The cannabinoid CB2 receptor-selective phytocannabinoid beta-caryophyllene exerts analgesic effects in mouse models of inflammatory and neuropathic pain

European Neuropsychopharmacology

Volumn 24, Issue 4, 2014, Pages 608-620

  Klauke, A L ^a   Racz, I ^a   Pradier, B ^a   Markert, A ^a   Zimmer, A M ^a   Gertsch, J ^b   Zimmer, A ^a  

^a UNIVERSITY OF BONN   (Germany)

^b UNIVERSITY OF BERN   (Switzerland)

Author keywords

Beta caryophyllene; Dietary cannabinoid; Inflammatory pain; Neuropathic pain

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; CANNABINOID 2 RECEPTOR; CARYOPHYLLENE; MORPHINE; CANNABINOID RECEPTOR AGONIST; CNR2 PROTEIN, MOUSE; NERVE PROTEIN; NONSTEROID ANTIINFLAMMATORY AGENT; PLANT MEDICINAL PRODUCT; SESQUITERPENE;

ALLODYNIA; ANALGESIC ACTIVITY; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AREA UNDER THE CURVE; ARTICLE; CHRONIC PAIN; CONTROLLED STUDY; DRUG TOLERANCE; FOOD CROP; FORMALIN TEST; GENE EXPRESSION; GLIA CELL; HYPERALGESIA; IMMUNOHISTOCHEMISTRY; MALE; MOUSE; NERVOUS SYSTEM INFLAMMATION; NEUROPATHIC PAIN; NONHUMAN; PARTIAL SCIATIC NERVE LIGATION INJURY; PERIPHERAL NERVE INJURY; PRIORITY JOURNAL; RECTUM TEMPERATURE; SPICE; ANALGESIA; BODY TEMPERATURE; HARGREAVES TEST; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; INFLAMMATORY PAIN; MOTOR ACTIVITY; NERVE LIGATION; OPEN FIELD TEST; PAIN ASSESSMENT; REAL TIME POLYMERASE CHAIN REACTION; TAIL FLICK TEST; TETRAD TEST; AGONISTS; ANIMAL; ANIMAL BEHAVIOR; CONGENIC STRAIN; DISEASE MODEL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; IMMUNOLOGY; METABOLISM; NERVE CELL; NEURALGIA; ORAL DRUG ADMINISTRATION; PAIN MEASUREMENT; SCIATIC NERVE; SCIATIC NEUROPATHY; SPINAL CORD;

ADMINISTRATION, ORAL; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; BEHAVIOR, ANIMAL; CANNABINOID RECEPTOR AGONISTS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HYPERALGESIA; MALE; MICE; MICE, CONGENIC; MOTOR ACTIVITY; NERVE TISSUE PROTEINS; NEURALGIA; NEURONS; PAIN MEASUREMENT; PHYTOCHEMICALS; RECEPTOR, CANNABINOID, CB2; SCIATIC NERVE; SCIATIC NEUROPATHY; SESQUITERPENES; SPINAL CORD;

EID: 84895856451     PISSN: 0924977X     EISSN: 18737862     Source Type: Journal    
DOI: 10.1016/j.euroneuro.2013.10.008     Document Type: Article

References (55)

