SUMO-specific protease 1 regulates mitochondrial biogenesis through PGC-1α

Journal of Biological Chemistry

Volumn 287, Issue 53, 2012, Pages 44464-44470

  Cai, Rong ^a   Yu, Tingting ^a   Huang, Chao ^a,e   Xia, Xuefeng ^c   Liu, Xiaobing ^a,e   Gu, Jianmin ^b   Xue, Song ^b   Yeh, Edward T H ^d,e   Cheng, Jinke ^a  

^a SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^b SHANGHAI JIAO TONG UNIVERSITY SCHOOL OF MEDICINE   (China)

^c HOUSTON METHODIST RESEARCH INSTITUTE   (United States)

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

^e TEXAS HEART INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELLULAR ENVIRONMENT; COACTIVATORS; MASTER REGULATORS; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL GENES; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR; SMALL UBIQUITIN-LIKE MODIFIERS; SUMOYLATION; TRANSCRIPTION ACTIVITY;

CYTOLOGY; TRANSCRIPTION;

PHYSIOLOGICAL MODELS;

BRINASE; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; SUMO SPECIFIC PROTEASE 1; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL FUNCTION; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; ENZYME SPECIFICITY; GENE OVEREXPRESSION; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL DYNAMICS; MITOCHONDRIAL GENE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SUMOYLATION; TRANSCRIPTION INITIATION; WILD TYPE;

ANIMALS; ENDOPEPTIDASES; HEK293 CELLS; HUMANS; MICE; MICE, KNOCKOUT; MITOCHONDRIA; MITOCHONDRIAL TURNOVER; SUMOYLATION; TRANS-ACTIVATORS;

MAMMALIA;

EID: 84871821904     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.422626     Document Type: Article

References (35)

