SRC-2 Is an Essential Coactivator for Orchestrating Metabolism and Circadian Rhythm

Cell Reports

Volumn 6, Issue 4, 2014, Pages 633-645

  Stashi, Erin ^a   Lanz, Rainer B ^a   Mao, Jianqiang ^a   Michailidis, George ^a,b   Zhu, Bokai ^a   Kettner, Nicole M ^a   Putluri, Nagireddy ^a   Reineke, Erin L ^a   Reineke, Lucas C ^a   Dasgupta, Subhamoy ^a   Dean, Adam ^a   Stevenson, Connor R ^c   Sivasubramanian, Natarajan ^a   Sreekumar, Arun ^a   DeMayo, Francesco ^a   York, Brian ^a   Fu, Loning ^a   O'Malley, Bert W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c TRINITY UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEAR RECEPTOR COACTIVATOR 2; PROTEIN BMAL1; TRANSCRIPTION FACTOR CLOCK;

ANIMAL CELL; ARTICLE; BINDING AFFINITY; BINDING SITE; CIRCADIAN RHYTHM; CONTROLLED STUDY; ENERGY METABOLISM; GENE EXPRESSION; METABOLOME; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; TRANSCRIPTION REGULATION; ANIMAL EXPERIMENT; ANIMAL TISSUE; GENE SEQUENCE; MALE; METABOLISM; PROTEIN LOCALIZATION;

MAMMALIA;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CIRCADIAN RHYTHM; CLOCK PROTEINS; LIVER; MALE; METABOLOME; MICE; NUCLEAR RECEPTOR COACTIVATOR 2; ORGAN SPECIFICITY; TRANSCRIPTOME;

EID: 84896715962     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2014.01.027     Document Type: Article

References (44)

