The Effect of Muscarinic Receptor Modulators on the Antinociception Induced by CB₂ Receptor Agonist, JWH133 in Mice

Abstract

There is no published study regarding the interaction between muscarinic receptor modulators and antinociception induced by cannabinoid receptor (CB₂) agonist. The effect of pilocarpine (a muscarinic agonist) and atropine (a muscarinic antagonist) on JWH-133 (a CB₂ agonist) induced analgesia in mice was studied. First the analgesic effect of JWH-133 (0.001–1 mg/Kg) or pilocarpine (2.5–20 mg/kg) or atropine (0.2–5 mg/kg) was evaluated. Subsequently, the effect of co-administration of pilocarpine (2.5 mg/kg) or atropine (5 mg/kg) and JWH-133 (0.001–1 mg/Kg) were studied too. JWH-133 and pilocarpine provoked antinociception in mice but atropine did not. Pilocarpine potentiated the analgesic effect of JWH-133 but atropine antagonized that. It can be concluded that JWH-133 induced antinociception is affected by muscarinic receptor modulators in mice.

Key words

antinociception - JWH-133 - pilocarpine - atropine - formalin test - mice

• References

• 1 Jhaveri MD, Sagar DR, Elmes SJ et al. Cannabinoid CB2 receptor-mediated anti-nociception in models of acute and chronic pain. Mol Neurobiol 2007; 36: 26-35
• 2 Volkow ND, Baler RD, Compton WM et al. Adverse health effects of marijuana use. N Engl J Med 2014; 370: 2219-2227
• 3 Deng L, Guindon J, Cornett BL et al. Chronic cannabinoid receptor 2 activation reverses paclitaxel neuropathy without tolerance or cannabinoid receptor 1-dependent withdrawal. Biol Psychiatry 2015; 77: 475-487
• 4 Han S, Thatte J, Buzard DJ et al. Therapeutic utility of cannabinoid receptor type 2 (CB(2)) selective agonists. J Med Chem 2013; 56: 8224-8256
• 5 Ehrhart J, Obregon D, Mori T et al. Stimulation of cannabinoid receptor 2 (CB2) suppresses microglial activation. J Neuroinflammation 2005; 2: 29
• 6 Dittel BN. Direct suppression of autoreactive lymphocytes in the central nervous system via the CB2 receptor. Br J Pharmacol 2008; 153: 271-276
• 7 Shoemaker JL, Seely KA, Reed RL et al. The CB2 cannabinoid agonist AM-1241 prolongs survival in a transgenic mouse model of amyotrophic lateral sclerosis when initiated at symptom onset. J Neurochem 2007; 101: 87-98
• 8 Sagredo O, Pazos MR, Valdeolivas S et al. Cannabinoids: novel medicines for the treatment of Huntington’s disease. Recent Pat CNS Drug Discov 2012; 7: 41-48
• 9 Pacher P, Hasko G. Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 2008; 153: 252-262
• 10 Mach F, Montecucco F, Steffens S. Cannabinoid receptors in acute and chronic complications of atherosclerosis. Br J Pharmacol 2008; 153: 290-298
• 11 Wright KL, Duncan M, Sharkey KA. Cannabinoid CB2 receptors in the gastrointestinal tract: a regulatory system in states of inflammation. Br J Pharmacol 2008; 153: 263-270
• 12 Feizi A, Jafari MR, Hamedivafa F et al. The preventive effect of cannabinoids on reperfusion-induced ischemia of mouse kidney. Experimental and toxicologic pathology: official journal of the Gesellschaft fur Toxikologische Pathologie 2008; 60: 405-410
• 13 Barutta F, Piscitelli F, Pinach S et al. Protective role of cannabinoid receptor type 2 in a mouse model of diabetic nephropathy. Diabetes 2011; 60: 2386-2396
• 14 Izzo AA, Camilleri M. Emerging role of cannabinoids in gastrointestinal and liver diseases: basic and clinical aspects. Gut 2008; 57: 1140-1155
• 15 Ofek O, Karsak M, Leclerc N et al. Peripheral cannabinoid receptor, CB2, regulates bone mass. Proc Natl Acad Sci USA 2006; 103: 696-701
