CB1 receptors mediate the analgesic effects of cannabinoids on colorectal distension-induced visceral pain in rodents

Journal of Neuroscience

Volumn 29, Issue 5, 2009, Pages 1554-1564

  Brusberg, Mikael ^a   Arvidsson, Susanne ^a   Kang, Daiwu ^a   Larsson, Håkan ^a   Lindström, Erik ^a   Martinez, Vicente ^a,b  

^a ASTRAZENECA R AND D   (Sweden)

^b UNIVERSITAT AUTÒNOMA DE BARCELONA   (Spain)

Author keywords

Cannabinoid receptors; Endocannabinoids; Hyperalgesia; SR141716; Visceral pain; WIN55,212 2

Indexed keywords

2,3 DIHYDRO 5 METHYL 3 (MORPHOLINOMETHYL) 6 (1 NAPHTHOYL)PYRROLO[1,2,3 DE][1,4]BENZOXAZINE; 5 (4 CHLORO 3 METHYLPHENYL) 1 (4 METHYLBENZYL) N (1,3,3 TRIMETHYLBICYCLO[2.2.1]HEPTAN 2 YL) 3 PYRAZOLECARBOXAMIDE; 5 METHYL 4 [3 METHYL 6 (1 CYCLOHEXEN 1 YL)] 1,3 BENZENEDIOL; ANANDAMIDE; CANNABINOID; CANNABINOID 1 RECEPTOR; CANNABINOID 1 RECEPTOR AGONIST; CANNABINOID 1 RECEPTOR ANTAGONIST; CANNABINOID 2 RECEPTOR; CANNABINOID RECEPTOR AGONIST; CANNABINOID RECEPTOR ANTAGONIST; G PROTEIN COUPLED RECEPTOR; G PROTEIN COUPLED RECEPTOR 55; NAPTHALEN 1 YL (4 PENTYLOXYNAPHTHALEN 1 YL)METHANONE; O 1602; RIMONABANT; SAB 378; UNCLASSIFIED DRUG; VIRODHAMINE; ANALGESIC AGENT;

ALLODYNIA; ANALGESIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; COLON DILATATION; CONTROLLED STUDY; DOSE RESPONSE; DRUG EFFECT; FEMALE; HYPERALGESIA; KNOCKOUT MOUSE; MOUSE; NONHUMAN; PAIN; PRIORITY JOURNAL; RAT; RECTUM; RODENT; VISCERAL PAIN; ANIMAL; C57BL MOUSE; COLON; COMPARATIVE STUDY; DRUG POTENTIATION; GASTROINTESTINAL DISEASE; METHODOLOGY; MOUSE MUTANT; PAIN ASSESSMENT; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; SENSORY NERVE; SPRAGUE DAWLEY RAT;

ANALGESICS, NON-NARCOTIC; ANIMALS; CANNABINOIDS; COLON; FEMALE; GASTROINTESTINAL DISEASES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PAIN; PAIN MEASUREMENT; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR, CANNABINOID, CB1; RECTUM; VISCERAL AFFERENTS;

EID: 59649119524     PISSN: 02706474     EISSN: 02706474     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.5166-08.2009     Document Type: Article

References (74)

