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Original

Interaction of the cannabinoid and opioid systems in the modulation of nociception

, PhD
Pages 143-151 | Published online: 11 Jul 2009

References

  • Ballantyne JC, Shin NS. Efficacy of opioids for chronic pain: A review of the evidence. Clinical Journal of Pain 2008; 24: 469–478
  • Berman Y, Devi L, Carr KD. Effects of streptozotocin-induced diabetes on prodynorphin-derived peptides in rat brain regions. Brain Research 1995; 685: 129–134
  • Bisogno T, Cascio MG, Saha B, Mahadevan A, Urbani P, Minassi A, et al. Development of the first potent and specific inhibitors of endocannabinoid biosynthesis. Biochim Biophys Acta 2006; 1761: 205–212
  • Bodnar RJ. Endogenous opiates and behavior: 2007. Peptides 2008; 29: 2292–2375
  • Brown AJ. Novel cannabinoid receptors. British Journal of Pharmacology 2007; 152: 567–575
  • Buckley NE. The peripheral cannabinoid receptor knockout mice: An update. British Journal of Pharmacology 2008; 153: 309–318
  • Calignano A, La Rana G, Giuffrida A. Control of pain initiation by endogenous cannabinoids. Nature 1998; 394: 277–281
  • Cherny N, Ripamonti C, Pereira J, Davis C, Fallon M, McQuay H, et al. Expert working group of the European association of palliative care network. Strategies to manage the adverse effects of oral morphine: An evidence-based report. Journal of Clinical Oncology 2001; 19: 2542–2554
  • Cheung CY, Tang F. The effects of streptozotocin diabetes on ß-endorphin level and proopiomelanocortin gene expression in the rat pituitary. Neuroscience Letters 1999; 261: 118–120
  • Cichewicz DL, McCarthy EA. Antinociceptive synergy between Δ9-tetrahydrocannabinol and opioids after oral administration. Journal of Pharmacology and Experimental Therapeutics 2003; 304: 1010–1015
  • Cichewicz DL, Welch SP. Modulation of oral morphine antinociceptive tolerance and naloxone-precipitated withdrawal signs by oral Δ9-THC. Journal of Pharmacology and Experimental Therapeutics 2003; 307: 812–817
  • Civelli O. The orphanin FQ/nociceptin (OFQ/N) system. Results in Problems of Cell Differentiation 2008; 46: 1–25
  • Cooper ZD, Haney M. Cannabis reinforcement and dependence: Role of the cannabinoid CB1 receptor. Addiction Biology 2008; 13(2)188–195
  • Corchero J, Avila MA, Fuentes JA. Delta-9-tetrahydrocannabinol increases prodynorphin and proenkephalin gene expression in the spinal cord of the rat. Life Sciences 1997; 61: PL39–43
  • Cox ML, Haller VL, Welch SP. The antinociceptive effect of delta 9-THC in the arthritic rat involves the CB2 cannabinoid receptor. European Journal of Pharmacology 2007; 570: 50–56
  • Cox ML, Welch SP. The antinociceptive effect of Δ9-THC in the arthritic rat. European Journal of Pharmacology 2004; 493: 65–74
  • Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, et al. Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proceedings of National Academy of Sciences 2001; 98: 9371–9376
  • Cravatt BF, Giang DK, Mayfield SP, Boger DL, Lerner RA, Gilula NB. Nature Nov 7, 1996; 384(6604)83–7
  • Cravatt BF, Lichtman AH. The endogenous cannabinoid system and its role in nociceptive behavior. Journal of Neurobiology 2004; 61: 149–160
  • Devane WA, Dysarz FA, III, Johnson MR, Melvin LS, Howlett AC. Determination and characterization of a cannabinoid receptor in rat brain. Molecular Pharmacology 1988; 34: 605–613
  • Devane WA, Hanus L, Breuer A, Pertwee RG, Stevenson LA, Griffin G, et al. Isolation and structure of a brain constituent that binds to the cannabinoid receptor. Science 1992; 258: 1946–1949
  • Di Marzo V, De Petrocellis L, Bisogno T. The biosynthesis, fate and pharmacological properties of endocannabinoids. Handbook of Experimental Pharmacology 2005; 168: 147–185
  • Di Marzo V, De Petrocellis L. Plant, synthetic, and endogenous cannabinoids in medicine. Annual Review of Medicine 2006; 57: 553–574
  • Di Marzo V, Petrosino S. Endocannabinoids and the regulation of their levels in health and disease. Current Opinions in Lipidology 2007; 18: 129–140
