Protective role of cannabinoid receptor 2 activation in galactosamine/lipopolysaccharide-induced acute liver failure through regulation of macrophage polarization and MicroRNAs

Journal of Pharmacology and Experimental Therapeutics

Volumn 353, Issue 2, 2015, Pages 369-379

  Tomar, Sunil ^a   Zumbrun, Elizabeth E ^a   Nagarkatti, Mitzi ^a,b   Nagarkatti, Prakash S ^a  

^a UNIVERSITY OF SOUTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WJB Dorn VA Medical Center   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

1 DEOXY 3 (1,1 DIMETHYLBUTYL) DELTA8 TETRAHYDROCANNABINOL; ALANINE AMINOTRANSFERASE; ARGINASE 1; CANNABINOID 2 RECEPTOR; GALACTOSAMINE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 3; INTERLEUKIN 10; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MICRORNA 145; MONOCYTE CHEMOTACTIC PROTEIN 1; PLACEBO; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; 1,1-DIMETHYLBUTYL-1-DEOXY-DELTA(9)-THC; CANNABINOID; CNR2 PROTEIN, MOUSE; CYTOKINE; INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE; MICRORNA; TLR4 PROTEIN, MOUSE;

ACUTE LIVER FAILURE; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; APOPTOSIS; ARTICLE; CHEMOPROPHYLAXIS; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; FEMALE; GENE ONTOLOGY; GENE TARGETING; HISTOPATHOLOGY; IMMUNOMODULATION; IMMUNOPHENOTYPING; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY INFILTRATE; LIVER INJURY; LIVER PROTECTION; MACROPHAGE ACTIVATION; MACROPHAGE MIGRATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RECEPTOR UPREGULATION; RNA ANALYSIS; RNA GENE; SIGNAL TRANSDUCTION; UPREGULATION; AGONISTS; ANIMAL; BIOSYNTHESIS; C57BL MOUSE; CHEMICALLY INDUCED; CYTOLOGY; DRUG EFFECTS; GENETICS; IMMUNOLOGY; LIVER; MACROPHAGE; METABOLISM; PATHOLOGY; PHENOTYPE;

ANIMALS; APOPTOSIS; CANNABINOIDS; CYTOKINES; DOWN-REGULATION; FEMALE; GALACTOSAMINE; INTERLEUKIN-1 RECEPTOR-ASSOCIATED KINASES; LIVER; LIVER FAILURE, ACUTE; MACROPHAGES; MICE; MICE, INBRED C57BL; MICRORNAS; PHENOTYPE; RECEPTOR, CANNABINOID, CB2; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 4;

EID: 84941554246     PISSN: 00223565     EISSN: 15210103     Source Type: Journal    
DOI: 10.1124/jpet.114.220368     Document Type: Article

References (45)