1. Ahluwalia J, Urban L, Capogna M, Bevan S, Nagy I (2000) Cannabinoid 1 receptors are expressed in nociceptive primary sensory neurons. Neuroscience 100:685-688.
2. Arvidsson S, Larsson M, Larsson H, Lindström E, Martinez V (2006) Assessment of visceral pain-related pseudo-affective responses to colorectal distension in mice by intracolonic manometric recordings. J Pain 7:108-118.
3. Ashton JC, Milligan ED (2008) Cannabinoids for the treatment of neuropathic pain: clinical evidence. Curr Opin Investig Drugs 9:65-75.
4. Bisogno T (2008) Endogenous cannabinoids: structure and metabolism. J Neuroendocrinol 20 [Suppl 1]:1-9.
5. Bridges D, Rice AS, Egertová M, Elphick MR, Winter J, Michael GJ (2003) Localisation of cannabinoid receptor 1 in rat dorsal root ganglion using in situ hybridisation and immunohistochemistry. Neuroscience 119:803-812.
6. Brown AJ (2007) Novel cannabinoid receptors. Br J Pharmacol 152:567-575.
7. Brusberg M, Ravnefjord A, Martinsson R, Larsson H, Martinez V, Lindström E (2009) The GABAb receptor agonist, baclofen, and the positive allosteric modulator, CGP7930, inhibit visceral pain-related responses to colorectal distension in rats. Neuropharmacology 56:362-367.
8. Canals M, Milligan G (2008) Constitutive activity of the cannabinoid CB1 receptor regulates the function of co-expressed Mu opioid receptors. J Biol Chem 283:11424-11434.
9. Capasso R, Matias I, Lutz B, Borrelli F, Capasso F, Marsicano G, Mascolo N, Petrosino S, Monory K, Valenti M, Di Marzo V, Izzo AA (2005) Fatty acid amide hydrolase controls mouse intestinal motility in vivo. Gastroenterology 129:941-951.
10. Casu MA, Porcella A, Ruiu S, Saba P, Marchese G, Carai MA, Reali R, Gessa GL, Pani L (2003) Differential distribution of functional cannabinoid CB1 receptors in the mouse gastroenteric tract. Eur J Pharmacol 459:97-105.
11. Cippitelli A, Cannella N, Braconi S, Duranti A, Tontini A, Bilbao A, Defonseca FR, Piomelli D, Ciccocioppo R (2008) Increase of brain endocannabinoid anandamide levels by FAAH inhibition and alcohol abuse behaviours in the rat. Psychopharmacology 198:449-460.
12. Coutts AA, Irving AJ, Mackie K, Pertwee RG, Anavi-Goffer S (2002) Localisation of cannabinoid CB(1) receptor immunoreactivity in the guinea pig and rat myenteric plexus. J Comp Neurol 448:410-422.
13. Cravatt BF, Demarest K, Patricelli MP, Bracey MH, Giang DK, Martin BR, Lichtman AH (2001) Supersensitivity to anandamide and enhanced endogenous cannabinoid signaling in mice lacking fatty acid amide hydrolase. Proc Natl Acad Sci U S A 98:9371-9376.
14. Cristino L, de Petrocellis L, Pryce G, Baker D, Guglielmotti V, Di Marzo V (2006) Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139:1405-1415.
15. Croxford JL, Miller SD (2003) Immunoregulation of a viral model of multiple sclerosis using the synthetic cannabinoid R + WIN55,212. J Clin Invest 111:1231-1240.
16. D'Ambra TE, Estep KG, Bell MR, Eissenstat MA, Josef KA, Ward SJ, Haycock DA, Baizman ER, Casiano FM, Beglin NC, et al (1992) Conformationally restrained analogues of pravadoline: nanomolar potent, enantioselective (aminoalkyl)indole agonists of the cannabinoid receptor. J Med Chem 35:124-135.
17. D'Argenio G, Calvani M, Casamassimi A, Petillo O, Margarucci S, Rienzo M, Peluso I, Calvani R, Ciccodicola A, Caporaso N, Peluso G (2006) Experimental colitis: decreased Octn2 and Atb0+ expression in rat colonocytes induces carnitine depletion that is reversible by carnitine-loaded liposomes. FASEB J 20:2544-2546.
18. Delgado-Aros S, Camilleri M (2005) Visceral hypersensitivity. J Clin Gastroenterol 39 [Suppl 3]:S194-S203.
19. De Petrocellis L, Bisogno T, Maccarrone M, Davis JB, Finazzi-Agro A, Di Marzo V (2001) The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. J Biol Chem 276:12856-12863.
