Multitarget Fatty acid amide hydrolase/cyclooxygenase blockade suppresses intestinal inflammation and protects against nonsteroidal anti-inflammatory drug-dependent gastrointestinal damage

FASEB Journal

Volumn 29, Issue 6, 2015, Pages 2616-2627

  Sasso, Oscar ^a   Migliore, Marco ^a   Habrant, Damien ^a,d   Armirotti, Andrea ^a   Albani, Clara ^a   Summa, Maria ^a   Moreno Sanz, Guillermo ^b   Scarpelli, Rita ^a   Piomelli, Daniele ^a,b,c  

^a ISTITUTO ITALIANO DI TECNOLOGIA   (Italy)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d IN CELL ART   (France)

Author keywords

Anandamide; Cannabinoid receptor; Inflammatory bowel disease; Multitarget inhibitors

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 6 OXOPROSTAGLANDIN F1 ALPHA; ANANDAMIDE; ARN 2508; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENDOCANNABINOID; FATTY ACID AMIDASE; FATTY ACID AMIDASE INHIBITOR; FLURBIPROFEN; NONSTEROID ANTIINFLAMMATORY AGENT; PROSTACYCLIN; PROSTAGLANDIN E2; PROSTAGLANDIN SYNTHASE INHIBITOR; UNCLASSIFIED DRUG; AMIDASE; ARN2508; CARBAMIC ACID DERIVATIVE; CARRAGEENAN; ENZYME INHIBITOR; FATTY-ACID AMIDE HYDROLASE; PHENYLPROPIONIC ACID DERIVATIVE;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; COLITIS; CONTROLLED STUDY; DIGESTIVE SYSTEM INJURY; DRUG BIOAVAILABILITY; DRUG EFFICACY; DRUG MECHANISM; DRUG POTENCY; DRUG SELECTIVITY; DRUG TARGETING; ENTERITIS; ENZYME INHIBITION; GASTROINTESTINAL PROTECTION; IC50; INFLAMMATORY BOWEL DISEASE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RAT; STOMACH PROTECTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMICAL STRUCTURE; CHEMICALLY INDUCED; CHEMISTRY; DRUG EFFECTS; ENZYMOLOGY; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; INFLAMMATION; INTESTINE; METABOLISM; PATHOLOGY; TIME; TREATMENT OUTCOME;

MUS;

AMIDOHYDROLASES; ANIMALS; ANTI-INFLAMMATORY AGENTS, NON-STEROIDAL; CARRAGEENAN; CYCLOOXYGENASE 1; CYCLOOXYGENASE 2; ENZYME INHIBITORS; GASTROINTESTINAL DISEASES; GASTROINTESTINAL TRACT; INFLAMMATION; INTESTINES; MICE; MOLECULAR STRUCTURE; PHENYLCARBAMATES; PHENYLPROPIONATES; TIME FACTORS; TREATMENT OUTCOME;

EID: 84933515012     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.15-270637     Document Type: Article

References (56)

