Spinal cannabinoid CB2 receptors as a target for neuropathic pain: An investigation using chronic constriction injury

Neuroscience

Volumn 203, Issue , 2012, Pages 180-193

  Brownjohn, P W ^a   Ashton, J C ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

Author keywords

Cannabinoid; CB2; Chronic constriction injury; GW405833; Neuropathic pain; Spinal cord

Indexed keywords

1 (2,3 DICHLOROBENZOYL) 5 METHOXY 2 METHYL 3 (2 MORPHOLINOETHYL)INDOLE; 1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; CANNABINOID 2 RECEPTOR; UNCLASSIFIED DRUG; WIN 55 212 2;

ALLODYNIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTINOCICEPTION; ARTICLE; CONTROLLED STUDY; DRUG ADMINISTRATION ROUTE; DRUG TARGETING; IMMUNOHISTOCHEMISTRY; LUMBAR SPINAL CORD; MALE; NERVE COMPRESSION; NEUROPATHIC PAIN; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TARGETING; RAT; SHAM PROCEDURE; WESTERN BLOTTING;

ANIMALS; BEHAVIOR, ANIMAL; BENZOXAZINES; CANNABINOIDS; CELLS, CULTURED; CHO CELLS; CRICETINAE; HYPERALGESIA; INDOLES; MALE; MORPHOLINES; NAPHTHALENES; NEURALGIA; PAIN MEASUREMENT; RATS; RATS, WISTAR; RECEPTOR, CANNABINOID, CB2; SPINAL CORD;

EID: 84856454306     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2011.12.028     Document Type: Article

References (54)

