Coactivator-Dependent Oscillation of Chromatin Accessibility Dictates Circadian Gene Amplitude via REV-ERB Loading

Molecular Cell

Volumn 60, Issue 5, 2015, Pages 769-783

  Zhu, Bokai ^a   Gates, Leah A ^a   Stashi, Erin ^a   Dasgupta, Subhamoy ^a   Gonzales, Naomi ^a   Dean, Adam ^a   Dacso, Clifford C ^a   York, Brian ^a   O'Malley, Bert W ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PROTEIN DERIVATIVE; REV PROTEIN; TRANSCRIPTION FACTOR CLOCK; ARNTL PROTEIN, MOUSE; CHROMATIN; NR1D1 PROTEIN, MOUSE; NUCLEAR RECEPTOR COACTIVATOR 2; NUCLEAR RECEPTOR NR1D1; RETINOID RELATED ORPHAN RECEPTOR ALPHA; RORA PROTEIN, MOUSE; TRANSCRIPTION FACTOR ARNTL;

ANIMAL TISSUE; ARTICLE; CHROMATIN; CHROMATIN ASSEMBLY AND DISASSEMBLY; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE EXPRESSION; GENE REPRESSION; GENETIC TRANSCRIPTION; MALE; MATHEMATICAL MODEL; MOUSE; NONHUMAN; OSCILLATION; TRANSCRIPTION INITIATION; ANIMAL; BIOLOGICAL MODEL; GENE EXPRESSION REGULATION; LIVER; METABOLISM;

ANIMALS; ARNTL TRANSCRIPTION FACTORS; CHROMATIN; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION; LIVER; MICE; MODELS, BIOLOGICAL; NUCLEAR RECEPTOR COACTIVATOR 2; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP D, MEMBER 1; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 1;

EID: 84952871218     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.10.024     Document Type: Article

References (37)

