Role of transcription factor acetylation in the regulation of metabolic homeostasis

Joo-Man Park, Seong-Ho Jo, Mi-Young Kim, Tae-Hyun Kim, Yong-Ho Ahn

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Protein Cell ›› 2015, Vol. 6 ›› Issue (11) : 804-813. DOI: 10.1007/s13238-015-0204-y
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Role of transcription factor acetylation in the regulation of metabolic homeostasis

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Abstract

Post-translational modifications (PTMs) of transcription factors play a crucial role in regulating metabolic homeostasis. These modifications include phosphorylation, methylation, acetylation, ubiquitination, SUMOylation, and O-GlcNAcylation. Recent studies have shed light on the importance of lysine acetylation at nonhistone proteins including transcription factors. Acetylation of transcription factors affects subcellular distribution, DNA affinity, stability, transcriptional activity, and current investigations are aiming to further expand our understanding of the role of lysine acetylation of transcription factors. In this review, we summarize recent studies that provide new insights into the role of protein lysine-acetylation in the transcriptional regulation of metabolic homeostasis.

Keywords

metabolic homeostasis / transcription factor / post-translational modification / type 2 diabetes mellitus

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Joo-Man Park, Seong-Ho Jo, Mi-Young Kim, Tae-Hyun Kim, Yong-Ho Ahn. Role of transcription factor acetylation in the regulation of metabolic homeostasis. Protein Cell, 2015, 6(11): 804‒813 https://doi.org/10.1007/s13238-015-0204-y

References

[1]
Abdou HS, Atlas E, Hache RJ(2011) Liver-enriched inhibitory protein (LIP) actively inhibits preadipocyte differentiation through histone deacetylase 1 (HDAC1). J Biol Chem 286: 21488−21499
CrossRef Google scholar
[2]
Allis CD, Berger SL, Cote J, Dent S, Jenuwien T, Kouzarides T, Pillus L, Reinberg D, Shi Y, Shiekhattar R, Shilatifard A, Workman J, Zhang Y (2007) New nomenclature for chromatin-modifying enzymes. Cell 131: 633−636
CrossRef Google scholar
[3]
Altarejos JY, Montminy M (2011) CREB and the CRTC co-activators: sensors for hormonal and metabolic signals. Nat Rev Mol Cell Biol 12: 141−151
CrossRef Google scholar
[4]
Banerjee A, Meyer K, Mazumdar B, Ray RB, Ray R (2010) Hepatitis C virus differentially modulates activation of forkhead transcription factors and insulin-induced metabolic gene expression. J Virol 84: 5936−5946
CrossRef Google scholar
[5]
Banks AS, Kon N, Knight C, Matsumoto M, Gutierrez-Juarez R, Rossetti L, Gu W, Accili D (2008) SirT1 gain of function increases energy efficiency and prevents diabetes in mice. Cell Metab 8: 333−341
CrossRef Google scholar
[6]
Bedford DC, Kasper LH, Wang R, Chang Y, Green DR, Brindle PK(2011) Disrupting the CH1 domain structure in the acetyltransferases CBP and p300 results in lean mice with increased metabolic control. Cell Metab 14: 219−230
CrossRef Google scholar
[7]
Bricambert J, Miranda J, Benhamed F, Girard J, Postic C, Dentin R (2010) Salt-inducible kinase 2 links transcriptional coactivator p300 phosphorylation to the prevention of ChREBP-dependent hepatic steatosis in mice. J Clin Invest 120: 4316−4331
CrossRef Google scholar
[8]
Calnan DR, Brunet A (2008) The FoxO code. Oncogene 27: 2276−2288
CrossRef Google scholar
[9]
Carrozza MJ, Utley RT, Workman JL, Cote J (2003) The diverse functions of histone acetyltransferase complexes. Trends Genet 19: 321−329
CrossRef Google scholar
[10]
Cesena TI, Cardinaux JR, Kwok R, Schwartz J (2007) CCAAT/ enhancer-binding protein (C/EBP) beta is acetylated at multiple lysines: acetylation of C/EBPbeta at lysine 39 modulates its ability to activate transcription. J Biol Chem 282: 956−967
