Pivotal Advance: Cannabinoid-2 receptor agonist HU-308 protects against hepatic ischemia/reperfusion injury by attenuating oxidative stress, inflammatory response, and apoptosis

Journal of Leukocyte Biology

Volumn 82, Issue 6, 2007, Pages 1382-1389

  Rajesh, Mohanraj ^a   Pan, Hao ^a   Mukhopadhyay, Partha ^a   Bátkai, Sándor ^a   Osei Hyiaman, Douglas ^a   Haskó, György ^b   Liaudet, Lucas ^c   Gao, Bin ^a   Pacher, Pál ^a  

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

^b RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

Adhesion; Endothelial activation; Inflammation; TNF

Indexed keywords

4 [4 (1,1 DIMETHYLHEPTYL) 2,6 DIMETHOXYPHENYL] 6,6 DIMETHYLBICYCLO[3.1.1]HEPT 2 EN 2 YLMETHANOL; ALANINE AMINOTRANSFERASE; CANNABINOID 2 RECEPTOR; CASPASE 3; DNA FRAGMENT; INTERCELLULAR ADHESION MOLECULE 1; LACTATE DEHYDROGENASE; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MACROPHAGE INFLAMMATORY PROTEIN 2; TUMOR NECROSIS FACTOR ALPHA; VASCULAR CELL ADHESION MOLECULE 1; AUTACOID; CANNABINOID; CANNABINOID RECEPTOR; CHEMOKINE; PEROXIDASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL ADHESION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVITY; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; LIPID PEROXIDATION; LIVER INJURY; LIVER ISCHEMIA; LIVER SINUSOID; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPERFUSION INJURY; ANIMAL; BLOOD; CYTOLOGY; DRUG EFFECT; DRUG POTENTIATION; ENZYMOLOGY; ISCHEMIA; LEUKOCYTE; LIVER; METABOLISM; PATHOLOGY;

ALANINE TRANSAMINASE; ANIMALS; APOPTOSIS; CANNABINOIDS; CELL ADHESION; CHEMOKINES; ENDOTHELIAL CELLS; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; INTERCELLULAR ADHESION MOLECULE-1; ISCHEMIA; L-LACTATE DEHYDROGENASE; LEUKOCYTES; LIPID PEROXIDATION; LIVER; MICE; OXIDATIVE STRESS; PEROXIDASE; RECEPTORS, CANNABINOID; REPERFUSION INJURY; TUMOR NECROSIS FACTOR-ALPHA; VASCULAR CELL ADHESION MOLECULE-1;

EID: 37249091964     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0307180     Document Type: Article

References (59)

