Abnormal cannabidiol attenuates experimental colitis in mice, promotes wound healing and inhibits neutrophil recruitment

Journal of Inflammation (United Kingdom)

Volumn 13, Issue 1, 2016, Pages

  Krohn, Regina M ^a,b   Parsons, Sean A ^b   Fichna, Jakub ^a,b,d   Patel, Kamala D ^b   Yates, Robin M ^a,b   Sharkey, Keith A ^b,c   Storr, Martin A ^a,b,e  

^a UNIVERSITY OF CALGARY   (Canada)

^b UNIVERSITY OF CALGARY   (Canada)

^c UNIVERSITY OF CALGARY   (Canada)

^d MEDICAL UNIVERSITY OF LODZ   (Poland)

^e UNIVERSITY OF MUNICH   (Germany)

Author keywords

Abnormal cannabidiol; Cannabinoids; Neutrophil recruitment; O 1918; TNBS colitis; Wound healing

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; 1,3 DIMETHOXY 5 METHYL 2 [3 METHYL 6 (1 METHYLETHENYL) 2 CYCLOHEXEN 1 YL]BENZENE; 6 IODO 3 (4 METHOXYBENZOYL) 2 METHYL 1 (2 MORPHOLINOETHYL)INDOLE; ABNORMAL CANNABIDIOL; ANTIINFLAMMATORY AGENT; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; GASTROINTESTINAL AGENT; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; DRUG MECHANISM; ENDOTHELIUM CELL; EPITHELIUM CELL; EXPERIMENTAL COLITIS; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PROPHYLAXIS; WOUND HEALING;

EID: 84979663957     PISSN: None     EISSN: 14769255     Source Type: Journal    
DOI: 10.1186/s12950-016-0129-0     Document Type: Article

References (50)

