Epigallocatechin-3-gallate attenuates apoptosis and autophagy in concanavalin a-induced hepatitis by inhibiting BNIP3

Drug Design, Development and Therapy

Volumn 10, Issue , 2016, Pages 631-647

  Li, Sainan ^a   Xia, Yujing ^a   Chen, Kan ^a   Li, Jingjing ^a   Liu, Tong ^a   Wang, Fan ^a   Lu, Jie ^a   Zhou, Yingqun ^a   Guo, Chuanyong ^a  

^a TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Apoptosis; Autophagy; BNIP3; Concanavalin A; EGCG; Hepatitis; IL 6; JAKs; STAT3

Indexed keywords

ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; BECLIN 1; CASPASE 3; CASPASE 9; EPIGALLOCATECHIN GALLATE; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERLEUKIN 6; JANUS KINASE 1; JANUS KINASE 2; MICROTUBULE ASSOCIATED PROTEIN 1; MICROTUBULE ASSOCIATED PROTEIN 1 LIGHT CHAIN 3; PROTEIN BAX; PROTEIN BCL 2; PROTEIN BNIP3; STAT3 PROTEIN; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; BNIP3 PROTEIN, MOUSE; CATECHIN; CONCANAVALIN A; CYTOKINE; JAK1 PROTEIN, MOUSE; JAK2 PROTEIN, MOUSE; MEMBRANE PROTEIN; MITOCHONDRIAL PROTEIN; STAT3 PROTEIN, MOUSE;

ALANINE AMINOTRANSFERASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; ASPARTATE AMINOTRANSFERASE BLOOD LEVEL; AUTOIMMUNE HEPATITIS; AUTOPHAGY; CELL PROLIFERATION; CONCANAVALIN A-INDUCED HEPATITIS; CONTROLLED STUDY; CYTOKINE RELEASE; DOSE RESPONSE; DOWN REGULATION; DRUG DOSE COMPARISON; DRUG EFFECT; DRUG MECHANISM; DRUG MEGADOSE; GENE EXPRESSION; LIVER CELL; LIVER FUNCTION; LIVER PROTECTION; LOW DRUG DOSE; MALE; MOUSE; NONHUMAN; PROTEIN DETERMINATION; SIGNAL TRANSDUCTION; ANALOGS AND DERIVATIVES; ANIMAL; ANTAGONISTS AND INHIBITORS; BAGG ALBINO MOUSE; BLOOD; CHEMICAL AND DRUG INDUCED LIVER INJURY; DRUG EFFECTS; PATHOLOGY; PHYSIOLOGY;

ANIMALS; APOPTOSIS; AUTOPHAGY; CATECHIN; CHEMICAL AND DRUG INDUCED LIVER INJURY; CONCANAVALIN A; CYTOKINES; JANUS KINASE 1; JANUS KINASE 2; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED BALB C; MITOCHONDRIAL PROTEINS; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR;

EID: 84958549780     PISSN: None     EISSN: 11778881     Source Type: Journal    
DOI: 10.2147/DDDT.S99420     Document Type: Article

References (83)

