Partitioning circadian transcription by SIRT6 leads to segregated control of cellular metabolism

Cell

Volumn 158, Issue 3, 2014, Pages 659-672

  Masri, Selma ^a   Rigor, Paul ^a,b   Cervantes, Marlene ^a   Ceglia, Nicholas ^a,b   Sebastian, Carlos ^c   Xiao, Cuiying ^d   Roqueta Rivera, Manuel ^e   Deng, Chuxia ^d   Osborne, Timothy F ^e   Mostoslavsky, Raul ^c   Baldi, Pierre ^a,b   Sassone Corsi, Paolo ^a,f  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b Irvine   (United States)

^c HARVARD MEDICAL SCHOOL   (United States)

^d NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^e BURNHAM INSTITUTE   (United States)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN BMAL1; SIRTUIN 1; SIRTUIN 6; STEROL REGULATORY ELEMENT BINDING PROTEIN 1; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTOME; ARNTL PROTEIN, MOUSE; CHROMATIN; CLOCK PROTEIN, MOUSE; SIRT1 PROTEIN, MOUSE; SIRT6 PROTEIN, MOUSE; SIRTUIN; TRANSCRIPTION FACTOR ARNTL;

ANIMAL EXPERIMENT; ARTICLE; CELL METABOLISM; CHOLESTEROL METABOLISM; CHROMATIN; CIRCADIAN RHYTHM; CONTROLLED STUDY; FATTY ACID METABOLISM; GENE EXPRESSION; METABOLOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN DOMAIN; ANIMAL; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; KNOCKOUT MOUSE; LIVER; METABOLISM;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CHROMATIN; CIRCADIAN RHYTHM; CLOCK PROTEINS; GENE EXPRESSION PROFILING; LIVER; MICE; MICE, KNOCKOUT; SIRTUIN 1; SIRTUINS; TRANSCRIPTION, GENETIC;

EID: 84905389924     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2014.06.050     Document Type: Article

References (61)

