Lipid-Induced Endoplasmic Reticulum Stress Impairs Selective Autophagy at the Step of Autophagosome-Lysosome Fusion in Hepatocytes

American Journal of Pathology

Volumn 186, Issue 7, 2016, Pages 1861-1873

  Miyagawa, Koichiro ^a   Oe, Shinji ^a   Honma, Yuichi ^a   Izumi, Hiroto ^a   Baba, Ryoko ^a   Harada, Masaru ^a  

^a UNIVERSITY OF OCCUPATIONAL AND ENVIRONMENTAL HEALTH   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MONOUNSATURATED FATTY ACID; PROTEIN P62; SATURATED FATTY ACID; UBIQUITIN; UBIQUITINATED PROTEIN; FATTY ACID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGOSOME; CELL CULTURE; CELL FUSION; CONTROLLED STUDY; ENDOPLASMIC RETICULUM STRESS; HUMAN; HUMAN CELL; LIPID DIET; LIVER CELL; LYSOSOME; MALE; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SELECTIVE AUTOPHAGY; STEATOSIS; ADVERSE EFFECTS; ANIMAL; AUTOPHAGY; C57BL MOUSE; DISEASE MODEL; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOBLOTTING; NONALCOHOLIC FATTY LIVER; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; AUTOPHAGOSOMES; AUTOPHAGY; CELL LINE, TUMOR; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; ENDOPLASMIC RETICULUM STRESS; FATTY ACIDS; FATTY ACIDS, MONOUNSATURATED; FLUORESCENT ANTIBODY TECHNIQUE; HEPATOCYTES; HUMANS; IMMUNOBLOTTING; LYSOSOMES; MALE; MICE; MICE, INBRED C57BL; NON-ALCOHOLIC FATTY LIVER DISEASE;

EID: 84997582052     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2016.03.003     Document Type: Article

References (52)

