Local activation of cannabinoid CB1 receptors in the urinary bladder reduces the inflammation-induced sensitization of bladder afferents

Molecular Pain

Volumn 7, Issue , 2011, Pages

  Walczak, Jean Sébastien ^a   Cervero, Fernando ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ANTIINFLAMMATORY AGENT; AZ 12646915; CANNABINOID 1 RECEPTOR; UNCLASSIFIED DRUG; VANILLOID RECEPTOR 1; CANNABINOID 2 RECEPTOR; CYCLOPHOSPHAMIDE; TRPV1 PROTEIN, MOUSE; VANILLOID RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLADDER FUNCTION; CONTROLLED STUDY; CYSTITIS; DRUG EFFECT; DRUG MECHANISM; ELECTRIC ACTIVITY; ELECTROPHYSIOLOGY; FEMALE; IMMUNOFLUORESCENCE; IMMUNOREACTIVITY; MOUSE; NERVE FIBER C; NOCICEPTIVE RECEPTOR; NONHUMAN; PRESSURE MEASUREMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; ACTION POTENTIAL; ANIMAL; ANIMAL BEHAVIOR; BLADDER; C57BL MOUSE; COMPLIANCE (PHYSICAL); DRUG POTENTIATION; FLUORESCENT ANTIBODY TECHNIQUE; IN VITRO STUDY; INFLAMMATION; INJECTION; INNERVATION; INTRAVESICAL DRUG ADMINISTRATION; METABOLISM; PATHOLOGY; PATHOPHYSIOLOGY; SENSORY NERVE CELL;

ACTION POTENTIALS; ADMINISTRATION, INTRAVESICAL; ANIMALS; BEHAVIOR, ANIMAL; COMPLIANCE; CYCLOPHOSPHAMIDE; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; INFLAMMATION; INJECTIONS; MICE; MICE, INBRED C57BL; NEURONS, AFFERENT; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2; TRPV CATION CHANNELS; URINARY BLADDER;

EID: 79955679078     PISSN: None     EISSN: 17448069     Source Type: Journal    
DOI: 10.1186/1744-8069-7-31     Document Type: Article

References (54)