1. Li J, Xia Y, Liu T, et al. Protective effects of astaxanthin on ConA-induced autoimmune hepatitis by the JNK/p-JNK pathway-mediated inhibition of autophagy and apoptosis. PLoS One. 2015;10:e0120440.
2. Hudspeth K, Pontarini E, Tentorio P, et al. The role of natural killer cells in autoimmune liver disease: a comprehensive review. J Autoimmun. 2013;46:55-65.
3. Stein-Streilein J, Sonoda KH, Faunce D, Zhang-Hoover J. Regulation of adaptive immune responses by innate cells expressing NK markers and antigen-transporting macrophages. J Leukoc Biol. 2000;67:488-494.
4. Tian Z, Gershwin ME, Zhang C. Regulatory NK cells in autoimmune disease. J Autoimmun. 2012;39:206-215.
5. Wang HX, Liu M, Weng SY, et al. Immune mechanisms of Concanavalin A model of autoimmune hepatitis. World J Gastroenterol. 2012;18:119-125.
6. Zhang H, Yang J, Zhu R, et al. Combination therapy of ursodeoxycholic acid and budesonide for PBC-AIH overlap syndrome: a meta-analysis. Drug Des Devel Ther. 2015;9:567-574.
7. Yin Q, Li J, Xia Y, et al. Systematic review and meta-analysis: bezafibrate in patients with primary biliary cirrhosis. Drug Des Devel Ther. 2015;9:5407-5419.
8. Zhang Y, Li S, He L, et al. Combination therapy of fenofibrate and ursodeoxycholic acid in patients with primary biliary cirrhosis who respond incompletely to UDCA monotherapy: a meta-analysis. Drug Des Devel Ther. 2015;9:2757-2766.
9. Heymann F, Hamesch K, Weiskirchen R, Tacke F. The concanavalin A model of acute hepatitis in mice. Lab Anim. 2015;49:12-20.
10. Tacke F, Luedde T, Trautwein C. Inflammatory pathways in liver homeostasis and liver injury. Clin Rev Allergy Immunol. 2009;36:4-12.
11. Zimmermann HW, Trautwein C, Tacke F. Functional role of monocytes and macrophages for the inflammatory response in acute liver injury. Front Physiol. 2012;3:56.
12. El Kasmi KC, Anderson AL, Devereaux MW, et al. Toll-like receptor 4-dependent Kupffer cell activation and liver injury in a novel mouse model of parenteral nutrition and intestinal injury. Hepatology. 2012;55:1518-1528.
13. Nemeth E, Baird AW, O’Farrelly C. Microanatomy of the liver immune system. Semin Immunopathol. 2009;31:333-343.
14. Thornberry NA, Lazebnik Y. Caspases: enemies within. Science. 1998;281:1312-1316.
15. Adams JM. Ways of dying: multiple pathways to apoptosis. Genes Dev. 2003;17:2481-2495.
16. Jacotot E, Costantini P, Laboureau E, et al. Mitochondrial membrane permeabilization during the apoptotic process. Ann N Y Acad Sci. 1999;887:18-30.
17. Kerr JF, Wyllie AH, Currie AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26:239-257.
18. Bantel H, Schulze-Osthoff K. Mechanisms of cell death in acute liver failure. Front Physiol. 2012;3:79.
19. Brenner C, Galluzzi L, Kepp O, Kroemer G. Decoding cell death signals in liver inflammation. J Hepatol. 2013;59:583-594.
20. Czaja AJ. Targeting apoptosis in autoimmune hepatitis. Dig Dis Sci. 2014;59:2890-2904.
21. Nikoletopoulou V, Markaki M, Palikaras K, Tavernarakis N. Crosstalk between apoptosis, necrosis and autophagy. Biochim Biophys Acta. 2013;1833:3448-3459.
22. Wang K. Molecular mechanisms of liver injury: apoptosis or necrosis. Exp Toxicol Pathol. 2014;66:351-356.
23. Wang K. Autophagy and apoptosis in liver injury. Cell Cycle. 2015;14:1631-1642.
24. Burton TR, Gibson SB. The role of Bcl-2 family member BNIP3 in cell death and disease: NIPping at the heels of cell death. Cell Death Differ. 2009;16:515-523.
25. Lomonosova E, Chinnadurai G. BH3-only proteins in apoptosis and beyond: an overview. Oncogene. 2008;27(Suppl 1):S2-S19.