1. G. Asher, D. Gatfield, M. Stratmann, H. Reinke, C. Dibner, F. Kreppel, R. Mostoslavsky, F.W. Alt, and U. Schibler SIRT1 regulates circadian clock gene expression through PER2 deacetylation Cell 134 2008 317 328
2. W.J. Belden, Z.A. Lewis, E.U. Selker, J.J. Loros, and J.C. Dunlap CHD1 remodels chromatin and influences transient DNA methylation at the clock gene frequency PLoS Genet. 7 2011 e1002166
3. M.M. Bellet, Y. Nakahata, M. Boudjelal, E. Watts, D.E. Mossakowska, K.A. Edwards, M. Cervantes, G. Astarita, C. Loh, and J.L. Ellis et al. Pharmacological modulation of circadian rhythms by synthetic activators of the deacetylase SIRT1 Proc. Natl. Acad. Sci. USA 110 2013 3333 3338
4. M.K. Bennett, J.M. Lopez, H.B. Sanchez, and T.F. Osborne Sterol regulation of fatty acid synthase promoter. Coordinate feedback regulation of two major lipid pathways J. Biol. Chem. 270 1995 25578 25583
5. H.C. Chang, and L. Guarente SIRT1 mediates central circadian control in the SCN by a mechanism that decays with aging Cell 153 2013 1448 1460
6. H.C. Chang, and L. Guarente SIRT1 and other sirtuins in metabolism Trends Endocrinol. Metab. 25 2014 138 145
7. G. Cretenet, M. Le Clech, and F. Gachon Circadian clock-coordinated 12 Hr period rhythmic activation of the IRE1alpha pathway controls lipid metabolism in mouse liver Cell Metab. 11 2010 47 57
8. K. Daily, V.R. Patel, P. Rigor, X. Xie, and P. Baldi MotifMap: integrative genome-wide maps of regulatory motif sites for model species BMC Bioinformatics 12 2011 495
9. L. DiTacchio, H.D. Le, C. Vollmers, M. Hatori, M. Witcher, J. Secombe, and S. Panda Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock Science 333 2011 1881 1885
10. M. Doi, J. Hirayama, and P. Sassone-Corsi Circadian regulator CLOCK is a histone acetyltransferase Cell 125 2006 497 508
11. J.E. Dominy Jr., Y. Lee, M.P. Jedrychowski, H. Chim, M.J. Jurczak, J.P. Camporez, H.B. Ruan, J. Feldman, K. Pierce, and R. Mostoslavsky et al. The deacetylase Sirt6 activates the acetyltransferase GCN5 and suppresses hepatic gluconeogenesis Mol. Cell 48 2012 900 913
12. H.A. Duong, M.S. Robles, D. Knutti, and C.J. Weitz A molecular mechanism for circadian clock negative feedback Science 332 2011 1436 1439
13. K.L. Eckel-Mahan, V.R. Patel, S. de Mateo, R. Orozco-Solis, N.J. Ceglia, S. Sahar, S.A. Dilag-Penilla, K.A. Dyar, P. Baldi, and P. Sassone-Corsi Reprogramming of the circadian clock by nutritional challenge Cell 155 2013 1464 1478
14. S. Elhanati, Y. Kanfi, A. Varvak, A. Roichman, I. Carmel-Gross, S. Barth, G. Gibor, and H.Y. Cohen Multiple regulatory layers of SREBP1/2 by SIRT6 Cell Rep. 4 2013 905 912
15. J.P. Etchegaray, C. Lee, P.A. Wade, and S.M. Reppert Rhythmic histone acetylation underlies transcription in the mammalian circadian clock Nature 421 2003 177 182
16. A.M. Evans, C.D. DeHaven, T. Barrett, M. Mitchell, and E. Milgram Integrated, nontargeted ultrahigh performance liquid chromatography/electrospray ionization tandem mass spectrometry platform for the identification and relative quantification of the small-molecule complement of biological systems Anal. Chem. 81 2009 6656 6667
17. J.L. Feldman, J. Baeza, and J.M. Denu Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins J. Biol. Chem. 288 2013 31350 31356
18. D. Feng, and M.A. Lazar Clocks, metabolism, and the epigenome Mol. Cell 47 2012 158 167
19. T. Finkel, C.X. Deng, and R. Mostoslavsky Recent progress in the biology and physiology of sirtuins Nature 460 2009 587 591
20. R. Gil, S. Barth, Y. Kanfi, and H.Y. Cohen SIRT6 exhibits nucleosome-dependent deacetylase activity Nucleic Acids Res. 41 2013 8537 8545
21. P. Gut, and E. Verdin The nexus of chromatin regulation and intermediary metabolism Nature 502 2013 489 498