1. Ricciotti, E., and Fitz Gerald, G. A. (2011) Prostaglandins and inflammation. Arterioscler. Thromb. Vasc. Biol. 31, 986-1000
2. Serhan, C. N., Chiang, N., and Van Dyke, T. E. (2008) Resolving inflammation: dual anti-inflammatory and pro-resolution lipid mediators. Nat. Rev. Immunol. 8, 349-361
3. Morisseau, C., and Hammock, B. D. (2013) Impact of soluble epoxide hydrolase and epoxyeicosanoids on human health. Annu. Rev. Pharmacol. Toxicol. 53, 37-58
4. Maccarrone, M., Bari, M., Battista, N., Di Rienzo, M., and Finazzi-Agrò, A. (2001) Endogenous cannabinoids in neuronal and immune cells: toxic effects, levels and degradation. Funct. Neurol. 16 (4, Suppl) 53-60
5. Liu, J., Wang, L., Harvey-White, J., Osei-Hyiaman, D., Razdan, R., Gong, Q., Chan, A. C., Zhou, Z., Huang, B. X., Kim, H. Y., and Kunos, G. (2006) A biosynthetic pathway for anandamide. Proc. Natl. Acad. Sci. USA 103, 13345-13350
6. Massa, F., Marsicano, G., Hermann, H., Cannich, A., Monory, K., Cravatt, B. F., Ferri, G. L., Sibaev, A., Storr, M., and Lutz, B. (2004) The endogenous cannabinoid system protects against colonic inflammation. J. Clin. Invest. 113, 1202-1209
7. Cencioni, M. T., Chiurchiù, V., Catanzaro, G., Borsellino, G., Bernardi, G., Battistini, L., and Maccarrone, M. (2010) Anandamide suppresses proliferation and cytokine release from primary human T-lymphocytes mainly via CB2 receptors. PLoS One 5, e8688
8. Chiurchiù, V., Cencioni, M. T., Bisicchia, E., De Bardi, M., Gasperini, C., Borsellino, G., Centonze, D., Battistini, L., and Maccarrone, M. (2013) Distinct modulation of human myeloid and plasmacytoid dendritic cells by anandamide in multiple sclerosis. Ann. Neurol. 73, 626-636
9. Piomelli, D., and Sasso, O. (2014) Peripheral gating of pain signals by endogenous lipid mediators. Nat. Neurosci. 17, 164-174
10. Storr, M. A., Keenan, C. M., Emmerdinger, D., Zhang, H., Yüce, B., Sibaev, A., Massa, F., Buckley, N. E., Lutz, B., Göke, B., Brand, S., Patel, K. D., and Sharkey, K. A. (2008) Targeting endocannabinoid degradation protects against experimental colitis in mice: involvement of CB1 and CB2 receptors. J. Mol. Med. 86, 925-936
11. Wilson, D. E. (1991) Role of prostaglandins in gastroduodenal mucosal protection. J. Clin. Gastroenterol. 13(Suppl 1), S65-S71
12. Wright, K., Rooney, N., Feeney, M., Tate, J., Robertson, D., Welham, M., and Ward, S. (2005) Differential expression of cannabinoid receptors in the human colon: cannabinoids promote epithelial wound healing. Gastroenterology 129, 437-453
13. Patrono, C., and Baigent, C. (2009) Low-dose aspirin, coxibs, and other NSAIDS: a clinical mosaic emerges. Mol. Interv. 9, 31-39
14. Richardson, D., Pearson, R. G., Kurian, N., Latif, M. L., Garle, M. J., Barrett, D. A., Kendall, D. A., Scammell, B. E., Reeve, A. J., and Chapman, V. (2008) Characterisation of the cannabinoid receptor system in synovial tissue and fluid in patients with osteoarthritis and rheumatoid arthritis. Arthritis Res. Ther. 10, R43
15. Singer, I. I., Kawka, D. W., Schloemann, S., Tessner, T., Riehl, T., and Stenson, W. F. (1998) Cyclooxygenase 2 is induced in colonic epithelial cells in inflammatory bowel disease. Gastroenterology 115, 297-306
16. Di Sabatino, A., Battista, N., Biancheri, P., Rapino, C., Rovedatti, L., Astarita, G., Vanoli, A., Dainese, E., Guerci, M., Piomelli, D., Pender, S. L., MacDonald, T. T., Maccarrone, M., and Corazza, G. R. (2011) The endogenous cannabinoid system in the gut of patients with inflammatory bowel disease. Mucosal Immunol. 4, 574-583