1. Fan, C., Zwacka, R. M., Engelhardt, J. F. (1999) Therapeutic approaches for ischemia/reperfusion injury in the liver. J. Mol. Med. 77, 577-592.
2. Jaeschke, H., Lemasters, J. J. (2003) Apoptosis versus oncotic necrosis in hepatic ischemia/reperfusion injury. Gastroenterology 125, 1246-1257.
3. Kupiec-Weglinski, J. W., Busuttil, R. W. (2005) Ischemia and reperfusion injury in liver transplantation. Transplant. Proc. 37, 1653-1656.
4. Husted, T. L., 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.
5. Szabo, G., Bahrle, S. (2005) Role of nitrosative stress and poly(ADP-ribose) polymerase activation in myocardial reperfusion injury. Curr. Vasc. Pharmacol. 3, 215-220.
6. Pacher, P., Nivorozhkin, A., Szabo, C. (2006) Therapeutic effects of xanthine oxidase inhibitors: renaissance half a century after the discovery of allopurinol. Pharmacol. Rev. 58, 87-114.
7. Pacher, P., Beckman, J. S., Liaudet, L. (2007) Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87, 315-424.
8. Di Marzo, V., Bifulco, M., De Petrocellis, L. (2004) The endocannabinoid system and its therapeutic exploitation. Nat. Rev. Drug Discov. 3, 771-784.
9. Massa, F., Storr, M., Lutz, B. (2005) The endocannabinoid system in the physiology and pathophysiology of the gastrointestinal tract. J. Mol. Med. 83, 944-954.
10. Gabbay, E., Avraham, Y., Ilan, Y., Israeli, E., Berry, E. M. (2005) Endocannabinoids and liver disease - review. Liver Int. 25, 921-926.
11. Zamora-Valdes, D., Ponciano-Rodriguez, G., Chavez-Tapia, N. C., Mendez-Sanchez, N. (2005) The endocannabinoid system in chronic liver disease. Ann. Hepatol. 4, 248-254.
12. Pacher, P., Batkai, S., Kunos, G. (2005) Cirrhotic cardiomyopathy: an endocannabinoid connection? Br. J. Pharmacol. 146, 313-314.
13. Mallat, A., Lotersztajn, S. (2006) Endocannabinoids as novel mediators of liver diseases. J. Endocrinol. Invest. 29, 58-65.
14. Pacher, P., Batkai, S., Kunos, G. (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol. Rev. 58, 389-462.
15. Kunos, G., Osei-Hyiaman, D., Batkai, S., Gao, B. (2006) Cannabinoids hurt, heal in cirrhosis. Nat. Med. 12, 608-610.
16. Panikashvili, D., Shein, N. A., Mechoulam, R., Trembovler, V., Kohen, R., Alexandrovich, A., Shohami, E. (2006) The endocannabinoid 2-AG protects the blood-brain barrier after closed head injury and inhibits mRNA expression of proinflammatory cytokines. Neurobiol. Dis. 22, 257-264.
17. Panikashvili, D., Mechoulam, R., Beni, S. M., Alexandrovich, A., Shohami, E. (2005) CB1 cannabinoid receptors are involved in neuroprotection via NF-κ B inhibition. J. Cereb. Blood Flow Metab. 25, 477-484.
18. Panikashvili, D., Simeonidou, C., Ben-Shabat, S., Hanus, L., Breuer, A., Mechoulam, R., Shohami, E. (2001) An endogenous cannabinoid (2-AG) is neuroprotective after brain injury. Nature 413, 527-531.
19. Mechoulam, R., Spatz, M., Shohami, E. (2002) Endocannabinoids and neuroprotection. Sci. STKE 2002, RE5.
20. Mechoulam, R., Panikashvili, D., Shohami, E. (2002) Cannabinoids and brain injury: therapeutic implications. Trends Mol. Med. 8, 58-61.
21. Klein, T. W. (2005) Cannabinoid-based drugs as anti-inflammatory therapeutics. Nat. Rev. Immunol. 5, 400-411.
22. Matsuda, L. A., Lolait, S. J., Brownstein, M. J., Young, A. C., Bonner, T. I. (1990) Structure of a cannabinoid receptor and functional expression of the cloned cDNA. Nature 346, 561-564.
23. Batkai, S., Pacher, P., Osei-Hyiaman, D., Radaeva, S., Liu, J., Harvey-White, J., Offertaler, L., Mackie, K., Rudd, M. A., Bukoski, R. D., Kunos, G. (2004) Endocannabinoids acting at cannabinoid-1 receptors regulate cardiovascular function in hypertension. Circulation 110, 1996-2002.
24. Pacher, P., Batkai, S., Osei-Hyiaman, D., Offertaler, L., Liu, J., Harvey-White, J., Brassai, A., Jarai, Z., Cravatt, B. F., 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-H541.