• 16 Huffman JW. CB2 receptor ligands. Mini Rev Med Chem 2005; 5: 641-649
• 17 Jafari MR, Golmohammadi S, Ghiasvand F et al. Influence of nicotinic receptor modulators on CB2 cannabinoid receptor agonist (JWH133)-induced antinociception in mice. Behavioural pharmacology 2007; 18: 691-697
• 18 Curto-Reyes V, Boto T, Hidalgo A et al. Antinociceptive effects induced through the stimulation of spinal cannabinoid type 2 receptors in chronically inflamed mice. Eur J Pharmacol 2011; 668: 184-189
• 19 Mukae T, Uchida H, Ueda H. Donepezil reverses intermittent stress-induced generalized chronic pain syndrome in mice. J Pharmacol Exp Ther 2015; 353: 471-479
• 20 Prestifilippo JP, Fernandez-Solari J, de la Cal C et al. Inhibition of salivary secretion by activation of cannabinoid receptors. Exp Biol Med (Maywood) 2006; 231: 1421-1429
• 21 Mang CF, Erbelding D, Kilbinger H. Differential effects of anandamide on acetylcholine release in the guinea-pig ileum mediated via vanilloid and non-CB1 cannabinoid receptors. Br J Pharmacol 2001; 134: 161-167
• 22 Nieri P, Martinotti E, Testai L et al. R+-methanandamide inhibits tracheal response to endogenously released acetylcholine via capsazepine-sensitive receptors. Eur J Pharmacol 2003; 459: 75-81
• 23 Baldassano S, Serio R, Mule F. Cannabinoid CB(1) receptor activation modulates spontaneous contractile activity in mouse ileal longitudinal muscle. Eur J Pharmacol 2008; 582: 132-138
• 24 Kojima S, Sugiura T, Waku K et al. Contractile response to a cannabimimetic eicosanoid, 2-arachidonoylglycerol, of longitudinal smooth muscle from the guinea-pig distal colon in vitro. Eur J Pharmacol 2002; 444: 203-207
• 25 Smid SD, Bjorklund CK, Svensson KM et al. The endocannabinoids anandamide and 2-arachidonoylglycerol inhibit cholinergic contractility in the human colon. Eur J Pharmacol 2007; 575: 168-176
• 26 Rinaldo L, Hansel C. Muscarinic acetylcholine receptor activation blocks long-term potentiation at cerebellar parallel fiber-Purkinje cell synapses via cannabinoid signaling. Proc Natl Acad Sci USA 2013; 110: 11181-11186
• 27 Nakamura-Palacios EM, Amodeo Bueno OF, Takahashi RN et al. Acute or chronic effects of cannabinoids on spontaneous or pharmacologically induced yawning in rats. Pharmacol Biochem Behav 2002; 74: 205-212
• 28 Jafari MR, Onsori S, Fekrmandi F et al. Influence of muscarinic receptor modulators on interacerebroventricular injection of arachydonylcyclopropylamide induced antinociception in mice. Physiology & behavior 2015; 138: 273-278
• 29 Tjolsen A, Berge OG, Hunskaar S et al. The formalin test: an evaluation of the method. Pain 1992; 51: 5-17
• 30 Zimmer A, Zimmer AM, Hohmann AG et al. Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci USA 1999; 96: 5780-5785
• 31 Ibrahim MM, Rude ML, Stagg NJ et al. CB2 cannabinoid receptor mediation of antinociception. Pain 2006; 122: 36-42
• 32 Greco R, Mangione AS, Sandrini G et al. Activation of CB2 receptors as a potential therapeutic target for migraine: evaluation in an animal model. J Headache Pain 2014; 15: 14
• 33 Wang ZY, Wang P, Bjorling DE. Activation of cannabinoid receptor 2 inhibits experimental cystitis. Am J Physiol Regul Integr Comp Physiol 2013; 304: R846-R853
• 34 Ikeda H, Ikegami M, Kai M et al. Activation of spinal cannabinoid CB2 receptors inhibits neuropathic pain in streptozotocin-induced diabetic mice. Neuroscience 2013; 250: 446-454
• 35 Gadotti VM, You H, Petrov RR et al. Analgesic effect of a mixed T-type channel inhibitor/CB2 receptor agonist. Mol Pain 2013; 9: 32