1. Michel, S., Wanet, A., De Pauw, A., Rommelaere, G., Arnould, T., and Renard, P. (2012) Crosstalk between mitochondrial (dys)function and mitochondrial abundance. J. Cell Physiol. 227, 2297-2310
2. Hock, M. B., and Kralli, A. (2009) Transcriptional control of mitochondrial biogenesis and function. Annu. Rev. Physiol. 71, 177-203
3. Rohas, L. M., St-Pierre, J., Uldry, M., Jäger, S., Handschin, C., and Spiegelman, B. M. (2007) A fundamental system of cellular energy homeostasis regulated by PGC-1α. Proc. Natl. Acad. Sci. U.S.A. 104, 7933-7938 (Pubitemid 47185854)
4. Wallace, D. C., and Fan, W. (2009) The pathophysiology of mitochondrial disease as modeled in the mouse. Genes Dev. 23, 1714-1736
5. Lin, J. D. (2009) Minireview: the PGC-1 coactivator networks: chromatin-remodeling and mitochondrial energy metabolism. Mol. Endocrinol. 23, 2-10
6. Wu, Z., Puigserver, P., Andersson, U., Zhang, C., Adelmant, G., Mootha, V., Troy, A., Cinti, S., Lowell, B., Scarpulla, R. C., and Spiegelman, B. M. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98, 115-124 (Pubitemid 29331201)
7. Vega, R. B., Huss, J. M., and Kelly, D. P. (2000) The coactivator PGC-1 cooperates with peroxisome proliferator-activated receptor α in transcriptional control of nuclear genes encoding mitochondrial fatty acid oxidation enzymes. Mol. Cell. Biol. 20, 1868-1876 (Pubitemid 30100203)
8. Lehman, J. J., Barger, P. M., Kovacs, A., Saffitz, J. E., Medeiros, D. M., and Kelly, D. P. (2000) Peroxisome proliferator-activated receptor γ coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106, 847-856
9. Puigserver, P., and Spiegelman, B. M. (2003) Peroxisome proliferator-activated receptor-γ coactivator 1 alpha (PGC-1α): transcriptional coactivator and metabolic regulator. Endocr. Rev. 24, 78-90 (Pubitemid 36223280)
10. Handschin, C., Choi, C. S., Chin, S., Kim, S., Kawamori, D., Kurpad, A. J., Neubauer, N., Hu, J., Mootha, V. K., Kim, Y. B., Kulkarni, R. N., Shulman, G. I., and Spiegelman, B. M. (2007) Abnormal glucose homeostasis in skeletal muscle-specific PGC-1α knockout mice reveals skeletal muscle-pancreatic β cell crosstalk. J. Clin. Invest. 117, 3463-3474 (Pubitemid 350097002)
11. Lin, J., Wu, P. H., Tarr, P. T., Lindenberg, K. S., St-Pierre, J., Zhang, C. Y., Mootha, V. K., Jäger, S., Vianna, C. R., Reznick, R. M., Cui, L., Manieri, M., Donovan, M. X., Wu, Z., Cooper, M. P., Fan, M. C., Rohas, L. M., Zavacki, A. M., Cinti, S., Shulman, G. I., Lowell, B. B., Krainc, D., and Spiegelman, B. M. (2004) Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1α null mice. Cell 119, 121-135 (Pubitemid 39349325)
12. Feige, J. N., and Auwerx, J. (2007) Transcriptional coregulators in the control of energy homeostasis. Trends Cell Biol. 17, 292-301 (Pubitemid 46829846)
13. Mootha, V. K., Handschin, C., Arlow, D., Xie, X., St Pierre, J., Sihag, S., Yang, W., Altshuler, D., Puigserver, P., Patterson, N., Willy, P. J., Schulman, I. G., Heyman, R. A., Lander, E. S., and Spiegelman, B. M. (2004) Erralpha and Gabpa/b specify PGC-1α-dependent oxidative phosphorylation gene expression that is altered in diabetic muscle. Proc. Natl. Acad. Sci. U.S.A. 101, 6570-6575 (Pubitemid 38586015)
14. Schreiber, S. N., Emter, R., Hock, M. B., Knutti, D., Cardenas, J., Podvinec, M., Oakeley, E. J., and Kralli, A. (2004) The estrogen-related receptor α (ERRα) functions in PPARγ coactivator 1α (PGC-1α)-induced mitochondrial biogenesis. Proc. Natl. Acad. Sci. U.S.A. 101, 6472-6477 (Pubitemid 38585998)
15. Arany, Z. (2008) PGC-1 coactivators and skeletal muscle adaptations in health and disease. Curr. Opin. Genet. Dev. 18, 426-434
16. Sakai, M., Matsumoto, M., Tujimura, T., Yongheng, C., Noguchi, T., Inagaki, K., Inoue, H., Hosooka, T., Takazawa, K., Kido, Y., Yasuda, K., Hiramatsu, R., Matsuki, Y., and Kasuga, M. (2012) CITED2 links hormonal signaling to PGC-1α acetylation in the regulation of gluconeogenesis. Nat. Med. 18, 612-617
