Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury

FASEB Journal

Volumn 21, Issue 8, 2007, Pages 1788-1800

  Bátkai, Sándor ^a   Osei Hyiaman, Douglas ^a   Pan, Hao ^a   El Assal, Osama ^a   Rajesh, Mohanraj ^a   Mukhopadhyay, Partha ^a   Hong, Feng ^a   Harvey White, Judith ^a   Jafri, Anjum ^a   Haskó, György ^b   Huffman, John W ^c   Gao, Bin ^a   Kunos, George ^a   Pacher, Pál ^a  

^a NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c CLEMSON UNIVERSITY   (United States)

Author keywords

2 arachidonoylglycerol; Anandamide; Endocannabinoids; Oxidative stress; Peroxynitrite

Indexed keywords

CANNABINOID 2 RECEPTOR; ENDOTOXIN; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ADHESION; CELL INFILTRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; IN VITRO STUDY; IN VIVO STUDY; KUPFFER CELL; LIPID PEROXIDATION; LIVER CELL; LIVER ISCHEMIA; MOUSE; NEUTROPHIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REPERFUSION INJURY;

ANIMALS; ARACHIDONIC ACIDS; DISEASE MODELS, ANIMAL; ENDOCANNABINOIDS; GLYCERIDES; HUMANS; INFLAMMATION; LIVER; LIVER DISEASES; MICE; MICE, KNOCKOUT; OXIDATIVE STRESS; POLYUNSATURATED ALKAMIDES; RECEPTOR, CANNABINOID, CB2; REPERFUSION INJURY; UP-REGULATION;

MUS;

EID: 34249788152     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fj.06-7451com     Document Type: Article

References (67)