  • Dinh TP, Freund TF, Piomelli D. A role for monoglyceride lipase in 2-arachidonoylglycerol inactivation. Chemistry and Physics of Lipids 2002; 121: 149–158
  • Fallucca F, Tonnarini G, Di Biase N, D'Alessandro M, Negri M. Plasma met-enkephalin levels in diabetic patients: Influence of autonomic neuropathy. Metabolism 1996; 45: 1065–1068
  • Fowler CJ, Tiger G, Ligresti A, Lopez-Rodriguez ML, Di Marzo V. Selective inhibition of anandamide cellular uptake versus enzymatic hydrolysis – A difficult issue to handle. European Journal of Pharmacology 2004; 492: 1–11
  • Gardell LR, Ossipov MH, Vanderah TW, Lai J, Porreca F. Dynorphin-independent spinal cannabinoid antinociception. Pain 2002; 100: 243–248
  • Ghosh P, Bhattacharya SK. Cannabis-induced potentiation of morphine analgesia in rat: Role of brain monoamines. Indian Journal of Medical Research 1979; 70: 275–280
  • Gidal B. New and emerging treatment options for neuropathic pain. American Journal of Managed Care 2006; 12: S269–278
  • Gomes I, Filipovska J, Jordan BA. Oligomerization of opioid receptors. Methods 2002; 27: 358–365
  • Gulyas AI, Cravatt BF, Braciey MH, Dinh TP, Piomelli D, Boscia F, et al. Segregation of two endocannabinoid-hydrolyzing enzymes into pre-and postsynaptic compartments in the rat hippocampus, cerebellum and amygdala. European Journal of Neuroscience 2004; 20: 441–458
  • Haller VL, Cichewicz DL, Welch SP. Non-cannabinoid CB1, non-cannabinoid CB2 antinociceptive effects of several novel compounds in the PPQ stretch test in mice. European Journal of Pharmacology 2006; 546: 60–68
  • Haller VL, Stevens DL, Welch SP. Modulation of opioids via protection of anandamide degradation by fatty acid amide hydrolase. European Journal of Pharmacology 2008; 600(1–3)50–58
  • Herzberg U, Eliav E, Bennett GJ. The analgesic effects of R(+)-WIN 55,212-2 mesylate, a high affinity cannabinoid agonist, in a rat model of neuropathic pain. Neuroscience Letters 1997; 221: 157–160
  • Hohmann AG, Suplita RL. Endocannabinoid mechanisms of pain modulation. AAPS Journal 2006; 8: E693–708
  • Hosking RD, Zajicek JP. Therapeutic potential of cannabis in pain medicine. British Journal of Anaesthesia 2008; 101: 59–68
  • Ibrahim MM, Deng H, Zvonok A. Activation of CB2 cannabinoid receptors by AM1241 inhibits experimental neuropathic pain: Pain inhibition by receptors not present in the CNS. PNAS 2003; 100: 10529–10533
  • Ibrahim MH, Porreca F, Lai J, Albrecht PJ, Rice FL, Khodorova A, et al. CB cannabinoid receptor activation produces antinociception by stimulating peripheral release of endogenous opioids. PNAS 2005; 102: 3093–3098
  • Kawasaki Y, Kohno T, Ji RR. Different effects of opioid and cannabinoid receptor agonists on C-fiber-induced extracellular signal-regulated kinase activation in dorsal horn neurons in normal and spinal nerve-ligated rats. Journal of Pharmacology and Experimental Therapeutics 2006; 316: 601–607
  • Ko MC, Woods JH. Local administration of delta-9-tetrahydrocannabinol attenuates capsaicin-induced thermal nociception in rhesus monkeys: A peripheral cannabinoid action. Psychopharmacology 1999; 143: 322–326
  • Kogan NM, Mechoulam R. The chemistry of endocannabinoids. Journal of Endocrin Inv 2006; 29: 3–14
  • Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, et al. Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockout mice. Science 1999; 283: 401–404
  • Li J, Daughters RS, Bullis C. The cannabinoid receptor agonist WIN 55,212-2 mesylate blocks the development of hyperalgesia produced by capsaicin in rats. Pain 1999; 81: 25–33
  • Lichtman AH, Martin BR. Spinal and supraspinal mechanisms of cannabinoid-induced antinociception. Journal of Pharmacol Exp Ther 1991; 258: 517–523
  • Lichtman AH, Sheikh SM, Loh HH, Martin BR. Opioid and cannabinoid modulation of precipitated withdrawal in delta (9)-tetrahydrocannabinol and morphine-dependent mice. Journal of Pharmacol Exp Ther 2001; 298: 1007–1014
  • Lim G, Sung B, Ji RR. 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
