Attenuation of Cystitis and Pain Sensation in Mice Lacking Fatty Acid Amide Hydrolase

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• 作者：Zun-Yi Wang (1)
  Peiqing Wang (1)
  Cecilia J. Hillard (2)
  Dale E. Bjorling (1) (3)
  
  1. Department of Surgical Sciences ; University of Wisconsin ; Madison ; WI ; USA
  2. Department of Pharmacology and Toxicology and Neuroscience Research Center ; Medical College of Wisconsin ; Milwaukee ; WI ; USA
  3. Department of Urology ; University of Wisconsin ; Madison ; WI ; USA
  
• 关键词：Fatty acid amide hydrolase ; N ; arachidonoylethanolamine ; Cystitis ; Pain ; Mice
• 刊名：Journal of Molecular Neuroscience
• 出版年：2015
• 出版时间：April 2015
• 年：2015
• 卷：55
• 期：4
• 页码：968-976
• 全文大小：778 KB
• 参考文献：1. Ahn, K, Johnson, DS, Mileni, M, Beidler, D, Long, JZ, McKinney, MK, Weerapana, E, Sadagopan, N, Liimatta, M, Smith, SE, Lazerwith, S, Stiff, C, Kamtekar, S, Bhattacharya, K, Zhang, Y, Swaney, S, Becelaere, K, Stevens, RC, Cravatt, BF (2009) Discovery and characterization of a highly selective FAAH inhibitor that reduces inflammatory pain. Chem Biol 16: pp. 411-420 CrossRef
  2. Aizawa N, Hedlund P, F眉llhase C, Ito H, Homma Y, Igawa Y (2014) Inhibition of peripheral FAAH depresses activities of bladder mechanosensitive Nerve Fibers of the Rat. J Urol
  3. Alvarez-Jaimes, LJ, Palmer, JA (2011) The role of endocannabinoids in pain modulation and the therapeutic potential of inhibiting their enzymatic degradation. Curr Pharm Biotechnol 12: pp. 1644-1659 CrossRef
  4. Anderson, WB, Gould, MJ, Torres, RD, Mitchell, VA, Vaughan, CW (2014) Actions of the dual FAAH/MAGL inhibitor JZL195 in a murine inflammatory pain model. Neuropharmacology 81: pp. 224-230 CrossRef
  5. Birder, L, Andersson, KE (2013) Urothelial signaling. Physiol Rev 93: pp. 653-680 CrossRef
  6. Birder, LA, Nakamura, Y, Kiss, S, Nealen, ML, Barrick, S, Kanai, AJ, Wang, E, Ruiz, G, Groat, WC, Apodaca, G, Watkins, S, Caterina, MJ (2002) Altered urinary bladder function in mice lacking the vanilloid receptor TRPV1. Nat Neurosci 5: pp. 856-860 CrossRef
  7. Bisogno, T, Maccarrone, M (2013) Latest advances in the discovery of fatty acid amide hydrolase inhibitors. Expert Opin Drug Discov 8: pp. 509-522 CrossRef
  8. Bjorling DE, Jerde TJ, Zine MJ, Busser BW, Saban MR, Saban R (1999) Mast cells mediate the severity of experimental cystitis in mice. J Urol 162:231鈥?36
  9. Bjorling DE, Elkahwaji JE, Bushman W, Janda LM, Boldon K, Hopkins WJ, Wang ZY (2007) Acute acrolein-induced cystitis in mice. BJU Int 99:1523鈥?529
  10. Bjorling, DE, Wang, ZY, Bushman, W (2011) Models of inflammation of the lower urinary tract. Neurourol Urodyn 30: pp. 673-682 CrossRef
  11. Blankman, JL, Cravatt, BF (2013) Chemical probes of endocannabinoid metabolism. Pharmacol 65: pp. 849-871
  12. Cencioni, MT, Chiurchi霉, V, Catanzaro, G, Borsellino, G, Bernardi, G, Battistini, L, Maccarrone, M (2010) Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors. PLoS One 5: pp. e8688 CrossRef
  13. Cervero, F, Laird, JM (2004) Understanding the signaling and transmission of visceral nociceptive events. J Neurobiol 61: pp. 45-54 CrossRef
  14. Chang, L, Luo, L, Palmer, JA, Sutton, S, Wilson, SJ, Barbier, AJ, Breitenbucher, JG, Chaplan, SR, Webb, M (2006) Inhibition of fatty acid amide hydrolase produces analgesia by multiple mechanisms. Br J Pharmacol 148: pp. 102-113 CrossRef
  15. Clapper, JR, Moreno-Sanz, G, Russo, R, Guijarro, A, Vacondio, F, Duranti, A, Tontini, A, Sanchini, S, Sciolino, NR, Spradley, JM, Hohmann, AG, Calignano, A, Mor, M, Tarzia, G, Piomelli, D (2010) Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism. Nat Neurosci 13: pp. 1265-1270 CrossRef