1. Di Marzo, V., Bifulco, M., and De Petrocellis, L. (2004) The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug. Discov. 3, 771-784
2. Massa, F., Storr, M., and Lutz, B. (2005) The endocannabinoid system in the physiology and pathophysiology of the gastrointestinal tract. J. Mol. Med. 83, 944-954
3. Gabbay, E., Avraham, Y., Ilan, Y., Israeli, E., and Berry, E. M. (2005) Endocannabinoids and liver disease-review. Liver. Int. 25, 921-926
4. Zamora-Valdes, D., Ponciano-Rodriguez, G., Chavez-Tapia, N. C., and Mendez-Sanchez, N. (2005) The endocannabinoid system in chronic liver disease. Ann. Hepatol. 4, 248-254
5. Pacher, P., Batkai, S., and Kunos, G. (2005) Cirrhotic cardiomyopathy: an endocannabinoid connection. Br. J. Pharmacol. 146, 313-314
6. Mallat, A., and Lotersztajn, S. (2006) Endocannabinoids as novel mediators of liver diseases. J. Endocrinol. Invest. 29, 58-65
7. Pacher, P., Batkai, S., and Kunos, G. (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 58, 389-462
8. Kunos, G., Osei-Hyiaman, D., Batkai, S., and Gao, B. (2006) Cannabinoids hurt, heal in cirrhosis. Nat. Med. 12, 608-610
9. Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., and Bonner, T. I. (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564
10. Batkai, S., Pacher, P., Osei-Hyiaman, D., Radaeva, S., Liu, J., Harvey-White, J., Offertaler, L., Mackie, K., Rudd, M. A., Bukoski, R. D., and Kunos, G. (2004) Endocannabinoids acting at cannabinoid-1 receptors regulate cardiovascular function in hypertension. Circulation 110, 1996-2002
11. Pacher, P., Batkai, S., Osei-Hyiaman, D., Offertaler, L., Liu, J., Harvey-White, J., Brassai, A., Jarai, Z., Cravatt, B. F., and Kunos, G. (2005) Hemodynamic profile, responsiveness to anandamide, and baroreflex sensitivity of mice lacking fatty acid amide hydrolase. Am. J. Physiol. Heart. Circ. Physiol. 289, H533-541
12. Gebremedhin, D., Lange, A. R., Campbell, W. B., Hillard, C. J., and Harder, D. R. (1999) Cannabinoid CB1 receptor of cat cerebral arterial muscle functions to inhibit L-type Ca2+ channel current. Amer. J. Physiol. 276, H2085-2093
13. Liu, J., Gao, B., Mirshahi, F., Sanyal, A. J., Khanolkar, A. D., Makriyannis, A., and Kunos, G. (2000) Functional CB1 cannabinoid receptors in human vascular endothelial cells. Biochem. J. 346, Pt. 3, 835-840
14. Batkai, S., Jarai, Z., Wagner, J. A., Goparaju, S. K., Varga, K., Liu, J., Wang, L., Mirshahi, F., Khanolkar, A. D., Makriyannis, A., Urbaschek, R., Garcia, N., Jr., Sanyal, A. J., and Kunos, G. (2001) Endocannabinoids acting at vascular CB1 receptors mediate the vasodilated state in advanced liver cirrhosis. Nat. Med. 7, 827-832
15. Engeli, S., Bohnke, J., Feldpausch, M., Gorzelniak, K., Janke, J., Batkai, S., Pacher, P., Harvey-White, J., Luft, F. C., Sharma, A. M., and Jordan, J. (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54, 2838-2843
16. Osei-Hyiaman, D., DePetrillo, M., Pacher, P., Liu, J., Radaeva, S., Batkai, S., Harvey-White, J., Mackie, K., Offertaler, L., Wang, L., and Kunos, G. (2005) Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J. Clin. Invest. 115, 1298-1305
17. Teixeira-Clerc, F., Julien, B., Grenard, P., Tran Van Nhieu, J., Deveaux, V., Li, L., Serriere-Lanneau, V., Ledent, C., Mallat, A., and Lotersztajn, S. (2006) CB1 cannabinoid receptor antagonism: a new strategy for the treatment of liver fibrosis. Nat. Med. 12, 671-676
18. Munro, S., Thomas, K. L., and Abu-Shaar, M. (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365, 61-65
19. Jarai, Z., Wagner, J. A., Varga, K., Lake, K. D., Compton, D. R., Martin, B. R., Zimmer, A. M., Bonner, T. I., Buckley, N. E., Mezey, E., Razdan, R. K., Zimmer, A., and Kunos, G. (1999) Cannabinoid-induced mesenteric vasodilation through an endothelial site distinct from CB1 or CB2 receptors. Proceed. Nat. Acad. Sci. USA 96, 14136-14141
20. Buckley, N. E., McCoy, K. L., Mezey, E., Bonner, T., Zimmer, A., Felder, C. C., Glass, M., and Zimmer, A. (2000) Immunomodulation by cannabinoids is absent in mice deficient for the cannabinoid CB(2) receptor. Eur. J. Pharmacol. 396, 141-149
21. Batkai, S., Pacher, P., Jarai, Z., Wagner, J. A., and Kunos, G. (2004) Cannabinoid antagonist SR-141716 inhibits endotoxic hypotension by a cardiac mechanism not involving CB1 or CB2 receptors. Am. J. Physiol. Heart. Circ. Physiol. 287, H595-600
22. Milman, G., Maor, Y., Abu-Lafi, S., Horowitz, M., Gallily, R., Batkai, S., Mo, F. M., Offertaler, L., Pacher, P., Kunos, G., and Mechoulam, R. (2006) N-arachidonoyl L-serine, an endocannabinoid-like brain constituent with vasodilatory properties. Proc. Nat. Acad. Sci. USA 103, 2428-2433
