The Protein Level of PGC-1α, a Key Metabolic Regulator, Is Controlled by NADH-NQO1

Molecular and Cellular Biology

Volumn 33, Issue 13, 2013, Pages 2603-2613

  Adamovich, Yaarit ^a   Shlomai, Amir ^a   Tsvetkov, Peter ^a   Umansky, Kfir B ^a   Reuven, Nina ^a   Estall, Jennifer L ^b   Spiegelman, Bruce M ^b   Shaul, Yosef ^a  

^a WEIZMANN INSTITUTE OF SCIENCE   (Israel)

^b DANA FARBER CANCER INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; PROTEASOME; PROTEIN; PROTEIN NQO1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENERGY METABOLISM; MALE; METABOLIC REGULATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTECTION; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION;

ANIMALS; CELL LINE; CYCLOHEXIMIDE; DICUMAROL; FASTING; GENE KNOCKDOWN TECHNIQUES; HEAT-SHOCK PROTEINS; HEPATOCYTES; HUMANS; LIVER; MALE; MICE; MICE, INBRED C57BL; MYOBLASTS; NAD; NAD(P)H DEHYDROGENASE (QUINONE); PROTEASOME ENDOPEPTIDASE COMPLEX; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

EID: 84880653289     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.01672-12     Document Type: Article

References (77)