  16. Conklin DJ, Haberzettl P, Lesgards JF, Prough RA, Srivastava S, Bhatnagar A (2009) Increased sensitivity of glutathione S-transferase Pnull mice to cyclophosphamide-induced urinary bladder toxicity. J Pharmacol Exp Ther 331:456鈥?69
  17. Cornelissen, LL, Misajet, B, Brooks, DP, Hicks, A (2008) Influence of genetic background and gender on bladder function in the mouse. Auton Neurosci 140: pp. 53-58 CrossRef
  18. Cravatt, BF, Lichtman, AH (2003) Fatty acid amide hydrolase: an emerging therapeutic target in the endocannabinoid system. Curr Opin Chem Biol 7: pp. 469-475 CrossRef
  19. 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: pp. 9371-9376 CrossRef
  20. D鈥橝rgenio, G, Valenti, M, Scaglione, G, Cosenza, V, Sorrentini, I, Marzo, V (2006) Up-regulation of anandamide levels as an endogenous mechanism and a pharmacological strategy to limit colon inflammation. FASEB J 20: pp. 568-570
  21. Daly, DM, Collins, VM, Chapple, CR, Grundy, D (2011) The afferent system and its role in lower urinary tract dysfunction. Curr Opin Urol 21: pp. 268-274 CrossRef
  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: pp. 11253-11263 CrossRef
  23. F眉llhase, C, Russo, A, Castiglione, F, Benigni, F, Campeau, L, Montorsi, F, Gratzke, C, Bettiga, A, Stief, C, Andersson, KE, Hedlund, P (2013) Spinal cord FAAH in normal micturition control and bladder overactivity in awake rats. J Urol 189: pp. 2364-2370 CrossRef
  24. Gandaglia G, Strittmatter F, La Croce G, Benigni F, Bettiga A, Castiglione F, Moschini M, Mistretta F, Gratzke C, Montorsi F, Stief C, Hedlund P (2013) The fatty acid amide hydrolase inhibitor oleoyl ethyl amide counteracts bladder overactivity in female rats. Neurourol Urodyn
  25. Gonzalez, EJ, Merrill, L, Vizzard, MA (2014) Bladder sensory physiology: neuroactive compounds and receptors, sensory transducers, and target-derived growth factors as targets to improve function. Am J Physiol Regul Integr Comp Physiol 306: pp. R869-R878 CrossRef
  26. Gratzke, C, Streng, T, Park, A, Christ, G, Stief, CG, Hedlund, P, Andersson, KE (2009) Distribution and function of cannabinoid receptors 1 and 2 in the rat, monkey and human bladder. J Urol 181: pp. 1939-1948 CrossRef
  27. Gratzke, C, Streng, T, Stief, CG, Downs, TR, Alroy, I, Rosenbaum, JS, Andersson, KE, Hedlund, P (2010) Effects of cannabinor, a novel selective cannabinoid 2 receptor agonist, on bladder function in normal rats. Eur Urol 57: pp. 1093-1100 CrossRef
  28. Hedlund, P (2014) Cannabinoids and the endocannabinoid system in lower urinary tract function and dysfunction. Neurourol Urodyn 33: pp. 46-53 CrossRef
  29. Hill WG. Control of urinary drainage and voiding (2014) Clin J Am Soc Nephrol
  30. Hillard, CJ, Manna, S, Greenberg, MJ, DiCamelli, R, Ross, RA, Stevenson, LA, Murphy, V, Pertwee, RG, Campbell, WB (1999) Synthesis and characterization of potent and selective agonists of the neuronal cannabinoid receptor (CB1). J Pharmacol Exp Ther 289: pp. 1427-1433
  31. Jayamanne, A, Greenwood, R, Mitchell, VA, Aslan, S, Piomelli, D, Vaughan, CW (2006) Actions of the FAAH inhibitor URB597 in neuropathic and inflammatory chronic pain models. Br J Pharmacol 147: pp. 281-288 CrossRef
  32. Keay SK, Birder LA, Chai TC (2014) Evidence for bladder urothelial pathophysiology in functional bladder disorders. Biomed Res Int
  33. Kinsey, SG, Naidu, PS, Cravatt, BF, Dudley, DT, Lichtman, AH (2011) Fatty acid amide hydrolase blockade attenuates the development of collagen-induced arthritis and related thermal hyperalgesia in mice. Pharmacol Biochem Behav 99: pp. 718-725 CrossRef
  34. Klinger, MB, Dattilio, A, Vizzard, MA (2007) Expression of cyclooxygenase-2 in urinary bladder in rats with cyclophosphamide-induced cystitis. Am J Physiol Regul Integr Comp Physiol 293: pp. R677-R685 CrossRef