26. Vasagiri N, Kutala VK. Structure, function, and epigenetic regulation of BNIP3: a pathophysiological relevance. Mol Biol Rep. 2014;41:7705-7714.
27. Chinnadurai G, Vijayalingam S, Gibson SB. BNIP3 subfamily BH3-only proteins: mitochondrial stress sensors in normal and pathological functions. Oncogene. 2008;27(Suppl 1):S114-S127.
28. Delgado M, Tesfaigzi Y. BH3-only proteins, Bmf and Bim, in autophagy. Cell Cycle. 2013;12:3453-3454.
29. Zhang H, Bosch-Marce M, Shimoda LA, et al. Mitochondrial autophagy is an HIF-1-dependent adaptive metabolic response to hypoxia. J Biol Chem. 2008;283:10892-10903.
30. Ray R, Chen G, Vande Velde C, et al. BNIP3 heterodimerizes with Bcl-2/Bcl-X(L) and induces cell death independent of a Bcl-2 homology 3 (BH3) domain at both mitochondrial and nonmitochondrial sites. J Biol Chem. 2000;275:1439-1448.
31. Cheng P, Wang F, Chen K, et al. Hydrogen sulfide ameliorates ischemia/reperfusion-induced hepatitis by inhibiting apoptosis and autophagy pathways. Mediators Inflamm. 2014;2014:935251.
32. Chen K, Li J, Wang J, et al. 15-Deoxy- gamma 12,14-prostaglandin J2 reduces liver impairment in a model of ConA-induced acute hepatic inflammation by activation of PPAR gamma and reduction in NF-kappa B activity. PPAR Res. 2014;2014:215631.
33. Shen M, Lu J, Dai W, et al. Ethyl pyruvate ameliorates hepatic ischemia-reperfusion injury by inhibiting intrinsic pathway of apoptosis and autophagy. Mediators Inflamm. 2013;2013:461536.
34. Li J, Wang F, Xia Y, et al. Astaxanthin pretreatment attenuates hepatic ischemia reperfusion-induced apoptosis and autophagy via the ROS/MAPK pathway in mice. Mar Drugs. 2015;13:3368-3387.
35. Wang C, Chen K, Xia Y, et al. N-acetylcysteine attenuates ischemia-reperfusion-induced apoptosis and autophagy in mouse liver via regulation of the ROS/JNK/Bcl-2 pathway. PLoS One. 2014;9:e108855.
36. Shen M, Chen K, Lu J, et al. Protective effect of astaxanthin on liver fibrosis through modulation of TGF-beta1 expression and autophagy. Mediators Inflamm. 2014;2014:954502.
37. Zhou Y, Chen K, He L, et al. The protective effect of resveratrol on concanavalin-A-induced acute hepatic injury in mice. Gastroenterol Res Pract. 2015;2015:506390.
38. Zhou Y, Dai W, Lin C, et al. Protective effects of necrostatin-1 against concanavalin A-induced acute hepatic injury in mice. Mediators Inflamm. 2013;2013:706156.
39. Cheng P, Chen K, Xia Y, et al. Hydrogen sulfide, a potential novel drug, attenuates concanavalin A-induced hepatitis. Drug Des Devel Ther. 2014;8:1277-1286.
40. Wang C, Xia Y, Zheng Y. Protective effects of N-acetylcysteine in concanavalin A-induced hepatitis in mice. Mediators Inflamm. 2015;2015:189785.
41. Mao Y, Wang J, Yu F, et al. Ghrelin reduces liver impairment in a model of concanavalin A-induced acute hepatitis in mice. Drug Des Devel Ther. 2015;9:5385-5396.
42. Maiuri MC, Le Toumelin G, Criollo A, et al. Functional and physical interaction between Bcl-X(L) and a BH3-like domain in Beclin-1. EMBO J. 2007;26:2527-2539.
43. Pratt J, Annabi B. Induction of autophagy biomarker BNIP3 requires a JAK2/STAT3 and MT1-MMP signaling interplay in Concanavalin-A-activated U87 glioblastoma cells. Cell Signal. 2014;26:917-924.
44. Pietrocola F, Izzo V, Niso-Santano M, et al. Regulation of autophagy by stress-responsive transcription factors. Semin Cancer Biol. 2013;23:310-322.
45. You L, Wang Z, Li H, et al. The role of STAT3 in autophagy. Autophagy. 2015;11:729-739.