1. Baar K, Wende AR, Jones TE, Marison M, Nolte LA, Chen M, Kelly DP, Holloszy JO. 2002. Adaptations of skeletal muscle to exercise: rapid increase in the transcriptional coactivator PGC-1. FASEB J. 16:1879-1886.
2. Michael LF, Wu Z, Cheatham RB, Puigserver P, Adelmant G, Lehman JJ, Kelly DP, Spiegelman BM. 2001. Restoration of insulin-sensitive glucose transporter (GLUT4) gene expression in muscle cells by the transcriptional coactivator PGC-1. Proc. Natl. Acad. Sci. U. S. A. 98:3820-3825.
3. Wu Z, Puigserver P, Andersson U, Zhang C, Adelmant G, Mootha V, Troy A, Cinti S, Lowell B, Scarpulla RC, Spiegelman BM. 1999. Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell 98:115-124.
4. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, Bauer A, Rudolph D, Schutz G, Yoon C, Puigserver P, Spiegelman B, Montminy M. 2001. CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413:179-183.
5. Yoon JC, Puigserver P, Chen G, Donovan J, Wu Z, Rhee J, Adelmant G, Stafford J, Kahn CR, Granner DK, Newgard CB, Spiegelman BM. 2001. Control of hepatic gluconeogenesis through the transcriptional coactivator PGC-1. Nature 413:131-138.
6. Estall JL, Kahn M, Cooper MP, Fisher FM, Wu MK, Laznik D, Qu L, Cohen DE, Shulman GI, Spiegelman BM. 2009. Sensitivity of lipid metabolism and insulin signaling to genetic alterations in hepatic peroxisome proliferator-activated receptor-gamma coactivator-1alpha expression. Diabetes 58:1499-1508.
7. Puigserver P, Wu Z, Park CW, Graves R, Wright M, Spiegelman BM. 1998. A cold-inducible coactivator of nuclear receptors linked to adaptive thermogenesis. Cell 92:829-839.
8. St-Pierre J, Drori S, Uldry M, Silvaggi JM, Rhee J, Jager S, Handschin C, Zheng K, Lin J, Yang W, Simon DK, Bachoo R, Spiegelman BM. 2006. Suppression of reactive oxygen species and neurodegeneration by the PGC-1 transcriptional coactivators. Cell 127:397-408.
9. Valle I, Alvarez-Barrientos A, Arza E, Lamas S, Monsalve M. 2005. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc. Res. 66:562-573.
10. Sahin E, Colla S, Liesa M, Moslehi J, Muller FL, Guo M, Cooper M, Kotton D, Fabian AJ, Walkey C, Maser RS, Tonon G, Foerster F, Xiong R, Wang YA, Shukla SA, JaskelioffM, Martin ES, Heffernan TP, Protopopov A, Ivanova E, Mahoney JE, Kost-Alimova M, Perry SR, Bronson R, Liao R, Mulligan R, Shirihai OS, Chin L, DePinho RA. 2011. Telomere dysfunction induces metabolic and mitochondrial compromise. Nature 470:359-365.
11. Finck BN, Kelly DP. 2006. PGC-1 coactivators: inducible regulators of energy metabolism in health and disease. J. Clin. Invest. 116:615-622.
12. Wenz T. 2009. PGC-1alpha activation as a therapeutic approach in mitochondrial disease. IUBMB Life 61:1051-1062.
13. Rona-Voros K, Weydt P. 2010. The role of PGC-1alpha in the pathogenesis of neurodegenerative disorders. Curr. Drug Targets 11:1262-1269.
14. Canto C, Auwerx J. 2009. PGC-1alpha, SIRT1 and AMPK, an energy sensing network that controls energy expenditure. Curr. Opin. Lipidol. 20:98-105.
15. Schilling J, Kelly DP. 2011. The PGC-1 cascade as a therapeutic target for heart failure. J. Mol. Cell. Cardiol. 51:578-583.
16. Qatanani M, Lazar MA. 2007. Mechanisms of obesity-associated insulin resistance: many choices on the menu. Genes Dev. 21:1443-1455.
17. Cao W, Daniel KW, Robidoux J, Puigserver P, Medvedev AV, Bai X, Floering LM, Spiegelman BM, Collins S. 2004. p38 mitogen-activated protein kinase is the central regulator of cyclic AMP-dependent transcription of the brown fat uncoupling protein 1 gene. Mol. Cell. Biol. 24:3057-3067.
18. Handschin C, Rhee J, Lin J, Tarr PT, Spiegelman BM. 2003. An autoregulatory loop controls peroxisome proliferator-activated receptor gamma coactivator 1alpha expression in muscle. Proc. Natl. Acad. Sci. U. S. A. 100:7111-7116.