1. Ben Amar M. Cannabinoids in medicine: A review of their therapeutic potential. J Ethnopharmacol. 2006;105:1-25.
2. Petrocellis LD, Cascio MG, Marzo VD. The endocannabinoid system: a general view and latest additions. Br J Pharmacol. 2004;141:765-74.
3. Izzo AA, Coutts AA. Cannabinoids and the digestive tract. Handb Exp Pharmacol. 2005:573-598. ISSN: 0171-2004.
4. Schicho R, Storr M. Topical and Systemic Cannabidiol Improves Trinitrobenzene Sulfonic Acid Colitis in Mice. Pharmacology. 2012;89:149-55.
5. Booz GW. Cannabidiol as an emergent therapeutic strategy for lessening the impact of inflammation on oxidative stress. Free Radic Biol Med. 2011;51:1054-61.
6. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson NO, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley PJ. The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol. 2007;152:1092-101.
7. Jarai Z, Wagner JA, Varga K, Lake KD, Compton DR, Martin BR, Zimmer AM, Bonner TI, Buckley NE, Mezey E, et al. Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proc Natl Acad Sci U S A. 1999;96:14136-41.
8. Borrelli F, Aviello G, Romano B, Orlando P, Capasso R, Maiello F, Guadagno F, Petrosino S, Capasso F, Di Marzo V, Izzo AA. Cannabidiol, a safe and non-psychotropic ingredient of the marijuana plant Cannabis sativa, is protective in a murine model of colitis. J Mol Med (Berl). 2009;87:1111-21.
9. Schicho R, Bashashati M, Bawa M, McHugh D, Saur D, Hu HM, Zimmer A, Lutz B, Mackie K, Bradshaw HB, et al. The atypical cannabinoid O-1602 protects against experimental colitis and inhibits neutrophil recruitment. Inflamm Bowel Dis. 2011;17:1651-64.
10. McHugh D, Hu S, Rimmerman N, Juknat A, Vogel Z, Walker JM, Bradshaw H. N-arachidonoyl glycine, an abundant endogenous lipid, potently drives directed cellular migration through GPR18, the putative abnormal cannabidiol receptor. BMC Neurosci. 2010;11:44.
11. Johns DG, Behm DJ, Walker DJ, Ao Z, Shapland EM, Daniels DA, Riddick M, Dowell S, Staton PC, Green P, et al. The novel endocannabinoid receptor GPR55 is activated by atypical cannabinoids but does not mediate their vasodilator effects. Br J Pharmacol. 2007;152:825-31.
12. Su EN, Kelly ME, Cringle SJ, Yu DY. Role of Endothelium in Abnormal Cannabidiol-Induced Vasoactivity in Retinal Arterioles. Invest Ophthalmol Vis Sci. 2015;56:4029-37.
13. Kreutz S, Koch M, Bottger C, Ghadban C, Korf HW, Dehghani F. 2-Arachidonoylglycerol elicits neuroprotective effects on excitotoxically lesioned dentate gyrus granule cells via abnormal-cannabidiol-sensitive receptors on microglial cells. Glia. 2009;57:286-94.
14. Frøslie KF, Jahnsen J, Moum BA, Vatn MH. Mucosal Healing in Inflammatory Bowel Disease: Results From a Norwegian Population-Based Cohort. Gastroenterology. 2007;133:412-22.
15. Seidelin JB, Coskun M, Nielsen OH. Mucosal healing in ulcerative colitis: pathophysiology and pharmacology. Adv Clin Chem. 2013;59:101-23.
16. Engel M, Kellerman C, Rau T, Burnat G, Hahn E, Konturek P. Ulcerative colitis in AKR mice is attenuated by intraperitoneally administered anandamide. Acta Physiol Pol. 2008;59:673.
17. Storr MA, Keenan CM, Zhang H, Patel KD, Makriyannis A, Sharkey KA. Activation of the cannabinoid 2 receptor (CB2) protects against experimental colitis. Inflamm Bowel Dis. 2009;15:1678-85.
18. Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology. 1984;87:1344-50.
19. Kimball ES, Wallace NH, Schneider CR, D'Andrea MR, Hornby PJ. Vanilloid receptor 1 antagonists attenuate disease severity in dextran sulphate sodium-induced colitis in mice. Neurogastroenterol Motil. 2004;16:811-8.
20. Cuvelier SL, Patel KD. Shear-dependent eosinophil transmigration on interleukin 4-stimulated endothelial cells: a role for endothelium-associated eotaxin-3. J Exp Med. 2001;194:1699-709.
21. Zimmerman GA, McIntyre TM, Prescott SM. Thrombin stimulates the adherence of neutrophils to human endothelial cells in vitro. J Clin Invest. 1985;76:2235-46.
22. Aepfelbacher M, Essler M, Huber E, Sugai M, Weber PC. Bacterial toxins block endothelial wound repair. Evidence that Rho GTPases control cytoskeletal rearrangements in migrating endothelial cells. Arterioscler Thromb Vasc Biol. 1997;17:1623-9.
23. Offertaler L, Mo FM, Batkai S, Liu J, Begg M, Razdan RK, Martin BR, Bukoski RD, Kunos G. Selective ligands and cellular effectors of a G protein-coupled endothelial cannabinoid receptor. Mol Pharmacol. 2003;63:699-705.
24. Soehnlein O. Multiple Roles for Neutrophils in Atherosclerosis. Circ Res. 2012;110:875-88.
25. Izzo RS, Witkon K, Chen AI, Hadjiyane C, Weinstein MI, Pellecchia C. Interleukin-8 and neutrophil markers in colonic mucosa from patients with ulcerative colitis. Am J Gastroenterol. 1992;87:1447-52.