1. Anand U., Otto W.R., Sanchez-Herrera D., Facer P., Yiangou Y., Korchev Y., Birch R., Benham C., Bountra C., Chessell I.P., Anand P. Cannabinoid receptor CB2 localisation and agonist-mediated inhibition of capsaicin responses in human sensory neurons. Pain 2008, 138:667-680.
2. Ashton J.C. Knockout controls and the specificity of cannabinoid CB(2) receptor antibodies. Br J Pharmacol 2011, 163:1113.
3. Ashton JC (in press) The use of knockout mice to test the specificity of antibodies for cannabinoid receptors. Hippocampus.
4. Ashton J.C., Milligan E.D. Cannabinoids for the treatment of neuropathic pain: clinical evidence. Curr Opin Investig Drugs 2008, 9:65-75.
5. Atwood B.K., Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010, 160:467-479.
6. Beltramo M., Bernardini N., Bertorelli R., Campanella M., Nicolussi E., Fredduzzi S., Reggiani A. CB2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms. Eur J Neurosci 2006, 23:1530-1538.
7. Bennett G.J., Xie Y.K. A peripheral mononeuropathy in rat that produces disorders of pain sensation like those seen in man. Pain 1988, 33:87-107.
8. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
9. Brownjohn P.W., Ashton J.C. Novel targets in pain research: the case for CB2 receptors as a biorational pain target. Curr Anaesthesia and Critical Care 2009, 20:198-203.
10. Cameron A.A., Cliffer K.D., Dougherty P.M., Garrison C.J., Willis W.D., Carlton S.M. Time course of degenerative and regenerative changes in the dorsal horn in a rat model of peripheral neuropathy. J Comp Neurol 1997, 379:428-442.
11. Cameron A.A., Cliffer K.D., Dougherty P.M., Willis W.D., Carlton S.M. Changes in lectin, GAP-43 and neuropeptide staining in the rat superficial dorsal horn following experimental peripheral neuropathy. Neurosci Lett 1991, 131:249-252.
12. Curto-Reyes V., Llames S., Hidalgo A., Menéndez L., Baamonde A. Spinal and peripheral analgesic effects of the CB2 cannabinoid receptor agonist AM1241 in two models of bone cancer-induced pain. Br J Pharmacol 2010, 160:561-573.
13. Dixon W.J. Efficient analysis of experimental observations. Annu Rev Pharmacol Toxicol 1980, 20:441-462.
14. Elmes S.J., Jhaveri M.D., Smart D., Kendall D.A., Chapman V. Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naïve rats and in rat models of inflammatory and neuropathic pain. Eur J Neurosci 2004, 20:2311-2320.
15. Gelderd J.B., Chopin S.F. The vertebral level of origin of spinal nerves in the rat. Anat Rec 1977, 188:45-47.
16. Gong J.P., Onaivi E.S., Ishiguro H., Liu Q.R., Tagliaferro P.A., Brusco A., Uhl G.R. Cannabinoid CB2 receptors: immunohistochemical localization in rat brain. Brain Res 2006, 1071:10-23.
17. Grimsey N.L., Goodfellow C.E., Scotter E.L., Dowie M.J., Glass M., Graham E.S. Specific detection of CB1 receptors; cannabinoid CB1 receptor antibodies are not all created equal!. J Neurosci Methods 2008, 171:78-86.
18. Gu X., Mei F., Liu Y., Zhang R., Zhang J., Ma Z. Intrathecal administration of the cannabinoid 2 receptor agonist JWH015 Can attenuate cancer pain and decrease mRNA expression of the 2B subunit of N-methyl-d-aspartic acid. Anesth Analg 2011, 113:405-411.
19. Hsieh G.C., Pai M., Chandran P., Hooker B.A., Zhu C.Z., Salyers A.K., Wensink E.J., Zhan C., Carroll W.A., Dart M.J., Yao B.B., Honore P., Meyer M.D. Central and peripheral sites of action for CB receptor mediated analgesic activity in chronic inflammatory and neuropathic pain models in rats. Br J Pharmacol 2011, 162:428-440.
20. Hu B., Doods H., Treede R.D., Ceci A. Depression-like behaviour in rats with mononeuropathy is reduced by the CB2-selective agonist GW405833. Pain 2009, 143:206-212.
21. Huffman J.W., Liddle J., Yu S., Aung M.M., Abood M.E., Wiley J.L., Martin B.R. 3-(1',1'-dimethylbutyl)-1-deoxy-delta8-THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg Med Chem 1999, 7:2905-2914.
22. 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 AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. Proc Natl Acad Sci U S A 2003, 100:10529-10533.
