Bioenergetic and autophagic control by Sirt3 in response to nutrient deprivation in mouse embryonic fibroblasts

Biochemical Journal

Volumn 454, Issue 2, 2013, Pages 249-257

  Liang, Qiuli ^a,b,c   Benavides, Gloria A ^a,b   Vassilopoulos, Athanassios ^d   Gius, David ^d   Darley Usmar, Victor ^a   Zhang, Jianhua ^a,b,c  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b University of Alabama at Birmingham   (United States)

^c BIRMINGHAM VA MEDICAL CENTER   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Apoptosis; Autophagy; C Jun; C Jun N terminal kinase (JNK); Sirtuin 3

Indexed keywords

CASPASE 3; LYSOSOME ASSOCIATED MEMBRANE PROTEIN 1; MAMMALIAN TARGET OF RAPAMYCIN; SIRTUIN 3; STRESS ACTIVATED PROTEIN KINASE;

ANIMAL CELL; ANIMAL CELL CULTURE; APOPTOSIS; ARTICLE; AUTOPHAGY; BIOENERGY; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; EMBRYO; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST; MITOCHONDRIAL RESPIRATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SYNTHESIS; STARVATION; STEADY STATE; WESTERN BLOTTING;

ANIMALS; APOPTOSIS; AUTOPHAGY; CASPASE 3; CELLS, CULTURED; CULTURE MEDIA; EMBRYO, MAMMALIAN; ENERGY METABOLISM; ENZYME ACTIVATION; FIBROBLASTS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; MICROTUBULE-ASSOCIATED PROTEINS; OXIDATIVE PHOSPHORYLATION; PHOSPHORYLATION; PROTEIN ISOFORMS; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIRTUIN 3; TOR SERINE-THREONINE KINASES; TUBULIN MODULATORS;

EID: 84881538902     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20130414     Document Type: Article

References (52)

