The autophagy-related gene 14 (Atg14) is regulated by forkhead box O transcription factors and circadian rhythms and plays a critical role in hepatic autophagy and lipid metabolism

Journal of Biological Chemistry

Volumn 287, Issue 46, 2012, Pages 39107-39114

  Xiong, Xiwen ^a   Tao, Rongya ^a   DePinho, Ronald A ^b   Dong, X Charlie ^a  

^a INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF TEXAS MD ANDERSON CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AGGREGATED PROTEIN; AUTOPHAGY; CELL SURVIVAL; CHROMATIN IMMUNOPRECIPITATION ASSAY; CIRCADIAN RHYTHMS; CIS-ELEMENTS; CORE CLOCK; ELEVATED LEVEL; ESSENTIAL GENE; FORKHEAD BOX O; GENE KNOCK DOWN; HYPERTRIGLYCERIDEMIA; KEY REGULATORS; KNOCK OUTS; LIPID METABOLISMS; METABOLIC FUNCTION; MOUSE LIVER; OVER-EXPRESSION; PROLONGED STARVATION; REPORTER ANALYSIS; TARGET GENES; WILD TYPES;

CLOCKS; MACHINERY; MAMMALS; METABOLISM; PHYSIOLOGY; TRANSCRIPTION FACTORS;

GENES;

FORKHEAD BOX O PROTEIN; FORKHEAD TRANSCRIPTION FACTOR; LIPID; LUCIFERASE; TRANSCRIPTION FACTOR ARNTL; TRANSCRIPTION FACTOR CLOCK; TRIACYLGLYCEROL; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; AUTOPHAGY RELATED GENE 14; CHROMATIN IMMUNOPRECIPITATION; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE OVEREXPRESSION; GENE SILENCING; HUMAN; HUMAN CELL; HYPERTRIGLYCERIDEMIA; LIPID DIET; LIPID LIVER LEVEL; LIPID METABOLISM; LIVER CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TRIACYLGLYCEROL BLOOD LEVEL; WILD TYPE;

ADAPTOR PROTEINS, VESICULAR TRANSPORT; ANIMALS; AUTOPHAGY; BASE SEQUENCE; CIRCADIAN RHYTHM; FORKHEAD TRANSCRIPTION FACTORS; HEK293 CELLS; HOMEOSTASIS; HUMANS; LIPID METABOLISM; LIPIDS; LIVER; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; TRIGLYCERIDES; VESICULAR TRANSPORT PROTEINS;

MUS;

EID: 84869005229     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.412569     Document Type: Article

References (48)