CrossRef Google scholar
[11]
Cesena TI, Cui TX, Subramanian L, Fulton CT, Iniguez-Lluhi JA, Kwok RP, Schwartz J (2008) Acetylation and deacetylation regulate CCAAT/enhancer binding protein beta at K39 in mediating gene transcription. Mol Cell Endocrinol 289: 94−101
CrossRef Google scholar
[12]
Chalkiadaki A, Guarente L (2012) High-fat diet triggers inflammationinduced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab 16: 180−188
CrossRef Google scholar
[13]
Chang HC, Guarente L (2014) SIRT1 and other sirtuins in metabolism. Trends Endocrinol Metab 25: 138−145
CrossRef Google scholar
[14]
Chen S, Feng B, George B, Chakrabarti R, Chen M, Chakrabarti S (2010) Transcriptional coactivator p300 regulates glucose-induced gene expression in endothelial cells. Am J Physiol Endocrinol Metab 298: E127−137
CrossRef Google scholar
[15]
Chen L, Magliano DJ, Zimmet PZ (2012) The worldwide epidemiology of type 2 diabetes mellitus−present and future perspectives. Nat Rev Endocrinol 8: 228−236
CrossRef Google scholar
[16]
Choudhary C, Weinert BT, Nishida Y, Verdin E, Mann M (2014) The growing landscape of lysine acetylation links metabolism and cell signalling. Nat Rev Mol Cell Biol 15: 536−550
CrossRef Google scholar
[17]
Eijkelenboom A, Burgering BM(2013) FOXOs: signalling integrators for homeostasis maintenance. Nat Rev Mol Cell Biol 14: 83−97
CrossRef Google scholar
[18]
Erion DM, Ignatova ID, Yonemitsu S, Nagai Y, Chatterjee P, Weismann D, Hsiao JJ, Zhang D, Iwasaki T, Stark R, Flannery C, Kahn M, Carmean CM, Yu XX, Murray SF, Bhanot S, Monia BP, Cline GW, Samuel VT, Shulman GI(2009) Prevention of hepatic steatosis and hepatic insulin resistance by knockdown of cAMP response element-binding protein. Cell Metab 10: 499−506
CrossRef Google scholar
[19]
Filhoulaud G, Guilmeau S, Dentin R, Girard J, Postic C (2013) Novel insights into ChREBP regulation and function. Trends Endocrinol Metab 24: 257−268
CrossRef Google scholar
[20]
Francis GA, Fayard E, Picard F, Auwerx J (2003) Nuclear receptors and the control of metabolism. Annu Rev Physiol 65: 261−311
CrossRef Google scholar
[21]
Frescas D, Valenti L, Accili D (2005) Nuclear trapping of the forkhead transcription factor FoxO1 via Sirt-dependent deacetylation promotes expression of glucogenetic genes. J Biol Chem 280: 20589−20595
CrossRef Google scholar
[22]
Gabay O, Zaal KJ, Sanchez C, Dvir-Ginzberg M, Gagarina V, Song Y, He XH, McBurney MW (2013) Sirt1-deficient mice exhibit an altered cartilage phenotype. Joint Bone Spine 80: 613−620
CrossRef Google scholar
[23]
Ganjam GK, Dimova EY, Unterman TG, Kietzmann T (2009) FoxO1 and HNF-4 are involved in regulation of hepatic glucokinase gene expression by resveratrol. J Biol Chem 284: 30783−30797
CrossRef Google scholar
[24]
Giandomenico V, Simonsson M, Gronroos E, Ericsson J (2003) Coactivator-dependent acetylation stabilizes members of the SREBP family of transcription factors. Mol Cell Biol 23: 2587−2599
CrossRef Google scholar
[25]
Glozak MA, Sengupta N, Zhang X, Seto E (2005) Acetylation and deacetylation of non-histone proteins. Gene 363: 15−23
CrossRef Google scholar
[26]
Gorrini C, Squatrito M, Luise C, Syed N, Perna D, Wark L, Martinato F, Sardella D, Verrecchia A, Bennett S, Confalonieri S, Cesaroni M, Marchesi F, Gasco M, Scanziani E, Capra M, Mai S, Nuciforo P, Crook T, Lough J, Amati B (2007) Tip60 is a haplo-insufficient tumour suppressor required for an oncogene-induced DNA damage response. Nature 448: 1063−1067
CrossRef Google scholar
[27]
Gross DN, Wan M, Birnbaum MJ (2009) The role of FOXO in the regulation of metabolism. Curr Diab Rep 9: 208−214
CrossRef Google scholar
[28]