26. Carlson M, Raab Y, Seveus L, Xu S, Hallgren R, Venge P. Human neutrophil lipocalin is a unique marker of neutrophil inflammation in ulcerative colitis and proctitis. Gut. 2002;50:501-6.
27. Foell D, Kucharzik T, Kraft M, Vogl T, Sorg C, Domschke W, Roth J. Neutrophil derived human S100A12 (EN-RAGE) is strongly expressed during chronic active inflammatory bowel disease. Gut. 2003;52:847-53.
28. Lampinen M, Sangfelt P, Taha Y, Carlson M. Accumulation, activation, and survival of neutrophils in ulcerative colitis: regulation by locally produced factors in the colon and impact of steroid treatment. Int J Colorectal Dis. 2008;23:939-46.
29. Ley K, Laudanna C, Cybulsky MI, Nourshargh S. Getting to the site of inflammation: the leukocyte adhesion cascade updated. Nat Rev Immunol. 2007;7:678-89.
30. Deanfield JE, Halcox JP, Rabelink TJ. Endothelial Function and Dysfunction: Testing and Clinical Relevance. Circulation. 2007;115:1285-95.
31. Sturm A, Dignass AU. Epithelial restitution and wound healing in inflammatory bowel disease. World J Gastroenterol. 2008;14:348-53.
32. Jager S, Stange EF, Wehkamp J. Inflammatory bowel disease: an impaired barrier disease. Langenbecks Arch Surg. 2013;398:1-12.
33. Wright K, Rooney N, Feeney M, Tate J, Robertson D, Welham M, Ward S. Differential expression of cannabinoid receptors in the human colon: cannabinoids promote epithelial wound healing. Gastroenterology. 2005;129:437-53.
34. Molodecky NA, Soon IS, Rabi DM, Ghali WA, Ferris M, Chernoff G, Benchimol EI, Panaccione R, Ghosh S, Barkema HW, Kaplan GG. Increasing incidence and prevalence of the inflammatory bowel diseases with time, based on systematic review. Gastroenterology. 2012;142:46-54. e42; quiz e30.
35. Izzo AA, Sharkey KA. Cannabinoids and the gut: new developments and emerging concepts. Pharmacol Ther. 2010;126:21-38.
36. Izzo AA, Camilleri M. Cannabinoids in intestinal inflammation and cancer. Pharmacol Res. 2009;60:117-25.
37. Pacher P, Mukhopadhyay P, Mohanraj R, Godlewski G, Batkai S, Kunos G. Modulation of the endocannabinoid system in cardiovascular disease: therapeutic potential and limitations. Hypertension. 2008;52:601-7.
38. WHO. CVD Fact Sheet N°317. 2015.
39. D'Argenio G, Valenti M, Scaglione G, Cosenza V, Sorrentini I, Di Marzo V. Up-regulation of anandamide levels as an endogenous mechanism and a pharmacological strategy to limit colon inflammation. FASEB J. 2006;20:568-70.
40. Gatley SJ, Lan R, Pyatt B, Gifford AN, Volkow ND, Makriyannis A. Binding of the non-classical cannabinoid CP 55,940, and the diarylpyrazole AM251 to rodent brain cannabinoid receptors. Life Sci. 1997;61:PL 191-197.
41. Henstridge CM, Balenga NA, Schroder R, Kargl JK, Platzer W, Martini L, Arthur S, Penman J, Whistler JL, Kostenis E, et al. GPR55 ligands promote receptor coupling to multiple signalling pathways. Br J Pharmacol. 2010;160:604-14.
42. Davignon J, Ganz P. Role of Endothelial Dysfunction in Atherosclerosis. Circulation. 2004;109:III-27-32.
43. Chin AC, Parkos CA. Neutrophil transepithelial migration and epithelial barrier function in IBD: potential targets for inhibiting neutrophil trafficking. Ann N Y Acad Sci. 2006;1072:276-87.
44. Kucharzik T, Walsh SV, Chen J, Parkos CA, Nusrat A. Neutrophil transmigration in inflammatory bowel disease is associated with differential expression of epithelial intercellular junction proteins. Am J Pathol. 2001;159:2001-9.
45. Podolsky DK. Inflammatory bowel disease. N Engl J Med. 2002;347:417-29.
46. Daig R, Andus T, Aschenbrenner E, Falk W, Scholmerich J, Gross V. Increased interleukin 8 expression in the colon mucosa of patients with inflammatory bowel disease. Gut. 1996;38:216-22.
47. Izutani R, Loh EY, Reinecker HC, Ohno Y, Fusunyan RD, Lichtenstein GR, Rombeau JL, Macdermott RP. Increased expression of interleukin-8 mRNA in ulcerative colitis and Crohn's disease mucosa and epithelial cells. Inflamm Bowel Dis. 1995;1:37-47.
48. Johnson Z, Proudfoot AE, Handel TM. Interaction of chemokines and glycosaminoglycans: a new twist in the regulation of chemokine function with opportunities for therapeutic intervention. Cytokine Growth Factor Rev. 2005;16:625-36.
49. Shaw SK, Ma S, Kim MB, Rao RM, Hartman CU, Froio RM, Yang L, Jones T, Liu Y, Nusrat A, et al. Coordinated redistribution of leukocyte LFA-1 and endothelial cell ICAM-1 accompany neutrophil transmigration. J Exp Med. 2004;200:1571-80.
50. McHugh D, Tanner C, Mechoulam R, Pertwee RG, Ross RA. Inhibition of human neutrophil chemotaxis by endogenous cannabinoids and phytocannabinoids: evidence for a site distinct from CB1 and CB2. Mol Pharmacol. 2008;73:441-50.