17. Suárez, J., Romero-Zerbo, Y., Márquez, L., Rivera, P., Iglesias, M., Bermúdez-Silva, F. J., Andreu, M., and Rodríguez De Fonseca, F. (2012) Ulcerative colitis impairs the acylethanolamide-based antiinflammatory system reversal by 5-aminosalicylic acid and glucocorticoids. PLoS One 7, e37729
18. Rouzer, C. A., and Marnett, L. J. (2011) Endocannabinoid oxygenation by cyclooxygenases, lipoxygenases, and cytochromes P450: cross-talk between the eicosanoid and endocannabinoid signaling pathways. Chem. Rev. 111, 5899-5921
19. Fowler, C. J., Naidu, P. S., Lichtman, A., and Onnis, V. (2009) The case for the development of novel analgesic agents targeting both fatty acid amide hydrolase and either cyclooxygenase or TRPV1. Br. J. Pharmacol. 156, 412-419
20. Favia, A. D., Habrant, D., Scarpelli, R., Migliore, M., Albani, C., Bertozzi, S. M., Dionisi, M., Tarozzo, G., Piomelli, D., Cavalli, A., and De Vivo, M. (2012) Identification and characterization of carprofen as a multitarget fatty acid amide hydrolase/cyclooxygenase inhibitor. J. Med. Chem. 55, 8807-8826
21. Johnson, D. S., Stiff, C., Lazerwith, S. E., Kesten, S. R., Fay, L. K., Morris, M., Beidler, D., Liimatta, M. B., Smith, S. E., Dudley, D. T., Sadagopan, N., Bhattachar, S. N., Kesten, S. J., Nomanbhoy, T. K., Cravatt, B. F., and Ahn, K. (2011) Discovery of PF-04457845: a highly potent, orally bioavailable, and selective urea FAAH inhibitor. ACS Med. Chem. Lett. 2, 91-96
22. Tarzia, G., Duranti, A., Tontini, A., Piersanti, G., Mor, M., Rivara, S., Plazzi, P. V., Park, C., Kathuria, S., and Piomelli, D. (2003) Design, synthesis, and structure-activity relationships of alkylcarbamic acid aryl esters, a new class of fatty acid amide hydrolase inhibitors. J. Med. Chem. 46, 2352-2360
23. Kathuria, S., Gaetani, S., Fegley, D., Valiño, F., Duranti, A., Tontini, A., Mor, M., Tarzia, G., La Rana, G., Calignano, A., Giustino, A., Tattoli, M., Palmery, M., Cuomo, V., and Piomelli, D. (2003) Modulation of anxiety through blockade of anandamide hydrolysis. Nat. Med. 9, 76-81
24. Clapper, J. R., Moreno-Sanz, G., Russo, R., Guijarro, A., Vacondio, F., Duranti, A., Tontini, A., Sanchini, S., Sciolino, N. R., Spradley, J. M., Hohmann, A. G., Calignano, A., Mor, M., Tarzia, G., and Piomelli, D. (2010) Anandamide suppresses pain initiation through a peripheral endocannabinoid mechanism. Nat. Neurosci. 13, 1265-1270
25. Wallace, J. L., Muscará, M. N., De Nucci, G., Zamuner, S., Cirino, G., Del Soldato, P., and Ongini, E. (2004) Gastric tolerability and prolonged prostaglandin inhibition in the brain with a nitric oxidereleasing flurbiprofen derivative, NCX-2216 [3-[4-(2-fluoro-alphamethyl-[1, 19-biphenyl]-4-acetyloxy)-3-methoxyphenyl]-2-propenoic acid 4-nitrooxy butyl ester]. J. Pharmacol. Exp. Ther. 309, 626-633
26. Chan, C. C., Boyce, S., Brideau, C., Ford-Hutchinson, A. W., Gordon, R., Guay, D., Hill, R. G., Li, C. S., Mancini, J., and Penneton, M. (1995) Pharmacology of a selective cyclooxygenase-2 inhibitor, L-745, 337: a novel nonsteroidal anti-inflammatory agent with an ulcerogenic sparing effect in rat and nonhuman primate stomach. J. Pharmacol. Exp. Ther. 274, 1531-1537