Guan KL, Xiong Y (2011) Regulation of intermediary metabolism by protein acetylation. Trends Biochem Sci 36: 108−116
CrossRef Google scholar
[29]
Guinez C, Filhoulaud G, Rayah-Benhamed F, Marmier S, Dubuquoy C, Dentin R, Moldes M, Burnol AF, Yang X, Lefebvre T, Girard J, Postic C (2011) O-GlcNAcylation increases ChREBP protein content and transcriptional activity in the liver. Diabetes 60: 1399−1413
CrossRef Google scholar
[30]
Haigis MC, Sinclair DA (2010) Mammalian sirtuins: biological insights and disease relevance. Annu Rev Pathol 5: 253−295
CrossRef Google scholar
[31]
He L, Naik K, Meng S, Cao J, Sidhaye AR, Ma A, Radovick S, Wondisford FE(2012) Transcriptional co-activator p300 maintains basal hepatic gluconeogenesis. J Biol Chem 287: 32069−32077
CrossRef Google scholar
[32]
He L, Cao J, Meng S, Ma A, Radovick S, Wondisford FE(2013) Activation of basal gluconeogenesis by coactivator p300 maintains hepatic glycogen storage. Mol Endocrinol 27: 1322−1332
CrossRef Google scholar
[33]
Howell JJ, Stoffel M (2009) Nuclear export-independent inhibition of Foxa2 by insulin. J Biol Chem 284: 24816−24824
CrossRef Google scholar
[34]
Huang H, Tindall DJ(2007) Dynamic FoxO transcription factors. J Cell Sci 120: 2479−2487
CrossRef Google scholar
[35]
Imai S, Guarente L (2014) NAD+ and sirtuins in aging and disease. Trends Cell Biol 24: 464−471
CrossRef Google scholar
[36]
Jeon TI, Osborne TF (2012) SREBPs: metabolic integrators in physiology and metabolism. Trends Endocrinol Metab 23: 65−72
CrossRef Google scholar
[37]
Jing E, Gesta S, Kahn CR(2007) SIRT2 regulates adipocyte differentiation through FoxO1 acetylation/deacetylation. Cell Metab 6: 105−114
CrossRef Google scholar
[38]
Kahn SE, Hull RL, Utzschneider KM(2006) Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840−846
CrossRef Google scholar
[39]
Khan O, La Thangue NB (2012) HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 90: 85−94
CrossRef Google scholar
[40]
Kim SY, Kim HI, Kim TH, Im SS, Park SK, Lee IK, Kim KS, Ahn YH(2004) SREBP-1c mediates the insulin-dependent hepatic glucokinase expression. J Biol Chem 279: 30823−30829
CrossRef Google scholar
[41]
Kim SC, Sprung R, Chen Y, Xu Y, Ball H, Pei J, Cheng T, Kho Y, Xiao H, Xiao L, Grishin NV, White M, Yang XJ, Zhao Y (2006) Substrate and functional diversity of lysine acetylation revealed by a proteomics survey. Mol Cell 23: 607−618
CrossRef Google scholar
[42]
Kimura A, Matsubara K, Horikoshi M (2005) A decade of histone acetylation: marking eukaryotic chromosomes with specific codes. J Biochem 138: 647−662
CrossRef Google scholar
[43]
Knutson SK, Chyla BJ, Amann JM, Bhaskara S, Huppert SS, Hiebert SW(2008) Liver-specific deletion of histone deacetylase 3 disrupts metabolic transcriptional networks. EMBO J 27: 1017−1028
CrossRef Google scholar
[44]
Lagger G, O’Carroll D, Rembold M, Khier H, Tischler J, Weitzer G, Schuettengruber B, Hauser C, Brunmeir R, Jenuwein T, Seiser C (2002) Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. EMBO J 21: 2672−2681
CrossRef Google scholar
[45]
Lalmansingh AS, Karmakar S, Jin Y, Nagaich AK (2012) Multiple modes of chromatin remodeling by Forkhead box proteins. Biochim Biophys Acta 1819: 707−715
CrossRef Google scholar
[46]
Lee KK, Workman JL (2007) Histone acetyltransferase complexes: one size doesn’t fit all. Nat Rev Mol Cell Biol 8: 284−295
CrossRef Google scholar
[47]
Li Y, Xu S, Giles A, Nakamura K, Lee JW, Hou X, Donmez G, Li J, Luo Z, Walsh K, Guarente L, Zang M (2011) Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J 25: 1664−1679
CrossRef Google scholar
[48]
Li Y, Varala K, Coruzzi GM(2015) From milliseconds to lifetimes: tracking the dynamic behavior of transcription factors in gene networks. Trends Genet.