1. Basbaum A.I., Bautista D.M., Scherrer G., Julius D. Cellular and molecular mechanisms of pain. Cell 2009, 139:267-284.
2. Beltramo M. Cannabinoid type 2 receptor as a target for chronic-pain. Mini Rev. Med. Chem. 2009, 9:11-25.
3. 2 receptor-mediated antihyperalgesia: possible direct involvement of neural mechanisms. Eur. J. Neurosci. 2006, 23:1530-1538.
4. Ben Amar M. Cannabinoids in medicine: a review of their therapeutic potential. J. Ethnopharmacol. 2006, 105:1-25.
5. 2 receptors and fatty acid amide hydrolase are specific markers of plaque cell subtypes in human multiple sclerosis. J. Neurosci. 2007, 27:2396-2402.
6. 2 receptor activation and PPARγ pathway. Am. J. Pathol. 2011, 178:1153-1166.
7. Berman J., Symonds C., Birch R. Efficacy of two cannabis based medicinal extracts for relief of central neuropathic pain from brachial plexus avulsion: results of a randomised controlled trial. Pain 2004, 112:299-306.
8. Bernardes W., Lucarini R., Tozatti M., Flauzino L., Souza M., Turatti I., Andrade e Silva M., Martins C., da Silva Filho A., Cunha W. Antibacterial activity of the essential oil from Rosmarinus officinalis and its major components against oral pathogens. Z. Naturforsch. C: J. Biosci. 2010, 65:588-593.
9. Buckley N.E., McCoy K.L., Mezey E., Bonner T., Zimmer A., Felder C.C., Glass M., Zimmer A. Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur. J. Pharmacol. 2000, 396:141-149.
10. Calabrese E.J. Drug therapies for stroke and traumatic brain injury often display U-shaped dose responses: occurrence, mechanisms, and clinical implications. Crit. Rev. Toxicol. 2008, 38:557-577.
11. Calleja M.A., Vieites J.M., Montero-Meterdez T., Torres M.I., Faus M.J., Gil A., Suárez A. The antioxidant effect of β-caryophyllene protects rat liver from carbon tetrachloride-induced fibrosis by inhibiting hepatic stellate cell activation. Br. J. Nutr. 2012, 1:1-8.
12. 2 cannabinoid receptors are implicated in inflammatory pain. Pain 2002, 96:253-260.
13. Costigan M., Scholz J., Woolf C.J. Neuropathic pain: a maladaptive response of the nervous system to damage. Annu. Rev. Neurosci. 2009, 32:1-32.
14. Devor M. Response to nerve injury in relation to neuropathic pain. Wall and Melzack's Textbook of Pain 2006, 905-927. Elsevier Churchill Livingstone, London. S. McMahon, M. Koltzenburg (Eds.).
15. Facci L., Dal Toso R., Romanello S., Buriani A., Skaper S., Leon A. Mast cells express a peripheral cannabinoid receptor with differential sensitivity to anandamide and palmitoylethanolamide. Proc. Natl. Acad. Sci. USA 1995, 92:3376-3380.
16. Galdino P.M., Nascimento M.V.M., Florentino I.F., Lino R.C., Fajemiroye J.O., Chaibub B.A., de Paula J.R., de Lima T.C.M., Costa E.A. The anxiolytic-like effect of an essential oil derived from Spiranthera odoratissima A. St. Hil. leaves and its major component, β-caryophyllene, in male mice. Prog. Neuropsychopharmacol. Biol. Psychiatry 2012, 38:276-284.
17. Gertsch J., Leonti M., Raduner S., Racz I., Chen J.Z., Xie X.Q., Altmann K.H., Karsak M., Zimmer A. Beta-caryophyllene is a dietary cannabinoid. Proc. Natl. Acad. Sci. USA 2008, 105:9099-9104.
18. Gertsch J., Pertwee R.G., Di Marzo V. Phytocannabinoids beyond the Cannabis plant-do they exist?. Br. J. Pharmacol. 2010, 160:523-529.
19. Ghelardini C., Galeotti N., Di Cesare Mannelli L., Mazzanti G., Bartolini A. Local anaesthetic activity of beta-caryophyllene. Farmaco 2001, 56:387-389.
20. 2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain. Br. J. Pharmacol. 2008, 153:319-334.
21. Hald A., Nedergaard S., Hansen R.R., Ding M., Heegaard A.-M. Differential activation of spinal cord glial cells in murine models of neuropathic and cancer pain. Eur. J. Pain 2009, 13:138-145.
22. Hauser J., Hsu B., Nader N.D. Inflammatory processes in complex regional pain syndromes. Immunol. Invest. 2013, 42:263-272.
23. 1 receptor messenger RNA in neuronal subpopulations of rat dorsal root ganglia: a double-label in situ hybridization study. Neuroscience 1999, 90:923-931.
24. Hohmann A.G., Farthing J.N., Zvonok A.M., Makriyannis A. Selective activation of cannabinoid CB 2 receptors suppresses hyperalgesia evoked by intradermal capsaicin. J. Pharmacol. Exp. Ther. 2004, 308:446-453.
25. Horváth B., Mukhopadhyay P., Kechrid M., Patel V., Tanchian G., Wink D.A., Gertsch J., Pacher P. β-Caryophyllene ameliorates cisplatin-induced nephrotoxicity in a cannabinoid 2 receptor-dependent manner. Free Radic. Biol. Med. 2012, 52:1325-1333.
26. Hudaib M., Speroni E., Di Pietra A.M., Cavrini V. GC/MS evaluation of thyme (Thymus vulgaris L.) oil composition and variations during the vegetative cycle. J. Pharm. Biomed. Anal. 2002, 29:691-700.
27. 2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: pain inhibition by receptors not present in the CNS. Proc. Natl. Acad. Sci. USA 2003, 100:10529-10533.