27. Cluny, N. L., Keenan, C. M., Duncan, M., Fox, A., Lutz, B., and Sharkey, K. A. (2010) Naphthalen-1-yl-(4-pentyloxynaphthalen-1-yl) methanone (SAB378), a peripherally restricted cannabinoid CB1/CB2 receptor agonist, inhibits gastrointestinalmotility but has no effect on experimental colitis in mice. J. Pharmacol. Exp. Ther. 334, 973-980
28. Bento, A. F., Claudino, R. F., Dutra, R. C., Marcon, R., and Calixto, J. B. (2011) Omega-3 fatty acid-derived mediators 17 (R)-hydroxy docosahexaenoic acid, aspirin-triggered resolvin D1 and resolvin D2 prevent experimental colitis in mice. J. Immunol. 187, 1957-1969
29. Bayly, C. I., Black, W. C., Léger, S., Ouimet, N., Ouellet, M., and Percival, M. D. (1999) Structure-based design of COX-2 selectivity into flurbiprofen. Bioorg. Med. Chem. Lett. 9, 307-312
30. Morphy, R., and Rankovic, Z. (2006) The physicochemical challenges of designing multiple ligands. J. Med. Chem. 49, 4961-4970
31. Araldi, D., Ferrari, L. F., Lotufo, C. M., Vieira, A. S., Athié, M. C., Figueiredo, J. G., Duarte, D. B., Tambeli, C. H., Ferreira, S. H., and Parada, C. A. (2013) Peripheral inflammatory hyperalgesia depends on the COX increase in the dorsal root ganglion. Proc. Natl. Acad. Sci. USA 110, 3603-3608
32. Mileni, M., Kamtekar, S., Wood, D. C., Benson, T. E., Cravatt, B. F., and Stevens, R. C. (2010) Crystal structure of fatty acid amide hydrolase bound to the carbamate inhibitor URB597: discovery of a deacylating water molecule and insight into enzyme inactivation. J. Mol. Biol. 400, 743-754
33. Kurumbail, R. G., Stevens, A. M., Gierse, J. K., McDonald, J. J., Stegeman, R. A., Pak, J. Y., Gildehaus, D., Miyashiro, J. M., Penning, T. D., Seibert, K., Isakson, P. C., and Stallings, W. C. (1996) Structural basis for selective inhibition of cyclooxygenase-2 by anti-inflammatory agents. Nature 384, 644-648
34. Blobaum, A. L., and Marnett, L. J. (2007) Structural and functional basis of cyclooxygenase inhibition. J. Med. Chem. 50, 1425-1441
35. Risdall, P. C., Adams, S. S., Crampton, E. L., and Marchant, B. (1978) The disposition and metabolism of flurbiprofen in several species including man. Xenobiotica 8, 691-703
36. Wallace, J. L. (2012) NSAID gastropathy and enteropathy: distinct pathogenesis likely necessitates distinct prevention strategies. Br. J. Pharmacol. 165, 67-74
37. Roberts, M. S., Magnusson, B. M., Burczynski, F. J., and Weiss, M. (2002) Enterohepatic circulation: physiological, pharmacokinetic and clinical implications. Clin. Pharmacokinet. 41, 751-790
38. Lauritsen, K., Laursen, L. S., Bukhave, K., and Rask-Madsen, J. (1988) Use of colonic eicosanoid concentrations as predictors of relapse in ulcerative colitis: double blind placebo controlled study on sulphasalazine maintenance treatment. Gut 29, 1316-1321
39. Costa-Romero, M., Coto-Segura, P., Suarez-Saavedra, S., Ramos-Polo, E., and Santos-Juanes, J. (2008) Guttate psoriasis induced by infliximab in a child with Crohn's disease. Inflamm. Bowel Dis. 14, 1462-1463
40. Blackler, R. W., Gemici, B., Manko, A., and Wallace, J. L. (2014) NSAID-gastroenteropathy: new aspects of pathogenesis and prevention. Curr. Opin. Pharmacol. 19, 11-16
41. Shi, Y., Qi, L., Wang, J., Xu, M. S., Zhang, D., Wu, L. Y., and Wu, H. G. (2011) Moxibustion activates mast cell degranulation at the ST25 in rats with colitis. World J. Gastroenterol. 17, 3733-3738
42. Lo Verme, J., Fu, J., Astarita, G., La Rana, G., Russo, R., Calignano, A., and Piomelli, D. (2005) The nuclear receptor peroxisome proliferator-activated receptor-alpha mediates the anti-inflammatory actions of palmitoylethanolamide. Mol. Pharmacol. 67, 15-19