CrossRef Google scholar
[49]
Lu Q, Hutchins AE, Doyle CM, Lundblad JR, Kwok RP (2003) Acetylation of cAMP-responsive element-binding protein (CREB) by CREB-binding protein enhances CREB-dependent transcription. J Biol Chem 278: 15727−15734
CrossRef Google scholar
[50]
Ma L, Robinson LN, Towle HC(2006) ChREBP*Mlx is the principal mediator of glucose-induced gene expression in the liver. J Biol Chem 281: 28721−28730
CrossRef Google scholar
[51]
Maiese K, Chong ZZ, Shang YC(2008) OutFOXOing disease and disability: the therapeutic potential of targeting FoxO proteins. Trends Mol Med 14: 219−227
CrossRef Google scholar
[52]
Marmier S, Dentin R, Daujat-Chavanieu M, Guillou H, Bertrand- Michel J, Gerbal-Chaloin S, Girard J, Lotersztajn S, Postic C (2015) Novel role for carbohydrate responsive element binding protein in the control of ethanol metabolism and susceptibility to binge drinking. Hepatology.
CrossRef Google scholar
[53]
Matsumoto M, Pocai A, Rossetti L, Depinho RA, Accili D (2007) Impaired regulation of hepatic glucose production in mice lacking the forkhead transcription factor Foxo1 in liver. Cell Metab 6: 208−216
CrossRef Google scholar
[54]
Matsuzaki H, Daitoku H, Hatta M, Aoyama H, Yoshimochi K, Fukamizu A (2005) Acetylation of Foxo1 alters its DNA-binding ability and sensitivity to phosphorylation. Proc Natl Acad Sci U S A 102: 11278−11283
CrossRef Google scholar
[55]
Meek DW, Anderson CW (2009) Posttranslational modification of p53: cooperative integrators of function. Cold Spring Harb Perspect Biol 1: a000950
CrossRef Google scholar
[56]
Mihaylova MM, Vasquez DS, Ravnskjaer K, Denechaud PD, Yu RT, Alvarez JG, Downes M, Evans RM, Montminy M, Shaw RJ(2011) Class IIa histone deacetylases are hormone-activated regulators of FOXO and mammalian glucose homeostasis. Cell 145: 607−621
CrossRef Google scholar
[57]
Montgomery RL, Potthoff MJ, Haberland M, Qi X, Matsuzaki S, Humphries KM, Richardson JA, Bassel-Duby R, Olson EN(2008) Maintenance of cardiac energy metabolism by histone deacetylase 3 in mice. J Clin Invest 118: 3588−3597
CrossRef Google scholar
[58]
Nakae J, Cao Y, Daitoku H, Fukamizu A, Ogawa W, Yano Y, Hayashi Y (2006) The LXXLL motif of murine forkhead transcription factor FoxO1 mediates Sirt1-dependent transcriptional activity. J Clin Invest 116: 2473−2483
CrossRef Google scholar
[59]
Nakae J, Cao Y, Oki M, Orba Y, Sawa H, Kiyonari H, Iskandar K, Suga K, Lombes M, Hayashi Y (2008) Forkhead transcription factor FoxO1 in adipose tissue regulates energy storage and expenditure. Diabetes 57: 563−576
CrossRef Google scholar
[60]
Nerlov C (2007) The C/EBP family of transcription factors: a paradigm for interaction between gene expression and proliferation control. Trends Cell Biol 17: 318−324
CrossRef Google scholar
[61]
Nerlov C (2008) C/EBPs: recipients of extracellular signals through proteome modulation. Curr Opin Cell Biol 20: 180−185
CrossRef Google scholar
[62]
Park BH, Qiang L, Farmer SR (2004) Phosphorylation of C/EBPbeta at a consensus extracellular signal-regulated kinase/glycogen synthase kinase 3 site is required for the induction of adiponectin gene expression during the differentiation of mouse fibroblasts into adipocytes. Mol Cell Biol 24: 8671−8680
CrossRef Google scholar
[63]