19. Jager S, Handschin C, St-Pierre J, Spiegelman BM. 2007. AMP-activated protein kinase (AMPK) action in skeletal muscle via direct phosphorylation of PGC-1alpha. Proc. Natl. Acad. Sci. U. S. A. 104:12017-12022.
20. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P. 2005. Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 434:113-118.
21. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, Elliott PJ, Puigserver P, Auwerx J. 2009. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458: 1056-1060.
22. Olson BL, Hock MB, Ekholm-Reed S, Wohlschlegel JA, Dev KK, Kralli A, Reed SI. 2008. SCFCdc4 acts antagonistically to the PGC-1alpha transcriptional coactivator by targeting it for ubiquitin-mediated proteolysis. Genes Dev. 22:252-264.
23. Anderson RM, Barger JL, Edwards MG, Braun KH, O'Connor CE, Prolla TA, Weindruch R. 2008. Dynamic regulation of PGC-1alpha localization and turnover implicates mitochondrial adaptation in calorie restriction and the stress response. Aging Cell 7:101-111.
24. Trausch-Azar J, Leone TC, Kelly DP, Schwartz AL. 2010. Ubiquitin proteasome dependent degradation of the transcriptional coactivator PGC-1alpha via the N-terminal pathway. J. Biol. Chem. 285:40192-40200.
25. Sano M, Tokudome S, Shimizu N, Yoshikawa N, Ogawa C, Shirakawa K, Endo J, Katayama T, Yuasa S, Ieda M, Makino S, Hattori F, Tanaka H, Fukuda K. 2007. Intramolecular control of protein stability, subnuclear compartmentalization, and coactivator function of peroxisome proliferator-activated receptor gamma coactivator 1alpha. J. Biol. Chem. 282:25970-25980.
26. Wei P, Pan D, Mao C, Wang YX. 2012. RNF34 is a cold-regulated E3 ubiquitin ligase for PGC-1alpha and modulates brown fat cell metabolism. Mol. Cell. Biol. 32:266-275.
27. Asher G, Reuven N, Shaul Y. 2006. 20S proteasomes and protein degradation "by default." Bioessays 28:844-849.
28. Shaul Y, Tsvetkov P, Reuven N. 2010. IDPs and protein degradation in the cell, p 3-36. In Uversky VN, Longhi S (ed), Instrumental analysis of intrinsically disordered proteins: assessing structure and conformation. John Wiley & Sons, Inc, Hoboken, NJ.
29. Tompa P. 2005. The interplay between structure and function in intrinsically unstructured proteins. FEBS Lett. 579:3346-3354.
30. Uversky VN, Dunker AK. 2010. Understanding protein non-folding. Biochim. Biophys. Acta 1804:1231-1264.
31. Babu MM, van der Lee R, de Groot NS, Gsponer J. 2011. Intrinsically disordered proteins: regulation and disease. Curr. Opin. Struct. Biol. 21:432-440.
32. Scarpulla RC. 2011. Metabolic control of mitochondrial biogenesis through the PGC-1 family regulatory network. Biochim. Biophys. Acta 1813:1269-1278.
33. Liu C, Lin JD. 2011. PGC-1 coactivators in the control of energy metabolism. Acta Biochim. Biophys. Sin. (Shanghai) 43:248-257.
34. Sugden MC, Caton PW, Holness MJ. 2010. PPAR control: it's SIRTainly as easy as PGC. J. Endocrinol. 204:93-104.
35. Hwang JH, Kim DW, Jo EJ, Kim YK, Jo YS, Park JH, Yoo SK, Park MK, Kwak TH, Kho YL, Han J, Choi HS, Lee SH, Kim JM, Lee I, Kyung T, Jang C, Chung J, Kweon GR, Shong M. 2009. Pharmacological stimulation of NADH oxidation ameliorates obesity and related phenotypes in mice. Diabetes 58:965-974.
36. Gaikwad A, Long DJ, II, Stringer JL, Jaiswal AK. 2001. In vivo role of NAD(P)H:quinone oxidoreductase 1 (NQO1) in the regulation of intracellular redox state and accumulation of abdominal adipose tissue. J. Biol. Chem. 276:22559-22564.
37. Lee JS, Park AH, Lee SH, Kim JH, Yang SJ, Yeom YI, Kwak TH, Lee D, Lee SJ, Lee CH, Kim JM, Kim D. 2012. Beta-lapachone, a modulator of NAD metabolism, prevents health declines in aged mice. PLoS One 7:e47122. doi:10.1371/journal.pone.0047122.
38. Ross D. 2004. Quinone reductases multitasking in the metabolic world. Drug Metab. Rev. 36:639-654.
39. Asher G, Tsvetkov P, Kahana C, Shaul Y. 2005. A mechanism of ubiquitin-independent proteasomal degradation of the tumor suppressors p53 and p73. Genes Dev. 19:316-321.