23. Jhaveri M.D., Elmes S.J., Richardson D., Barrett D.A., Kendall D.A., Mason R., Chapman V. Evidence for a novel functional role of cannabinoid CB(2) receptors in the thalamus of neuropathic rats. Eur J Neurosci 2008, 27:1722-1730.
24. Kim J.K., Yoon Y.W., Chung J.M. Comparison of three rodent neuropathic pain models. Exp Brain Res 1997, 113:200-206.
25. LaBuda C.J., Koblish M., Little P.J. Cannabinoid CB2 receptor agonist activity in the hindpaw incision model of postoperative pain. Eur J Pharmacol 2005, 527:172-174.
26. Leichsenring A., Andriske M., Bäcker I., Stichel C.C., Lübbert H. Analgesic and antiinflammatory effects of cannabinoid receptor agonists in a rat model of neuropathic pain. Naunyn Schmiedebergs Arch Pharmacol 2009, 379:627-636.
27. Lemberg K.K., Kontinen V.K., Siiskonen A.O., Viljakka K.M., Yli-Kauhaluoma J.T., Korpi E.R., Kalso E.A. Antinociception by spinal and systemic oxycodone: why does the route make a difference?. In vitro and in vivo studies in rats. Anesthesiology 2006, 105:801-812.
28. Lim G., Sung B., Ji R.R., Mao J. Upregulation of spinal cannabinoid-1-receptors following nerve injury enhances the effects of Win 55,212-2 on neuropathic pain behaviors in rats. Pain 2003, 105:275-283.
29. Liu Q.R., Pan C.H., Hishimoto A., Li C.Y., Xi Z.X., Llorente-Berzal A., Viveros M.P., Ishiguro H., Arinami T., Onaivi E.S., Uhl G.R. Species differences in cannabinoid receptor 2 (CNR2 gene): identification of novel human and rodent CB2 isoforms, differential tissue expression and regulation by cannabinoid receptor ligands. Genes Brain Behav 2009, 8:519-530.
30. Milligan E.D., Mehmert K.K., Hinde J.L., Harvey L.O., Martin D., Tracey K.J., Maier S.F., Watkins L.R. Thermal hyperalgesia and mechanical allodynia produced by intrathecal administration of the human immunodeficiency virus-1 (HIV-1) envelope glycoprotein, gp120. Brain Res 2000, 861:105-116.
31. Milligan E.D., Sloane E.M., Langer S.J., Cruz P.E., Chacur M., Spataro L., Wieseler-Frank J., Hammack S.E., Maier S.F., Flotte T.R., Forsayeth J.R., Leinwand L.A., Chavez R., Watkins L.R. Controlling neuropathic pain by adeno-associated virus driven production of the anti-inflammatory cytokine, interleukin-10. Mol Pain 2005, 1:9.
32. Paszcuk A.F., Dutra R.C., da Silva K.A., Quintão N.L., Campos M.M., Calixto J.B. Cannabinoid agonists inhibit neuropathic pain induced by brachial plexus avulsion in mice by affecting glial cells and MAP kinases. PLoS One 2011, 6:e24034.
33. Paxinos G., Watson C. The rat brain in stereotaxic coordinates 1986, Academic Press, San Diego.
34. Racz I., Nadal X., Alferink J., Baños J.E., Rehnelt J., Martín M., Pintado B., Gutierrez-Adan A., Sanguino E., Manzanares J., Zimmer A., Maldonado R. Crucial role of CB(2) cannabinoid receptor in the regulation of central immune responses during neuropathic pain. J Neurosci 2008, 28:12125-12135.
35. Ramer M.S., Bisby M.A. Adrenergic innervation of rat sensory ganglia following proximal or distal painful sciatic neuropathy: distinct mechanisms revealed by anti-NGF treatment. Eur J Neurosci 1999, 11:837-846.
36. Ramer M.S., French G.D., Bisby M.A. Wallerian degeneration is required for both neuropathic pain and sympathetic sprouting into the DRG. Pain 1997, 72:71-78.
37. Rigaud M., Gemes G., Barabas M.E., Chernoff D.I., Abram S.E., Stucky C.L., Hogan Q.H. Species and strain differences in rodent sciatic nerve anatomy: implications for studies of neuropathic pain. Pain 2008, 136:188-201.
38. 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.
39. Romero-Sandoval A., Nutile-McMenemy N., DeLeo J.A. Spinal microglial and perivascular cell cannabinoid receptor type 2 activation reduces behavioral hypersensitivity without tolerance after peripheral nerve injury. Anesthesiology 2008, 108:722-734.