1. Akashi M., Takumi T. The orphan nuclear receptor RORalpha regulates circadian transcription of the mammalian core-clock Bmal1. Nat. Struct. Mol. Biol. 2005, 12:441-448.
2. Asher G., Schibler U. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 2011, 13:125-137.
3. Bass J., Takahashi J.S. Circadian integration of metabolism and energetics. Science 2010, 330:1349-1354.
4. Bugge A., Feng D., Everett L.J., Briggs E.R., Mullican S.E., Wang F., Jager J., Lazar M.A. Rev-erbα and Rev-erbβ coordinately protect the circadian clock and normal metabolic function. Genes Dev. 2012, 26:657-667.
5. Bunger M.K., Wilsbacher L.D., Moran S.M., Clendenin C., Radcliffe L.A., Hogenesch J.B., Simon M.C., Takahashi J.S., Bradfield C.A. Mop3 is an essential component of the master circadian pacemaker in mammals. Cell 2000, 103:1009-1017.
6. Cho H., Zhao X., Hatori M., Yu R.T., Barish G.D., Lam M.T., Chong L.-W., DiTacchio L., Atkins A.R., Glass C.K., et al. Regulation of circadian behaviour and metabolism by REV-ERB-α and REV-ERB-β. Nature 2012, 485:123-127.
7. Chopra A.R., Louet J.F., Saha P., An J., Demayo F., Xu J., York B., Karpen S., Finegold M., Moore D., et al. Absence of the SRC-2 coactivator results in a glycogenopathy resembling Von Gierke's disease. Science 2008, 322:1395-1399.
8. Chopra A.R., Kommagani R., Saha P., Louet J.-F., Salazar C., Song J., Jeong J., Finegold M., Viollet B., DeMayo F., et al. Cellular energy depletion resets whole-body energy by promoting coactivator-mediated dietary fuel absorption. Cell Metab. 2011, 13:35-43.
9. Curtis A.M., Seo S.B., Westgate E.J., Rudic R.D., Smyth E.M., Chakravarti D., FitzGerald G.A., McNamara P. Histone acetyltransferase-dependent chromatin remodeling and the vascular clock. J.Biol. Chem. 2004, 279:7091-7097.
10. DiTacchio L., Le H.D., Vollmers C., Hatori M., Witcher M., Secombe J., Panda S. Histone lysine demethylase JARID1a activates CLOCK-BMAL1 and influences the circadian clock. Science 2011, 333:1881-1885.
11. Dufour C.R., Levasseur M.-P., Pham N.H.H., Eichner L.J., Wilson B.J., Charest-Marcotte A., Duguay D., Poirier-Héon J.-F., Cermakian N., Giguère V. Genomic convergence among ERRα, PROX1, and BMAL1 in the control of metabolic clock outputs. PLoS Genet. 2011, 7:e1002143.
12. Eckel-Mahan K.L., Patel V.R., Mohney R.P., Vignola K.S., Baldi P., Sassone-Corsi P. Coordination of the transcriptome and metabolome by the circadian clock. Proc. Natl. Acad. Sci. USA 2012, 109:5541-5546.
13. Feng D., Liu T., Sun Z., Bugge A., Mullican S.E., Alenghat T., Liu X.S., Lazar M.A. A circadian rhythm orchestrated by histone deacetylase 3 controls hepatic lipid metabolism. Science 2011, 331:1315-1319.
14. Fustin J.-M., Doi M., Yamada H., Komatsu R., Shimba S., Okamura H. Rhythmic nucleotide synthesis in the liver: temporal segregation of metabolites. Cell Rep 2012, 1:341-349.
15. Gehin M., Mark M., Dennefeld C., Dierich A., Gronemeyer H., Chambon P. The function of TIF2/GRIP1 in mouse reproduction is distinct from those of SRC-1 and p/CIP. Mol. Cell. Biol. 2002, 22:5923-5937.
16. Hartig S.M., He B., Long W., Buehrer B.M., Mancini M.A. Homeostatic levels of SRC-2 and SRC-3 promote early human adipogenesis. J.Cell Biol. 2011, 192:55-67.
17. Hatanaka F., Matsubara C., Myung J., Yoritaka T., Kamimura N., Tsutsumi S., Kanai A., Suzuki Y., Sassone-Corsi P., Aburatani H., et al. Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. Mol. Cell. Biol. 2010, 30:5636-5648.
18. Jeong J.-W., Kwak I., Lee K.Y., White L.D., Wang X.P., Brunicardi F.C., O'Malley B.W., DeMayo F.J. The genomic analysis of the impact of steroid receptor coactivators ablation on hepatic metabolism. Mol. Endocrinol. 2006, 20:1138-1152.
19. Koike N., Yoo S.H., Huang H.C., Kumar V., Lee C., Kim T.K., Takahashi J.S. Transcriptional architecture and chromatin landscape of the core circadian clock in mammals. Science 2012, 338:349-354.
20. Kondratov R.V., Kondratova A.A., Gorbacheva V.Y., Vykhovanets O.V., Antoch M.P. Early aging and age-related pathologies in mice deficient in BMAL1, the core componentof the circadian clock. Genes Dev. 2006, 20:1868-1873.
21. Lamia K.A., Sachdeva U.M., DiTacchio L., Williams E.C., Alvarez J.G., Egan D.F., Vasquez D.S., Juguilon H., Panda S., Shaw R.J., et al. AMPK regulates the circadian clock by cryptochrome phosphorylation and degradation. Science 2009, 326:437-440.
22. Lamia K.A., Papp S.J., Yu R.T., Barish G.D., Uhlenhaut N.H., Jonker J.W., Downes M., Evans R.M. Cryptochromes mediate rhythmic repression of the glucocorticoid receptor. Nature 2011, 480:552-556.