40. Moscovitz O, Tsvetkov P, Hazan N, Michaelevski I, Keisar H, Ben-Nissan G, Shaul Y, Sharon M. 2012. A mutually inhibitory feedback loop between the 20S proteasome and its regulator, NQO1. Mol. Cell 47:76-86.
41. Hershkovitz Rokah O, Shpilberg O, Granot G. 2010. NAD(P)H quinone oxidoreductase protects TAp63gamma from proteasomal degradation and regulates TAp63gamma-dependent growth arrest. PLoS One 5:e11401. doi:10.1371/journal.pone.0011401.
42. Garate M, Wong RP, Campos EI, Wang Y, Li G. 2008. NAD(P)H quinone oxidoreductase 1 inhibits the proteasomal degradation of the tumour suppressor p33(ING1b). EMBO Rep. 9:576-581.
43. Asher G, Bercovich Z, Tsvetkov P, Shaul Y, Kahana C. 2005. 20S proteasomal degradation of ornithine decarboxylase is regulated byNQO1. Mol. Cell 17:645-655.
44. Patrick BA, Gong X, Jaiswal AK. 2011. Disruption of NAD(P)H:quinone oxidoreductase 1 gene in mice leads to 20S proteasomal degradation of p63 resulting in thinning of epithelium and chemical-induced skin cancer. Oncogene 30:1098-1107.
45. Adler J, Reuven N, Kahana C, Shaul Y. 2010. c-Fos proteasomal degradation is activated by a default mechanism, and its regulation by NAD-(P)H:quinone oxidoreductase 1 determines c-Fos serum response kinetics. Mol. Cell. Biol. 30:3767-3778.
46. Patrick BA, Jaiswal AK. 2012. Stress-induced NQO1 controls stability of C/EBPalpha against 20S proteasomal degradation to regulate p63 expression with implications in protection against chemical-induced skin cancer. Oncogene 31:4362-4371.
47. Sollner S, Schober M, Wagner A, Prem A, Lorkova L, Palfey BA, Groll M, Macheroux P. 2009. Quinone reductase acts as a redox switch of the 20S yeast proteasome. EMBO Rep. 10:65-70.
48. Levy D, Adamovich Y, Reuven N, Shaul Y. 2007. The Yes-associated protein 1 stabilizes p73 by preventing Itch-mediated ubiquitination of p73. Cell Death Differ. 14:743-751.
49. Lin J, Wu PH, Tarr PT, Lindenberg KS, St-Pierre J, Zhang CY, Mootha VK, Jager S, Vianna CR, Reznick RM, Cui L, Manieri M, Donovan MX, Wu Z, Cooper MP, Fan MC, Rohas LM, Zavacki AM, Cinti S, Shulman GI, Lowell BB, Krainc D, Spiegelman BM. 2004. Defects in adaptive energy metabolism with CNS-linked hyperactivity in PGC-1alpha null mice. Cell 119:121-135.
50. Zammit PS, Relaix F, Nagata Y, Ruiz AP, Collins CA, Partridge TA, Beauchamp JR. 2006. Pax7 and myogenic progression in skeletal muscle satellite cells. J. Cell Sci. 119:1824-1832.
51. Luo J, Deng ZL, Luo X, Tang N, Song WX, Chen J, SharffKA, Luu HH, Haydon RC, Kinzler KW, Vogelstein B, He TC. 2007. A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat. Protoc. 2:1236-1247.
52. Fulco M, Cen Y, Zhao P, Hoffman EP, McBurney MW, Sauve AA, Sartorelli V. 2008. Glucose restriction inhibits skeletal myoblast differentiation by activating SIRT1 through AMPK-mediated regulation of Nampt. Dev. Cell 14:661-673.
53. Krishna TS, Kong XP, Gary S, Burgers PM, Kuriyan J. 1994. Crystal structure of the eukaryotic DNA polymerase processivity factor PCNA. Cell 79:1233-1243.
54. Tompa P. 2002. Intrinsically unstructured proteins. Trends Biochem. Sci. 27:527-533.
55. Devarakonda S, Gupta K, Chalmers MJ, Hunt JF, Griffin PR, Van Duyne GD, Spiegelman BM. 2011. Disorder-to-order transition underlies the structural basis for the assembly of a transcriptionally active PGC- 1alpha/ERRgamma complex. Proc. Natl. Acad. Sci. U. S. A. 108:18678-18683.
56. Liu CW, Corboy MJ, DeMartino GN, Thomas PJ. 2003. Endoproteolytic activity of the proteasome. Science 299:408-411.
57. Tsvetkov P, Asher G, Paz A, Reuven N, Sussman JL, Silman I, Shaul Y. 2008. Operational definition of intrinsically unstructured protein sequences based on susceptibility to the 20S proteasome. Proteins 70:1357-1366.
58. Tsvetkov P, Shaul Y. 2012. Determination of IUP based on susceptibility for degradation by default. Methods Mol. Biol. 895:3-18.