1. Asher G., Schibler U. Crosstalk between components of circadian and metabolic cycles in mammals. Cell Metab. 2011, 13:125-137.
2. Banerjee S., Wang Y., Solt L.A., Griffett K., Kazantzis M., Amador A., El-Gendy B.M., Huitron-Resendiz S., Roberts A.J., Shin Y., et al. Pharmacological targeting of the mammalian clock regulates sleep architecture and emotional behaviour. Nat. Commun. 2014, 5:5759.
3. Bollinger T., Schibler U. Circadian rhythms - from genes to physiology and disease. Swiss Med. Wkly. 2014, 144:w13984.
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. 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.
6. 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.
7. Clapier C.R., Cairns B.R. The biology of chromatin remodeling complexes. Annu. Rev. Biochem. 2009, 78:273-304.
8. Fang B., Everett L.J., Jager J., Briggs E., Armour S.M., Feng D., Roy A., Gerhart-Hines Z., Sun Z., Lazar M.A. Circadian enhancers coordinate multiple phases of rhythmic gene transcription in vivo. Cell 2014, 159:1140-1152.
9. Feng D., Lazar M.A. Clocks, metabolism, and the epigenome. Mol. Cell 2012, 47:158-167.
10. 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.
11. Fleet T., Zhang B., Lin F., Zhu B., Dasgupta S., Stashi E., Tackett B., Thevananther S., Rajapakshe K.I., Gonzales N., et al. SRC-2 orchestrates polygenic inputs for fine-tuning glucose homeostasis. Proc. Natl. Acad. Sci. USA 2015, 112:E6068-E6077.
12. Foulds C.E., Feng Q., Ding C., Bailey S., Hunsaker T.L., Malovannaya A., Hamilton R.A., Gates L.A., Zhang Z., Li C., et al. Proteomic analysis of coregulators bound to ERα on DNA and nucleosomes reveals coregulator dynamics. Mol. Cell 2013, 51:185-199.
13. Guilding C., Hughes A.T., Brown T.M., Namvar S., Piggins H.D. A riot of rhythms: neuronal and glial circadian oscillators in the mediobasal hypothalamus. Mol. Brain 2009, 2:28.
14. Jager J., O'Brien W.T., Manlove J., Krizman E.N., Fang B., Gerhart-Hines Z., Robinson M.B., Klein P.S., Lazar M.A. Behavioral changes and dopaminergic dysregulation in mice lacking the nuclear receptor Rev-erbα. Mol. Endocrinol. 2014, 28:490-498.
15. Kim J.Y., Kwak P.B., Weitz C.J. Specificity in circadian clock feedback from targeted reconstitution of the NuRD corepressor. Mol. Cell 2014, 56:738-748.
16. 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.
17. Lee H.M., Chen R., Kim H., Etchegaray J.P., Weaver D.R., Lee C. The period of the circadian oscillator is primarily determined by the balance between casein kinase 1 and protein phosphatase 1. Proc. Natl. Acad. Sci. USA 2011, 108:16451-16456.
18. Lemon B., Inouye C., King D.S., Tjian R. Selectivity of chromatin-remodelling cofactors for ligand-activated transcription. Nature 2001, 414:924-928.
19. Liu A.C., Tran H.G., Zhang E.E., Priest A.A., Welsh D.K., Kay S.A. Redundant function of REV-ERBalpha and beta and non-essential role for Bmal1 cycling in transcriptional regulation of intracellular circadian rhythms. PLoS Genet. 2008, 4:e1000023.
20. Malovannaya A., Lanz R.B., Jung S.Y., Bulynko Y., Le N.T., Chan D.W., Ding C., Shi Y., Yucer N., Krenciute G., et al. Analysis of the human endogenous coregulator complexome. Cell 2011, 145:787-799.
21. Menet J.S., Pescatore S., Rosbash M. CLOCK:BMAL1 is a pioneer-like transcription factor. Genes Dev. 2014, 28:8-13.
22. Meng Q.J., McMaster A., Beesley S., Lu W.Q., Gibbs J., Parks D., Collins J., Farrow S., Donn R., Ray D., Loudon A. Ligand modulation of REV-ERBalpha function resets the peripheral circadian clock in a phasic manner. J. Cell Sci. 2008, 121:3629-3635.
23. 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.
24. Solt L.A., Wang Y., Banerjee S., Hughes T., Kojetin D.J., Lundasen T., Shin Y., Liu J., Cameron M.D., Noel R., et al. Regulation of circadian behaviour and metabolism by synthetic REV-ERB agonists. Nature 2012, 485:62-68.
25. 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.
26. Stashi E., Lanz R.B., Mao J., Michailidis G., Zhu B., Kettner N.M., Putluri N., Reineke E.L., Reineke L.C., Dasgupta S., et al. SRC-2 is an essential coactivator for orchestrating metabolism and circadian rhythm. Cell Rep. 2014, 6:633-645.
27. Takeda Y., Jothi R., Birault V., Jetten A.M. RORγ directly regulates the circadian expression of clock genes and downstream targets in vivo. Nucleic Acids Res. 2012, 40:8519-8535.
28. Takeda Y., Kang H.S., Lih F.B., Jiang H., Blaner W.S., Jetten A.M. Retinoid acid-related orphan receptor γ, RORγ, participates in diurnal transcriptional regulation of lipid metabolic genes. Nucleic Acids Res. 2014, 42:10448-10459.
29. Vierstra J., Rynes E., Sandstrom R., Zhang M., Canfield T., Hansen R.S., Stehling-Sun S., Sabo P.J., Byron R., Humbert R., et al. Mouse regulatory DNA landscapes reveal global principles of cis-regulatory evolution. Science 2014, 346:1007-1012.
30. Voss T.C., Schiltz R.L., Sung M.H., Yen P.M., Stamatoyannopoulos J.A., Biddie S.C., Johnson T.A., Miranda T.B., John S., Hager G.L. Dynamic exchange at regulatory elements during chromatin remodeling underlies assisted loading mechanism. Cell 2011, 146:544-554.
31. Xu F., Flowers S., Moran E. Essential role of ARID2 protein-containing SWI/SNF complex in tissue-specific gene expression. J. Biol. Chem. 2012, 287:5033-5041.
32. Yan Z., Cui K., Murray D.M., Ling C., Xue Y., Gerstein A., Parsons R., Zhao K., Wang W. PBAF chromatin-remodeling complex requires a novel specificity subunit, BAF200, to regulate expression of selective interferon-responsive genes. Genes Dev. 2005, 19:1662-1667.
33. Zaret K.S., Carroll J.S. Pioneer transcription factors: establishing competence for gene expression. Genes Dev. 2011, 25:2227-2241.
34. Zhang E.E., Kay S.A. Clocks not winding down: unravelling circadian networks. Nat. Rev. Mol. Cell Biol. 2010, 11:764-776.
35. Zhang E.E., Liu A.C., Hirota T., Miraglia L.J., Welch G., Pongsawakul P.Y., Liu X., Atwood A., Huss J.W., Janes J., et al. A genome-wide RNAi screen for modifiers of the circadian clock in human cells. Cell 2009, 139:199-210.
36. Zhang Y., Fang B., Emmett M.J., Damle M., Sun Z., Feng D., Armour S.M., Remsberg J.R., Jager J., Soccio R.E., et al. GENE REGULATION. Discrete functions of nuclear receptor Rev-erbα couple metabolism to the clock. Science 2015, 348:1488-1492.
37. Zhao X., Cho H., Yu R.T., Atkins A.R., Downes M., Evans R.M. Nuclear receptors rock around the clock. EMBO Rep. 2014, 15:518-528.