1. Adhikary S, Kocieda VP, Yen JH, Tuma RF, and Ganea D (2012) Signaling through cannabinoid receptor 2 suppresses murine dendritic cell migration by inhibiting matrix metalloproteinase 9 expression. Blood 120:3741-3749.
2. Antoniades CG, Berry PA, Wendon JA, and Vergani D (2008) The importance of immune dysfunction in determining outcome in acute liver failure. J Hepatol 49:845-861.
3. Bátkai S, Osei-Hyiaman D, Pan H, El-Assal O, Rajesh M, Mukhopadhyay P, Hong F, Harvey-White J, Jafri A, Haskó G, et al. (2007) Cannabinoid-2 receptor mediates protection against hepatic ischemia/reperfusion injury. FASEB J 21:1788-1800.
4. Bernal W, Auzinger G, Dhawan A, and Wendon J (2010) Acute liver failure. Lancet 376:190-201.
5. Bindea G, Mlecnik B, Hackl H, Charoentong P, Tosolini M, Kirilovsky A, Fridman WH, Pagès F, Trajanoski Z, and Galon J (2009) ClueGO: a Cytoscape plug-in to decipher functionally grouped gene ontology and pathway annotation networks. Bioinformatics 25:1091-1093.
6. Correa F, Mestre L, Docagne F, and Guaza C (2005) Activation of cannabinoid CB2 receptor negatively regulates IL-12p40 production in murine macrophages: role of IL-10 and ERK1/2 kinase signaling. Br J Pharmacol 145:441-448.
7. Dong ZJ, Wei HM, Sun R, Tian ZG, and Gao B (2004) Isolation of murine hepatic lymphocytes using mechanical dissection for phenotypic and functional analysis of NK1.1+ cells. World J Gastroenterol 10:1928-1933.
8. Dweep H, Sticht C, Pandey P, and Gretz N (2011) miRWalk-database: prediction of possible miRNA binding sites by "walking" the genes of three genomes. J Biomed Inform 44:839-847.
9. Floreani A, Lazzari R, Macchi V, Porzionato A, Variola A, Colavito D, Leon A, Guido M, Baldo V, De Caro R, et al. (2010) Hepatic expression of endocannabinoid receptors and their novel polymorphisms in primary biliary cirrhosis. J Gastroenterol 45:68-76.
10. Han KH, Lim S, Ryu J, Lee CW, Kim Y, Kang JH, Kang SS, Ahn YK, Park CS, and Kim JJ (2009) CB1 and CB2 cannabinoid receptors differentially regulate the production of reactive oxygen species by macrophages. Cardiovasc Res 84:378-386.
11. Hegde VL, Hegde S, Cravatt BF, Hofseth LJ, Nagarkatti M, and Nagarkatti PS (2008) Attenuation of experimental autoimmune hepatitis by exogenous and endogenous cannabinoids: involvement of regulatory T cells. Mol Pharmacol 74:20-33.
12. Hegde VL, Nagarkatti PS, and Nagarkatti M (2011) Role of myeloid-derived suppressor cells in amelioration of experimental autoimmune hepatitis following activation of TRPV1 receptors by cannabidiol. PLoS ONE 6:e18281.
13. Jeong WI, Osei-Hyiaman D, Park O, Liu J, Bátkai S, Mukhopadhyay P, Horiguchi N, Harvey-White J, Marsicano G, Lutz B, et al. (2008) Paracrine activation of hepatic CB1 receptors by stellate cell-derived endocannabinoids mediates alcoholic fatty liver. Cell Metab 7:227-235.
14. Julien B, Grenard P, Teixeira-Clerc F, Van Nhieu JT, 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.
15. Kobayashi K, Hernandez LD, Galán JE, Janeway CA, Jr, Medzhitov R, and Flavell RA (2002) IRAK-M is a negative regulator of Toll-like receptor signaling. Cell 110:191-202.
16. Kunos G and Osei-Hyiaman D (2008) Endocannabinoids and liver disease. IV. Endocannabinoid involvement in obesity and hepatic steatosis. Am J Physiol Gastrointest Liver Physiol 294:G1101-G1104.
17. Lee WM (2012) Acute liver failure. Semin Respir Crit Care Med 33:36-45.
18. Leifeld L, Fielenbach M, Dumoulin FL, Speidel N, Sauerbruch T, and Spengler U (2002) Inducible nitric oxide synthase (iNOS) and endothelial nitric oxide synthase (eNOS) expression in fulminant hepatic failure. J Hepatol 37:613-619.
19. Leist M, Gantner F, Bohlinger I, Tiegs G, Germann PG, and Wendel A (1995) Tumor necrosis factor-induced hepatocyte apoptosis precedes liver failure in experimental murine shock models. Am J Pathol 146:1220-1234.
20. Liang DY, Liu LM, Ye CG, Zhao L, Yu FP, Gao DY, Wang YY, Yang ZW, and Wang YY (2014) Inhibition of UII/UTR system relieves acute inflammation of liver through preventing activation of NF-κB pathway in ALF mice. PLoS ONE 8:e64895.
21. Lotersztajn S, Teixeira-Clerc F, Julien B, Deveaux V, Ichigotani Y, Manin S, Tran-Van-Nhieu J, Karsak M, Zimmer A, and Mallat A (2008) CB2 receptors as new therapeutic targets for liver diseases. Br J Pharmacol 153:286-289.