17. Iwabu, M., Yamauchi, T., Okada-Iwabu, M., Sato, K., Nakagawa, T., Funata, M., Yamaguchi, M., Namiki, S., Nakayama, R., Tabata, M., Ogata, H., Kubota, N., Takamoto, I., Hayashi, Y. K., Yamauchi, N., Waki, H., Fukayama, M., Nishino, I., Tokuyama, K., Ueki, K., Oike, Y., Ishii, S., Hirose, K., Shimizu, T., Touhara, K., and Kadowaki, T. (2010) Adiponectin and AdipoR1 regulate PGC-1α and mitochondria by Ca(2+) and AMPK/SIRT1. Nature 464, 1313-1319
18. Cantó, C., Jiang, L. Q., Deshmukh, A. S., Mataki, C., Coste, A., Lagouge, M., Zierath, J. R., and Auwerx, J. (2010) Interdependence of AMPK and SIRT1 for metabolic adaptation to fasting and exercise in skeletal muscle. Cell metabolism 11, 213-219
19. Kelly, T. J., Lerin, C., Haas, W., Gygi, S. P., and Puigserver, P. (2009) GCN5- mediated transcriptional control of the metabolic coactivator PGC-1β through lysine acetylation. J. Biol. Chem. 284, 19945-19952
20. Jäger, S., Handschin, C., St-Pierre, J., and Spiegelman, B. M. (2007) AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1α. Proc. Natl. Acad. Sci. U.S.A. 104, 12017-12022 (Pubitemid 47185622)
21. Lustig, Y., Ruas, J. L., Estall, J. L., Lo, J. C., Devarakonda, S., Laznik, D., Choi, J. H., Ono, H., Olsen, J. V., and Spiegelman, B. M. (2011) Separation of the gluconeogenic and mitochondrial functions of PGC-1{α} through S6 kinase. Genes Dev. 25, 1232-1244
22. Yeh, E. T. (2009) SUMOylation and De-SUMOylation: wrestling with life's processes. J. Biol. Chem. 284, 8223-8227
23. Hay, R. T. (2005) SUMO: a history of modification. Mol. Cell 18, 1-12
24. Gill, G. (2005) Something aboutSUMOinhibits transcription. Curr. Opin. Genet. Dev. 15, 536-541
25. Hay, R. T. (2007) SUMO-specific proteases: a twist in the tail. Trends Cell Biol. 17, 370-376
26. Cheng, J., Kang, X., Zhang, S., and Yeh, E. T. (2007) SUMO-specific protease 1 is essential for stabilization of HIF1α during hypoxia. Cell 131, 584-595 (Pubitemid 350007694)
27. Kang, X., Qi, Y., Zuo, Y., Wang, Q., Zou, Y., Schwartz, R. J., Cheng, J., and Yeh, E. T. (2010) SUMO-specific protease 2 is essential for suppression of polycomb group protein-mediated gene silencing during embryonic development. Mol. Cell 38, 191-201
28. Van Nguyen, T., Angkasekwinai, P., Dou, H., Lin, F. M., Lu, L. S., Cheng, J., Chin, Y. E., Dong, C., and Yeh, E. T. (2012) SUMO-specific protease 1 is critical for early lymphoid development through regulation of STAT5 activation. Mol. Cell 45, 210-221
29. Rytinki, M. M., and Palvimo, J. J. (2009) SUMOylation attenuates the function of PGC-1α. J. Biol. Chem. 284, 26184-26193
30. Lai, L., Leone, T. C., Zechner, C., Schaeffer, P. J., Kelly, S. M., Flanagan, D. P., Medeiros, D. M., Kovacs, A., and Kelly, D. P. (2008) Transcriptional coactivators PGC-1α and PGC-1β control overlapping programs required for perinatal maturation of the heart. Genes Dev. 22, 1948-1961 (Pubitemid 352008642)
31. Arany, Z., Lebrasseur, N., Morris, C., Smith, E., Yang, W., Ma, Y., Chin, S., and Spiegelman, B. M. (2007) The transcriptional coactivator PGC-1β drives the formation of oxidative type IIX fibers in skeletal muscle. Cell Metab. 5, 35-46 (Pubitemid 44939399)
32. Vianna, C. R., Huntgeburth, M., Coppari, R., Choi, C. S., Lin, J., Krauss, S., Barbatelli, G., Tzameli, I., Kim, Y. B., Cinti, S., Shulman, G. I., Spiegelman, B. M., and Lowell, B. B. (2006) Hypomorphic mutation of PGC-1β causes mitochondrial dysfunction and liver insulin resistance. Cell Metab. 4, 453-464 (Pubitemid 44817352)
33. Lin, J., Yang, R., Tarr, P. T., Wu, P. H., Handschin, C., Li, S., Yang, W., Pei, L., Uldry, M., Tontonoz, P., Newgard, C. B., and Spiegelman, B. M. (2005) Hyperlipidemic effects of dietary saturated fats mediated through PGC-1beta coactivation of SREBP. Cell 120, 261-273 (Pubitemid 40174768)
34. Zunino, R., Schauss, A., Rippstein, P., Andrade-Navarro, M., and McBride, H. M. (2007) The SUMO protease SENP5 is required to maintain mitochondrial morphology and function. J. Cell Sci. 120, 1178-1188 (Pubitemid 46711836)
35. Zunino, R., Braschi, E., Xu, L., and McBride, H. M. (2009) Translocation of SenP5 from the nucleoli to the mitochondria modulates DRP1-dependent fission during mitosis. J. Biol. Chem. 284, 17783-17795