23. Lande-Diner L., Boyault C., Kim J.Y., Weitz C.J. A positive feedback loop links circadian clock factor CLOCK-BMAL1 to the basic transcriptional machinery. Proc. Natl. Acad. Sci. USA 2013, 110:16021-16026.
24. Li H., Kim J.H., Koh S.S., Stallcup M.R. Synergistic effects of coactivators GRIP1 and beta-catenin on gene activation: cross-talk between androgen receptor and Wnt signaling pathways. J.Biol. Chem. 2004, 279:4212-4220.
25. Li D.-Q., Pakala S.B., Reddy S.D.N., Peng S., Balasenthil S., Deng C.-X., Lee C.C., Rea M.A., Kumar R. Metastasis-associated protein 1 is an integral component of the circadian molecular machinery. Nat Commun 2013, 4:2545.
26. Liu C., Li S., Liu T., Borjigin J., Lin J.D. Transcriptional coactivator PGC-1α integrates the mammalian clock and energy metabolism. Nature 2007, 447:477-481.
27. Marcheva B., Ramsey K.M., Buhr E.D., Kobayashi Y., Su H., Ko C.H., Ivanova G., Omura C., Mo S., Vitaterna M.H., et al. Disruption of the clock components CLOCK and BMAL1 leads to hypoinsulinaemia and diabetes. Nature 2010, 466:627-631.
28. Mohawk J.A., Green C.B., Takahashi J.S. Central and peripheral circadian clocks in mammals. Annu. Rev. Neurosci. 2012, 35:445-462.
29. O'Donnell K.A., Keng V.W., York B., Reineke E.L., Seo D., Fan D., Silverstein K.A., Schrum C.T., Xie W.R., Mularoni L., et al. A Sleeping Beauty mutagenesis screen reveals a tumor suppressor role for Ncoa2/Src-2 in liver cancer. Proc. Natl. Acad. Sci. USA 2012, 109:E1377-E1386.
30. Picard F., Géhin M., Annicotte J.S., Rocchi S., Champy M.-F., O'Malley B.W., Chambon P., Auwerx J. SRC-1 and TIF2 control energy balance between white and brown adipose tissues. Cell 2002, 111:931-941.
31. Poliandri A.H.B., Gamsby J.J., Christian M., Spinella M.J., Loros J.J., Dunlap J.C., Parker M.G. Modulation of clock gene expression by the transcriptional coregulator receptor interacting protein 140 (RIP140). J.Biol. Rhythms 2011, 26:187-199.
32. Preitner N., Damiola F., Lopez-Molina L., Zakany J., Duboule D., Albrecht U., Schibler U. The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell 2002, 110:251-260.
33. Ptitsyn A.A., Zvonic S., Conrad S.A., Scott L.K., Mynatt R.L., Gimble J.M. Circadian clocks are resounding in peripheral tissues. PLoS Comput. Biol. 2006, 2:e16.
34. Rey G., Cesbron F., Rougemont J., Reinke H., Brunner M., Naef F. Genome-wide and phase-specific DNA-binding rhythms of BMAL1 control circadian output functions in mouse liver. PLoS Biol. 2011, 9:e1000595.
35. Rudic R.D., McNamara P., Curtis A.-M., Boston R.C., Panda S., Hogenesch J.B., Fitzgerald G.A. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis. PLoS Biol. 2004, 2:e377.
36. Sato T.K., Panda S., Miraglia L.J., Reyes T.M., Rudic R.D., McNamara P., Naik K.A., FitzGerald G.A., Kay S.A., Hogenesch J.B. A functional genomics strategy reveals Rora as a component of the mammalian circadian clock. Neuron 2004, 43:527-537.
37. Schmutz I., Ripperger J.A., Baeriswyl-Aebischer S., Albrecht U. The mammalian clock component PERIOD2 coordinates circadian output by interaction with nuclear receptors. Genes Dev. 2010, 24:345-357.
38. Somanath P.R., Podrez E.A., Chen J., Ma Y., Marchant K., Antoch M., Byzova T.V. Deficiency in core circadian protein Bmal1 is associated with a prothrombotic and vascular phenotype. J.Cell. Physiol. 2011, 226:132-140.
39. Stashi E., Wang L., Mani S.K., York B., O'Malley B.W. Research resource: loss of the steroid receptor coactivators confers neurobehavioral consequences. Mol. Endocrinol. 2013, 27:1776-1787.
40. Takahashi J.S., Hong H.-K., Ko C.H., McDearmon E.L. The genetics of mammalian circadian order and disorder: implications for physiology and disease. Nat. Rev. Genet. 2008, 9:764-775.
41. Ueda H.R., Chen W., Adachi A., Wakamatsu H., Hayashi S., Takasugi T., Nagano M., Nakahama K.-I., Suzuki Y., Sugano S., et al. A transcription factor response element for gene expression during circadian night. Nature 2002, 418:534-539.
42. Um J.H., Pendergast J.S., Springer D.A., Foretz M., Viollet B., Brown A., Kim M.K., Yamazaki S., Chung J.H. AMPK regulates circadian rhythms in a tissue- and isoform-specific manner. PLoS ONE 2011, 6:e18450.
43. Ye R., Selby C.P., Ozturk N., Annayev Y., Sancar A. Biochemical analysis of the canonical model for the mammalian circadian clock. J.Biol. Chem. 2011, 286:25891-25902.
44. York B., Sagen J.V., Tsimelzon A., Louet J.F., Chopra A.R., Reineke E.L., Zhou S., Stevens R.D., Wenner B.R., Ilkayeva O., et al. Research resource: tissue- and pathway-specific metabolomic profiles of the steroid receptor coactivator (SRC) family. Mol. Endocrinol. 2013, 27:366-380.