Park JM, Kim TH, Bae JS, Kim MY, Kim KS, Ahn YH (2010) Role of resveratrol in FOXO1-mediated gluconeogenic gene expression in the liver. Biochem Biophys Res Commun 403: 329−334
CrossRef Google scholar
[64]
Paz JC, Park S, Phillips N, Matsumura S, Tsai WW, Kasper L, Brindle PK, Zhang G, Zhou MM, Wright PE, Montminy M (2014) Combinatorial regulation of a signal-dependent activator by phosphorylation and acetylation. Proc Natl Acad Sci U S A 111: 17116−17121
CrossRef Google scholar
[65]
Perrot V, Rechler MM(2005) The coactivator p300 directly acetylates the forkhead transcription factor Foxo1 and stimulates Foxo1-induced transcription. Mol Endocrinol 19: 2283−2298
CrossRef Google scholar
[66]
Perry RJ, Samuel VT, Petersen KF, Shulman GI(2014) The role of hepatic lipids in hepatic insulin resistance and type 2 diabetes. Nature 510: 84−91
CrossRef Google scholar
[67]
Ponugoti B, Kim DH, Xiao Z, Smith Z, Miao J, Zang M, Wu SY, Chiang CM, Veenstra TD, Kemper JK (2010) SIRT1 deacetylates and inhibits SREBP-1C activity in regulation of hepatic lipid metabolism. J Biol Chem 285: 33959−33970
CrossRef Google scholar
[68]
Postic C, Dentin R, Denechaud PD, Girard J (2007) ChREBP, a transcriptional regulator of glucose and lipid metabolism. Annu Rev Nutr 27: 179−192
CrossRef Google scholar
[69]
Purushotham A, Schug TT, Xu Q, Surapureddi S, Guo X, Li X (2009) Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab 9: 327−338
CrossRef Google scholar
[70]
Ravnskjaer K, Hogan MF, Lackey D, Tora L, Dent SY, Olefsky J, Montminy M (2013) Glucagon regulates gluconeogenesis through KAT2B- and WDR5-mediated epigenetic effects. J Clin Invest 123: 4318−4328
CrossRef Google scholar
[71]
Rebel VI, Kung AL, Tanner EA, Yang H, Bronson RT, Livingston DM(2002) Distinct roles for CREB-binding protein and p300 in hematopoietic stem cell self-renewal. Proc Natl Acad Sci U S A 99: 14789−14794
CrossRef Google scholar
[72]
Schrem H, Klempnauer J, Borlak J (2004) Liver-enriched transcription factors in liver function and development. Part II: the C/EBPs and D site-binding protein in cell cycle control, carcinogenesis, circadian gene regulation, liver regeneration, apoptosis, and liverspecific gene regulation. Pharmacol Rev 56: 291−330
CrossRef Google scholar
[73]
Shao W, Espenshade PJ (2012) Expanding roles for SREBP in metabolism. Cell Metab 16: 414−419
CrossRef Google scholar
[74]
Shimano H (2009) SREBPs: physiology and pathophysiology of the SREBP family. FEBS J 276: 616−621
CrossRef Google scholar
[75]
Shirakawa K, Chavez L, Hakre S, Calvanese V, Verdin E (2013) Reactivation of latent HIV by histone deacetylase inhibitors. Trends Microbiol 21: 277−285
CrossRef Google scholar
[76]
Soyal SM, Nofziger C, Dossena S, Paulmichl M, Patsch W (2015) Targeting SREBPs for treatment of the metabolic syndrome. Trends Pharmacol Sci 36: 406−416
CrossRef Google scholar
[77]
Sun Z, Miller RA, Patel RT, Chen J, Dhir R, Wang H, Zhang D, Graham MJ, Unterman TG, Shulman GI, Sztalryd C, Bennett MJ, Ahima RS, Birnbaum MJ, Lazar MA(2012) Hepatic Hdac3 promotes gluconeogenesis by repressing lipid synthesis and sequestration. Nat Med 18: 934−942
CrossRef Google scholar
[78]
Sundqvist A, Ericsson J (2003) Transcription-dependent degradation controls the stability of the SREBP family of transcription factors. Proc Natl Acad Sci U S A 100: 13833−13838
