Inhibiting autophagy promotes endoplasmic reticulum stress and the ROS-induced nod-like receptor 3-dependent proinflammatory response in HepG2 cells

Molecular Medicine Reports

Volumn 14, Issue 4, 2016, Pages 3999-4007

  Yin, Jia Jing ^a   Xie, Guangying ^a   Zhang, Ning ^a   Li, Yanbo ^a  

^a THE FIRST AFFILIATED HOSPITAL OF HARBIN MEDICAL UNIVERSITY   (China)

Author keywords

Apoptosis; Autophagy; Endoplasmic reticulum stress; Inflammation; Reactive oxygen species

Indexed keywords

CRYOPYRIN; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; INFLAMMASOME; INTERLEUKIN 18; INTERLEUKIN 1BETA; INTERLEUKIN 1BETA CONVERTING ENZYME; LIPOPOLYSACCHARIDE; NOD LIKE RECEPTOR 3; REACTIVE OXYGEN METABOLITE; RECEPTOR; UNCLASSIFIED DRUG; NLRP3 PROTEIN, HUMAN;

APOPTOSIS; ARTICLE; AUTOPHAGOSOME; AUTOPHAGY INHIBITION; BIOACCUMULATION; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; CYTOKINE PRODUCTION; ENDOPLASMIC RETICULUM STRESS; FLOW CYTOMETRY; FLUORESCENCE ANALYSIS; HEPG2 CELL LINE; HUMAN; INFLAMMATION; INTRACELLULAR SIGNALING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; TRANSMISSION ELECTRON MICROSCOPY; WESTERN BLOTTING; AUTOPHAGY; CYTOLOGY; HEP-G2 CELL LINE; IMMUNOLOGY; LIVER CELL;

AUTOPHAGY; ENDOPLASMIC RETICULUM STRESS; HEP G2 CELLS; HEPATOCYTES; HUMANS; INFLAMMASOMES; INFLAMMATION; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; NLR FAMILY, PYRIN DOMAIN-CONTAINING 3 PROTEIN; REACTIVE OXYGEN SPECIES;

EID: 84988527681     PISSN: 17912997     EISSN: 17913004     Source Type: Journal    
DOI: 10.3892/mmr.2016.5708     Document Type: Article

References (50)