22. J.A. Hall, J.E. Dominy, Y. Lee, and P. Puigserver The sirtuin family's role in aging and age-associated pathologies J. Clin. Invest. 123 2013 973 979
23. J. Hirayama, S. Sahar, B. Grimaldi, T. Tamaru, K. Takamatsu, Y. Nakahata, and P. Sassone-Corsi CLOCK-mediated acetylation of BMAL1 controls circadian function Nature 450 2007 1086 1090
24. J.D. Horton, N.A. Shah, J.A. Warrington, N.N. Anderson, S.W. Park, M.S. Brown, and J.L. Goldstein Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes Proc. Natl. Acad. Sci. USA 100 2003 12027 12032
25. R.H. Houtkooper, E. Pirinen, and J. Auwerx Sirtuins as regulators of metabolism and healthspan Nat. Rev. Mol. Cell Biol. 13 2012 225 238
26. W. Huang da, B.T. Sherman, and R.A. Lempicki Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists Nucleic Acids Res. 37 2009 1 13
27. W. Huang da, B.T. Sherman, and R.A. Lempicki Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources Nat. Protoc. 4 2009 44 57
28. M.E. Hughes, J.B. Hogenesch, and K. Kornacker JTK-CYCLE: an efficient nonparametric algorithm for detecting rhythmic components in genome-scale data sets J. Biol. Rhythms 25 2010 372 380
29. S.B. Joseph, B.A. Laffitte, P.H. Patel, M.A. Watson, K.E. Matsukuma, R. Walczak, J.L. Collins, T.F. Osborne, and P. Tontonoz Direct and indirect mechanisms for regulation of fatty acid synthase gene expression by liver X receptors J. Biol. Chem. 277 2002 11019 11025
30. Y. Kanfi, V. Peshti, R. Gil, S. Naiman, L. Nahum, E. Levin, N. Kronfeld-Schor, and H.Y. Cohen SIRT6 protects against pathological damage caused by diet-induced obesity Aging Cell 9 2010 162 173
31. S. Katada, and P. Sassone-Corsi The histone methyltransferase MLL1 permits the oscillation of circadian gene expression Nat. Struct. Mol. Biol. 17 2010 1414 1421
32. S. Katada, A. Imhof, and P. Sassone-Corsi Connecting threads: epigenetics and metabolism Cell 148 2012 24 28
33. T.L. Kawahara, E. Michishita, A.S. Adler, M. Damian, E. Berber, M. Lin, R.A. McCord, K.C. Ongaigui, L.D. Boxer, H.Y. Chang, and K.F. Chua SIRT6 links histone H3 lysine 9 deacetylation to NF-kappaB-dependent gene expression and organismal life span Cell 136 2009 62 74
34. T.L. Kawahara, N.A. Rapicavoli, A.R. Wu, K. Qu, S.R. Quake, and H.Y. Chang Dynamic chromatin localization of Sirt6 shapes stress- and aging-related transcriptional networks PLoS Genet. 7 2011 e1002153
35. H.S. Kim, C. Xiao, R.H. Wang, T. Lahusen, X. Xu, A. Vassilopoulos, G. Vazquez-Ortiz, W.I. Jeong, O. Park, and S.H. Ki et al. Hepatic-specific disruption of SIRT6 in mice results in fatty liver formation due to enhanced glycolysis and triglyceride synthesis Cell Metab. 12 2010 224 236
36. Y.B. Kiyohara, K. Nishii, M. Ukai-Tadenuma, H.R. Ueda, Y. Uchiyama, and K. Yagita Detection of a circadian enhancer in the mDbp promoter using prokaryotic transposon vector-based strategy Nucleic Acids Res. 36 2008 e23
37. N. Koike, S.H. Yoo, H.C. Huang, V. Kumar, C. Lee, T.K. Kim, and J.S. Takahashi Transcriptional architecture and chromatin landscape of the core circadian clock in mammals Science 338 2012 349 354
38. G. Le Martelot, T. Claudel, D. Gatfield, O. Schaad, B. Kornmann, G. Lo Sasso, A. Moschetta, and U. Schibler REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis PLoS Biol. 7 2009 e1000181
39. S. Masri, and P. Sassone-Corsi Plasticity and specificity of the circadian epigenome Nat. Neurosci. 13 2010 1324 1329
40. E. Michishita, R.A. McCord, E. Berber, M. Kioi, H. Padilla-Nash, M. Damian, P. Cheung, R. Kusumoto, T.L. Kawahara, and J.C. Barrett et al. SIRT6 is a histone H3 lysine 9 deacetylase that modulates telomeric chromatin Nature 452 2008 492 496
41. E. Michishita, R.A. McCord, L.D. Boxer, M.F. Barber, T. Hong, O. Gozani, and K.F. Chua Cell cycle-dependent deacetylation of telomeric histone H3 lysine K56 by human SIRT6 Cell Cycle 8 2009 2664 2666