• 36 Vincenzi F, Targa M, Corciulo C et al. Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models. Pain 2013; 154: 864-873
• 37 Berger ND, Gadotti VM, Petrov RR et al. NMP-7 inhibits chronic inflammatory and neuropathic pain via block of Cav3.2T-type calcium channels and activation of CB2 receptors. Mol Pain 2014; 10: 77
• 38 Deng L, Guindon J, Vemuri VK et al. The maintenance of cisplatin- and paclitaxel-induced mechanical and cold allodynia is suppressed by cannabinoid CB(2) receptor activation and independent of CXCR4 signaling in models of chemotherapy-induced peripheral neuropathy. Mol Pain 2012; 8: 71
• 39 Naik SR, Kelkar MR, Amladi SR et al. Effect of muscimol, a central GABA receptor agonist, on the catalepsy, striatal homovanillic acid increase, and analgesia induced by pilocarpine in rats. Psychopharmacology (Berl) 1981; 74: 393-394
• 40 Lewis JW, Cannon JT, Liebeskind JC. Involvement of central muscarinic cholinergic mechanisms in opioid stress analgesia. Brain Res 1983; 270: 289-293
• 41 Sperber ES, Kramer E, Bodnar RJ. Effects of muscarinic receptor antagonism upon two forms of stress-induced analgesia. Pharmacol Biochem Behav 1986; 25: 171-179
• 42 Hartvig P, Gillberg PG, Gordh Jr. T et al. Cholinergic mechanisms in pain and analgesia. Trends Pharmacol Sci 1989; Suppl: 75-79
• 43 de Oliveira RC, de Oliveira R, Biagioni AF et al. Dorsal raphe nucleus acetylcholine-mediated neurotransmission modulates post-ictal antinociception: The role of muscarinic and nicotinic cholinergic receptors. Brain Res 2015;
• 44 Prado WA, Dias TB. Postoperative analgesia induced by intrathecal neostigmine or bethanechol in rats. Clin Exp Pharmacol Physiol 2009; 36: 648-654
• 45 Iwamoto ET, Marion L. Characterization of the antinociception produced by intrathecally administered muscarinic agonists in rats. J Pharmacol Exp Ther 1993; 266: 329-338
• 46 Naguib M, Yaksh TL. Characterization of muscarinic receptor subtypes that mediate antinociception in the rat spinal cord. Anesth Analg 1997; 85: 847-853
• 47 Eisenach JC. Muscarinic-mediated analgesia. Life Sci 1999; 64: 549-554
• 48 Barocelli E, Ballabeni V, Bertoni S et al. Evidence for specific analgesic activity of a muscarinic agonist selected among a new series of acetylenic derivatives. Life Sci 2001; 68: 1775-1785
• 49 Duttaroy A, Gomeza J, Gan JW et al. Evaluation of muscarinic agonist-induced analgesia in muscarinic acetylcholine receptor knockout mice. Mol Pharmacol 2002; 62: 1084-1093
• 50 Kender RG, Harte SE, Munn EM et al. Affective analgesia following muscarinic activation of the ventral tegmental area in rats. J Pain 2008; 9: 597-605
• 51 Tata AM. Muscarinic acetylcholine receptors: new potential therapeutic targets in antinociception and in cancer therapy. Recent Pat CNS Drug Discov 2008; 3: 94-103
• 52 de Freitas RL, Bolognesi LI, Twardowschy A et al. Neuroanatomical and neuropharmacological approaches to postictal antinociception-related prosencephalic neurons: the role of muscarinic and nicotinic cholinergic receptors. Brain Behav 2013; 3: 286-301
• 53 Ghelardini C, Malmberg-Aiello P, Giotti A et al. Investigation into atropine-induced antinociception. Br J Pharmacol 1990; 101: 49-54
• 54 Spicuzza L, Haddad EB, Birrell M et al. Characterization of the effects of cannabinoids on guinea-pig tracheal smooth muscle tone: role in the modulation of acetylcholine release from parasympathetic nerves. Br J Pharmacol 2000; 130: 1720-1726