1. Yang, Z., and Klionsky, D. J. (2010) Eaten alive. A history of macroautophagy. Nat. Cell Biol. 12, 814-822
2. Itakura, E., Kishi, C., Inoue, K., and Mizushima, N. (2008) Beclin 1 forms two distinct phosphatidylinositol 3-kinase complexes with mammalian Atg14 and UVRAG. Mol. Biol. Cell 19, 5360-5372
3. Sun, Q., Fan, W., Chen, K., Ding, X., Chen, S., and Zhong, Q. (2008) Identification of Barkor as a mammalian autophagy-specific factor for Beclin 1 and class III phosphatidylinositol 3-kinase. Proc. Natl. Acad. Sci. U.S.A. 105, 19211-19216
4. Zhong, Y., Wang, Q. J., Li, X., Yan, Y., Backer, J. M., Chait, B. T., Heintz, N., and Yue, Z. (2009) Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nat. Cell Biol. 11, 468-476
5. Fan, W., Nassiri, A., and Zhong, Q. (2011) Autophagosome targeting and membrane curvature sensing by Barkor/Atg14(L). Proc. Natl. Acad. Sci. U.S.A. 108, 7769-7774
6. Matsunaga, K., Morita, E., Saitoh, T., Akira, S., Ktistakis, N. T., Izumi, T., Noda, T., and Yoshimori, T. (2010) Autophagy requires endoplasmic reticulum targeting of the PI3-kinase complex via Atg14L. J. Cell Biol. 190, 511-521
7. Yang, P., and Zhang, H. (2011) The coiled-coil domain protein EPG-8 plays an essential role in the autophagy pathway in C. elegans. Autophagy 7, 159-165
8. Rubinsztein, D. C., Mariño, G., and Kroemer, G. (2011) Autophagy and aging. Cell 146, 682-695
9. Jaber, N., Dou, Z., Chen, J. S., Catanzaro, J., Jiang, Y. P., Ballou, L. M., Selinger, E., Ouyang, X., Lin, R. Z., Zhang, J., and Zong, W. X. (2012) Class III PI3K Vps34 plays an essential role in autophagy and in heart and liver function. Proc. Natl. Acad. Sci. U.S.A. 109, 2003-2008
10. Singh, R., Kaushik, S., Wang, Y., Xiang, Y., Novak, I., Komatsu, M., Tanaka, K., Cuervo, A. M., and Czaja, M. J. (2009) Autophagy regulates lipid metabolism. Nature 458, 1131-1135
11. Yang, L., Li, P., Fu, S., Calay, E. S., and Hotamisligil, G. S. (2010) Defective hepatic autophagy in obesity promotes ER stress and causes insulin resistance. Cell Metab. 11, 467-478
12. Tao, R., Wei, D., Gao, H., Liu, Y., DePinho, R. A., and Dong, X. C. (2011) Hepatic FoxOs regulate lipid metabolism via modulation of expression of the nicotinamide phosphoribosyltransferase gene. J. Biol. Chem. 286, 14681-14690
13. Hou, T. Y., Ward, S. M., Murad, J. M., Watson, N. P., Israel, M. A., and Duffield, G. E. (2009) ID2 (inhibitor of DNA binding 2) is a rhythmically expressed transcriptional repressor required for circadian clock output in mouse liver. J. Biol. Chem. 284, 31735-31745
14. Ding, W. X., and Yin, X. M. (2009) Analyzing macroautophagy in hepatocytes and the liver. Methods Enzymol. 453, 397-416
15. Komatsu, M., Kageyama, S., and Ichimura, Y. (2012) p62/SQSTM1/A170: Physiology and pathology. Pharmacol. Res., in press
16. Yang, Z., and Klionsky, D. J. (2010) Mammalian autophagy. Core molecular machinery and signaling regulation. Curr. Opin. Cell Biol. 22, 124-131
17. Ma, D., Panda, S., and Lin, J. D. (2011) Temporal orchestration of circadian autophagy rhythm by C/EBPβ. EMBO J. 30, 4642-4651
18. Rouschop, K. M., van den Beucken, T., Dubois, L., Niessen, H., Bussink, J., Savelkouls, K., Keulers, T., Mujcic, H., Landuyt, W., Voncken, J. W., Lambin, P., van der Kogel, A. J., Koritzinsky, M., and Wouters, B. G. (2010) The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. J. Clin. Invest. 120, 127-141