1. Hotamisligil GS: Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
2. Jager J, Grémeaux T, Cormont M, Le Marchand-Brustel Y and Tanti JF: Interleukin-1beta-induced insulin resistance in adipocytes through down-regulation of insulin receptor substrate-1 expression. Endocrinology 148: 241-251, 2007.
3. Lagathu C, Yvan-Charvet L, Bastard JP, Maachi M, Quignard-Boulangé A, Capeau J and Caron M: Long-term treatment with interleukin-1beta induces insulin resistance in murine and human adipocytes. Diabetologia 49: 2162-2173, 2006.
4. Kubes P and Mehal WZ: Sterile inflammation in the liver. Gastroenterology 143: 1158-1172, 2012.
5. Navab M, Gharavi N and Watson AD: Inflammation and metabolic disorders. Curr Opin Clin Nutr Metab Care 11: 459-464, 2008.
6. Amyot J, Semache M, Ferdaoussi M, Fontés G and Poitout V: Lipopolysaccharides impair insulin gene expression in isolated islets of Langerhans via toll-like receptor-4 and NF-B signalling. PloS one 7: e36200, 2012.
7. De Nardo D and Latz E: NLRP3 inflammasomes link inflammation and metabolic disease. Trends Immunol 32: 373-379, 2011.
8. Ting JP, Willingham SB and Bergstralh DT: NLRs at the intersection of cell death and immunity. Nat Rev Immunol 8: 372-379, 2008.
9. Schroder K and Tschopp J: The inflammasomes. Cell 140: 821-832, 2010.
10. Vandanmagsar B, Youm YH, Ravussin A, Galgani JE, Stadler K, Mynatt RL, Ravussin E, Stephens JM and Dixit VD: The NLRP3 inflammasome instigates obesity-induced inflammation and insulin resistance. Nat Med 17: 179-188, 2011.
11. Brenner C, Galluzzi L, Kepp O and Kroemer G: Decoding cell death signals in liver inflammation. J Hepatol 59: 583-594, 2013.
12. Ogata M, Hino S, Saito A, Morikawa K, Kondo S, Kanemoto S, Murakami T, Taniguchi M, Tanii I, Yoshinaga K, et al: Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26: 9220-9231, 2006.
13. Nishitoh H: CHOP is a multifunctional transcription factor in the ER stress response. J Biochem 151: 217-219, 2012.
14. Zhang L, Ren F, Zhang X, Wang X, Shi H, Zhou L, Zheng S, Chen Y, Chen D, Li L, Zhao C and Duan Z: Peroxisome proliferator-activated receptor alpha acts as a mediator of endoplasmic reticulum stress-induced hepatocyte apoptosis in acute liver failure. Dis Model Mech 9: 799-809, 2016.
15. González-Rodríguez A, Mayoral R, Agra N, Valdecantos MP, Pardo V, Miquilena-Colina ME, Vargas-Castrillón J, Lo Iacono O, Corazzari M, Fimia GM, et al: Impaired autophagic flux is associated with increased endoplasmic reticulum stress during the development of NAFLD. Cell Death Dis 5: e1179, 2014.
16. Green DR, Galluzzi L and Kroemer G: Mitochondria and the autophagy-inflammation-cell death axis in organismal aging. Science 333: 1109-1112, 2011.
17. Singh R, Kaushik S, Wang Y, Xiang Y, Novak I, Komatsu M, Tanaka K, Cuervo AM and Czaja MJ: Autophagy regulates lipid metabolism. Nature 458: 1131-1135, 2009.
18. Goldman SJ, Taylor R, Zhang Y and Jin S: Autophagy and the degradation of mitochondria. Mitochondrion 10: 309-315, 2010.
19. Klionsky DJ and Emr SD: Autophagy as a regulated pathway of cellular degradation. Science 290: 1717-1721, 2000.
20. Wang Y, Li YB, Yin JJ, Wang Y, Zhu LB, Xie GY and Pan SH: Autophagy regulates inflammation following oxidative injury in diabetes. Autophagy 9: 272-277, 2013.
21. Kuballa P, Nolte WM, Castoreno AB and Xavier RJ: Autophagy and the immune system. Annu Rev Immunol 30: 611-646, 2012.
22. Yang L, Li P, Fu S, Calay ES and Hotamisligil GS: Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 11: 467-478, 2010.
23. Saitoh T, Fujita N, Jang MH, Uematsu S, Yang BG, Satoh T, Omori H, Noda T, Yamamoto N, Komatsu M, et al: Loss of the autophagy protein Atg16L1 enhances endotoxin-induced IL-1beta production. Nature 456: 264-268, 2008.
24. Hotamisligil GS: Endoplasmic reticulum stress and the inflammatory basis of metabolic disease. Cell 140: 900-917, 2010.
25. Wree A, Eguchi A, McGeough MD, Pena CA, Johnson CD, Canbay A, Hoffman HM and Feldstein AE: NLRP3 inflammasome activation results in hepatocyte pyroptosis, liver inflammation and fibrosis in mice. Hepatology 59: 898-910, 2014.
26. Wen H, Gris D, Lei Y, Jha S, Zhang L, Huang MT, Brickey WJ and Ting JP: Fatty acid-induced NLRP3-ASC inflammasome activation interferes with insulin signaling. Nat Immunol 12: 408-415, 2011.
27. LeBel CP, Ischiropoulos H and Bondy SC: Evaluation of the probe 2',7'-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5: 227-231, 1992.