20. Di Marzo V (2008) Endocannabinoids: synthesis and degradation. Rev Physiol Biochem Pharmacol 160:1-24.
21. Di Marzo V, Izzo AA (2006) Endocannabinoid overactivity and intestinal inflammation. Gut 55:1373-1376.
22. Dinis P, Charrua A, Avelino A, Yaqoob M, Bevan S, Nagy I, Cruz F (2004) Anandamide-evoked activation of vanilloid receptor 1 contributes to the development of bladder hyperreflexia and nociceptive transmission to spinal dorsal horn neurons in cystitis. J Neurosci 24:11253-11263.
23. Dziadulewicz EK, Bevan SJ, Brain CT, Coote PR, Culshaw AJ, Davis AJ, Edwards LJ, Fisher AJ, Fox AJ, Gentry C, Groarke A, Hart TW, Huber W, James IF, Kesingland A, La Vecchia L, Loong Y, Lyothier I, McNair K, O'Farrell C, et al. (2007) Naphthalen-1-yl-(4-pentyloxynaphthalen-1-yl)methanone: a potent, orally bioavailable human CB1/CB2 dual agonist with antihyperalgesic properties and restricted central nervous system penetration. J Med Chem 50:3851-3856.
24. Esfandyari T, Camilleri M, Busciglio I, Burton D, Baxter K, Zinsmeister AR (2007) Effects of a cannabinoid receptor agonist on colonic motor and sensory functions in humans: a randomized, placebo-controlled study. Am J Physiol Gastrointest Liver Physiol 293:G137-G145.
25. Farquhar-Smith WP, Egertová M, Bradbury EJ, McMahon SB, Rice AS, Elphick MR (2000) Cannabinoid CB(1) receptor expression in rat spinal cord. Mol Cell Neurosci 15:510-521.
26. Farquhar-Smith WP, Jaggar SI, Rice AS (2002) Attenuation of nerve growth factor-induced visceral hyperalgesia via cannabinoid CB(1) and CB(2)-like receptors. Pain 97:11-21.
27. 1 receptor is required for behavioral response to noxious chemical stimulation of TRPV1: antinociceptive actions of CB1 inverse agonists. J Neurosci 28:11593-11602.
28. Fox A, Bevan S (2005) Therapeutic potential of cannabinoid receptor agonists as analgesic agents. Expert Opin Investig Drugs 14:695-703.
29. Hentges ST, Low MJ, Williams JT (2005) Differential regulation of synaptic inputs by constitutively released endocannabinoids and exogenous cannabinoids. J Neurosci 25:9746-9751.
30. Hong S, Fan J, Kemmerer ES, Evans S, Li Y, Wiley JW (2009) Reciprocal changes in vanilloid (TRPV1) and endocannabinoid (CB1) receptors contribute to visceral hyperalgesia in the water avoidance stressed rat. Gut 58:202-210.
31. Hornby PJ, Prouty SM (2004) Involvement of cannabinoid receptors in gut motility and visceral perception. Br J Pharmacol 141:1335-1345.
32. Hosking RD, Zajicek JP (2008) Therapeutic potential of cannabis in pain medicine. Br J Anaesth 101:59-68.
33. Howlett AC, Barth F, Bonner TI, Cabral G, Casellas P, Devane WA, Felder CC, Herkenham M, Mackie K, Martin BR, Mechoulam R, Pertwee RG (2002) International Union of Pharmacology. XXVII. Classification of cannabinoid receptors. Pharmacol Rev 54:161-202.
34. Izzo AA, Mascolo N, Pinto L, Capasso R, Capasso F (1999) The role of cannabinoid receptors in intestinal motility, defaecation and diarrhoea in rats. Eur J Pharmacol 384:37-42.
35. Jaggar SI, Hasnie FS, Sellaturay S, Rice AS (1998) The anti-hyperalgesic actions of the cannabinoid anandamide and the putative CB2 receptor agonist palmitoylethanolamide in visceral and somatic inflammatory pain. Pain 76:189-199.
36. Jeske NA, Patwardhan AM, Gamper N, Price TJ, Akopian AN, Hargreaves KM (2006) Cannabinoid WIN 55,212-2 regulates TRPV1 phosphorylation in sensory neurons. J Biol Chem 281:32879-32890.
37. Käll E, Lindström E, Martinez V (2007) The serotonin reuptake inhibitor citalopram does not affect colonic sensitivity or compliance in rats. Eur J Pharmacol 570:203-211.
38. Khanolkar AD, Makriyannis A (1999) Structure-activity relationships of anandamide, an endogenous cannabinoid ligand. Life Sci 65:607-616.