23. Ofek, O., Karsak, M., Leclerc, N., Fogel, M., Frenkel, B., Wright, K., Tam, J., Attar-Namdar, M., Kram, V., Shohami, E., Mechoulam, R., Zimmer, A., and Bab, I. (2006) Peripheral cannabinoid receptor, CB2, regulates bone mass. Proc. Nat. Acad. Sci. USA 103, 696-701
24. Fan, C., Zwacka, R. M., and Engelhardt, J. F. (1999) Therapeutic approaches for ischemia/reperfusion injury in the liver. J. Mol. Med. 77, 577-592
25. Jaeschke, H., and Lemasters, J. J. (2003) Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125, 1246-1257
26. Kupiec-Weglinski, J. W., and Busuttil, R. W. (2005) Ischemia and reperfusion injury in liver transplantation. Transpl. Proc. 37, 1653-1656
27. Husted, T. L., and Lentsch, A. B. (2005) Anti-inflammatory approaches to the prevention of ischemia/reperfusion injury in solid organ transplantation. Curr. Opin. Investig. Drugs 6, 508-512
28. Szabo, G., and Bahrle, S. (2005) Role of nitrosative stress and poly(ADP-ribose) polymerase activation in myocardial reperfusion injury. Curr. Vasc. Pharmacol. 3, 215-220
29. Pacher, P., Nivorozhkin, A., and Szabo, C. (2006) Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 58, 87-114
30. Pacher, P., Batkai, S., and Kunos, G. (2005) Cardiovascular pharmacology of cannabinoids. Handbook of Experimental Pharmacology, pp. 599-625
31. Pacher, P., Batkai, S., and Kunos, G. (2005) Blood pressure regulation by endocannabinoids and their receptors. Neuropharmacology 48, 1130-1138
32. Pertwee, R. G. (2005) Pharmacological actions of cannabinoids. Handbook of Experimental Pharmacology, pp. 1-51
33. Huffman, J. W., Liddle, J., Yu, S., Aung, M. M., Abood, M. E., Wiley, J. L., and Martin, B. R. (1999) 3-(1′,1′-Dimethylbutyl)-1-deoxy-delta8- THC and related compounds: synthesis of selective ligands for the CB2 receptor. Bioorg. Med. Chem. 7, 2905-2914
34. Elmes, S. J., Jhaveri, M. D., Smart, D., Kendall, D. A., and Chapman, V. (2004) Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naive rats and in rat models of inflammatory and neuropathic pain. Eur. J. Neurosci. 20, 2311-2320
35. Elmes, S. J., Winyard, L. A., Medhurst, S. J., Clayton, N. M., Wilson, A. W., Kendall, D. A., and Chapman, V. (2005) Activation of CB1 and CB2 receptors attenuates the induction and maintenance of inflammatory pain in the rat. Pain 118, 327-335
36. Kimball, E. S., Schneider, C. R., Wallace, N. H., and Hornby, P. J. (2006) Agonists of cannabinoid receptor 1 and 2 inhibit experimental colitis induced by oil of mustard and by dextran sulfate sodium. Amer. J. Physiol. 291, G364-371
37. Huffman, J. W. (2005) CB2 receptor ligands. Mini Rev. Med. Chem. 5, 641-649
38. Liaudet, L., Murthy, K. G., Mabley, J. G., Pacher, P., Soriano, F. G., Salzman, A. L., and Szabo, C. (2002) Comparison of inflammation, organ damage, and oxidant stress induced by Salmonella enterica serovar Muenchen flagellin and serovar Enteritidis lipopolysaccharide. Infect. Immun. 70, 192-198
39. Bhunia, A. K., Arai, T., Bulkley, G., and Chatterjee, S. (1998) Lactosylceramide mediates tumor necrosis factor-alpha-induced intercellular adhesion molecule-1 (ICAM-1) expression and the adhesion of neutrophil in human umbilical vein endothelial cells. J. Biol. Chem. 273, 34349-34357
40. Arai, T., Bhunia, A. K., Chatterjee, S., and Bulkley, G. B. (1998) Lactosylceramide stimulates human neutrophils to upregulate Mac-1, adhere to endothelium, and generate reactive oxygen metabolites in vitro. Circ. Res. 82, 540-547
41. Wang, L., Liu, J., Harvey-White, J., Zimmer, A., and Kunos, G. (2003) Endocannabinoid signaling via cannabinoid receptor 1 is involved in ethanol preference and its age-dependent decline in mice. Proc. Nat. Acad. Sci. USA 100, 1393-1398
42. Pacher, P., Batkai, S., and Kunos, G. (2004) Haemodynamic profile and responsiveness to anandamide of TRPV1 receptor knock-out mice. J. Physiol. 558, 647-657
43. Pacher, P., Beckman, J. S., and Liaudet, L. (2007) Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315-424
44. Schmid, P. C., Krebsbach, R. J., Perry, S. R., Dettmer, T. M., Maasson, J. L., and Schmid, H. H. (1995) Occurrence and postmortem generation of anandamide and other long-chain N-acylethanolamines in mammalian brain. FEBS Lett. 375, 117-120
45. Schabitz, W. R., Giuffrida, A., Berger, C., Aschoff, A., Schwaninger, M., Schwab, S., and Piomelli, D. (2002) Release of fatty acid amides in a patient with hemispheric stroke: a microdialysis study. Stroke 33, 2112-2114