  35. Krishnan, G, Chatterjee, N (2012) Endocannabinoids alleviate proinflammatory conditions by modulating innate immune response in muller glia during inflammation. Glia 60: pp. 1629-1645 CrossRef
  36. Lichtman, AH, Shelton, CC, Advani, T, Cravatt, BF (2004) Mice lacking fatty acid amide hydrolase exhibit a cannabinoid receptor-mediated phenotypic hypoalgesia. Pain 109: pp. 319-327 CrossRef
  37. Maione, S, Costa, B, Marzo, V (2013) Endocannabinoids: a unique opportunity to develop multitarget analgesics. Pain 154: pp. S87-S93 CrossRef
  38. Malley, SE, Vizzard, MA (2002) Changes in urinary bladder cytokine mRNA and protein after cyclophosphamide-induced cystitis. Physiol Genomics 9: pp. 5-13 CrossRef
  39. Massa, F, Marsicano, G, Hermann, H, Cannich, A, Monory, K, Cravatt, BF, Ferri, GL, Sibaev, A, Storr, M, Lutz, B (2004) The endogenous cannabinoid system protects against colonic inflammation. J Clin Invest 113: pp. 1202-1209 CrossRef
  40. Merriam FV, Wang ZY, Hillard CJ, Stuhr KL, Bjorling DE (2011) Inhibition of fatty acid amide hydrolase suppresses referred hyperalgesia induced by bladder inflammation. BJU Int 108:1145鈥?149
  41. Merrill L, Malley S, Vizzard MA (2013) Repeated variate stress in male rats induces increased voiding frequency, somatic sensitivity, and urinary bladder nerve growth factor expression. Am J Physiol Regul Integr Comp Physiol 305:R147鈥?6
  42. Patel, S, Rademacher, DJ, Hillard, CJ (2003) Differential regulation of the endocannabinoids anandamide and 2-arachidonylglycerol within the limbic forebrain by dopamine receptor activity. J Pharmacol Exp Ther 306: pp. 880-888 CrossRef
  43. Salaga M, Mokrowiecka A, Zakrzewski PK, Cygankiewicz A, Leishman E, Sobczak M, Zatorski H, Ma艂ecka-Panas E, Kordek R, Storr M, Krajewska WM, Bradshaw HB, Fichna J (2014)a Experimental colitis in mice is attenuated by changes in the levels of endocannabinoid metabolites induced by selective inhibition of fatty acid amide hydrolase (FAAH). J Crohns Colitis
  44. Salaga M, Sobczak M, Fichna J (2014)b Inhibition of fatty acid amide hydrolase (FAAH) as a novel therapeutic strategy in the treatment of pain and inflammatory diseases in the gastrointestinal tract. Eur J Pharm Sci
  45. Schlosburg, JE, Kinsey, SG, Lichtman, AH (2009) Targeting fatty acid amide hydrolase (FAAH) to treat pain and inflammation. AAPS J 11: pp. 39-44 CrossRef
  46. Schrepf A, O鈥橠onnell M, Luo Y, Bradley CS, Kreder K, Lutgendorf S (2014) Inflammation and inflammatory control in interstitial cystitis/bladder pain syndrome: associations with painful symptoms. Multidisciplinary Approach to the Study of Chronic Pelvic Pain (MAPP) Research Network. Pain
  47. Selo-Ojeme, DO, Onwude, JL (2004) Diagnostic criteria, classification, and nomenclature for painful bladder syndrome/interstitial cystitis: an ESSIC proposal. Interstitial cystitis. J Obstet Gynaecol 24: pp. 216-225 CrossRef
  48. Stanford, EJ, Dell, JR, Parsons, CL (2007) The emerging presence of interstitial cystitis in gynecologic patients with chronic pelvic pain. Urology 69: pp. 53-59 CrossRef
  49. Storr, MA, Keenan, CM, Emmerdinger, D, Zhang, H, Y眉ce, B, Sibaev, A, Massa, F, Buckley, NE, Lutz, B, G枚ke, B, Brand, S, Patel, KD, Sharkey, KA (2008) Targeting endocannabinoid degradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors. J Mol Med (Berl) 86: pp. 925-936 CrossRef
  50. Storr, MA, Keenan, CM, Zhang, H, Patel, KD, Makriyannis, A, Sharkey, KA (2009) Activation of the cannabinoid 2 receptor (CB2) protects against experimental colitis. Inflamm Bowel Dis 15: pp. 1678-1685 CrossRef
  51. Strittmatter, F, Gandaglia, G, Benigni, F, Bettiga, A, Rigatti, P, Montorsi, F, Gratzke, C, Stief, C, Colciago, G, Hedlund, P (2012) Expression of fatty acid amide hydrolase (FAAH) in human, mouse, and rat urinary bladder and effects of FAAH inhibition on bladder function in awake rats. Eur Urol 61: pp. 98-106 CrossRef