39. Kikuchi A, Ohashi K, Sugie Y, Sugimoto H, Omura H (2008) Pharmacological evaluation of a novel cannabinoid 2 (CB2) ligand, PF-03550096, in vitro and in vivo by using a rat model of visceral hypersensitivity. J Pharmacol Sci 106:219-224.
40. Kulkarni-Narla A, Brown DR (2000) Localization of CB1-cannabinoid receptor immunoreactivity in the porcine enteric nervous system. Cell Tissue Res 302:73-80.
41. Landsman RS, Burkey TH, Consroe P, Roeske WR, Yamamura HI (1997) SR141716A is an inverse agonist at the human cannabinoid CB1 receptor. Eur J Pharmacol 334:R1-R2.
42. Leterrier C, Lainé J, Darmon M, Boudin H, Rossier J, Lenkei Z (2006) Constitutive activation drives compartment-selective endocytosis and axonal targeting of type 1 cannabinoid receptors. J Neurosci 26:3141-3153.
43. Ligresti A, Bisogno T, Matias I, De Petrocellis L, Cascio MG, Cosenza V, D'argenio G, Scaglione G, Bifulco M, Sorrentini I, Di Marzo V (2003) Possible endocannabinoid control of colorectal cancer growth. Gastroenterology 125:677-687.
44. Lindström E, Brusberg M, Hughes PA, Martin CM, Brierley SM, Phillis BD, Martinsson R, Abrahamsson C, Larsson H, Martinez V, Blackshaw LA (2008) Involvement of metabotropic glutamate 5 receptor in visceral pain. Pain 137:295-305.
45. MacNaughton WK, Van Sickle MD, Keenan CM, Cushing K, Mackie K, Sharkey KA (2004) Distribution and function of the cannabinoid-1 receptor in the modulation of ion transport in the guinea pig ileum: relationship to capsaicin-sensitive nerves. Am J Physiol Gastrointest Liver Physiol 286:G863-G871.
46. Malan TP Jr, Ibrahim MM, Deng H, Liu Q, Mata HP, Vanderah T, Porreca F, Makriyannis A (2001) CB2 cannabinoid receptor-mediated peripheral antinociception. Pain 93:239-245.
47. Martinez V, Melgar S (2008) Lack of colonic inflammation-induced acute visceral hypersensitivity to colorectal distension in Na. (v) 1.9 knockout mice. Eur J Pain 12:934-944.
48. Martínez V, Ryttinger M, Kjerling M, Astin-Nielsen M (2007) Characterisation of colonic accommodation in Wistar Kyoto rats with impaired gastric accommodation. Naunyn Schmiedebergs Arch Pharmacol 376:205-216.
49. Matsuda LA, Lolait SJ, Brownstein MJ, Young AC, Bonner TI (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346:561-564.
50. Matsuda LA, Bonner TI, Lolait SJ (1992) Cannabinoid receptors: which cells, where, how, and why? NIDA Res Monogr 126:48-56.
51. Moreira FA, Kaiser N, Monory K, Lutz B (2008) Reduced anxiety-like behaviour induced by genetic and pharmacological inhibition of the endocannabinoid-degrading enzyme fatty acid amide hydrolase (FAAH) is mediated by CB1 receptors. Neuropharmacology 54:141-150.
52. Munro S, Thomas KL, Abu-Shaar M (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365:61-65.
53. Nackley AG, Zvonok AM, Makriyannis A, Hohmann AG (2004) Activation of cannabinoid CB2 receptors suppresses C-fiber responses and windup in spinal wide dynamic range neurons in the absence and presence of inflammation. J Neurophysiol 92:3562-3574.
54. Narushima M, Uchigashima M, Fukaya M, Matsui M, Manabe T, Hashimoto K, Watanabe M, Kano M (2007) Tonic enhancement of endocannabinoid-mediated retrograde suppression of inhibition by cholinergic interneuron activity in the striatum. J Neurosci 27:496-506.
55. Palmer JA, Higuera ES, Chang L, Chaplan SR (2008) Fatty acid amide hydrolase inhibition enhances the anti-allodynic actions of endocannabinoids in a model of acute pain adapted for the mouse. Neuroscience 154:1554-1561.
56. Patwardhan AM, Jeske NA, Price TJ, Gamper N, Akopian AN, Hargreaves KM (2006) The cannabinoid WIN 55,212-2 inhibits transient receptor potential vanilloid 1 (TRPV1) and evokes peripheral antihyperalgesia via calcineurin. Proc Natl Acad Sci U S A 103:11393-11398.