1. Tyagi P, Tyagi V, Yoshimura N, Chancellor M. Functional role of cannabinoid receptors in urinary bladder. Indian J Urol 2010, 26:26-35.
2. Merriam FV, Wang ZY, Guerios SD, Bjorling DE. Cannabinoid receptor 2 is increased in acutely and chronically inflamed bladder of rats. Neurosci Lett 2008, 445:130-134.
3. Walczak JS, Price TJ, Cervero F. Cannabinoid CB1 receptors are expressed in the mouse urinary bladder and their activation modulates afferent bladder activity. Neuroscience 2009, 159:1154-1163.
4. Gratzke C, Streng T, Park A, Christ G, Stief CG, Hedlund P, Andersson KE. Distribution and function of cannabinoid receptors 1 and 2 in the rat, monkey and human bladder. J Urol 2009, 181:1939-1948.
5. Tyagi V, Philips BJ, Su R, Smaldone MC, Erickson VL, Chancellor MB, Yoshimura N, Tyagi P. Differential expression of functional cannabinoid receptors in human bladder detrusor and urothelium. J Urol 2009, 181:1932-1938.
6. Hayn MH, Ballesteros I, de Miguel F, Coyle CH, Tyagi S, Yoshimura N, Chancellor MB, Tyagi P. Functional and immunohistochemical characterization of CB1 and CB2 receptors in rat bladder. Urology 2008, 72:1174-1178.
7. Mukerji G, Yiangou Y, Agarwal SK, Anand P. Increased cannabinoid receptor 1-immunoreactive nerve fibers in overactive and painful bladder disorders and their correlation with symptoms. Urology 2010, 75:1514. e1515-1520.
8. Martin RS, Luong LA, Welsh NJ, Eglen RM, Martin GR, MacLennan SJ. Effects of cannabinoid receptor agonists on neuronally-evoked contractions of urinary bladder tissues isolated from rat, mouse, pig, dog, monkey and human. Br J Pharmacol 2000, 129:1707-1715.
9. Pertwee RG, Fernando SR. Evidence for the presence of cannabinoid CB1 receptors in mouse urinary bladder. Br J Pharmacol 1996, 118:2053-2058.
10. Dmitrieva N, Berkley KJ. Contrasting effects of WIN 55212-2 on motility of the rat bladder and uterus. J Neurosci 2002, 22:7147-7153.
11. Hiragata S, Ogawa T, Hayashi Y, Tyagi P, Seki S, Nishizawa O, de Miguel F, Chancellor MB, Yoshimura N. Effects of IP-751, ajulemic acid, on bladder overactivity induced by bladder irritation in rats. Urology 2007, 70:202-208.
12. Gratzke C, Streng T, Stief CG, Downs TR, Alroy I, Rosenbaum JS, Andersson KE, Hedlund P. Effects of Cannabinor, a Novel Selective Cannabinoid 2 Receptor Agonist, on Bladder Function in Normal Rats. Eur Urol 2010,
13. Sanchez Freire V, Burkhard FC, Kessler TM, Kuhn A, Draeger A, Monastyrskaya K. MicroRNAs may mediate the down-regulation of neurokinin-1 receptor in chronic bladder pain syndrome. Am J Pathol 2010, 176:288-303.
14. Jaggar SI, Hasnie FS, Sellaturay S, Rice AS. The anti-hyperalgesic actions of the cannabinoid anandamide and the putative CB2 receptor agonist palmitoylethanolamide in visceral and somatic inflammatory pain. Pain 1998, 76:189-199.
15. Farquhar-Smith WP, Rice AS. Administration of endocannabinoids prevents a referred hyperalgesia associated with inflammation of the urinary bladder. Anesthesiology 2001, 94:507-513. discussion 506A.
16. Cui JH, Kim WM, Lee HG, Kim YO, Kim CM, Yoon MH. Antinociceptive effect of intrathecal cannabinoid receptor agonist WIN 55,212-2 in a rat bone tumor pain model. Neurosci Lett 2011,
17. Zhu CZ, Mikusa JP, Fan Y, Hollingsworth PR, Pai M, Chandran P, Daza AV, Yao BB, Dart MJ, Meyer MD, et al. Peripheral and central sites of action for the non-selective cannabinoid agonist WIN 55,212-2 in a rat model of post-operative pain. Br J Pharmacol 2009, 157:645-655.
18. Welch SP, Thomas C, Patrick GS. Modulation of cannabinoid-induced antinociception after intracerebroventricular versus intrathecal administration to mice: possible mechanisms for interaction with morphine. J Pharmacol Exp Ther 1995, 272:310-321.
19. Fox A, Kesingland A, Gentry C, McNair K, Patel S, Urban L, James I. The role of central and peripheral Cannabinoid1 receptors in the antihyperalgesic activity of cannabinoids in a model of neuropathic pain. Pain 2001, 92:91-100.
20. Yu XH, Cao CQ, Martino G, Puma C, Morinville A, St-Onge S, Lessard E, Perkins MN, Laird JM. A peripherally restricted cannabinoid receptor agonist produces robust anti-nociceptive effects in rodent models of inflammatory and neuropathic pain. Pain 2010, 151:337-344.
21. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, Rubino T, Michalski CW, Marsicano G, Monory K, et al. Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 2007, 10:870-879.
22. Hillsley K, McCaul C, Aerssens J, Peeters PJ, Gijsen H, Moechars D, Coulie B, Grundy D, Stead RH. Activation of the cannabinoid 2 (CB2) receptor inhibits murine mesenteric afferent nerve activity. Neurogastroenterol Motil 2007, 19:769-777.
23. Yuce B, Kemmer M, Qian G, Muller M, Sibaev A, Li Y, Kreis ME, Storr M. Cannabinoid 1 receptors modulate intestinal sensory and motor function in rat. Neurogastroenterol Motil 2010, 22:672-e205.
24. Farquhar-Smith WP, Jaggar SI, Rice AS. Attenuation of nerve growth factor-induced visceral hyperalgesia via cannabinoid CB(1) and CB(2)-like receptors. Pain 2002, 97:11-21.
25. Olivar T, Laird JM. Cyclophosphamide cystitis in mice: behavioural characterisation and correlation with bladder inflammation. Eur J Pain 1999, 3:141-149.
