Foxo3a-dependent Bim transcription protects mice from a high fat diet via inhibition of activation of the NLRP3 inflammasome by facilitating autophagy flux in Kupffer cells

Oncotarget

Volumn 8, Issue 21, 2017, Pages 34258-34267

  Yan, Liu ^a,b   Wenfeng, Zhang ^a   Xiaoling, Wu ^a   Jianping, Gong ^a  

^a THE SECOND AFFILIATED HOSPITAL OF CHONGQING MEDICAL UNIVERSITY   (China)

^b Radiotherapy Department The Fifth People's Hospital of Chengdu   (China)

Author keywords

Autophagy; Bim; Foxo3a; NAFLD; NLRP3 inflammasome

Indexed keywords

BECLIN 1; BIM PROTEIN; CRYOPYRIN; DYNEIN ADENOSINE TRIPHOSPHATASE; FAS LIGAND; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; PROTEIN P21; PROTEIN P27; PUMA PROTEIN; S PHASE KINASE ASSOCIATED PROTEIN 2; TRANSCRIPTION FACTOR FKHRL1; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND; BCL2L11 PROTEIN, MOUSE; CYCLOPEPTIDE; FOXO3 PROTEIN, MOUSE; ITURIN A; LIPOPOLYSACCHARIDE; NLRP3 PROTEIN, MOUSE;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BINDING SITE; CONTROLLED STUDY; DNA BINDING; DOWN REGULATION; ENZYME PHOSPHORYLATION; KUPFFER CELL; LIPID DIET; MOUSE; NONHUMAN; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; UPREGULATION; ADVERSE EVENT; ANIMAL; CYTOLOGY; DISEASE MODEL; DRUG EFFECT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM;

ANIMALS; AUTOPHAGY; BCL-2-LIKE PROTEIN 11; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; FORKHEAD BOX PROTEIN O3; GENE EXPRESSION REGULATION; INFLAMMASOMES; KUPFFER CELLS; LIPOPOLYSACCHARIDES; MICE; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; PEPTIDES, CYCLIC; TRANSCRIPTION, GENETIC;

EID: 85019837334     PISSN: None     EISSN: 19492553     Source Type: Journal    
DOI: 10.18632/oncotarget.15946     Document Type: Article

References (37)