CrossRef Google scholar
[79]
Vahid F, Zand H, Nosrat-Mirshekarlou E, Najafi R, Hekmatdoost A (2015) The role dietary of bioactive compounds on the regulation of histone acetylases and deacetylases: a review. Gene 562: 8−15
CrossRef Google scholar
[80]
van der Heide LP, Smidt MP (2005) Regulation of FoxO activity by CBP/p300-mediated acetylation. Trends Biochem Sci 30: 81−86
CrossRef Google scholar
[81]
van der Horst A, Burgering BM (2007) Stressing the role of FoxO proteins in lifespan and disease. Nat Rev Mol Cell Biol 8: 440−450
CrossRef Google scholar
[82]
van Gent R, Di Sanza C, van den Broek NJ, Fleskens V, Veenstra A, Stout GJ, Brenkman AB(2014) SIRT1 mediates FOXA2 breakdown by deacetylation in a nutrient-dependent manner. PloS One 9: e98438
CrossRef Google scholar
[83]
von Meyenn F, Porstmann T, Gasser E, Selevsek N, Schmidt A, Aebersold R, Stoffel M (2013) Glucagon-induced acetylation of Foxa2 regulates hepatic lipid metabolism. Cell Metab 17: 436−447
CrossRef Google scholar
[84]
Walker AK, Yang F, Jiang K, Ji JY, Watts JL, Purushotham A, Boss O, Hirsch ML, Ribich S, Smith JJ, Israelian K, Westphal CH, Rodgers JT, Shioda T, Elson SL, Mulligan P, Najafi-Shoushtari H, Black JC, Thakur JK, Kadyk LC, Whetstine JR, Mostoslavsky R, Puigserver P, Li X, Dyson NJ, Hart AC, Naar AM (2010) Conserved role of SIRT1 orthologs in fasting-dependent inhibition of the lipid/cholesterol regulator SREBP. Genes Dev 24: 1403−1417
CrossRef Google scholar
[85]
Wang F, Tong Q (2009) SIRT2 suppresses adipocyte differentiation by deacetylating FOXO1 and enhancing FOXO1’s repressive interaction with PPARgamma. Mol Biol Cell 20: 801−808
CrossRef Google scholar
[86]
Wang C, Tian L, Popov VM, Pestell RG(2011) Acetylation and nuclear receptor action. J Steroid Biochem Mol Biol 123: 91−100
CrossRef Google scholar
[87]
Wiper-Bergeron N, Salem HA, Tomlinson JJ, Wu D, Hache RJ (2007) Glucocorticoid-stimulated preadipocyte differentiation is mediated through acetylation of C/EBPbeta by GCN5. Proc Natl Acad Sci U S A 104: 2703−2708
CrossRef Google scholar
[88]
Wolfrum C, Asilmaz E, Luca E, Friedman JM, Stoffel M (2004) Foxa2 regulates lipid metabolism and ketogenesis in the liver during fasting and in diabetes. Nature 432: 1027−1032
CrossRef Google scholar
[89]
Xu F, Gao Z, Zhang J, Rivera CA, Yin J, Weng J, Ye J (2010) Lack of SIRT1 (Mammalian Sirtuin 1) activity leads to liver steatosis in the SIRT1+/- mice: a role of lipid mobilization and inflammation. Endocrinology 151: 2504−2514
CrossRef Google scholar
[90]
Yamauchi T, Oike Y, Kamon J, Waki H, Komeda K, Tsuchida A, Date Y, Li MX, Miki H, Akanuma Y, Nagai R, Kimura S, Saheki T, Nakazato M, Naitoh T, Yamamura K, Kadowaki T (2002) Increased insulin sensitivity despite lipodystrophy in Crebbp heterozygous mice. Nat Genet 30: 221−226
CrossRef Google scholar
[91]
Zhao Y, Wang Y, Zhu WG(2011) Applications of post-translational modifications of FoxO family proteins in biological functions. J Mol Cell Biol 3: 276−282
CrossRef Google scholar
[92]
Zivkovic AM, German JB, Sanyal AJ (2007) Comparative review of diets for the metabolic syndrome: implications for nonalcoholic fatty liver disease. Am J Clin Nutr 86: 285−300

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