59. Tsvetkov P, Reuven N, Shaul Y. 2009. The nanny model for IDPs. Nat. Chem. Biol. 5:778-781.
60. Uversky VN, Oldfield CJ, Dunker AK. 2008. Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu. Rev. Biophys. 37:215-246.
61. Asher G, Dym O, Tsvetkov P, Adler J, Shaul Y. 2006. The crystal structure of NAD(P)H quinone oxidoreductase 1 in complex with its potent inhibitor dicoumarol. Biochemistry 45:6372-6378.
62. Ma Q, Cui K, Xiao F, Lu AY, Yang CS. 1992. Identification of a glycine-rich sequence as an NAD(P)H-binding site and tyrosine 128 as a dicumarol-binding site in rat liver NAD(P)H:quinone oxidoreductase by site-directed mutagenesis. J. Biol. Chem. 267:22298-22304.
63. Fulco M, Schiltz RL, Iezzi S, King MT, Zhao P, Kashiwaya Y, Hoffman E, Veech RL, Sartorelli V. 2003. Sir2 regulates skeletal muscle differentiation as a potential sensor of the redox state. Mol. Cell 12:51-62.
64. Dinkova-Kostova AT, Talalay P. 2010. NAD(P)H:quinone acceptor oxidoreductase 1 (NQO1), a multifunctional antioxidant enzyme and exceptionally versatile cytoprotector. Arch. Biochem. Biophys. 501:116-123.
65. Bitterman KJ, Anderson RM, Cohen HY, Latorre-Esteves M, Sinclair DA. 2002. Inhibition of silencing and accelerated aging by nicotinamide, a putative negative regulator of yeast sir2 and human SIRT1. J. Biol. Chem. 277:45099-45107.
66. Daitoku H, Yamagata K, Matsuzaki H, Hatta M, Fukamizu A. 2003. Regulation of PGC-1 promoter activity by protein kinase B and the forkhead transcription factor FKHR. Diabetes 52:642-649.
67. Louet JF, Hayhurst G, Gonzalez FJ, Girard J, Decaux JF. 2002. The coactivator PGC-1 is involved in the regulation of the liver carnitine palmitoyltransferase I gene expression by cAMP in combination with HNF4 alpha and cAMP-response element-binding protein (CREB). J. Biol. Chem. 277:37991-38000.
68. Cooper MP, Qu L, Rohas LM, Lin J, Yang W, Erdjument-Bromage H, Tempst P, Spiegelman BM. 2006. Defects in energy homeostasis in Leigh syndrome French Canadian variant through PGC-1alpha/LRP130 complex. Genes Dev. 20:2996-3009.
69. Williamson DH, Lund P, Krebs HA. 1967. The redox state of free nicotinamide- adenine dinucleotide in the cytoplasm and mitochondria of rat liver. Biochem. J. 103:514-527.
70. Puigserver P, Rhee J, Donovan J, Walkey CJ, Yoon JC, Oriente F, Kitamura Y, Altomonte J, Dong H, Accili D, Spiegelman BM. 2003. Insulin-regulated hepatic gluconeogenesis through FOXO1-PGC-1alpha interaction. Nature 423:550-555.
71. Li X, Monks B, Ge Q, Birnbaum MJ. 2007. Akt/PKB regulates hepatic metabolism by directly inhibiting PGC-1alpha transcription coactivator. Nature 447:1012-1016.
72. Ross D, Siegel D. 2004. NAD(P)H:quinone oxidoreductase 1 (NQO1, DT-diaphorase), functions and pharmacogenetics. Methods Enzymol. 382:115-144.
73. Gsponer J, Futschik ME, Teichmann SA, Babu MM. 2008. Tight regulation of unstructured proteins: from transcript synthesis to protein degradation. Science 322:1365-1368.
74. Rosenfeld N, Alon U. 2003. Response delays and the structure of ranscription networks. J. Mol. Biol. 329:645-654.
75. Belle A, Tanay A, Bitincka L, Shamir R, O'Shea EK. 2006. Quantification of protein half-lives in the budding yeast proteome. Proc. Natl. Acad. Sci. U. S. A. 103:13004-13009.
76. Tsvetkov P, Reuven N, Prives C, Shaul Y. 2009. The susceptibility of the p53 unstructured N-terminus to 20S proteasomal degradation programs stress response. J. Biol. Chem. 284:26234-26242.
77. Kim SY, Jeoung NH, Oh CJ, Choi YK, Lee HJ, Kim HJ, Kim JY, Hwang JH, Tadi S, Yim YH, Lee KU, Park KG, Huh S, Min KN, Jeong KH, Park MG, Kwak TH, Kweon GR, Inukai K, Shong M, Lee IK. 2009. Activation of NAD(P)H:quinone oxidoreductase 1 prevents arterial restenosis by suppressing vascular smooth muscle cell proliferation. Circ. Res. 104:842-850.