46. Yurkova N, Shaw J, Blackie K, et al. The cell cycle factor E2F-1 activates Bnip3 and the intrinsic death pathway in ventricular myocytes. Circ Res. 2008;102:472-479.
47. Horn F, Henze C, Heidrich K. Interleukin-6 signal transduction and lymphocyte function. Immunobiology. 2000;202:151-167.
48. Lutticken C, Wegenka UM, Yuan J, et al. Association of transcription factor APRF and protein kinase Jak1 with the interleukin-6 signal transducer gp130. Science. 1994;263:89-92.
49. Wang SW, Sun YM. The IL-6/JAK/STAT3 pathway: potential therapeutic strategies in treating colorectal cancer (Review). Int J Oncol. 2014;44:1032-1040.
50. Byun JK, Yoon BY, Jhun JY, et al. Epigallocatechin-3-gallate ameliorates both obesity and autoinflammatory arthritis aggravated by obesity by altering the balance among CD4+ T-cell subsets. Immunol Lett. 2014;157:51-59.
51. Fiorini RN, Donovan JL, Rodwell D, et al. Short-term administration of (-)-epigallocatechin gallate reduces hepatic steatosis and protects against warm hepatic ischemia/reperfusion injury in steatotic mice. Liver Transpl. 2005;11:298-308.
52. Jamal MH, Ali H, Dashti A, et al. Effect of epigallocatechin gallate on uncoupling protein 2 in acute liver injury. Int J Clin Exp Pathol. 2015;8:649-654.
53. Pang JY, Zhao KJ, Wang JB, Ma ZJ, Xiao XH. Green tea polyphenol, epigallocatechin-3-gallate, possesses the antiviral activity necessary to fight against the hepatitis B virus replication in vitro. J Zhejiang Univ Sci B. 2014;15:533-539.
54. Singh BN, Shankar S, Srivastava RK. Green tea catechin, epigallocatechin-3-gallate (EGCG): mechanisms, perspectives and clinical applications. Biochem Pharmacol. 2011;82:1807-1821.
55. Tipoe GL, Leung TM, Liong EC, et al. Epigallocatechin-3-gallate (EGCG) reduces liver inflammation, oxidative stress and fibrosis in carbon tetrachloride (CCl4)-induced liver injury in mice. Toxicology. 2010;273:45-52.
56. Wu D, Wang J, Pae M, Meydani SN. Green tea EGCG, T cells, and T cell-mediated autoimmune diseases. Mol Aspects Med. 2012;33:107-118.
57. Wang Y, Mei Y, Feng D, Xu L. (-)-Epigallocatechin-3-gallate protects mice from concanavalin A-induced hepatitis through suppressing immune-mediated liver injury. Clin Exp Immunol. 2006;145:485-492.
58. Liu D, Zhang X, Jiang L, Guo Y, Zheng C. Epigallocatechin-3-gallate (EGCG) attenuates concanavalin A-induced hepatic injury in mice. Acta Histochem. 2014;116:654-662.
59. Lee YK, Bone ND, Strege AK, et al. VEGF receptor phosphorylation status and apoptosis is modulated by a green tea component, epigallocatechin-3-gallate (EGCG), in B-cell chronic lymphocytic leukemia. Blood. 2004;104:788-794.
60. Lee YK, Shanafelt TD, Bone ND, et al. VEGF receptors on chronic lymphocytic leukemia (CLL) B cells interact with STAT 1 and 3: implication for apoptosis resistance. Leukemia. 2005;19:513-523.
61. Shanafelt TD, Call TG, Zent CS, et al. Phase 2 trial of daily, oral Polyphenon E in patients with asymptomatic, Rai stage 0 to II chronic lymphocytic leukemia. Cancer. 2013;119:363-370.
62. Shanafelt TD, Call TG, Zent CS, et al. Phase I trial of daily oral Polyphenon E in patients with asymptomatic Rai stage 0 to II chronic lymphocytic leukemia. J Clin Oncol. 2009;27:3808-3814.
63. Wang Y, Ren X, Deng C, et al. Mechanism of the inhibition of the STAT3 signaling pathway by EGCG. Oncol Rep. 2013;30:2691-2696.
64. Yang EJ, Lee J, Lee SY, et al. EGCG attenuates autoimmune arthritis by inhibition of STAT3 and HIF-1alpha with Th17/Treg control. PLoS One. 2014;9:e86062.