42. R. Mostoslavsky, K.F. Chua, D.B. Lombard, W.W. Pang, M.R. Fischer, L. Gellon, P. Liu, G. Mostoslavsky, S. Franco, and M.M. Murphy et al. Genomic instability and aging-like phenotype in the absence of mammalian SIRT6 Cell 124 2006 315 329
43. Y. Nakahata, M. Kaluzova, B. Grimaldi, S. Sahar, J. Hirayama, D. Chen, L.P. Guarente, and P. Sassone-Corsi The NAD+-dependent deacetylase SIRT1 modulates CLOCK-mediated chromatin remodeling and circadian control Cell 134 2008 329 340
44. V.R. Patel, K. Eckel-Mahan, P. Sassone-Corsi, and P. Baldi CircadiOmics: integrating circadian genomics, transcriptomics, proteomics and metabolomics Nat. Methods 9 2012 772 773
45. C.B. Peek, A.H. Affinati, K.M. Ramsey, H.Y. Kuo, W. Yu, L.A. Sena, O. Ilkayeva, B. Marcheva, Y. Kobayashi, and C. Omura et al. Circadian clock NAD+ cycle drives mitochondrial oxidative metabolism in mice Science 342 2013 1243417
46. O. Ram, A. Goren, I. Amit, N. Shoresh, N. Yosef, J. Ernst, M. Kellis, M. Gymrek, R. Issner, and M. Coyne et al. Combinatorial patterning of chromatin regulators uncovered by genome-wide location analysis in human cells Cell 147 2011 1628 1639
47. G. Rey, F. Cesbron, J. Rougemont, H. Reinke, M. Brunner, and F. Naef Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver PLoS Biol. 9 2011 e1000595
48. J.A. Ripperger, and U. Schibler Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions Nat. Genet. 38 2006 369 374
49. S. Rozen, and H. Skaletsky Primer3 on the WWW for general users and for biologist programmers Methods Mol. Biol. 132 2000 365 386
50. S. Sahar, and P. Sassone-Corsi Regulation of metabolism: the circadian clock dictates the time Trends Endocrinol. Metab. 23 2012 1 8
51. Y.K. Seo, H.K. Chong, A.M. Infante, S.S. Im, X. Xie, and T.F. Osborne Genome-wide analysis of SREBP-1 binding in mouse liver chromatin reveals a preference for promoter proximal binding to a new motif Proc. Natl. Acad. Sci. USA 106 2009 13765 13769
52. Y.K. Seo, T.I. Jeon, H.K. Chong, J. Biesinger, X. Xie, and T.F. Osborne Genome-wide localization of SREBP-2 in hepatic chromatin predicts a role in autophagy Cell Metab. 13 2011 367 375
53. R.I. Tennen, and K.F. Chua Chromatin regulation and genome maintenance by mammalian SIRT6 Trends Biochem. Sci. 36 2011 39 46
54. R.I. Tennen, E. Berber, and K.F. Chua Functional dissection of SIRT6: identification of domains that regulate histone deacetylase activity and chromatin localization Mech. Ageing Dev. 131 2010 185 192
55. D. Toiber, F. Erdel, K. Bouazoune, D.M. Silberman, L. Zhong, P. Mulligan, C. Sebastian, C. Cosentino, B. Martinez-Pastor, and S. Giacosa et al. SIRT6 recruits SNF2H to DNA break sites, preventing genomic instability through chromatin remodeling Mol. Cell 51 2013 454 468
56. H. Wijnen, and M.W. Young Interplay of circadian clocks and metabolic rhythms Annu. Rev. Genet. 40 2006 409 448
57. C. Xiao, H.S. Kim, T. Lahusen, R.H. Wang, X. Xu, O. Gavrilova, W. Jou, D. Gius, and C.X. Deng SIRT6 deficiency results in severe hypoglycemia by enhancing both basal and insulin-stimulated glucose uptake in mice J. Biol. Chem. 285 2010 36776 36784
58. X. Xie, P. Rigor, and P. Baldi MotifMap: a human genome-wide map of candidate regulatory motif sites Bioinformatics 25 2009 167 174
59. B. Yang, B.M. Zwaans, M. Eckersdorff, and D.B. Lombard The sirtuin SIRT6 deacetylates H3 K56Ac in vivo to promote genomic stability Cell Cycle 8 2009 2662 2663
60. L. Zhong, A. D'Urso, D. Toiber, C. Sebastian, R.E. Henry, D.D. Vadysirisack, A. Guimaraes, B. Marinelli, J.D. Wikstrom, and T. Nir et al. The histone deacetylase Sirt6 regulates glucose homeostasis via Hif1alpha Cell 140 2010 280 293
61. C.D. Dehaven, A.M. Evans, H. Dai, and K.A. Lawton Organization of GC/MS and LC/MS metabolomics data into chemical libraries J. Cheminform. 2 2010 9