β-Caryophyllene alleviates d-galactosamine and lipopolysaccharide-induced hepatic injury through suppression of the TLR4 and RAGE signaling pathways

European Journal of Pharmacology

Volumn 764, Issue , 2015, Pages 613-621

  Cho, Hong Ik ^a   Hong, Jeong Min ^a   Choi, Joo Wan ^a   Choi, Hyo Sun ^a   Hwan Kwak, Jong ^a   Lee, Dong Ung ^b   Kook Lee, Sang ^c   Lee, Sun Mee ^a  

^a Sungkyunkwan University   (South Korea)

^b Dongguk University   (South Korea)

^c Seoul National University   (South Korea)

Author keywords

Fulminant hepatic failure; High mobility group box 1; Receptor for advanced glycation end products; Toll like receptor 4; Caryophyllene

Indexed keywords

ADVANCED GLYCATION END PRODUCT; AMINOTRANSFERASE; CARYOPHYLLENE; EARLY GROWTH RESPONSE FACTOR 1; GALACTOSAMINE; HIGH MOBILITY GROUP B1 PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; LIPOPOLYSACCHARIDE; MACROPHAGE INFLAMMATORY PROTEIN 2; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; SYNAPTOPHYSIN; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; ADVANCED GLYCATION END PRODUCT RECEPTOR; AGER PROTEIN, MOUSE; ANTIINFLAMMATORY AGENT; AUTACOID; CYTOKINE; SESQUITERPENE; TLR4 PROTEIN, MOUSE;

AGASTACHE; AGASTACHE RUGOSA; AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DOWN REGULATION; HISTOPATHOLOGY; KUPFFER CELL; LIVER FAILURE; LIVER INJURY; LIVER PROTECTION; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN SYNTHESIS; PROTEIN SYNTHESIS REGULATION; SIGNAL TRANSDUCTION; SURVIVAL RATE; ANIMAL; CELL CULTURE; CELL PROTECTION; DISEASE MODEL; DRUG EFFECTS; DRUG-INDUCED LIVER INJURY; INSTITUTE FOR CANCER RESEARCH MOUSE; LIVER; METABOLISM; PATHOLOGY; TIME FACTOR;

ADVANCED GLYCOSYLATION END PRODUCT-SPECIFIC RECEPTOR; ANIMALS; ANTI-INFLAMMATORY AGENTS; CELLS, CULTURED; CYTOKINES; CYTOPROTECTION; DISEASE MODELS, ANIMAL; DRUG-INDUCED LIVER INJURY; GALACTOSAMINE; INFLAMMATION MEDIATORS; KUPFFER CELLS; LIPOPOLYSACCHARIDES; LIVER; LIVER FAILURE; MALE; MICE, INBRED ICR; MITOGEN-ACTIVATED PROTEIN KINASES; SESQUITERPENES; SIGNAL TRANSDUCTION; TIME FACTORS; TOLL-LIKE RECEPTOR 4;

EID: 84939170213     PISSN: 00142999     EISSN: 18790712     Source Type: Journal    
DOI: 10.1016/j.ejphar.2015.08.001     Document Type: Article

References (32)