40. Sain N.M., Liang A., Kane S.A., Urban M.O. Antinociceptive effects of the non-selective cannabinoid receptor agonist CP 55,940 are absent in CB1(-/-) and not CB2(-/-) mice in models of acute and persistent pain. Neuropharmacology 2009, 57:235-241.
41. Showalter V.M., Compton D.R., Martin B.R., Abood M.E. Evaluation of binding in a transfected cell line expressing a peripheral cannabinoid receptor (CB2): identification of cannabinoid receptor subtype selective ligands. J Pharmacol Exp Ther 1996, 278:989-999.
42. Smith P.B., Martin B.R. Spinal mechanisms of delta 9-tetrahydrocannabinol-induced analgesia. Brain Res 1992, 578:8-12.
43. Stewart L.S., Martin W.J. Influence of postoperative analgesics on the development of neuropathic pain in rats. Comp Med 2003, 53:29-36.
44. Valenzano K.J., Tafesse L., Lee G., Harrison J.E., Boulet J.M., Gottshall S.L., Mark L., Pearson M.S., Miller W., Shan S., Rabadi L., Rotshteyn Y., Chaffer S.M., Turchin P.I., Elsemore D.A., Toth M., Koetzner L., Whiteside G.T. Pharmacological and pharmacokinetic characterization of the cannabinoid receptor 2 agonist, GW405833, utilizing rodent models of acute and chronic pain, anxiety, ataxia and catalepsy. Neuropharmacology 2005, 48:658-672.
45. Viscomi M.T., Oddi S., Latini L., Pasquariello N., Florenzano F., Bernardi G., Molinari M., Maccarrone M. Selective CB2 receptor agonism protects central neurons from remote axotomy-induced apoptosis through the PI3K/Akt pathway. J Neurosci 2009, 29:4564-4570.
46. Walczak J.S., Pichette V., Leblond F., Desbiens K., Beaulieu P. Behavioral, pharmacological and molecular characterization of the saphenous nerve partial ligation: a new model of neuropathic pain. Neuroscience 2005, 132:1093-1102.
47. Whiteside G.T., Gottshall S.L., Boulet J.M., Chaffer S.M., Harrison J.E., Pearson M.S., Turchin P.I., Mark L., Garrison A.E., Valenzano K.J. A role for cannabinoid receptors, but not endogenous opioids, in the antinociceptive activity of the CB2-selective agonist, GW405833. Eur J Pharmacol 2005, 528:65-72.
48. Wotherspoon G., Fox A., McIntyre P., Colley S., Bevan S., Winter J. Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 2005, 135:235-245.
49. Wu W.P., Xu X.J., Hao J.X. Chronic lumbar catheterization of the spinal subarachnoid space in mice. J Neurosci Methods 2004, 133:65-69.
50. Yamamoto W., Mikami T., Iwamura H. Involvement of central cannabinoid CB2 receptor in reducing mechanical allodynia in a mouse model of neuropathic pain. Eur J Pharmacol 2008, 583:56-61.
51. Yao B.B., Hsieh G., Daza A., Fan Y., Grayson G., Garrison T., El Kouhen O., Hooker B., Pai M., Wensink E., Salyers A., Chandran P., Zhu C., Zhong C., Ryther K., Gallagher M., Chin C.L., Tovcimak A., Hradil V., Fox G., Dart M., Honore P., Meyer M. Characterization of a cannabinoid CB2 receptor selective agonist, A-836339, in in vitro pharmacological assays and in vivo pain models. J Pharmacol Exp Ther 2008.
52. Yao B.B., Hsieh G., Daza A.V., Fan Y., Grayson G.K., Garrison T.R., El Kouhen O., Hooker B.A., Pai M., Wensink E.J., Salyers A.K., Chandran P., Zhu C.Z., Zhong C., Ryther K., Gallagher M.E., Chin C.L., Tovcimak A.E., Hradil V.P., Fox G.B., Dart M.J., Honore P., Meyer M.D. Characterization of a cannabinoid CB2 receptor-selective agonist, A-836339 [2,2,3,3-tetramethyl-cyclopropanecarboxylic acid [3-(2-methoxy-ethyl)-4,5-dimethyl-3H-thiazol-(2Z)-ylidene]-amide], using in vitro pharmacological assays, in vivo pain models, and pharmacological magnetic resonance imaging. J Pharmacol Exp Ther 2009, 328:141-151.
53. Yao B.B., Hsieh G.C., Frost J.M., Fan Y., Garrison T.R., Daza A.V., Grayson G.K., Zhu C.Z., Pai M., Chandran P., Salyers A.K., Wensink E.J., Honore P., Sullivan J.P., Dart M.J., Meyer M.D. In vitro and in vivo characterization of A-796260: a selective cannabinoid CB2 receptor agonist exhibiting analgesic activity in rodent pain models. Br J Pharmacol 2008, 153:390-401.
54. Yoon M.H., Choi J.I. Pharmacologic interaction between cannabinoid and either clonidine or neostigmine in the rat formalin test. Anesthesiology 2003, 99:701-707.