  • Mailleux P, Vanderhaeghen JJ. Localization of cannabinoid receptor in the human developing and adult basal ganglia. Higher levels in the striatonigral neurons. Neurosci Letts 1992; 148: 173–176
  • Manzanares J, Corchero J, Romero J. Pharmacological and biochemical interactions between opioids and cannabinoids. Trends in Pharmacological Sciences 1999; 20: 287–294
  • Mao J, Price DD, Lu J. Two distinctive antinociceptive systems in rats with pathological pain. Neurosci Letts 2000; 280(1)13–16
  • Martin BR, Sim-Selley LJ, Selley DE. Signaling pathways involved in the development of cannabinoid tolerance. Trends in Pharmacol Science 2004; 25: 325–330
  • Martin M, Ledent C, Parmentier M, Maldonado R, Valverde O. Cocaine, but not morphine, induces conditioned place preference and sensitization to locomotor responses in CB1 knockout mice. European Journal of Neuroscience 2000; 12: 4038–4046
  • Martin WJ, Loo CM, Basbaum AI. Spinal cannabinoids are antiallodynic in rats with persistent inflammation. Pain 1999; 82: 199–205
  • Mason DL, Welch SP. A diminution of 9-tetrahydrocannabinol modulation of dynorphin A-(1-17) in conjunction with tolerance development. European Journal of Pharmacology 1999a; 381: 105–111
  • Mason DJ, Welch SP. Cannabinoid modulation of dynorphin A: Correlation to cannabinoid-induced antinociception. European Journal of Pharmacology 1999b; 378: 237–248
  • Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI. Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 1990; 346: 561–564
  • Mechoulam R, Lander N, Srebnik M, Zamir I, Breuer A, Shalita B, . Recent advances in the use of cannabinoids as therapeutic agents. The cannabinoids: Chemical, pharmacological and therapeutic aspects, S Agurell, W Dewey, R Willette, et al. Academic Press, New York 1984; 777–793
  • Moss DE, Johnson RL. Tonic analgesic effects of delta 9 tetrahydrocannabinol as measured with the formalin test. European Journal of Pharmacology 1980; 61: 313–315
  • Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993; 365: 61–65
  • Naef M, Curatolo M, Petersen-Felix S, Arendt-Nielsen L, Zbinden A, Brenneisen R. The analgesic effect of oral delta-9-tetrahydrocannabinol (Δ9-THC), morphine, and a Δ9-THC-morphine combination in healthy subjects under experimental pain conditions. Pain 2003; 105: 79–88
  • Noyes R, Jr, Brunk SF, Avery DA, Canter AC. The analgesic properties of delta-9-tetrahydrocannabinol and codeine. Clinical Pharmacology Therapy 1975; 18: 84–89
  • Price DD, Von der Gruen A, Miller J, Rafii A, Price C. A psychophysical analysis of morphine analgesia. Pain 1985; 22: 261–269
  • Pugh GJ, Smith PB, Dombrowski DS. The role of endogenous opioids in enhancing the antinociception produced by the combination of delta-9-THC and morphine in the spinal cord. Journal of Pharmacology and Experimental Therapeutics 1996; 279: 608–616
  • Richardson J, Aanonsen L, Hargreaves KM. SR141716A, a cannabinoid receptor antagonist, produces hyperalgesia in untreated mice. European Journal of Pharmacology 1997; 319: 3R–5R
  • Rinaldi-Carmona M, Barth F, Millan J, Deroq JM, Casellas P, Congy C, et al. SR144528, the first potent and selective antagonist of the CB2 cannabinoid receptor. Journal of Pharmacology and Experimental Therapeutics 1998; 284: 644–650
  • Rinaldi-Carmona M, Barth F, Heaulme M, Shire D, Calandra B, Congy C, et al. SR141716A, a potent and selective antagonist of the cannbinoid receptor. FEBS Lett 1994; 350: 240–244
  • Rios C, Gomes I, Devi LA. Opioid and CB1 cannabinoid receptor interactions: Reciprocal inhibition of receptor signaling and neuritogenesis. British Journal of Pharmacology 2006; 148: 387–395
  • Roberts JD, Gennings C, Shih M. Synergistic affective analgesic interaction between delta-9-tetrahydrocannabinol and morphine. European Journal of Pharmacology 2006; 13, 530(1–2)54–58
  • Rowen DW, Embrey JP, Moore CH. Antisense oligodeoxynucleotides to the kappa1 receptor enhance delta9-THC-induced antinociceptive tolerance. Pharmacology, Biochemistry and Behavior 1998; 59: 399–404
  • Siegling A, Hofmann HA, Denzer D. Cannabinoid CB(1) receptor upregulation in a rat model of chronic neuropathic pain. European Journal of Pharmacology 2001; 415: R5–7