1. Reggiori, F. and Klionsky, D. J. (2002) Autophagy in the eukaryotic cell. Eukaryotic Cell 1, 11-21
2. Yang, Z. and Klionsky, D. J. (2009) An overview of the molecular mechanism of autophagy. Curr. Top. Microbiol. Immunol. 335, 1-32
3. Scherz-Shouval, R., Weidberg, H., Gonen, C., Wilder, S., Elazar, Z. and Oren, M. (2010) p53-dependent regulation of autophagy protein LC3 supports cancer cell survival under prolonged starvation. Proc. Natl. Acad. Sci. U.S.A. 107, 18511-18516
4. Pan, T., Kondo, S., Le, W. and Jankovic, J. (2008) The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease. Brain 131, 1969-1978
5. Klionsky, D. J., Cuervo, A. M. and Seglen, P. O. (2007) Methods for monitoring autophagy from yeast to human. Autophagy 3, 181-206
6. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y. and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
7. Kabeya, Y., Mizushima, N., Yamamoto, A., Oshitani-Okamoto, S., Ohsumi, Y. and Yoshimori, T. (2004) LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117, 2805-2812
8. Hill, B. G., Benavides, G. A., Lancaster, J. R., Ballinger, S., Dell'italia, L., Zhang, J. and Darley-Usmar, V. M. (2012) Integration of cellular bioenergetics with mitochondrial quality control and autophagy. Biol. Chem. 393, 1485-1512
9. Lee, J., Giordano, S. and Zhang, J. (2012) Autophagy, mitochondria and oxidative stress: cross-talk and redox signalling. Biochem. J. 441, 523-540
10. Kawamura, Y., Uchijima, Y., Horike, N., Tonami, K., Nishiyama, K., Amano, T., Asano, T., Kurihara, Y. and Kurihara, H. (2010) Sirt3 protects in vitro-fertilized mouse preimplantation embryos against oxidative stress-induced p53-mediated developmental arrest. J. Clin. Invest. 120, 2817-2828
11. Guarente, L. and Picard, F. (2005) Calorie restriction-the SIR2 connection. Cell 120, 473-482
12. Finkel, T., Deng, C. X. and Mostoslavsky, R. (2009) Recent progress in the biology and physiology of sirtuins. Nature 460, 587-591
13. Schwer, B. and Verdin, E. (2008) Conserved metabolic regulatory functions of sirtuins. Cell Metab. 7, 104-112
14. Longo, V. D. and Kennedy, B. K. (2006) Sirtuins in aging and age-related disease. Cell 126, 257-268
15. Lee, I. H., Cao, L., Mostoslavsky, R., Lombard, D. B., Liu, J., Bruns, N. E., Tsokos, M., Alt, F. W. and Finkel, T. (2008) A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc. Natl. Acad. Sci. U.S.A. 105, 3374-3379
16. Onyango, P., Celic, I., McCaffery, J. M., Boeke, J. D. and Feinberg, A. P. (2002) SIRT3, a human SIR2 homologue, is an NAD-dependent deacetylase localized to mitochondria. Proc. Natl. Acad. Sci. U.S.A. 99, 13653-13658
17. Schwer, B., North, B. J., Frye, R. A., Ott, M. and Verdin, E. (2002) The human silent information regulator (Sir)2 homologue hSIRT3 is a mitochondrial nicotinamide adenine dinucleotide-dependent deacetylase. J. Cell Biol. 158, 647-657
18. Michan, S. and Sinclair, D. (2007) Sirtuins in mammals: insights into their biological function. Biochem. J. 404, 1-13
19. Kim, S. C., Sprung, R., Chen, Y., Xu, Y., Ball, H., Pei, J., Cheng, T., Kho, Y., Xiao, H., Xiao, L. et al. (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol. Cell 23, 607-618
20. Lombard, D. B., Alt, F. W., Cheng, H. L., Bunkenborg, J., Streeper, R. S., Mostoslavsky, R., Kim, J., Yancopoulos, G., Valenzuela, D., Murphy, A. et al. (2007) Mammalian Sir2 homolog SIRT3 regulates global mitochondrial lysine acetylation. Mol. Cell. Biol. 27, 8807-8814
21. Hallows, W. C., Lee, S. and Denu, J. M. (2006) Sirtuins deacetylate and activate mammalian acetyl-CoA synthetases. Proc. Natl. Acad. Sci. U.S.A. 103, 10230-10235
22. Schwer, B., Bunkenborg, J., Verdin, R. O., Andersen, J. S. and Verdin, E. (2006) Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc. Natl. Acad. Sci. U.S.A. 103, 10224-10229
23. Tao, R., Coleman, M. C., Pennington, J. D., Ozden, O., Park, S. H., Jiang, H., Kim, H. S., Flynn, C. R., Hill, S., Hayes McDonald, W. et al. (2010) Sirt3-mediated deacetylation of evolutionarily conserved lysine 122 regulates MnSOD activity in response to stress. Mol. Cell 40, 893-904
24. Palacios, O. M., Carmona, J. J., Michan, S., Chen, K. Y., Manabe, Y., Ward, 3rd, J. L., Goodyear, L. J. and Tong, Q. (2009) Diet and exercise signals regulate SIRT3 and activate AMPK and PGC-1α in skeletal muscle. Aging 1, 771-783
25. Hirschey, M. D., Shimazu, T., Goetzman, E., Jing, E., Schwer, B., Lombard, D. B., Grueter, C. A., Harris, C., Biddinger, S., Ilkayeva, O. R. et al. (2010) SIRT3 regulates mitochondrial fatty-acid oxidation by reversible enzyme deacetylation. Nature 464, 121-125
26. Someya, S., Yu, W., Hallows, W. C., Xu, J., Vann, J. M., Leeuwenburgh, C., Tanokura, M., Denu, J. M. and Prolla, T. A. (2010) Sirt3 mediates reduction of oxidative damage and prevention of age-related hearing loss under caloric restriction. Cell 143, 802-812
27. Ahn, B. H., Kim, H. S., Song, S., Lee, I. H., Liu, J., Vassilopoulos, A., Deng, C. X. and Finkel, T. (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc. Natl. Acad. Sci. U.S.A. 105, 14447-14452
28. Kim, H. S., Patel, K., Muldoon-Jacobs, K., Bisht, K. S., Aykin-Burns, N., Pennington, J. D., van der Meer, R., Nguyen, P., Savage, J., Owens, K. M. et al. (2010) SIRT3 is a mitochondria-localized tumor suppressor required for maintenance of mitochondrial integrity and metabolism during stress. Cancer Cell 17, 41-52