1. S.A. Arancibia, C.J. Beltran, I.M. Aguirre, P. Silva, A.L. Peralta, F. Malinarich, and M.A. Hermoso Toll-like receptors are key participants in innate immune responses Biol. Res. 40 2007 97 112
2. A.F. Barrero, J. Molina, J.E. Oltra, J. Altarejos, A. Barragan, A. Lara, and M. Segura Stereochemistry of 14-hydroxy-beta-caryophyllene and related-compounds Tetrahedron 51 1995 3813 3822
3. Z. Ben Ari, O. Avlas, O. Pappo, V. Zilbermints, Y. Cheporko, L. Bachmetov, R. Zemel, A. Shainberg, E. Sharon, F. Grief, and E. Hochhauser Reduced hepatic injury in Toll-like receptor 4-deficient mice following d-galactosamine/lipopolysaccharide-induced fulminant hepatic failure Cell. Physiol. Biochem. 29 2012 41 50
4. A. Bierhaus, P.M. Humpert, M. Morcos, T. Wendt, T. Chavakis, B. Arnold, D.M. Stern, and P.P. Nawroth Understanding RAGE, the receptor for advanced glycation end products J. Mol. Med. (Berl.) 83 2005 876 886
5. I. Botos, D.M. Segal, and D.R. Davies The structural biology of Toll-like receptors Structure 19 2011 447 459
6. M.A. Calleja, J.M. Vieites, T. Montero-Melendez, M.I. Torres, M.J. Faus, A. Gil, and A. Suarez The antioxidant effect of beta-caryophyllene protects rat liver from carbon tetrachloride-induced fibrosis by inhibiting hepatic stellate cell activation Br. J. Nutr 109 2013 394 401
7. H.J. Chang, J.M. Kim, J.C. Lee, W.K. Kim, and H.S. Chun Protective effect of beta-caryophyllene, a natural bicyclic sesquiterpene, against cerebral ischemic injury J. Med. Food 16 2013 471 480
8. J. Gertsch, M. Leonti, S. Raduner, I. Racz, J.Z. Chen, X.Q. Xie, K.H. Altmann, M. Karsak, and A. Zimmer Beta-caryophyllene is a dietary cannabinoid Proc. Natl. Acad. Sci. USA 105 2008 9099 9104
9. R. Hasunuma, H. Maruyama, H. Takimoto, R. Ryll, S. Tanaka, and Y. Kumazawa Does high mobility group 1 protein function as a late mediator for LPS- or TNF-induced shock in galactosamine-sensitized mice? J. Endotoxin Res. 8 2002 391 398
10. P. He, Y. Noda, and K. Sugiyama Green tea suppresses lipopolysaccharide-induced liver injury in d-galactosamine-sensitized rats J. Nutr. 131 2001 1560 1567
11. Z.A. Ibrahim, C.L. Armour, S. Phipps, and M.B. Sukkar RAGE and TLRs: relatives, friends or neighbours? Mol. Immunol. 56 2013 739 744
12. C.A. Janeway Jr., and R. Medzhitov Innate immune recognition Annu. Rev. Immunol. 20 2002 197 216
13. J.W. Kang, D.W. Kim, J.S. Choi, Y.S. Kim, and S.M. Lee Scoparone attenuates d-galactosamine/lipopolysaccharide-induced fulminant hepatic failure through inhibition of toll-like receptor 4 signaling in mice Food Chem. Toxicol. 57 2013 132 139
14. D.W. Kim, H.I. Cho, K.M. Kim, S.J. Kim, J.S. Choi, Y.S. Kim, and S.M. Lee Isorhamnetin-3-O-galactoside protects against CCl4-induced hepatic injury in mice Biomol. Ther. 20 2012 406 412
15. T. Kitazawa, T. Tsujimoto, H. Kawaratani, and H. Fukui Salvage effect of E5564, Toll-like receptor 4 antagonist on d-galactosamine and lipopolysaccharide-induced acute liver failure in rats J. Gastroenterol. Hepatol. 25 2010 1009 1012
16. A. Kuhla, J. Norden, K. Abshagen, M.D. Menger, and B. Vollmar RAGE blockade and hepatic microcirculation in experimental endotoxaemic liver failure Br. J. Surg. 100 2013 1229 1239
17. J. Legault, and A. Pichette Potentiating effect of beta-caryophyllene on anticancer activity of alpha-humulene, isocaryophyllene and paclitaxel J. Pharm. Pharmacol. 59 2007 1643 1647
18. T. Nakama, S. Hirono, A. Moriuchi, S. Hasuike, K. Nagata, T. Hori, A. Ido, K. Hayashi, and H. Tsubouchi Etoposide prevents apoptosis in mouse liver with d-galactosamine/lipopolysaccharide-induced fulminant hepatic failure resulting in reduction of lethality Hepatology 33 2001 1441 1450