1. 1 Bechmann, L.P., Hannivoort, R.A., Gerken, G., Hotamisligil, G.S., Trauner, M., Canbay, A., The interaction of hepatic lipid and glucose metabolism in liver diseases. J Hepatol 56 (2012), 952–964.
2. 2 Ortiz-Lopez, C., Lomonaco, R., Orsak, B., Finch, J., Chang, Z., Kochunov, V.G., Hardies, J., Cusi, K., Prevalence of prediabetes and diabetes and metabolic profile of patients with nonalcoholic fatty liver disease (NAFLD). Diabetes Care 35 (2012), 873–878.
3. 3 Loomba, R., Abraham, M., Unalp, A., Wilson, L., Lavine, J., Doo, E., Bass, N.M., Nonalcoholic Steatohepatitis Clinical Research Network. Association between diabetes, family history of diabetes, and risk of nonalcoholic steatohepatitis and fibrosis. Hepatology 56 (2012), 943–951.
4. 4 Paredes, A.H., Torres, D.M., Harrison, S.A., Nonalcoholic fatty liver disease. Clin Liver Dis 16 (2012), 397–419.
5. 5 Milić, S., Stimac, D., Nonalcoholic fatty liver disease/steatohepatitis: epidemiology, pathogenesis, clinical presentation and treatment. Dig Dis 30 (2012), 158–162.
6. 6 Fabbrini, E., Sullivan, S., Klein, S., Obesity and nonalcoholic fatty liver disease: biochemical, metabolic, and clinical implications. Hepatology 51 (2010), 679–689.
7. 7 Gregor, M.F., Hotamisligil, G.S., Thematic review series: adipocyte biology. Adipocyte stress: the endoplasmic reticulum and metabolic disease. J Lipid Res 48 (2007), 1905–1914.
8. 8 Dara, L., Ji, C., Kaplowitz, N., The contribution of endoplasmic reticulum stress to liver diseases. Hepatology 53 (2011), 1752–1763.
9. 9 Malhi, H., Kaufman, R.J., Endoplasmic reticulum stress in liver disease. J Hepatol 54 (2011), 795–809.
10. 10 Ron, D., Walter, P., Signal integration in the endoplasmic reticulum unfolded protein response. Nat Rev Mol Cell Biol 8 (2007), 519–529.
11. 11 McCracken, A.A., Brodsky, J.L., Assembly of ER-associated protein degradation in vitro: dependence on cytosol, calnexin, and ATP. J Cell Biol 132 (1996), 291–298.
12. 12 Hamel, F.G., Preliminary report: inhibition of cellular proteasome activity by free fatty acids. Metabolism 58 (2009), 1047–1049.
13. 13 Harada, M., Hanada, S., Toivola, D.M., Ghori, N., Omary, M.B., Autophagy activation by rapamycin eliminates mouse Mallory-Denk bodies and blocks their proteasome inhibitor-mediated formation. Hepatology 47 (2008), 2026–2035.
14. 14 Kroeger, H., Miranda, E., MacLeod, I., Pérez, J., Crowther, D.C., Marciniak, S.J., Lomas, D.A., Endoplasmic reticulum-associated degradation (ERAD) and autophagy cooperate to degrade polymerogenic mutant serpins. J Biol Chem 284 (2009), 22793–22802.
15. 15 Tremblay, F., Krebs, M., Dombrowski, L., Brehm, A., Bernroider, E., Roth, E., Nowotny, P., Waldhäusl, W., Marette, A., Roden, M., Overactivation of S6 kinase 1 as a cause of human insulin resistance during increased amino acid availability. Diabetes 54 (2005), 2674–2684.
16. 16 Yang, L., Li, P., Fu, S., Calay, E.S., Hotamisligil, G.S., Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab 11 (2010), 467–478.
17. 17 Rautou, P.E., Mansouri, A., Lebrec, D., Durand, F., Valla, D., Moreau, R., Autophagy in liver diseases. J Hepatol 53 (2010), 1123–1134.
18. 18 Otoda, T., Takamura, T., Misu, H., Ota, T., Murata, S., Hayashi, H., Takayama, H., Kikuchi, A., Kanamori, T., Shima, K.R., Lan, F., Takeda, T., Kurita, S., Ishikura, K., Kita, Y., Iwayama, K., Kato, K., Uno, M., Takeshita, Y., Yamamoto, M., Tokuyama, K., Iseki, S., Tanaka, K., Kaneko, S., Proteasome dysfunction mediates obesity-induced endoplasmic reticulum stress and insulin resistance in the liver. Diabetes 62 (2013), 811–824.
19. 19 Mehrpour, M., Esclatine, A., Beau, I., Codogno, P., Autophagy in health and disease. 1. Regulation and significance of autophagy: an overview. Am J Physiol Cell Physiol 298 (2010), C776–C785.
20. 20 Orenstein, S.J., Cuervo, A.M., Chaperone-mediated autophagy: molecular mechanisms and physiological relevance. Semin Cell Dev Biol 21 (2010), 719–726.
21. 21 Mizushima, N., Komatsu, M., Autophagy: renovation of cells and tissues. Cell 147 (2011), 728–741.
22. 22 Nixon, R.A., The role of autophagy in neurodegenerative disease. Nat Med 19 (2013), 983–997.
23. 23 Komatsu, M., Liver autophagy: physiology and pathology. J Biochem 152 (2012), 5–15.
24. 24 Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., Mizushima, N., Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441 (2006), 885–889.
25. 25 Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A.M., Czaja, M.J., Autophagy regulates lipid metabolism. Nature 458 (2009), 1131–1135.
26. 26 Harada, M., Strnad, P., Toivola, D.M., Omary, M.B., Autophagy modulates keratin-containing inclusion formation and apoptosis in cell culture in a context-dependent fashion. Exp Cell Res 314 (2008), 1753–1764.
27. 27 Inami, Y., Yamashina, S., Izumi, K., Ueno, T., Tanida, I., Ikejima, K., Watanabe, S., Hepatic steatosis inhibits autophagic proteolysis via impairment of autophagosomal acidification and cathepsin expression. Biochem Biophys Res Commun 412 (2011), 618–625.