65. Tao YY, Yan XC, Zhou T, et al. Fuzheng Huayu recipe alleviates hepatic fibrosis via inhibiting TNF-alpha induced hepatocyte apoptosis. BMC Complement Altern Med. 2014;14:449.
66. Klionsky DJ, Abdalla FC, Abeliovich H, et al. Guidelines for the use and interpretation of assays for monitoring autophagy. Autophagy. 2012;8:445-544.
67. Klionsky DJ, Abeliovich H, Agostinis P, et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy. 2008;4:151-175.
68. Guo K, Searfoss G, Krolikowski D, et al. Hypoxia induces the expression of the pro-apoptotic gene BNIP3. Cell Death Differ. 2001;8:367-376.
69. Dorn GW 2nd, Diwan A. The rationale for cardiomyocyte resuscitation in myocardial salvage. J Mol Med (Berl). 2008;86:1085-1095.
70. Mammucari C, Milan G, Romanello V, et al. FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 2007;6:458-471.
71. McFarlane IG. Pathogenesis of autoimmune hepatitis. Biomed Pharmacother. 1999;53:255-263.
72. Sass G, Heinlein S, Agli A, et al. Cytokine expression in three mouse models of experimental hepatitis. Cytokine. 2002;19:115-120.
73. Kammouni W, Wong K, Ma G, et al. Regulation of apoptosis in fibroblast-like synoviocytes by the hypoxia-induced Bcl-2 family member Bcl-2/adenovirus E1B 19-kd protein-interacting protein 3. Arthritis Rheum. 2007;56:2854-2863.
74. Renton JP, Xu N, Clark JJ, Hansen MR. Interaction of neurotrophin signaling with Bcl-2 localized to the mitochondria and endoplasmic reticulum on spiral ganglion neuron survival and neurite growth. J Neurosci Res. 2010;88:2239-2251.
75. Cui J, Sim TH, Gong Z, Shen HM. Generation of transgenic zebrafish with liver-specific expression of EGFP-Lc3: a new in vivo model for investigation of liver autophagy. Biochem Biophys Res Commun. 2012;422:268-273.
76. Zhou J, Farah BL, Sinha RA, et al. Epigallocatechin-3-gallate (EGCG), a green tea polyphenol, stimulates hepatic autophagy and lipid clearance. PLoS One. 2014;9:e87161.
77. Yamagata K, Xie Y, Suzuki S, Tagami M. Epigallocatechin-3-gallate inhibits VCAM-1 expression and apoptosis induction associated with LC3 expressions in TNFalpha-stimulated human endothelial cells. Phytomedicine. 2015;22:431-437.
78. Liu J, Tang Y, Feng Z, et al. Acetylated FoxO1 mediates high-glucose induced autophagy in H9c2 cardiomyoblasts: regulation by a polyphenol-(-)-epigallocatechin-3-gallate. Metabolism. 2014;63:1314-1323.
79. Liu J, Tang Y, Feng Z, et al. (-)-Epigallocatechin-3-gallate attenuated myocardial mitochondrial dysfunction and autophagy in diabetic Goto-Kakizaki rats. Free Radic Res. 2014;48:898-906.
80. Chen L, Ye HL, Zhang G, et al. Autophagy inhibition contributes to the synergistic interaction between EGCG and doxorubicin to kill the hepatoma Hep3B cells. PLoS One. 2014;9:e85771.
81. Li CP, Yao J, Tao ZF, et al. Epigallocatechin-gallate (EGCG) regulates autophagy in human retinal pigment epithelial cells: a potential role for reducing UVB light-induced retinal damage. Biochem Biophys Res Commun. 2013;438:739-745.
82. Hashimoto K, Sakagami H. Induction of apoptosis by epigallocatechin gallate and autophagy inhibitors in a mouse macrophage-like cell line. Anticancer Res. 2008;28:1713-1718.
83. Santamarina AB, Carvalho-Silva M, Gomes LM, et al. Decaffeinated green tea extract rich in epigallocatechin-3-gallate prevents fatty liver disease by increased activities of mitochondrial respiratory chain complexes in diet-induced obesity mice. J Nutr Biochem. 2015;26:1348-1356.