28. Iskedjian M., Bereza B., Gordon A., Piwko C., Einarson T. Meta-analysis of cannabis based treatments for neuropathic and multiple sclerosis-related pain. Curr. Med. Res. Opinions 2007, 23:17-24.
29. Jayaprakasha G.K., Jagan Mohan Rao L., Sakariah K.K. Volatile constituents from Cinnamomum zeylanicum fruit stalks and their antioxidant activities. J. Agric. Food Chem. 2003, 51:4344-4348.
30. Katsuyama S., Mizoguchi H., Kuwahata H., Komatsu T., Nagaoka K., Nakamura H., Bagetta G., Sakurada T., Sakurada S. Involvement of peripheral cannabinoid and opioid receptors in beta-caryophyllene-induced antinociception. Eur. J. Pain 2012, 17:664-675.
31. 2 cannabinoid receptor-selective agonist O-3223 reduces pain and inflammation without apparent cannabinoid behavioral effects. Neuropharmacology 2011, 60:244-251.
32. Legault J., Pichette A. Potentiating effect of β-caryophyllene on anticancer activity of α-humulene, isocaryophyllene and paclitaxel. J. Pharm. Pharmacol. 2007, 59:1643-1647.
33. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Methods 2001, 25:402-408.
34. Loizzo M.R., Tundis R., Menichini F., Saab A.M., Statti G.A., Menichini F. Antiproliferative effects of essential oils and their major constituents in human renal adenocarcinoma and amelanotic melanoma cells. Cell Proliferation 2008, 41:1002-1012.
35. 2 agonist, alleviates neuropathic pain through functional microglial changes in mice. Neurobiol. Dis. 2010, 37:177-185.
36. Lynch M.E., Campbell F. Cannabinoids for treatment of chronic non-cancer pain; a systematic review of randomized trials. Br. J. Clin. Pharmacol. 2011, 72:735-744.
37. Malfait A.M., Gallily R., Sumariwalla P.F., Malik A.S., Andreakos E., Mechoulam R., Feldmann M. The nonpsychoactive cannabis constituent cannabidiol is an oral anti-arthritic therapeutic in murine collagen-induced arthritis. Proc. Natl. Acad Sci. USA 2000, 97:9561-9566.
38. Maresz K., Carrier E.J., Ponomarev E.D., Hillard C.J., Dittel B.N. Modulation of the cannabinoid CB 2 receptor in microglial cells in response to inflammatory stimuli. J. Neurochem. 2005, 95:437-445.
39. Martin B.R., Compton D.R., Thomas B.F., Prescott W.R., Little P.J., Razdan R.K., Johnson M.R., Melvin L.S., Mechoulam R., Ward S.J. Behavioral, biochemical, and molecular modeling evaluations of cannabinoid analogs. Pharmacol. Biochem. Behav. 1991, 40:471-478.
40. Mockute D., Bernotiene G., Judzentiene A. The essential oil of Origanum vulgare L. ssp. vulgare growing wild in Vilnius district (Lithuania). Phytochemistry 2001, 57:65-69.
41. Naef M., Curatolo M., Petersen-Felix S., Arendt-Nielsen L., Zbinden A., Brenneisen R. The analgesic effect of oral delta-9-tetrahydrocannabinol (THC), morphine, and a THC-morphine combination in healthy subjects under experimental pain conditions. Pain 2003, 105:79-88.
42. Orav A., Stulova I., Kailas T., Müürisepp M. Effect of storage on the essential oil composition of Piper nigrum L. fruits of different ripening states. J. Agric. Food Chem. 2004, 52:2582-2586.
43. Ou M.C., Hsu T.F., Lai A.C., Lin Y.T., Lin C.C. Pain relief assessment by aromatic essential oil massage on outpatients with primary dysmenorrhea: a randomized, double-blind clinical trial. J. Obstet. Gynaecol. Res. 2012, 38:817-822.
44. 2 cannabinoid receptor in the regulation of central immune responses during neuropathic pain. J. Neurosci. 2008, 28:12125-12135.
45. Rahn E.J., Thakur G.A., Anne J., Wood T., Zvonok A.M., Makriyannis A., Hohmann A.G. Pharmacological characterization of AM1710, a putative cannabinoid CB 2 agonist from the cannabilactone class: antinociception without central nervous system side-effects. Pharmacol. Biochem. Behav. 2011, 98:493-502.
46. Reagan-Shaw S., Nihal M., Ahmad N. Dose translation from animal to human studies revisited. FASEB J. 2008, 22:659-661.
47. Russo E.B. Taming THC: potential cannabis synergy and phytocannabinoid-terpenoid entourage effects. Br. J. Pharmacol. 2011, 163:1344-1364.
48. Scholz J., Woolf C.J. The neuropathic pain triad: neurons, immune cells and glia. Nat. Neurosci. 2007, 10:1361-1368.
49. 2 receptors. J. Pharmacol. Exp. Ther. 2005, 315:828-838.
50. Sulcova E., Mechoulam R., Fride E. Biphasic effects of anandamide. Pharmacol. Biochem. Behav. 1998, 59:347-352.
51. Tanga F.Y., Raghavendra V., DeLeo J.A. Quantitative real-time RT-PCR assessment of spinal microglial and astrocytic activation markers in a rat model of neuropathic pain. Neurochem. Int. 2004, 45:397-407.
52. Woolf C.J., Ma Q. Nociceptors-noxious stimulus detectors. Neuron 2007, 55:353-364.
53. 2 receptor in reducing mechanical allodynia in a mouse model of neuropathic pain. Eur. J. Pharmacol. 2008, 583:56-61.
54. Zheng G., Kenney P., Lam L. Sesquiterpenes from clove (Eugenia caryophyllata) as potential anticarcinogenic agents. J. Nat. Prod. 1992, 55:999-1003.
55. Zias J., Stark H., Sellgman J., Levy R., Werker E., Breuer A., Mechoulam R. Early medical use of cannabis. Nature 1993, 363:215.