28. 28 Koga, H., Kaushik, S., Cuervo, A.M., Altered lipid content inhibits autophagic vesicular fusion. FASEB J 24 (2010), 3052–3065.
29. 29 Malhi, H., Bronk, S.F., Werneburg, N.W., Gores, G.J., Free fatty acids induce JNK-dependent hepatocyte lipoapoptosis. J Biol Chem 281 (2006), 12093–12101.
30. 30 Akazawa, Y., Cazanave, S., Mott, J.L., Elmi, N., Bronk, S.F., Kohno, S., Chariton, M.R., Gores, G.J., Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis. J Hepatol 52 (2010), 586–593.
31. 31 Cousin, S.P., Hügl, S.R., Wrede, C.E., Kajio, H., Myers, M.G. Jr., Rhodes, C.J., Free fatty acid-induced inhibition of glucose and insulin-like growth factor I-induced deoxyribonucleic acid synthesis in the pancreatic beta-cell line INS-1. Endocrinology 142 (2001), 229–240.
32. 32 Greenspan, P., Mayer, E.P., Fowler, S.D., Nile red: a selective fluorescent stain for intracellular lipid droplets. J Cell Biol 100 (1985), 965–973.
33. 33 Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., Yoshimori, T., LC3, a mammalian homologue of yeast Apg8p, is localized in ahtophagosome membranes after processing. EMBO J 19 (2000), 5720–5728.
34. 34 Mizushima, N., Yoshimori, T., How to interpret LC3 immunoblotting. Autophagy 3 (2007), 542–545.
35. 35 Mizushima, N., Yoshimori, T., Levine, B., Methods in mammalian autophagy research. Cell 140 (2010), 313–326.
36. 36 He, C., Levine, B., The Beclin 1 interactome. Curr Opin Cell Biol 22 (2010), 140–149.
37. 37 Mei, S., Ni, H.M., Manley, S., Bockus, A., Kassel, K.M., Luyendyk, J.P., Copple, B.L., Ding, W.X., Differential roles of unsaturated and saturated fatty acid on autophagy and apoptosis in hepatocytes. J Pharmacol Exp Ther 339 (2011), 487–498.
38. 38 Baylin, A., Kabagambe, E.K., Siles, X., Campos, H., Adipose tissue biomarkers of fatty acid intake. Am J Clin Nutr 76 (2002), 750–757.
39. 39 Rubinsztein, D.C., Cuervo, A.M., Ravikumar, B., Sarkar, S., Korolchuk, V., Kaushik, S., Koionsky, D.J., In search of an “autophagomometer”. Autophagy 5 (2009), 585–589.
40. 40 Kimura, S., Noda, T., Yoshimori, T., Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3 (2007), 452–460.
41. 41 Bampton, E.T., Goemans, C.G., Niranjan, D., Mizushima, N., Tolkovsky, A.M., The dynamics of autophagy visualized in live cells: from autophagosome formation to fusion with endo/lysosomes. Autophagy 1 (2005), 23–36.
42. 42 Ni, H.M., Bockus, A., Wozniak, A.L., Jones, K., Weinman, S., Yin, X.M., Ding, W.X., Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy 7 (2011), 188–204.
43. 43 Zatloukal, K., French, S.W., Stumptner, C., Strnad, P., Harada, M., Toivola, D.M., Cadrin, M., Omary, M.B., From Mallory to Mallory-Denk bodies: what, how and why?. Exp Cell Res 313 (2007), 2033–2049.
44. 44 Taguchi, K., Fujikawa, N., Komatsu, M., Ishii, T., Unno, M., Akaike, T., Motohashi, H., Yamamoto, M., Keap1 degradation by autophagy for the maintenance of redox homeostasis. Proc Natl Acad Sci U S A 109 (2012), 13561–13566.
45. 45 Hanada, S., Harada, M., Kumemura, H., Bishr Omary, M., Koga, H., Kawaguchi, T., Taniguchi, E., Yoshida, T., Hisamoto, T., Yanagimoto, C., Maeyama, M., Ueno, T., Sata, M., Oxidative stress induces the endoplasmic reticulum stress and facilitates inclusion formation in cultured cells. J Hepatol 47 (2007), 93–102.
46. 46 Yanagitani, K., Imagawa, Y., Iwawaki, T., Hosoda, A., Saito, M., Kimata, Y., Kohno, K., Cotranslational targeting of XBP1 protein to the membrane promotes cytoplasmic splicing of its own mRNA. Mol Cell 34 (2009), 191–200.
47. 47 Sahani, M.H., Itakura, E., Mizushima, N., Expression of the autophagy substrate SQSTM1/p62 is restored during prolonged starvation depending on transcriptional upregulation and autophagy-derived amino acids. Autophagy 10 (2014), 431–441.
48. 48 Zatloukal, K., Stumptner, C., Fuchsbichler, A., Heid, H., Schnoelzer, M., Kenner, L., Kleinert, R., Prinz, M., Aguzzi, A., Denk, H., p62 is a common component of cytoplasmic inclusions in protein aggregation diseases. Am J Pathol 160 (2002), 255–263.
49. 49 Ogata, M., Hino, S., Saito, A., Morikawa, K., Kondo, S., Kanemoto, S., Murakami, T., Taniguchi, M., Tanii, I., Yoshinaga, K., Shiosaka, S., Hammarback, J.A., Urano, F., Imaizumi, K., Autophagy is activated for cell survival after endoplasmic reticulum stress. Mol Cell Biol 26 (2006), 9220–9231.
50. 50 Ganley, I.G., Wong, P.M., Gammoh, N., Jiang, X., Distinct autophagosomal-lysosomal fusion mechanism revealed by thapsigargin-induced autophagy arrest. Mol Cell 42 (2011), 731–743.
51. 51 Kim, D.S., Li, B., Rhew, K.Y., Oh, H.W., Lim, H.D., Lee, W., Chae, H.J., Kim, H.R., The regulatory mechanism of 4-phenylbutyric acid against ER stress-induced autophagy in human gingival fibroblasts. Arch Pharm Res 35 (2012), 1269–1278.
52. 52 Yang, Z., Klionsky, D.J., Eaten alive: a history of macroautophagy. Nat Cell Biol 12 (2010), 814–822.