  52. Tambaro S, Casu MA, Mastinu A, Lazzari P (2014) Evaluation of selective cannabinoid CB(1) and CB(2) receptor agonists in a mouse model of lipopolysaccharide-induced interstitial cystitis. Eur J Pharmacol
  53. Tripp DA, Nickel JC, Wong J, Pontari M, Moldwin R, Mayer R, Carr LK, Doggweiler R, Yang CC, Mishra N, Nordling J (2012) Mapping of pain phenotypes in female patients with bladder pain syndrome/interstitial cystitis and controls. Eur Urol 62:1188鈥?194
  54. Tyagi, V, Philips, BJ, Su, R, Smaldone, MC, Erickson, VL, Chancellor, MB, Yoshimura, N, Tyagi, P (2009) Differential expression of functional cannabinoid receptors in human bladder detrusor and urothelium. J Urol 181: pp. 1932-1938 CrossRef
  55. Merwe, JP, Nordling, J, Bouchelouche, P, Bouchelouche, K, Cervigni, M, Daha, LK, Elneil, S, Fall, M, Hohlbrugger, G, Irwin, P, Mortensen, S, Ophoven, A, Osborne, JL, Peeker, R, Richter, B, Riedl, C, Sairanen, J, Tinzl, M, Wyndaele, JJ (2008) Visceral pain is the most debilitating symptom of painful bladder syndrome. Eur Urol 53: pp. 60-67 CrossRef
  56. Walczak, JS, Cervero, F (2011) Local activation of cannabinoid CB1 receptors in the urinary bladder reduces the inflammation-induced sensitization of bladder afferents. Mol Pain 7: pp. 31 CrossRef
  57. Wang, ZY, Wang, P, Merriam, FV, Bjorling, DE (2008) Lack of TRPV1 inhibits cystitis-induced increased mechanical sensitivity in mice. Pain 139: pp. 158-167 CrossRef
  58. Wang, ZY, Wang, P, Bjorling, DE (2009) Role of mast cells and protease-activated receptor-2 in cyclooxygenase-2 expression in urothelial cells. Am J Physiol Regul Integr Comp Physiol 297: pp. R1127-R1135 CrossRef
  59. Wang, ZY, Wang, P, Bjorling, DE (2013) Activation of cannabinoid receptor 2 inhibits experimental cystitis. Am J Physiol Regul Integr Comp Physiol 304: pp. R846-R853 CrossRef
  60. Wang, ZY, Wang, P, Bjorling, DE (2014) Treatment with a cannabinoid receptor 2 agonist decreases severity of established cystitis. J Urol 191: pp. 1153-1158 CrossRef
  61. Wise, LE, Cannavacciulo, R, Cravatt, BF, Martin, BF, Lichtman, AH (2007) Evaluation of fatty acid amides in the carrageenan-induced paw edema model. Neuropharmacology 54: pp. 181-188 CrossRef
  
• 刊物主题：Neurosciences; Neurochemistry; Cell Biology; Proteomics; Neurology;
• 出版者：Springer US
• ISSN：1559-1166

文摘

Endocannabinoids, such as N-arachidonoylethanolamine (AEA, also called anandamide), exert potent analgesic and anti-inflammatory effects. Fatty acid amide hydrolase (FAAH) is primarily responsible for degradation of AEA, and deletion of FAAH increases AEA content in various tissues. Since FAAH has been shown to be present in the bladder of various species, we compared bladder function, severity of experimental cystitis, and cystitis-associated referred hyperalgesia in male wild-type (WT) and FAAH knock-out (KO) mice. Basal concentrations of AEA were greater, and the severity of cyclophosphamide (CYP)-induced cystitis was reduced in bladders from FAAH KO compared to WT mice. Cystitis-associated increased peripheral sensitivity to mechanical stimuli and enhanced bladder activity (as reflected by increased voiding frequency) were attenuated in FAAH KO compared to WT mice. Further, abundances of mRNA for several pro-inflammatory compounds were increased in the bladder mucosa after CYP treatment of WT mice, and this increase was inhibited in FAAH KO mice. These data indicate that endogenous substrates of FAAH, including the cannabinoid AEA, play an inhibitory role in bladder inflammation and subsequent changes in pain perception. Therefore, FAAH could be a therapeutic target to treat clinical symptoms of painful inflammatory bladder diseases.