29. Klionsky, D. J., Abeliovich, H., Agostinis, P., Agrawal, D. K., Aliev, G., Askew, D. S., Baba, M., Baehrecke, E. H., Bahr, B. A., Ballabio, A. et al. (2008) Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 4, 151-175
30. Geeraert, C., Ratier, A., Pfisterer, S. G., Perdiz, D., Cantaloube, I., Rouault, A., Pattingre, S., Proikas-Cezanne, T., Codogno, P. and Pous, C. (2010) Starvation-induced hyperacetylation of tubulin is required for the stimulation of autophagy by nutrient deprivation. J. Biol. Chem. 285, 24184-24194
31. Tanida, I., Minematsu-Ikeguchi, N., Ueno, T. and Kominami, E. (2005) Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 1, 84-91
32. Ni, H. M., Bockus, A., Wozniak, A. L., Jones, K., Weinman, S., Yin, X. M. and Ding, W. X. (2011) Dissecting the dynamic turnover of GFP-LC3 in the autolysosome. Autophagy 7, 188-204
33. Kimura, S., Noda, T. and Yoshimori, T. (2007) Dissection of the autophagosome maturation process by a novel reporter protein, tandem fluorescent-tagged LC3. Autophagy 3, 452-460
34. Pfisterer, S. G., Mauthe, M., Codogno, P. and Proikas-Cezanne, T. (2011) Ca2+ /calmodulin-dependent kinase (CaMK) signaling via CaMKI and AMP-activated protein kinase contributes to the regulation of WIPI-1 at the onset of autophagy. Mol. Pharmacol. 80, 1066-1075
35. Chen, B., Sun, X., Zhang, Y., Zhu, X. Q. and Shen, H. M. (2012) Use of inducible Atg5 deletion and expression cell lines in study of the pro-survival function of autophagy under starvation. Biochem. Biophys. Res. Commun. 427, 11-17
36. Gerencser, A. A., Neilson, A., Choi, S. W., Edman, U., Yadava, N., Oh, R. J., Ferrick, D. A., Nicholls, D. G. and Brand, M. D. (2009) Quantitative microplate-based respirometry with correction for oxygen diffusion. Anal. Chem. 81, 6868-6878
37. Ferrick, D. A., Neilson, A. and Beeson, C. (2008) Advances in measuring cellular bioenergetics using extracellular flux. Drug Discovery Today 13, 268-274
38. Dranka, B. P., Benavides, G. A., Diers, A. R., Giordano, S., Zelickson, B. R., Reily, C., Zou, L., Chatham, J. C., Hill, B. G., Zhang, J. et al. (2011) Assessing bioenergetic function in response to oxidative stress by metabolic profiling. Free Radical Biol. Med. 51, 1621-1635
39. Giordano, S., Lee, J., Darley-Usmar, V. M. and Zhang, J. (2012) Distinct effects of rotenone, 1-methyl-4-phenylpyridinium and 6-hydroxydopamine on cellular bioenergetics and cell death. PLoS ONE 7, e44610
40. Schneider, L., Giordano, S., Zelickson, B. R., Johnson, M. S., Benavides, G. A., Ouyang, X., Fineberg, N., Darley-Usmar, V. M. and Zhang, J. (2011) Differentiation of SH-SY5Y cells to a neuronal phenotype changes cellular bioenergetics and the response to oxidative stress. Free Radical Biol. Med. 51, 2007-2017
41. Zhao, S., Xu, W., Jiang, W., Yu, W., Lin, Y., Zhang, T., Yao, J., Zhou, L., Zeng, Y., Li, H. et al. (2010) Regulation of cellular metabolism by protein lysine acetylation. Science 327, 1000-1004
42. Shi, T., Wang, F., Stieren, E. and Tong, Q. (2005) SIRT3, a mitochondrial sirtuin deacetylase, regulates mitochondrial function and thermogenesis in brown adipocytes. J. Biol. Chem. 280, 13560-13567
43. Sundaresan, N. R., Gupta, M., Kim, G., Rajamohan, S. B., Isbatan, A. and Gupta, M. P. (2009) Sirt3 blocks the cardiac hypertrophic response by augmenting Foxo3a-dependent antioxidant defense mechanisms in mice. J. Clin. Invest. 119, 2758-2771
44. Sundaresan, N. R., Samant, S. A., Pillai, V. B., Rajamohan, S. B. and Gupta, M. P. (2008) SIRT3 is a stress-responsive deacetylase in cardiomyocytes that protects cells from stress-mediated cell death by deacetylation of Ku70. Mol. Cell. Biol. 28, 6384-6401
45. Allison, S. J. and Milner, J. (2007) SIRT3 is pro-apoptotic and participates in distinct basal apoptotic pathways. Cell Cycle 6, 2669-2677
46. Bao, J., Lu, Z., Joseph, J. J., Carabenciov, D., Dimond, C. C., Pang, L., Samsel, L., McCoy, Jr, J. P., Leclerc, J., Nguyen, P. et al. (2010) Characterization of the murine SIRT3 mitochondrial localization sequence and comparison of mitochondrial enrichment and deacetylase activity of long and short SIRT3 isoforms. J. Cell. Biochem. 110, 238-247
47. Jung, C. H., Ro, S. H., Cao, J., Otto, N. M. and Kim, D. H. (2010) mTOR regulation of autophagy. FEBS Lett. 584, 1287-1295
48. Qiao, L., Hamamichi, S., Caldwell, K. A., Caldwell, G. A., Yacoubian, T. A., Wilson, S., Xie, Z. L., Speake, L. D., Parks, R., Crabtree, D. et al. (2008) Lysosomal enzyme cathepsin D protects against α-synuclein aggregation and toxicity. Mol. Brain 1, 17
49. Liang, Q., Ouyang, X., Schneider, L. and Zhang, J. (2011) Reduction of mutant huntingtin accumulation and toxicity by lysosomal cathepsins D and B in neurons. Mol. Neurodegener. 6, 37
50. Jing, E., Emanuelli, B., Hirschey, M. D., Boucher, J., Lee, K. Y., Lombard, D., Verdin, E. M. and Kahn, C. R. (2011) Sirtuin-3 (Sirt3) regulates skeletal muscle metabolism and insulin signaling via altered mitochondrial oxidation and reactive oxygen species production. Proc. Natl. Acad. Sci. U.S.A. 108, 14608-14613
51. Chen, Y., Zhang, J., Lin, Y., Lei, Q., Guan, K. L., Zhao, S. and Xiong, Y. (2011) Tumour suppressor SIRT3 deacetylates and activates manganese superoxide dismutase to scavenge ROS. EMBO Rep. 12, 534-541
52. Qiu, X., Brown, K., Hirschey, M. D., Verdin, E. and Chen, D. (2010) Calorie restriction reduces oxidative stress by SIRT3-mediated SOD2 activation. Cell Metab. 12, 662-667