19. Polager, S., Ofir, M., and Ginsberg, D. (2008) E2F1 regulates autophagy and the transcription of autophagy genes. Oncogene 27, 4860-4864
20. Sengupta, A., Molkentin, J. D., and Yutzey, K. E. (2009) FoxO transcription factors promote autophagy in cardiomyocytes. J. Biol. Chem. 284, 28319-28331
21. Mammucari, C., Milan, G., Romanello, V., Masiero, E., Rudolf, R., Del Piccolo, P., Burden, S. J., Di Lisi, R., Sandri, C., Zhao, J., Goldberg, A. L., Schiaffino, S., and Sandri, M. (2007) FoxO3 controls autophagy in skeletal muscle in vivo. Cell Metab. 6, 458-471 (Pubitemid 350163055)
22. Zhao, J., Brault, J. J., Schild, A., Cao, P., Sandri, M., Schiaffino, S., Lecker, S. H., and Goldberg, A. L. (2007) FoxO3 coordinately activates protein degradation by the autophagic/lysosomal and proteasomal pathways in atrophying muscle cells. Cell Metab. 6, 472-483 (Pubitemid 350163056)
23. Liu, H. Y., Han, J., Cao, S. Y., Hong, T., Zhuo, D., Shi, J., Liu, Z., and Cao, W. (2009) Hepatic autophagy is suppressed in the presence of insulin resistance and hyperinsulinemia. Inhibition of FoxO1-dependent expression of key autophagy genes by insulin. J. Biol. Chem. 284, 31484-31492
24. Comb, W. C., Cogswell, P., Sitcheran, R., and Baldwin, A. S. (2011) IKK-dependent, NF-κB-independent control of autophagic gene expression. Oncogene 30, 1727-1732
25. Chaanine, A. H., Jeong, D., Liang, L., Chemaly, E. R., Fish, K., Gordon, R. E., and Hajjar, R. J. (2012) JNK modulates FOXO3a for the expression of the mitochondrial death and mitophagy marker BNIP3 in pathological hypertrophy and in heart failure. Cell Death Dis. 3, 265
26. Han, J., Pan, X. Y., Xu, Y., Xiao, Y., An, Y., Tie, L., Pan, Y., and Li, X. J. (2012) Curcumin induces autophagy to protect vascular endothelial cell survival from oxidative stress damage. Autophagy 8, 812-825
27. Hariharan, N., Maejima, Y., Nakae, J., Paik, J., Depinho, R. A., and Sadoshima, J. (2010) Deacetylation of FoxO by Sirt1 Plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ. Res. 107, 1470-1482
28. Kong, D. K., Georgescu, S. P., Cano, C., Aronovitz, M. J., Iovanna, J. L., Patten, R. D., Kyriakis, J. M., and Goruppi, S. (2010) Deficiency of the transcriptional regulator p8 results in increased autophagy and apoptosis and causes impaired heart function. Mol. Biol. Cell 21, 1335-1349
29. Kume, S., Uzu, T., Horiike, K., Chin-Kanasaki, M., Isshiki, K., Araki, S., Sugimoto, T., Haneda, M., Kashiwagi, A., and Koya, D. (2010) Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 120, 1043-1055
30. Lipinski, M. M., Hoffman, G., Ng, A., Zhou, W., Py, B. F., Hsu, E., Liu, X., Eisenberg, J., Liu, J., Blenis, J., Xavier, R. J., and Yuan, J. (2010) A genomewide siRNA screen reveals multiple mTORC1 independent signaling pathways regulating autophagy under normal nutritional conditions. Dev. Cell 18, 1041-1052
31. Sadagurski, M., Cheng, Z., Rozzo, A., Palazzolo, I., Kelley, G. R., Dong, X., Krainc, D., and White, M. F. (2011) IRS2 increases mitochondrial dysfunction and oxidative stress in a mouse model of Huntington disease. J. Clin. Invest. 121, 4070-4081
32. Sanchez, A. M., Csibi, A., Raibon, A., Cornille, K., Gay, S., Bernardi, H., and Candau, R. (2012) AMPK promotes skeletal muscle autophagy through activation of forkhead FoxO3a and interaction with Ulk1. J. Cell Biochem. 113, 695-710
33. Schips, T. G., Wietelmann, A., Höhn, K., Schimanski, S., Walther, P., Braun, T., Wirth, T., and Maier, H. J. (2011) FoxO3 induces reversible cardiac atrophy and autophagy in a transgenic mouse model. Cardiovasc. Res. 91, 587-597