25. Gebremedhin, D., Lange, A. R., Campbell, W. B., Hillard, C. J., Harder, D. R. (1999) Cannabinoid CB1 receptor of cat cerebral arterial muscle functions to inhibit L-type Ca2+ channel current. Am. J. Physiol. 276, H2085-H2093.
26. Liu, J., Gao, B., Mirshahi, F., Sanyal, A. J., Khanolkar, A. D., Makriyannis, A., Kunos, G. (2000) Functional CB1 cannabinoid receptors in human vascular endothelial cells. Biochem. J. 346, 835-840.
27. 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 Jr., N., Sanyal, A. J., Kunos, G. (2001) Endocannabinoids acting at vascular CB1 receptors mediate the vasodilated state in advanced liver cirrhosis. Nat. Med. 7, 827-832.
28. Engeli, S., Bohnke, J., Feldpausch, M., Gorzelniak, K., Janke, J., Batkai, S., Pacher, P., Harvey-White, J., Luft, F. C., Sharma, A. M., Jordan, J. (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54, 2838-2843.
29. Osei-Hyiaman, D., DePetrillo, M., Pacher, P., Liu, J., Radaeva, S., Batkai, S., Harvey-White, J., Mackie, K., Offertaler, L., Wang, L., 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.
30. Teixeira-Clerc, F., Julien, B., Grenard, P., Tran Van Nhieu, J., Deveaux, V., Li, L., Serriere-Lanneau, V., Ledent, C., Mallat, A., Lotersztajn, S. (2006) CB1 cannabinoid receptor antagonism: a new strategy for the treatment of liver fibrosis. Nat. Med. 12, 671-676.
31. Munro, S., Thomas, K. L., Abu-Shaar, M. (1993) Molecular characterization of a peripheral receptor for cannabinoids. Nature 365, 61-65.
32. Van Sickle, M. D., Duncan, M., Kingsley, P. J., Mouihate, A., Urbani, P., Mackie, K., Stella, N., Makriyannis, A., Piomelli, D., Davison, J. S., Marnett, L. J., Di Marzo, V., Pittman, Q. J., Patel, K. D., Sharkey, K. A. (2005) Identification and functional characterization of brainstem cannabinoid CB2 receptors. Science 310, 329-332.
33. Mukhopadhyay, P., Batkai, S., Rajesh, M., Czifra, N., Harvey-White, J., Hasko, G., Zsengeller, Z., Gerard, N. P., Liaudet, L., Kunos, G., Pacher, P. (2007) Pharmacological inhibition of cannabinoid receptor-1 protects against doxorubicin-induced cardiotoxicity. J. Am. Coll. Cardiol. 50, 528-536.
34. Shmist, Y. A., Goncharov, I., Eichler, M., Shneyvays, V., Isaac, A., Vogel, Z., Shainberg, A. (2006) δ-9-Tetrahydrocannabinol protects cardiac cells from hypoxia via CB2 receptor activation and nitric oxide production. Mol. Cell. Biochem. 283, 75-83.
35. Zoratti, C., Kipmen-Korgun, D., Osibow, K., Malli, R., Graier, W. F. (2003) Anandamide initiates Ca(2+) signaling via CB2 receptor linked to phospholipase C in calf pulmonary endothelial cells. Br. J. Pharmacol. 140, 1351-1362.
36. Golech, S. A., McCarron, R. M., Chen, Y., Bembry, J., Lenz, F., Mechoulam, R., Shohami, E., Spatz, M. (2004) Human brain endothelium: coexpression and function of vanilloid and endocannabinoid receptors. Brain Res. Mol. Brain Res. 132, 87-92.
37. Blazquez, C., Casanova, M. L., Planas, A., Del Pulgar, T. G., Villanueva, C., Fernandez-Acenero, M. J., Aragones, J., Huffman, J. W., Jorcano, J. L., Guzman, M. (2003) Inhibition of tumor angiogenesis by cannabinoids. FASEB J. 17, 529-531.
38. Mestre, L., Correa, F., Docagne, F., Clemente, D., Guaza, C. (2006) The synthetic cannabinoid WIN 55,212-2 increases COX-2 expression and PGE2 release in murine brain-derived endothelial cells following Theiler's virus infection. Biochem. Pharmacol. 72, 869-880.
39. Pacher, P., Batkai, S., Kunos, G. (2005) Cardiovascular pharmacology of cannabinoids. Handb. Exp. Pharmacol. 2005, 599-625.
40. Pacher, P., Batkai, S., Kunos, G. (2005) Blood pressure regulation by endocannabinoids and their receptors. Neuropharmacology 48, 1130-1138.
41. Lamontagne, D., Lepicier, P., Lagneux, C., Bouchard, J. F. (2006) The endogenous cardiac cannabinoid system: a new protective mechanism against myocardial ischemia. Arch. Mal. Coeur Vaiss. 99, 242-246.
42. Pertwee, R.G. (2005) Pharmacological actions of cannabinoids. Handb. Exp. Pharmacol. 2005, 1-51.