28. Dangi A, Huang C, Tandon A, Stolz D, Wu T and Gandhi CR: Endotoxin-stimulated rat hepatic stellate cells induce autophagy in hepatocytes as a survival mechanism. J Cell Physiol 231: 94-105, 2016.
29. Czaja MJ, Ding WX, Donohue TM Jr, Friedman SL, Kim JS, Komatsu M, Lemasters JJ, Lemoine A, Lin JD, Ou JH, et al: Functions of autophagy in normal and diseased liver. Autophagy 9: 1131-1158, 2013.
30. Malhotra JD and Kaufman RJ: Endoplasmic reticulum stress and oxidative stress: A vicious cycle or a double-edged sword? Antioxid Redox Signal 9: 2277-2293, 2007.
31. Scull CM and Tabas I: Mechanisms of ER stress-induced apoptosis in atherosclerosis. Arterioscler Thromb Vasc Biol 31: 2792-2797, 2011.
32. Ding WX, Ni HM, Gao W, Yoshimori T, Stolz DB, Ron D and Yin XM: Linking of autophagy to ubiquitin-proteasome system is important for the regulation of endoplasmic reticulum stress and cell viability. Am J Pathol 171: 513-524, 2007.
33. Uysal KT, Wiesbrock SM, Marino MW and Hotamisligil GS: Protection from obesity-induced insulin resistance in mice lacking TNF-alpha function. Nature 389: 610-614, 1997.
34. Sabio G, Das M, Mora A, Zhang Z, Jun JY, Ko HJ, Barrett T, Kim JK and Davis RJ: A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322: 1539-1543, 2008.
35. Franchi L, Muñoz-Planillo R, Reimer T, Eigenbrod T and Núñez G: Inflammasomes as microbial sensors. Eur J Immunol 40: 611-615, 2010.
36. Dostert C, Pétrilli V, Van Bruggen R, Steele C, Mossman BT and Tschopp J: Innate immune activation through Nalp3 inflammasome sensing of asbestos and silica. Science 320: 674-677, 2008.
37. Napoli C, de Nigris F and Palinski W: Multiple role of reactive oxygen species in the arterial wall. J Cell Biochem 82: 674-682, 2001.
38. Yuan XM, Li W, Olsson AG and Brunk UT: The toxicity to macrophages of oxidized low-density lipoprotein is mediated through lysosomal damage. Atherosclerosis 133: 153-161, 1997.
39. Larsen CM, Faulenbach M, Vaag A, Vølund A, Ehses JA, Seifert B, Mandrup-Poulsen T and Donath MY: Interleukin-1-receptor antagonist in type 2 diabetes mellitus. N Engl J Med 356: 1517-1526, 2007.
40. Gandhi CR, Kuddus RH, Nemoto EM and Murase N: Endotoxin treatment causes an upregulation of the endothelin system in the liver: Amelioration of increased portal resistance by endothelin receptor antagonism. J Gastroenterol Hepatol 16: 61-69, 2001.
41. Xie Q, Khaoustov VI, Chung CC, Sohn J, Krishnan B, Lewis DE and Yoffe B: Effect of tauroursodeoxycholic acid on endoplasmic reticulum stress-induced caspase-12 activation. Hepatology 36: 592-601, 2002.
42. Kouroku Y, Fujita E, Tanida I, Ueno T, Isoai A, Kumagai H, Ogawa S, Kaufman RJ, Kominami E and Momoi T: ER stress (PERK/eIF2alpha phosphorylation) mediates the polyglutamine-induced LC3 conversion, an essential step for autophagy formation. Cell Death Differ 14: 230-239, 2007.
43. Qin L, Wang Z, Tao L and Wang Y: ER stress negatively regulates AKT/TSC/mTOR pathway to enhance autophagy. Autophagy 6: 239-247, 2010.
44. Høyer-Hansen M and Jäättelä M: Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 14: 1576-1582, 2007.
45. Corcelle EA, Puustinen P and Jäättelä M: Apoptosis and autophagy: Targeting autophagy signalling in cancer cells-'trick or treats'? FEBS J 276: 6084-6096, 2009.
46. Zhou R, Yazdi AS, Menu P and Tschopp J: A role for mitochondria in NLRP3 inflammasome activation. Nature 469: 221-225, 2011.
47. Nakahira K, Haspel JA, Rathinam VA, Lee SJ, Dolinay T, Lam HC, Englert JA, Rabinovitch M, Cernadas M, Kim HP, et al: Autophagy proteins regulate innate immune responses by inhibiting the release of mitochondrial DNA mediated by the NALP3 inflammasome. Nat Immunol 12: 222-230, 2011.
48. Degenhardt K, Mathew R, Beaudoin B, Bray K, Anderson D, Chen G, Mukherjee C, Shi Y, Gélinas C, Fan Y, et al: Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 10: 51-64, 2006.
49. Luo MX, Wong SH, Chan MT, Yu L, Yu SS, Wu F, Xiao Z, Wang X, Zhang L, Cheng AS, et al: Autophagy mediates HBx-induced nuclear factor-B activation and release of IL-6, IL-8 and CXCL2 in hepatocytes. J Cell Physiol 230: 2382-2389, 2015.
50. Talero E, Alcaide A, Ávila-Román J, García-Mauriño S, Vendramini-Costa D and Motilva V: Expression patterns of sirtuin 1-AMPK-autophagy pathway in chronic colitis and inflammation-associated colon neoplasia in IL-10-deficient mice. Int Immunopharmacol 35: 248-256, 2016.