1. Abdelmalek MF. NAFLD: The clinical and economic burden of NAFLD: time to turn the tide. Nat Rev Gastroenterol Hepatol. 2016; 13:685-6
2. Rinella ME, Sanyal AJ. Management of NAFLD: a stagebased approach. Nat Rev Gastroenterol Hepatol. 2016; 13:196-205
3. Haas JT, Francque S, Staels B. Pathophysiology and Mechanisms of Nonalcoholic Fatty Liver Disease. Annu Rev Physiol. 2016; 78:181-205
4. Wan J, Benkdane M, Teixeira-Clerc F, Bonnafous S, Louvet A, Lafdil F, Pecker F, Tran A, Gual P, Mallat A, Lotersztajn S, Pavoine C. M2 Kupffer cells promote M1 Kupffer cell apoptosis: a protective mechanism against alcoholic and nonalcoholic fatty liver disease. Hepatology. 2014; 59:130-42
5. Wenfeng Z, Yakun W, Di M, Jianping G, Chuanxin W, Chun H. Kupffer cells: increasingly significant role in nonalcoholic fatty liver disease. Ann Hepatol. 2014; 13:489-95
6. Leroux A, Ferrere G, Godie V, Cailleux F, Renoud ML, Gaudin F, Naveau S, Prévot S, Makhzami S, Perlemuter G, Cassard-Doulcier AM. Toxic lipids stored by Kupffer cells correlates with their pro-inflammatory phenotype at an early stage of steatohepatitis. J Hepatol. 2012; 57:141-9
7. Sookoian S, Flichman D, Scian R, Rohr C, Dopazo H, Gianotti TF, Martino JS, Castaño GO, Pirola CJ. Mitochondrial genome architecture in non-alcoholic fatty liver disease. J Pathol. 2016; 240:437-49
8. Lamkanfi M, Dixit VM. Mechanisms and functions of inflammasomes. Cell. 2014; 157:1013-22
9. Moon JS, Nakahira K, Chung KP, DeNicola GM, Koo MJ, Pabón MA, Rooney KT, Yoon JH, Ryter SW, Stout-Delgado H, Choi AM. NOX4-dependent fatty acid oxidation promotes NLRP3 inflammasome activation in macrophages. Nat Med. 2016; 22:1002-12
10. Lamkanfi M. Emerging inflammasome effector mechanisms. Nat Rev Immunol. 2011; 11:213-20
11. Kayagaki N, Stowe IB, Lee BL, O'Rourke K, Anderson K, Warming S, Cuellar T, Haley B, Roose-Girma M, Phung QT, Liu PS, Lill JR, Li H, et al. Caspase-11 cleaves gasdermin D for non-canonical inflammasome signalling. Nature. 2015; 526:666-71
12. Shi J, Zhao Y, Wang K, Shi X, Wang Y, Huang H, Zhuang Y, Cai T, Wang F, Shao F. Cleavage of GSDMD by inflammatory caspases determines pyroptotic cell death. Nature. 2015; 526:660-5
13. He Y, Hara H, Núñez G. Mechanism and Regulation of NLRP3 Inflammasome Activation. Trends Biochem Sci. 2016; 41:1012-21
14. Francque SM, van der Graaff D, Kwanten WJ. Nonalcoholic fatty liver disease and cardiovascular risk: Pathophysiological mechanisms and implications. J Hepatol. 2016; 65:425-43
15. Liu K, Zhao E, Ilyas G, Lalazar G, Lin Y, Haseeb M, Tanaka KE, Czaja MJ. Impaired macrophage autophagy increases the immune response in obese mice by promoting proinflammatory macrophage polarization. Autophagy. 2015; 11:271-84
16. Lin YC, Chang PF, Lin HF, Liu K, Chang MH, Ni YH. Variants in the autophagy-related gene IRGM confer susceptibility to non-alcoholic fatty liver disease by modulating lipophagy. J Hepatol. 2016; 65:1209-16
17. Messer JS. The cellular autophagy/apoptosis checkpoint during inflammation. Cell Mol Life Sci. 2016
18. Cadwell K. Crosstalk between autophagy and inflammatory signalling pathways: balancing defence and homeostasis. Nat Rev Immunol. 2016; 16:661-75
19. Shin HJ, Kim H, Oh S, Lee JG, Kee M, Ko HJ, Kweon MN, Won KJ, Baek SH. AMPK-SKP2-CARM1 signalling cascade in transcriptional regulation of autophagy. Nature. 2016; 534:553-7
20. Tong W, Ju L, Qiu M, Xie Q, Chen Y, Shen W, Sun W, Wang W, Tian J. Liraglutide ameliorates non-alcoholic fatty liver disease by enhancing mitochondrial architecture and promoting autophagy through the SIRT1/SIRT3-FOXO3a pathway. Hepatol Res. 2016; 46:933-43
21. Thompson MG, Larson M, Vidrine A, Barrios K, Navarro F, Meyers K, Simms P, Prajapati K, Chitsike L, Hellman LM, Baker BM, Watkins SK. FOXO3-NF-κB RelA Protein Complexes Reduce Proinflammatory Cell Signaling and Function. J Immunol. 2015; 195:5637-47
22. Joseph J, Ametepe ES, Haribabu N, Agbayani G, Krishnan L, Blais A, Sad S. Inhibition of ROS and upregulation of inflammatory cytokines by FoxO3a promotes survival against Salmonella typhimurium. Nat Commun. 2016; 7: 12748
23. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ, Ting JP. Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol. 2011; 12: 408-15
24. Giegerich AK, Kuchler L, Sha LK, Knape T, Heide H, Wittig I, Behrends C, Brüne B, and von KA. Autophagydependent PELI3 degradation inhibits proinflammatory IL1B expression. Autophagy. 2014; 10:1937-52
25. Wang RC, Wei Y, An Z, Zou Z, Xiao G, Bhagat G, White M, Reichelt J, Levine B. Akt-mediated regulation of autophagy and tumorigenesis through Beclin 1 phosphorylation. Science. 2012; 338:956-9
26. Cusi K. Role of obesity and lipotoxicity in the development of nonalcoholic steatohepatitis: pathophysiology and clinical implications. Gastroenterology. 2012; 142:711-25.e6
27. Tonan T, Fujimoto K, Qayyum A, Morita Y, Nakashima O, Ono N, Kawahara A, Kage M, Hayabuchi N, Ueno T. CD14 expression and Kupffer cell dysfunction in non-alcoholic steatohepatitis: superparamagnetic iron oxide-magnetic resonance image and pathologic correlation. J Gastroenterol Hepatol. 2012; 27:789-96
28. Deretic V. Autophagy as an innate immunity paradigm: expanding the scope and repertoire of pattern recognition receptors. Curr Opin Immunol. 2012; 24: 21-31
29. Chen Y, Lv L, Pi H, Qin W, Chen J, Guo D, Lin J, Chi X, Jiang Z, Yang H, Jiang Y. Dihydromyricetin protects against liver ischemia/reperfusion induced apoptosis via activation of FOXO3a-mediated autophagy. Oncotarget. 2016; 7:76508-76522. doi: 10.18632/oncotarget.12894
30. Liu G, Fan X, Tang M, Chen R, Wang H, Jia R, Zhou X, Jing W, Wang H, Yang Y, Yin F, Wei H, Li B, et al. Osteopontin induces autophagy to promote chemoresistance in human hepatocellular carcinoma cells. Cancer Lett. 2016; 383: 171-82
31. Maiese K, Chong ZZ, Shang YC. OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med. 2008; 14: 219-27
32. McClelland DDL, Satoorian TS, Walker LM, Sparks NR, Pulyanina PY, Zur NNI. Glucose-Induced Oxidative Stress Reduces Proliferation in Embryonic Stem Cells via FOXO3A/β-Catenin-Dependent Transcription of p21(cip1). Stem Cell Reports. 2016; 7: 55-68
33. Contreras AU, Mebratu Y, Delgado M, Montano G, Hu CA, Ryter SW, Choi AM, Lin Y, Xiang J, Chand H, Tesfaigzi Y. Deacetylation of p53 induces autophagy by suppressing Bmf expression. J Cell Biol. 2013; 201: 427-37
34. Delgado M, Tesfaigzi Y. BH3-only proteins, Bmf and Bim, in autophagy. Cell Cycle. 2013; 12: 3453-4
35. Li PZ, Li JZ, Li M, Gong JP, He K. An efficient method to isolate and culture mouse Kupffer cells. Immunol Lett. 2014; 158: 52-6
36. Dey G, Bharti R, Dhanarajan G, Das S, Dey KK, Kumar BN, Sen R, Mandal M. Marine lipopeptide Iturin A inhibits Akt mediated GSK3β and FoxO3a signaling and triggers apoptosis in breast cancer. Sci Rep. 2015; 5: 10316
37. Kleiner DE, Brunt EM, Van Natta M, Behling C, Contos MJ, Cummings OW, Ferrell LD, Liu YC, Torbenson MS, Unalp-Arida A, Yeh M, McCullough AJ, Sanyal AJ. Design and validation of a histological scoring system for nonalcoholic fatty liver disease. Hepatology. 2005; 41: 1313-21