  • Salio C, Fischer J, Franzoni MF. CB1-cannabinoid and mu-opioid receptor co-localization on postsynaptic target in the rat dorsal horn. Neuroreport 2001; 12: 3689–3692
  • Sañudo-Peña MC, Tsou K, Walker JM. Motor actions of cannabinoids in the basal ganglia output nuclei. Life Sciences 1999; 65: 703–713
  • Sim LJ, Selley DE, Dworkin SI, Childers SR. Effects of chronic GTPγS morphine administration on mu opioid receptor-stimulated [35S]autoradiography in rat brain. Journal of Neuroscience 1996; 16: 2684–2692
  • Sim-Selley LJ, Martin BR. Effect or chronic administration of R-(+)-[2,3-Dihydro-5-mthyl-3-[(morpholinyl)methyl]pyrrolo[1,2,3,-dej-1,4-benzoxazinyl]-(1naphthalenyl)methanonemesylate(WIN55.212-2) or delta(9)-tetrahydrocannabinol on cannabinoid receptor adaptation in mice. Journal of Pharmacology and Experimental Therapeutics 2002; 303: 36–44
  • Smith FL, Fujimori K, Lowe J, Welch SP. Characterization of delta 9-tetrahydrocannabinol and anandamide antinociception in nonarthritic and arthritic rats. Pharmacology, Biochemistry and Behavior 1998; 60: 183–191
  • Smith PA, Sim-Selley LJ, Selley DE, Welch SP. Low dose combination of morphine and Δ9-tetrahydrocannabinol circumvents antinociceptive tolerance and apparent desensitization of receptors. European Journal of Pharmacology 2007; 571: 129–137
  • Smith PB, Welch SP, Martin BR. Interactions between delta 9-tetrahydrocannabinol and kappa opioids in mice. Journal of Pharmacology and Experimental Therapeutics 1994; 268: 1382–1387
  • Sofia RD, Nalepa SD, Harakal JJ. Anti-edema and analgesic properties of delta-9-tetrahydrocannabinol (THC). Journal of Pharmacology and Experimental Therapeutics 1973; 186: 646–655
  • Strangman NM, Patrick SL, Hohmann AG. Evidence for a role of endogenous cannabinoids in the modulation of acute and tonic pain sensitivity. Brain Research 1998; 813: 323–328
  • Tanda G, Goldberg SR. Cannabinoids: Reward, dependence, and underlying neurochemical mechanisms – A review of recent preclinical data. Psychopharmacology 2003; 169: 115–134
  • Trescott AM, Datta S, Lee M, Hansen H. Opioid pharmacology. Pain Physician 2008; 11: S133–153
  • Tseng L. Evidence for e-opioid receptor-mediated b-endorphin-induced analgesia. Trends in Pharmacological Sciences 2001; 22: 623–630
  • Valenzano KJ, Tafesse L, Lee G. 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
  • Vigano D, Rubino T, Parolaro D. Molecular and cellular basis of cannabinoid and opioid interactions. Pharmacology, Biochemistry and Behavior 2005; 81: 360–368
  • Vigano D, Cascio MG, Rubino T, Fezza F, Vaccani A, Di Marzo V, et al. Chronic morphine modulates the contents of the endocannabinoid, 2-arachidonoyl glycerol, in rat brain. Neuropsychopharmacology 2003; 28: 1160–1167
  • Vigano D, Valenti M, Cascio MG, Di Marzo V, Parolaro D. Changes in endocannabinoid levels in a rat model of behavioral sensitization to morphine. European Journal of Neuroscience 2004; 20: 1849–1857
  • Walker JM, Hohmann AG, Martin WJ. The neurobiology of cannabinoid analgesia. Life Sciences 1999; 65: 665–673
  • Walker JM, Huang SM. Endocannabinoids in pain modulation. Prostaglandins, Leukotrienes and Essentential Fatty Acids 2002; 66: 235–242
  • Williams IJ, Stevens DL, Haller VL, Welch SP. Decreased basal endogenous opioid levels in diabetic rodents: Effects on morphine and delta-9-tetrahydrocannabinoid-induced antinociception. European Journal of Pharmacology 2008; 584: 78–86
  • Wotherspoon G, Fox A, McIntyre P. Peripheral nerve injury induces cannabinoid receptor 2 protein expression in rat sensory neurons. Neuroscience 2005; 135: 235–245
  • Zimmer A, Zimmer AM, Hohmann AG. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proceedings of the National Academy of Science 1999; 96: 5780–5785
  • Zimmer A, Valjent E, Konig M. Absence of delta-9-tetrahydrocannabinol dysphoric effects in dynorphin-deficient mice. Journal of Neuroscience 2001; 21: 9499–9505

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