46. Berger, C., Schmid, P. C., Schabitz, W. R., Wolf, M., Schwab, S., and Schmid, H. H. (2004) Massive accumulation of N-acylethanolamines after stroke. Cell signalling in acute cerebral ischemia. J. Neurochem. 88, 1159-1167
47. Muthian, S., Rademacher, D. J., Roelke, C. T., Gross, G. J., and Hillard, C. J. (2004) Anandamide content is increased and CB1 cannabinoid receptor blockade is protective during transient, focal cerebral ischemia. Neuroscience 129, 743-750
48. Nagayama, T., Sinor, A. D., Simon, R. P., Chen, J., Graham, S. H., Jin, K., and Greenberg, D. A. (1999) Cannabinoids and neuroprotection in global and focal cerebral ischemia and in neuronal cultures. J. Neurosci. 19, 2987-2995
49. Sinor, A. D., Irvin, S. M., and Greenberg, D. A. (2000) Endocannabinoids protect cerebral cortical neurons from in vitro ischemia in rats. Neurosci. Lett. 278, 157-160
50. Mauler, F., Mittendorf, J., Horvath, E., and De Vry, J. (2002) Characterization of the diarylether sulfonylester (-)-(R)-3-(2- hydroxymethylindanyl-4-oxy)phenyl-4,4,4-trifluoro-1-sulfonate (BAY 38-7271) as a potent cannabinoid receptor agonist with neuroprotective properties. J. Pharmacol. Exp. Ther. 302, 359-368
51. Parmentier-Batteur, S., Jin, K., Mao, X. O., Xie, L., and Greenberg, D. A. (2002) Increased severity of stroke in CB1 cannabinoid receptor knock-out mice. J. Neurosci. 22, 9771-9775
52. Leker, R. R., Gai, N., Mechoulam, R., and Ovadia, H. (2003) Drug-induced hypothermia reduces ischemic damage: effects of the cannabinoid HU-210. Stroke. 34, 2000-2006
53. Hayakawa, K., Mishima, K., Abe, K., Hasebe, N., Takamatsu, F., Yasuda, H., Ikeda, T., Inui, K., Egashira, N., Iwasaki, K., and Fujiwara, M. (2004) Cannabidiol prevents infarction via the non-CB1 cannabinoid receptor mechanism. Neuroreport 15, 2381-2385
54. Louw, D. F., Yang, F. W., and Sutherland, G. R. (2000) The effect of delta-9-tetrahydrocannabinol on forebrain ischemia in rat. Brain. Res. 857, 183-187
55. Lamontagne, D., Lepicier, P., Lagneux, C., and Bouchard, J. F. (2006) The endogenous cardiac cannabinoid system: a new protective mechanism against myocardial ischemia. Arch. Mal. Coeur. Vaiss. 99, 242-246
56. Di Filippo, C., Rossi, F., Rossi, S., and D'Amico, M. (2004) Cannabinoid CB2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: involvement of cytokine/chemokines and PMN. J. Leuk. Biol. 75, 453-459
57. Jaeschke, H., Smith, C. W., Clemens, M. G., Ganey, P. E., and Roth, R. A. (1996) Mechanisms of inflammatory liver injury: adhesion molecules and cytotoxicity of neutrophils. Toxicol. Appl. Pharmacol. 139, 213-226
58. Jaeschke, H. (1997) Cellular adhesion molecules: regulation and functional significance in the pathogenesis of liver diseases. Amer. J. Physiol. 273, G602-611
59. Jaeschke, H. (2006) Mechanisms of liver injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemiareperfusion and other acute inflammatory conditions. Amer. J. Physiol. 290, G1083-1088
60. Ohkohchi, N., Shibuya, H., Tsukamoto, S., Sakurada, M., Oikawa, K., Terashima, T., and Satomi, S. (1999) Kupffer's cells modulate neutrophile activity by superoxide anion and tumor necrosis factor-delta in reperfusion injury of liver transplantation-mechanisms of radical generation and reperfusion injury after cold ischemia. Transplantation Proc. 31, 1055-1058
61. Carlos, T. M., and Harlan, J. M. (1994) Leukocyte-endothelial adhesion molecules. Blood 84, 2068-2101
62. Walter, L., and Stella, N. (2004) Cannabinoids and neuroinflammation. Br. J. Pharmacol. 141, 775-785
63. Maresz, K., Carrier, E. J., Ponomarev, E. D., Hillard, C. J., and Dittel, B. N. (2005) Modulation of the cannabinoid CB2 receptor in microglial cells in response to inflammatory stimuli. J. Neurochem. 95, 437-445
64. Klein, T. W. (2005) Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat. Rev. Immunol. 5, 400-411
65. Siegmund, S. V., Uchinami, H., Osawa, Y., Brenner, D. A., and Schwabe, R. F. (2005) Anandamide induces necrosis in primary hepatic stellate cells. Hepatology 41, 1085-1095
66. Siegmund, S. V., Seki, E., Osawa, Y., Uchinami, H., Cravatt, B. F., and Schwabe, R. F. (2006) Fatty acid amide hydrolase determines anandamide-induced cell death in the liver. J. Biol. Chem. 281, 10431-10438
67. Julien, B., Grenard, P., Teixeira-Clerc, F., Van Nhieu, J. T., Li, L., Karsak, M., Zimmer, A., Mallat, A., and Lotersztajn, S. (2005) Antifibrogenic role of the cannabinoid receptor CB2 in the liver. Gastroenterology 128, 742-755