43. Hanus, L., Breuer, A., Tchilibon, S., Shiloah, S., Goldenberg, D., Horowitz, M., Pertwee, R. G., Ross, R. A., Mechoulam, R., Fride, E. (1999) HU-308: a specific agonist for CB(2), a peripheral cannabinoid receptor. Proc. Natl. Acad. Sci. USA 96, 14228-14233.
44. Batkai, S., Osei-Hyiaman, D., Pan, H., El-Assal, O., Rajesh, M., Mukhopadhyay, P., Hong, F., Harvey-White, J., Jafri, A., Hasko, G., Huffman, J. W., Gao, B., Kunos, G., Pacher, P. (2007) Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury. FASEB J. 21, 1788-1800.
45. Liaudet, L., Murthy, K. G., Mabley, J. G., Pacher, P., Soriano, F. G., Salzman, A. L., 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.
46. Di Filippo, C., Rossi, F., Rossi, S., D'Amico, M. (2004) Cannabinoid CB2 receptor activation reduces mouse myocardial ischemia-reperfusion injury: involvement of cytokine/chemokines and PMN. J. Leukoc. Biol. 75, 453-459.
47. Zhang, M., Martin, B. R., Adler, M. W., Razdan, R. K., Jallo, J. I., Tuma, R. F. (2007) Cannabinoid CB(2) receptor activation decreases cerebral infarction in a mouse focal ischemia/reperfusion model. J. Cereb. Blood Flow Metab. 27, 1387-1396.
48. Ashton, J. C., Rahman, R. M., Nair, S. M., Sutherland, B. A., Glass, M., Appleton, I. (2007) Cerebral hypoxia-ischemia and middle cerebral artery occlusion induce expression of the cannabinoid CB2 receptor in the brain. Neurosci. Lett. 412, 114-117.
49. Schmid, P. C., Krebsbach, R. J., Perry, S. R., Dettmer, T. M., Maasson, J. L., Schmid, H. H. (1995) Occurrence and postmortem generation of anandamide and other long-chain N-acylethanolamines in mammalian brain. FEBS Lett. 375, 117-120.
50. Schabitz, W. R., Giuffrida, A., Berger, C., Aschoff, A., Schwaninger, M., Schwab, S., Piomelli, D. (2002) Release of fatty acid amides in a patient with hemispheric stroke: a microdialysis study. Stroke 33, 2112-2114.
51. Berger, C., Schmid, P. C., Schabitz, W. R., Wolf, M., Schwab, S., Schmid, H. H. (2004) Massive accumulation of N-acylethanolamines after stroke. Cell signaling in acute cerebral ischemia? J. Neurochem. 88, 1159-1167.
52. Muthian, S., Rademacher, D. J., Roelke, C. T., Gross, G. J., Hillard, C. J. (2004) Anandamide content is increased and CB1 cannabinoid receptor blockade is protective during transient, focal cerebral ischemia. Neuroscience 129, 743-750.
53. Kurabayashi, M., Takeyoshi, I., Yoshinari, D., Matsumoto, K., Maruyama, I., Morishita, Y. (2005) 2-Arachidonoylglycerol increases in ischemia-reperfusion injury of the rat liver. J. Invest. Surg. 18, 25-31.
54. Carlos, T. M., Harlan, J. M. (1994) Leukocyte-endothelial adhesion molecules. Blood 84, 2068-2101.
55. Jaeschke, H. (1997) Cellular adhesion molecules: regulation and functional significance in the pathogenesis of liver diseases. Am. J. Physiol. 273, G602-G611.
56. Jaeschke, H., Smith, C. W., Clemens, M. G., Ganey, P. E., Roth, R. A. (1996) Mechanisms of inflammatory liver injury: adhesion molecules and cytotoxicity of neutrophils. Toxicol. Appl. Pharmacol. 139, 213-226.
57. Jaeschke, H. (2006) Mechanisms of liver injury. II. Mechanisms of neutrophil-induced liver cell injury during hepatic ischemia-reperfusion and other acute inflammatory conditions. Am. J. Physiol. Gastrointest. Liver Physiol. 290, G1083-G1088.
58. Ohkohchi, N., Shibuya, H., Tsukamoto, S., Sakurada, M., Oikawa, K., Terashima, T., Satomi, S. (1999) Kupffer's cells modulate neutrophile activity by superoxide anion and tumor necrosis factor-δ in reperfusion injury of liver transplantation-mechanisms of radical generation and reperfusion injury after cold ischemia. Transplant. Proc. 31, 1055-1058.
59. Julien, B., Grenard, P., Teixeira-Clerc, F., Van Nhieu, J. T., Li, L., Karsak, M., Zimmer, A., Mallat, A., Lotersztajn, S. (2005) Antifibrogenic role of the cannabinoid receptor CB2 in the liver. Gastroenterology 128, 742-755.