J., Langer S., Martin D., Green P., Fleshner M., Leinwand L., Maier S.F., Watkins L.R. A role for proinflammatory cytokines and fractalkine in analgesia, tolerance, and subsequent pain facilitation induced by chronic intrathecal morphine. J. Neurosci. 2004, 24:7353-7365.
21. Li X., Angst M.S., Clark J.D. A murine model of opioid-induced hyperalgesia. Mol. Brain Res. 2001, 86:56-62.
22. Lim G., Wang S., Mao J. Central glucocorticoid receptors modulate the expression of spinal cannabinoid receptors induced by chronic morphine exposure. Brain Res. 2005, 1059:20-27.
23. Lozano-Ondoua A.N., Wright C., Vardanyan A., King T., Largent-Milnes T.M., Nelson M., Jimenez-Andrade J.M., Mantyh P.W., Vanderah T.W. A Cannabinoid 2 receptor agonist attenuates bone cancer-induced pain and bone loss. Life Sci. 2010, 86:646-653.
24. Mahajan S.D., Schwartz S.A., Aalinkeel R., Chawda R.P., Sykes D.E., Nair M.P. Morphine modulates chemokine gene regulation in normal human astrocytes. Clin. Immunol. 2005, 115:323-332.
25. Mao J., Price D.D., Mayer D.J. Thermal hyperalgesia in association with the development of morphine tolerance in rats: roles of excitatory amino acid receptors and protein kinase C. J. Neurosci. 1994, 14:2301-2312.
26. Maresz K., Carrier E.J., Ponomarev E.D., Hillard C.J., Ditte l B.N. Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J. Neurochem. 2005, 95:437-445.
27. Mika J. Modulation of microglia can attenuate neuropathic pain symptoms and enhance morphine effectiveness. Pharmacol. Rep. 2008, 60:297-307.
28. Mika J., Osikowicz M., Makuch W., Przewlocka B. Minocycline and pentoxifylline attenuate allodynia and hyperalgesia and potentiate the effects of morphine in rat and mouse models of neuropathic pain. Eur. J. Pharmacol. 2007, 560:142-149.
29. Moulédous L., Diaz M.F., Gutstein H.B. Modulation of extracellular signal-regulated kinase (ERK) activity by acute and chronic opioid treatment in neuronal and glial cell lines. J. Neurochem. 2004, 90:1371-1377.
30. Ossipov M.H., Lai J., King T., Vanderah T.W., Porreca F. Underlying mechanisms of pronociceptive consequences of prolonged morphine exposure. Biopolymers 2005, 80:319-324.
31. Pocock J.M., Kettenmann H. Neurotransmitter receptors on microglia. Trends Neurosci. 2007, 30:527-535.
32. Raghavendra V., Rutkowsk i M.D., DeLeo J.A. The role of spinal neuroimmune activation in morphine tolerance/hyperalgesia in neuropathic and sham-operated rats. J. Neurosci. 2002, 22:9980-9989.
33. Raghavendra V., Tanga F., DeLeo J.A. Inhibition of microglial activation attenuates the development but not existing hypersensitivity in a rat model of neuropathy. J. Pharmacol. Exp. Ther. 2003, 306:624-630.
34. Romero-Sandoval A., Eisenach J.C. Spinal cannabinoid receptor type 2 activation reduces hypersensitivity and spinal cord glial activation after paw incision. Anesthesiology 2007, 106:787-794.
35. Romero-Sandoval E.A., Horvath R., Landry R.P., DeLeo J.A. Cannabinoid receptor type 2 activation induces a microglial anti-inflammatory phenotype and reduces migration via MKP induction and ERK dephosphorylation. Mol. Pain 2009, 5:25.
36. Song P., Zhao Z.Q. The involvement of glial cells in the development of morphine tolerance. Neurosci. Res. 2001, 39:281-286.
37. Stella N. Cannabinoid signaling in glial cells. Glia 2004, 48:267-277.
38. Takayama N., Ueda H. Morphine-induced chemotaxis and brain-derived neurotrophic factor expression in microglia. J. Neurosci. 2005, 25:430-435.
39. Trang T., McNaul l B., Quirion R., Jhamandas K. Involvement of spinal lipoxygenase metabolites in hyperalgesia and opioid tolerance. Eur. J. Pharmacol. 2004, 491:21-30.
40. Tumati S., Roeske W.R., Vanderah T.W., Varga E.V. Sustained morphine treatment augments prostaglandin E2-evoked calcitonin gene-related peptide release from primary sensory neurons in a PKA-dependent manner. Eur. J. Pharmacol. 2010, 648:95-101.
41. Vanderah T.W., Gardell L.R., Burgess S.E., Ibrahim M., Dogrul A., Zhong C.M., Zhang E.T., Malan T.P., Ossipov M.H., Lai J., Porreca F. Dynorphin promotes abnormal pain and spinal opioid antinociceptive tolerance. J. Neurosci. 2000, 20:7074-7079.
42. Vanderah T.W., Ossipov M.H., Lai J., Malan T.P., Porreca F. Mechanisms of opioid-induced pain and antinociceptive tolerance: Descending facilitation and spinal dynorphin. Pain 2001, 92:5-9.
43. Vanderah T.W., Suenaga N.M., Ossipov M.H., Malan T.P., Lai J., Porreca F. Tonic descending facilitation from the rostral ventromedial medulla mediates opioid-induced abnormal pain and antinociceptive tolerance. J. Neurosci. 2001, 21:279-286.
44. Wang Z., Ma W., Chabot J.G., Quirion R. Cell-type specific activation of p38 and ERK mediates calcitonin gene-related peptide involvement in tolerance to morphine-induced analgesia. FASEB J. 2009, 23:2576-2586.
45. Wanigasekera V., Lee M.C.H., Rogers R., Hu P., Tracey I. Neural correlates of an injury-free model of central sensitization induced by opioid withdrawal in humans. J. Neurosci. 2011, 31:2835-2842.
46. Watkins L.R., Hutchinson H.R., Johnston J.N., Maier S.F. Glia: novel counter-regulators of opioid analgesia. Trends Neurosci. 2005, 28:661-669.
47. Watkins L.R., Hutchinson M.R., Ledeboer A., Wieseler-Frank J., Milligan E.D., Maier S.F. Glia as the "bad guys": implications for improving clinical pain control and the clinical utility of opioids. Brain Behav. Immun. 2007, 21:131-146.