34. Sengupta, A., Molkentin, J. D., Paik, J. H., DePinho, R. A., and Yutzey, K. E. (2011) FoxO transcription factors promote cardiomyocyte survival upon induction of oxidative stress. J. Biol. Chem. 286, 7468-7478
35. van der Vos, K. E., Eliasson, P., Proikas-Cezanne, T., Vervoort, S. J., van Boxtel, R., Putker, M., van Zutphen, I. J., Mauthe, M., Zellmer, S., Pals, C., Verhagen, L. P., Groot Koerkamp, M. J., Braat, A. K., Dansen, T. B., Holstege, F. C., Gebhardt, R., Burgering, B. M., and Coffer, P. J. (2012) Modulation of glutamine metabolism by the PI(3)K-PKB-FOXO network regulates autophagy. Nat. Cell Biol. 14, 829-837
36. Vidal, R. L., Figueroa, A., Court, F. A., Thielen, P., Molina, C., Wirth, C., Caballero, B., Kiffin, R., Segura-Aguilar, J., Cuervo, A. M., Glimcher, L. H., and Hetz, C. (2012) Targeting the UPR transcription factor XBP1 protects against Huntington disease through the regulation of FoxO1 and autophagy. Hum. Mol. Genet 21, 2245-2262
37. Wang, X., and Su, H. (2011) FoxO3 hastens autophagy and shrinks the heart but does not curtail pathological hypertrophy in adult mice. Cardiovasc. Res. 91, 561-562
38. Xu, P., Das, M., Reilly, J., and Davis, R. J. (2011) JNK regulates FoxO-dependent autophagy in neurons. Genes Dev. 25, 310-322
39. Chiacchiera, F., Matrone, A., Ferrari, E., Ingravallo, G., Lo Sasso, G., Murzilli, S., Petruzzelli, M., Salvatore, L., Moschetta, A., and Simone, C. (2009) p38α blockade inhibits colorectal cancer growth in vivo by inducing a switch from HIF1α- to FoxO-dependent transcription. Cell Death Differ. 16, 1203-1214
40. Zhao, Y., Yang, J., Liao, W., Liu, X., Zhang, H., Wang, S., Wang, D., Feng, J., Yu, L., and Zhu, W. G. (2010) Cytosolic FoxO1 is essential for the induction of autophagy and tumorsuppressor activity. Nat. Cell Biol. 12, 665-675
41. Youle, R. J., and Narendra, D. P. (2011) Mechanisms of mitophagy. Nat. Rev. Mol. Cell Biol. 12, 9-14
42. Velikkakath, A. K., Nishimura, T., Oita, E., Ishihara, N., and Mizushima, N. (2012) Mammalian Atg2 proteins are essential for autophagosome formation and important for regulation of size and distribution of lipid droplets. Mol. Biol. Cell 23, 896-909
43. Skop, V., Cahová, M., Papáčková, Z., Páleníčková, E., Daňková, H., Baranowski, M., Zabielski, P., Zdychová, J., Zídková, J., and Kazdová, L. (2012) Autophagy-lysosomal pathway is involved in lipid degradation in rat liver. Physiol. Res. 61, 287-297
44. Sinha, R. A., You, S. H., Zhou, J., Siddique, M. M., Bay, B. H., Zhu, X., Privalsky, M. L., Cheng, S. Y., Stevens, R. D., Summers, S. A., Newgard, C. B., Lazar, M. A., and Yen, P. M. (2012) Thyroid hormone stimulates hepatic lipid catabolism via activation of autophagy. J. Clin. Invest. 122, 2428-2438
45. Ding, W. X., Li, M., Chen, X., Ni, H. M., Lin, C. W., Gao, W., Lu, B., Stolz, D. B., Clemens, D. L., and Yin, X. M. (2010) Autophagy reduces acute ethanol-induced hepatotoxicity and steatosis in mice. Gastroenterology 139, 1740-1752
46. Weidberg, H., Shvets, E., and Elazar, Z. (2009) Lipophagy. selective catabolism designed for lipids. Dev. Cell 16, 628-630
47. Singh, R., and Cuervo, A. M. (2012) Lipophagy. Connecting autophagy and lipid metabolism. Int. J. Cell Biol. 2012, 282041
48. Ding, W. X., Li, M., and Yin, X. M. (2011) Selective taste of ethanol-induced autophagy for mitochondria and lipid droplets. Autophagy 7, 248-249