22. Louvet A, Teixeira-Clerc F, Chobert MN, Deveaux V, Pavoine C, Zimmer A, Pecker F, Mallat A, and Lotersztajn S (2011) Cannabinoid CB2 receptors protect against alcoholic liver disease by regulating Kupffer cell polarization in mice. Hepatology 54:1217-1226.
23. Lu YC, Yeh WC, and Ohashi PS (2008) LPS/TLR4 signal transduction pathway. Cytokine 42:145-151.
24. Mallat A and Lotersztajn S (2008) Endocannabinoids and liver disease. I. Endocannabinoids and their receptors in the liver. Am J Physiol Gastrointest Liver Physiol 294:G9-G12.
25. Mas A and Rodés J (1997) Fulminant hepatic failure. Lancet 349:1081-1085.
26. Masaki T, Chiba S, Tatsukawa H, Yasuda T, Noguchi H, Seike M, and Yoshimatsu H (2004) Adiponectin protects LPS-induced liver injury through modulation of TNF-alpha in KK-Ay obese mice. Hepatology 40:177-184.
27. Miller AM and Stella N (2008) CB2 receptor-mediated migration of immune cells: it can go either way. Br J Pharmacol 153:299-308.
28. Muñoz-Luque J, Ros J, Fernández-Varo G, Tugues S, Morales-Ruiz M, Alvarez CE, Friedman SL, Arroyo V, and Jiménez W (2008) Regression of fibrosis after chronic stimulation of cannabinoid CB2 receptor in cirrhotic rats. J Pharmacol Exp Ther 324:475-483.
29. Neuberger J (2005) Prediction of survival for patients with fulminant hepatic failure. Hepatology 41:19-22.
30. Nolan JP (2010) The role of intestinal endotoxin in liver injury: a long and evolving history. Hepatology 52:1829-1835.
31. Nowak M, Gaines GC, Rosenberg J, Minter R, Bahjat FR, Rectenwald J, MacKay SL, Edwards CK, 3rd, and Moldawer LL (2000) LPS-induced liver injury in D-galactosamine-sensitized mice requires secreted TNF-alpha and the TNF-p55 receptor. Am J Physiol Regul Integr Comp Physiol 278:R1202-R1209.
32. Odegaard JI, Ricardo-Gonzalez RR, Red Eagle A, Vats D, Morel CR, Goforth MH, Subramanian V, Mukundan L, Ferrante AW, and Chawla A (2008) Alternative M2 activation of Kupffer cells by PPARdelta ameliorates obesity-induced insulin resistance. Cell Metab 7:496-507.
33. O'Connell RM, Rao DS, Chaudhuri AA, and Baltimore D (2010) Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 10:111-122.
34. O'Neill LA, Sheedy FJ, and McCoy CE (2011) MicroRNAs: the fine-tuners of Toll-like receptor signalling. Nat Rev Immunol 11:163-175.
35. Pacher P, Bátkai S, and Kunos G (2006) The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58:389-462.
36. Rahman TM and Hodgson HJ (2000) Animal models of acute hepatic failure. Int J Exp Pathol 81:145-157.
37. Santucci L, Fiorucci S, Chiorean M, Brunori PM, Di Matteo FM, Sidoni A, Migliorati G, and Morelli A (1996) Interleukin 10 reduces lethality and hepatic injury induced by lipopolysaccharide in galactosamine-sensitized mice. Gastroenterology 111:736-744.
38. Sass G, Koerber K, Bang R, Guehring H, and Tiegs G (2001) Inducible nitric oxide synthase is critical for immune-mediated liver injury in mice. J Clin Invest 107:439-447.
39. Sica A and Mantovani A (2012) Macrophage plasticity and polarization: in vivo veritas. J Clin Invest 122:787-795.
40. Singh UP, Singh NP, Singh B, Price RL, Nagarkatti M, and Nagarkatti PS (2012) Cannabinoid receptor-2 (CB2) agonist ameliorates colitis in IL-10(-/-) mice by attenuating the activation of T cells and promoting their apoptosis. Toxicol Appl Pharmacol 258:256-267.
41. Tam J, Liu J, Mukhopadhyay B, Cinar R, Godlewski G, and Kunos G (2011) Endocannabinoids in liver disease. Hepatology 53:346-355.
42. Teixeira-Clerc F, Belot MP, Manin S, Deveaux V, Cadoudal T, Chobert MN, Louvet A, Zimmer A, Tordjmann T, Mallat A, et al. (2010) Beneficial paracrine effects of cannabinoid receptor 2 on liver injury and regeneration. Hepatology 52:1046-1059.
43. 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.
44. Tuñón MJ, Alvarez M, Culebras JM, and González-Gallego J (2009) An overview of animal models for investigating the pathogenesis and therapeutic strategies in acute hepatic failure. World J Gastroenterol 15:3086-3098.
45. Zhan Y, Wang Z, Yang P, Wang T, Xia L, Zhou M, Wang Y, Wang S, Hua Z, and Zhang J (2014) Adenosine 59-monophosphate ameliorates D-galactosamine/ lipopolysaccharide-induced liver injury through an adenosine receptor-independent mechanism in mice. Cell Death Dis 5:e985.