57. Petrosino S, Palazzo E, de Novellis V, Bisogno T, Rossi F, Maione S, Di Marzo V (2007) Changes in spinal and supraspinal endocannabinoid levels in neuropathic rats. Neuropharmacology 52:415-422.
58. Pinto L, Izzo AA, Cascio MG, Bisogno T, Hospodar-Scott K, Brown DR, Mascolo N, Di Marzo V, Capasso F (2002) Endocannabinoids as physiological regulators of colonic propulsion in mice. Gastroenterology 123:227-234.
59. Ravnefjord A, Brusberg M, Larsson H, Lindström E, Martínez V (2008) Effects of pregabalin on visceral pain responses and colonic compliance in rats. Br J Pharmacol 155:407-416.
60. Rice AS, Farquhar-Smith WP, Nagy I (2002) Endocannabinoids and pain: spinal and peripheral analgesia in inflammation and neuropathy. Prostaglandins Leukot Essent Fatty Acids 66:243-256.
61. Rinaldi-Carmona M, Barth F, Héaulme M, Alonso R, Shire D, Congy C, Soubrié P, Brelière JC, Le Fur G (1995) Biochemical and pharmacological characterisation of SR141716A, the first potent and selective brain cannabinoid receptor antagonist. Life Sci 56:1941-1947.
62. Rinaldi-Carmona M, Barth F, Millan J, Derocq JM, Casellas P, Congy C, Oustric D, Sarran M, Bouaboula M, Calandra B, Portier M, Shire D, Brelière JC, Le Fur GL (1998) SR 144528, the first potent and selective antagonist of the CB2 cannabinoid receptor. J Pharmacol Exp Ther 284:644-650.
63. Rousseaux C, Thuru X, Gelot A, Barnich N, Neut C, Dubuquoy L, Dubuquoy C, Merour E, Geboes K, Chamaillard M, Ouwehand A, Leyer G, Carcano D, Colombel JF, Ardid D, Desreumaux P (2007) Lactobacillus acidophilus modulates intestinal pain and induces opioid and cannabinoid receptors. Nat Med 13:35-37.
64. Ryberg E, Larsson N, Sjögren S, Hjorth S, Hermansson NO, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley PJ (2007) The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol 152:1092-1101.
65. Salio C, Doly S, Fischer J, Franzoni MF, Conrath M (2002a) Neuronal and astrocytic localization of the cannabinoid receptor-1 in the dorsal horn of the rat spinal cord. Neurosci Lett 329:13-16.
66. Salio C, Fischer J, Franzoni MF, Conrath M (2002b) Pre- and postsynaptic localizations of the CB1 cannabinoid receptor in the dorsal horn of the rat spinal cord. Neuroscience 110:755-764.
67. Sanson M, Bueno L, Fioramonti J (2006) Involvement of cannabinoid receptors in inflammatory hypersensitivity to colonic distension in rats. Neurogastroenterol Motil 18:949-956.
68. Shire D, Calandra B, Bouaboula M, Barth F, Rinaldi-Carmona M, Casellas P, Ferrara P (1999) Cannabinoid receptor interactions with the antagonists SR 141716A and SR 144528. Life Sci 65:627-635.
69. Silvestri R, Cascio MG, La Regina G, Piscitelli F, Lavecchia A, Brizzi A, Pasquini S, Botta M, Novellino E, Di Marzo V, Corelli F (2008) Synthesis, cannabinoid receptor affinity, and molecular modeling studies of substituted 1-aryl-5-(1H-pyrrol-1-yl)-1H-pyrazole-3-carboxamides. J Med Chem 51:1560-1576.
70. Storr MA, Sharkey KA (2007) The endocannabinoid system and gut-brain signalling. Curr Opin Pharmacol 7:575-582.
71. Storr MA, Yüce B, Andrews CN, Sharkey KA (2008) The role of the endocannabinoid system in the pathophysiology and treatment of irritable bowel syndrome. Neurogastroenterol Motil 20:857-868.
72. Tammpere A, Brusberg M, Axenborg J, Hirsch I, Larsson H, Lindström E (2005) Evaluation of pseudo-affective responses to noxious colorectal distension in rats by manometric recordings. Pain 116:220-226.
73. Wright KL, Duncan M, Sharkey KA (2008) Cannabinoid CB2 receptors in the gastrointestinal tract: a regulatory system in states of inflammation. Br J Pharmacol 153:263-270.
74. Zimmer A, Zimmer AM, Hohmann AG, Herkenham M, Bonner TI (1999) Increased mortality, hypoactivity, and hypoalgesia in cannabinoid CB1 receptor knockout mice. Proc Natl Acad Sci U S A 96:5780-5785.