19. L.I. Paula-Freire, M.L. Andersen, V.S. Gama, G.R. Molska, and E.L. Carlini The oral administration of trans-caryophyllene attenuates acute and chronic pain in mice Phytomedicine 21 2014 356 362
20. G. Pearson, F. Robinson, T. Beers Gibson, B.E. Xu, M. Karandikar, K. Berman, and M.H. Cobb Mitogen-activated protein (MAP) kinase pathways: regulation and physiological functions Endocr. Rev. 22 2001 153 183
21. M.T. Pritchard, S. Roychowdhury, M.R. McMullen, L. Guo, G.E. Arteel, and L.E. Nagy Early growth response-1 contributes to galactosamine/lipopolysaccharide-induced acute liver injury in mice Am. J. Physiol. Gastrointest. Liver Physiol. 293 2007 G1124 G1133
22. S. Sain, P.K. Naoghare, S.S. Devi, A. Daiwile, K. Krishnamurthi, P. Arrigo, and T. Chakrabarti Beta caryophyllene and caryophyllene oxide, isolated from Aegle marmelos, as the potent anti-inflammatory agents against lymphoma and neuroblastoma cells Antiinflamm. Antiallergy Agents Med. Chem. 13 2014 45 55
23. M. Sakaguchi, H. Murata, K. Yamamoto, T. Ono, Y. Sakaguchi, A. Motoyama, T. Hibino, K. Kataoka, and N.H. Huh TIRAP, an adaptor protein for TLR2/4, transduces a signal from RAGE phosphorylated upon ligand binding PLoS One 6 2011 e23132
24. G. Srikrishna, and H.H. Freeze Endogenous damage-associated molecular pattern molecules at the crossroads of inflammation and cancer Neoplasia 11 2009 615 628
25. A. Tsung, R. Sahai, H. Tanaka, A. Nakao, M.P. Fink, M.T. Lotze, H. Yang, J. Li, K.J. Tracey, D.A. Geller, and T.R. Billiar The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia-reperfusion J. Exp. Med. 201 2005 1135 1143
26. A. Visintin, E. Latz, B.G. Monks, T. Espevik, and D.T. Golenbock Lysines 128 and 132 enable lipopolysaccharide binding to MD-2, leading to Toll-like receptor-4 aggregation and signal transduction J. Biol. Chem. 278 2003 48313 48320
27. W. Wang, L. Sun, Y. Deng, and J. Tang Synergistic effects of antibodies against high-mobility group box 1 and tumor necrosis factor-alpha antibodies on d-(+)-galactosamine hydrochloride/lipopolysaccharide-induced acute liver failure FEBS J. 280 2013 1409 1419
28. S.F. Yan, T. Fujita, J. Lu, K. Okada, Y. Shan Zou, N. Mackman, D.J. Pinsky, and D.M. Stern Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress Nat. Med. 6 2000 1355 1361
29. H. Yang, P. Lundback, L. Ottosson, H. Erlandsson-Harris, E. Venereau, M.E. Bianchi, Y. Al-Abed, U. Andersson, K.J. Tracey, and D.J. Antoine Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1) Mol. Med. 18 2012 250 259
30. H. Yang, M. Ochani, J. Li, X. Qiang, M. Tanovic, H.E. Harris, S.M. Susarla, L. Ulloa, H. Wang, R. DiRaimo, C.J. Czura, H. Wang, J. Roth, H.S. Warren, M.P. Fink, M.J. Fenton, U. Andersson, and K.J. Tracey Reversing established sepsis with antagonists of endogenous high-mobility group box 1 Proc. Natl. Acad. Sci. USA 101 2004 296 301
31. T. Yasuda, T. Ueda, M. Shinzeki, H. Sawa, T. Nakajima, Y. Takeyama, and Y. Kuroda Increase of high-mobility group box chromosomal protein 1 in blood and injured organs in experimental severe acute pancreatitis Pancreas 34 2007 487 488
32. H. Zhang, S. Tasaka, Y. Shiraishi, K. Fukunaga, W. Yamada, H. Seki, Y. Ogawa, K. Miyamoto, Y. Nakano, N. Hasegawa, T. Miyasho, I. Maruyama, and A. Ishizaka Role of soluble receptor for advanced glycation end products on endotoxin-induced lung injury Am. J. Respir. Crit. Care Med. 178 2008 356 362