43. Riccardi, L., Mazzon, E., Bruscoli, S., Esposito, E., Crisafulli, C., Di Paola, R., Caminiti, R., Riccardi, C., and Cuzzocrea, S. (2009) Peroxisome proliferator-activated receptor-alpha modulates the anti-inflammatory effect of glucocorticoids in a model of inflammatory bowel disease in mice. Shock 31, 308-316
44. Solorzano, C., Zhu, C., Battista, N., Astarita, G., Lodola, A., Rivara, S., Mor, M., Russo, R., Maccarrone, M., Antonietti, F., Duranti, A., Tontini, A., Cuzzocrea, S., Tarzia, G., and Piomelli, D. (2009) Selective N-acylethanolamine-hydrolyzing acid amidase inhibition reveals a key role for endogenous palmitoylethanolamide in inflammation. Proc. Natl. Acad. Sci. USA 106, 20966-20971
45. Hoffmann, J. C., Pawlowski, N. N., Kuhl, A. A., Hohne, W., and Zeitz, M. (2002) Animal models of inflammatory bowel disease: an overview. Pathobiology 70, 121-130
46. Strober, W., Fuss, I. J., and Blumberg, R. S. (2002) The immunology of mucosal models of inflammation. Annu. Rev. Immunol. 20, 495-549
47. Naidu, P. S., Booker, L., Cravatt, B. F., and Lichtman, A. H. (2009) Synergy between enzyme inhibitors of fatty acid amide hydrolase and cyclooxygenase in visceral nociception. J. Pharmacol. Exp. Ther. 329, 48-56
48. Sasso, O., Bertorelli, R., Bandiera, T., Scarpelli, R., Colombano, G., Armirotti, A., Moreno-Sanz, G., Reggiani, A., and Piomelli, D. (2012) Peripheral FAAH inhibition causes profound antinociception and protects against indomethacin-induced gastric lesions. Pharmacol. Res. 65, 553-563
49. Calignano, A., La Rana, G., Giuffrida, A., and Piomelli, D. (1998) Control of pain initiation by endogenous cannabinoids. Nature 394, 277-281
50. Holt, S., Paylor, B., Boldrup, L., Alajakku, K., Vandevoorde, S., Sundström, A., Cocco, M. T., Onnis, V., and Fowler, C. J. (2007) Inhibition of fatty acid amide hydrolase, a key endocannabinoid metabolizing enzyme, by analogues of ibuprofen and indomethacin. Eur. J. Pharmacol. 565, 26-36
51. Di Paola, R., Esposito, E., Mazzon, E., Paterniti, I., Galuppo, M., and Cuzzocrea, S. (2010) GW0742, a selective PPAR-beta/delta agonist, contributes to the resolution of inflammation after gut ischemia/reperfusion injury. J. Leukoc. Biol. 88, 291-301
52. Russo, R., Lo Verme, J., La Rana, G., D'Agostino, G., Sasso, O., Calignano, A., and Piomelli, D. (2007) Synergistic antinociception by the cannabinoid receptor agonist anandamide and the PPARalpha receptor agonist GW7647. Eur. J. Pharmacol. 566, 117-119
53. Saghatelian, A., McKinney, M. K., Bandell, M., Patapoutian, A., and Cravatt, B. F. (2006) A FAAH-regulated class of N-acyl taurines that activates TRP ion channels. Biochemistry 45, 9007-9015
54. Bradshaw, H. B., Rimmerman, N., Hu, S. S., Burstein, S., and Walker, J. M. (2009) Novel endogenous N-acyl glycines identification and characterization. Vitam. Horm. 81, 191-205
55. Duggan, K. C., Hermanson, D. J., Musee, J., Prusakiewicz, J. J., Scheib, J. L., Carter, B. D., Banerjee, S., Oates, J. A., and Marnett, L. J. (2011) (R)-Profens are substrate-selective inhibitors of endocannabinoid oxygenation by COX-2. Nat. Chem. Biol. 7, 803-809
56. Kappelman, M. D., Rifas-Shiman, S. L., Kleinman, K., Ollendorf, D., Bousvaros, A., Grand, R. J., and Finkelstein, J. A. (2007) The prevalence and geographic distribution of Crohn's disease and ulcerative colitis in the United States. Clin. Gastroenterol. Hepatol. 5, 1424-1429