26. Wantuch C, Piesla M, Leventhal L. Pharmacological validation of a model of cystitis pain in the mouse. Neurosci Lett 2007, 421:250-252.
27. Wood R, Eichel L, Messing EM, Schwarz E. Automated noninvasive measurement of cyclophosphamide-induced changes in murine voiding frequency and volume. J Urol 2001, 165:653-659.
28. Vizzard MA, Erdman SL, de Groat WC. Increased expression of neuronal nitric oxide synthase in bladder afferent pathways following chronic bladder irritation. J Comp Neurol 1996, 370:191-202.
29. Dang K, Lamb K, Cohen M, Bielefeldt K, Gebhart GF. Cyclophosphamide-induced bladder inflammation sensitizes and enhances P2X receptor function in rat bladder sensory neurons. J Neurophysiol 2008, 99:49-59.
30. Yoshimura N, de Groat WC. Increased excitability of afferent neurons innervating rat urinary bladder after chronic bladder inflammation. J Neurosci 1999, 19:4644-4653.
31. Yu Y, de Groat WC. Sensitization of pelvic afferent nerves in the in vitro rat urinary bladder-pelvic nerve preparation by purinergic agonists and cyclophosphamide pretreatment. Am J Physiol Renal Physiol 2008, 294:F1146-1156.
32. Sengupta JN, Gebhart GF. Mechanosensitive properties of pelvic nerve afferent fibers innervating the urinary bladder of the rat. J Neurophysiol 1994, 72:2420-2430.
33. Shea VK, Cai R, Crepps B, Mason JL, Perl ER. Sensory fibers of the pelvic nerve innervating the Rat's urinary bladder. J Neurophysiol 2000, 84:1924-1933.
34. Juszczak K, Ziomber A, Wyczolkowski M, Thor PJ. Urodynamic effects of the bladder C-fiber afferent activity modulation in chronic model of overactive bladder in rats. J Physiol Pharmacol 2009, 60:85-91.
35. Giglio D, Aronsson P, Eriksson L, Tobin G. In vitro characterization of parasympathetic and sympathetic responses in cyclophosphamide-induced cystitis in the rat. Basic Clin Pharmacol Toxicol 2007, 100:96-108.
36. Mok MH, Knight GE, Andrews PL, Hoyle CH, Burnstock G. The effects of cyclophosphamide on neurotransmission in the urinary bladder of Suncus murinus, the house musk shrew. J Auton Nerv Syst 2000, 80:130-136.
37. Seybold VS. The role of peptides in central sensitization. Handb Exp Pharmacol 2009, 451-491.
38. Atwood BK, Mackie K. CB2: a cannabinoid receptor with an identity crisis. Br J Pharmacol 2010, 160:467-479.
39. Bracci-Laudiero L, Aloe L, Caroleo MC, Buanne P, Costa N, Starace G, Lundeberg T. Endogenous NGF regulates CGRP expression in human monocytes, and affects HLA-DR and CD86 expression and IL-10 production. Blood 2005, 106:3507-3514.
40. Ma W, Dumont Y, Vercauteren F, Quirion R. Lipopolysaccharide induces calcitonin gene-related peptide in the RAW264.7 macrophage cell line. Immunology 2010, 130:399-409.
41. Wang H, Xing L, Li W, Hou L, Guo J, Wang X. Production and secretion of calcitonin gene-related peptide from human lymphocytes. J Neuroimmunol 2002, 130:155-162.
42. Graham ES, Angel CE, Schwarcz LE, Dunbar PR, Glass M. Detailed characterisation of CB2 receptor protein expression in peripheral blood immune cells from healthy human volunteers using flow cytometry. Int J Immunopathol Pharmacol 2010, 23:25-34.
43. Munro S, Thomas KL, Abu-Shaar M. Molecular characterization of a peripheral receptor for cannabinoids. Nature 1993, 365:61-65.
44. Price TJ, Flores CM. Critical evaluation of the colocalization between calcitonin gene-related peptide, substance P, transient receptor potential vanilloid subfamily type 1 immunoreactivities, and isolectin B4 binding in primary afferent neurons of the rat and mouse. J Pain 2007, 8:263-272.
45. Yoshimura N. Lower urinary tract symptoms (LUTS) and bladder afferent activity. Neurourol Urodyn 2007, 26:908-913.
46. Avelino A, Cruz C, Nagy I, Cruz F. Vanilloid receptor 1 expression in the rat urinary tract. Neuroscience 2002, 109:787-798.
47. Dickson A, Avelino A, Cruz F, Ribeiro-da-Silva A. Peptidergic sensory and parasympathetic fiber sprouting in the mucosa of the rat urinary bladder in a chronic model of cyclophosphamide-induced cystitis. Neuroscience 2006, 139:671-685.
48. Birder LA, Nakamura Y, Kiss S, Nealen ML, Barrick S, Kanai AJ, Wang E, Ruiz G, De Groat WC, Apodaca G, et al. Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 2002, 5:856-860.
49. Daly D, Rong W, Chess-Williams R, Chapple C, Grundy D. Bladder afferent sensitivity in wild-type and TRPV1 knockout mice. J Physiol 2007, 583:663-674.
50. Hermann H, De Petrocellis L, Bisogno T, Schiano Moriello A, Lutz B, Di Marzo V. Dual effect of cannabinoid CB1 receptor stimulation on a vanilloid VR1 receptor-mediated response. Cell Mol Life Sci 2003, 60:607-616.
51. Patwardhan AM, Jeske NA, Price TJ, Gamper N, Akopian AN, Hargreaves KM. The cannabinoid WIN 55,212-2 inhibits transient receptor potential vanilloid 1 (TRPV1) and evokes peripheral antihyperalgesia via calcineurin. Proc Natl Acad Sci USA 2006, 103:11393-11398.
52. Khandelwal P, Abraham SN, Apodaca G. Cell biology and physiology of the uroepithelium. Am J Physiol Renal Physiol 2009, 297:F1477-1501.
53. Zimmermann M. Ethical guidelines for investigations of experimental pain in conscious animals. Pain 1983, 16:109-110.
54. Rasband WS. ImageJ, U. S. National Institutes of Health, Bethesda, Maryland, USA. 1997, , http://rsb.info.nih.gov/ij/