Differential Display of DNA-binding Proteins Reveals Heat-shock Factor 1 As a Circadian Transcription Factor

Overview

Journal Genes Dev

Specialty Molecular Biology

Date 2008 Feb 5

PMID 18245447

Citations 103

Authors

Hans Reinke

Camille Saini

Fabienne Fleury-Olela

Charna Dibner

Ivor J Benjamin

Ueli Schibler

Affiliations

Soon will be listed here.

Abstract

The circadian clock enables the anticipation of daily recurring environmental changes by presetting an organism's physiology and behavior. Driven and synchronized by a central pacemaker in the brain, circadian output genes fine-tune a wide variety of physiological parameters in peripheral organs. However, only a subset of circadianly transcribed genes seems to be directly regulated by core clock proteins. Assuming that yet unidentified transcription factors may exist in the circadian transcriptional network, we set out to develop a novel technique, differential display of DNA-binding proteins (DDDP), which we used to screen mouse liver nuclear extracts. In addition to several established circadian transcription factors, we found DNA binding of heat-shock factor 1 (HSF1) to be highly rhythmic. HSF1 drives the expression of heat-shock proteins at the onset of the dark phase, when the animals start to be behaviorally active. Furthermore, Hsf1-deficient mice have a longer free-running period than wild-type littermates, suggesting a combined role for HSF1 in the mammalian timekeeping and cytoprotection systems. Our results also suggest that the new screening method DDDP is not limited to the identification of circadian transcription factors but can be applied to discover novel transcriptional regulators in various biological systems.

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References

Kornmann B, Schaad O, Bujard H, Takahashi J, Schibler U . System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock. PLoS Biol. 2007; 5(2):e34. PMC: 1783671. DOI: 10.1371/journal.pbio.0050034. View

Calkhoven C, Ab G . Multiple steps in the regulation of transcription-factor level and activity. Biochem J. 1996; 317 ( Pt 2):329-42. PMC: 1217492. DOI: 10.1042/bj3170329. View

Refinetti R . Comparison of the body temperature rhythms of diurnal and nocturnal rodents. J Exp Zool. 1996; 275(1):67-70. DOI: 10.1002/(SICI)1097-010X(19960501)275:1<67::AID-JEZ10>3.0.CO;2-U. View

Feillet C, Ripperger J, Magnone M, Dulloo A, Albrecht U, Challet E . Lack of food anticipation in Per2 mutant mice. Curr Biol. 2006; 16(20):2016-22. DOI: 10.1016/j.cub.2006.08.053. View

Miller B, McDearmon E, Panda S, Hayes K, Zhang J, Andrews J . Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation. Proc Natl Acad Sci U S A. 2007; 104(9):3342-7. PMC: 1802006. DOI: 10.1073/pnas.0611724104. View

Damiola F, Le Minh N, Preitner N, Kornmann B, Schibler U . Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus. Genes Dev. 2000; 14(23):2950-61. PMC: 317100. DOI: 10.1101/gad.183500. View

Gallego M, Virshup D . Post-translational modifications regulate the ticking of the circadian clock. Nat Rev Mol Cell Biol. 2007; 8(2):139-48. DOI: 10.1038/nrm2106. View

Kornmann B, Preitner N, Rifat D, Schibler U . Analysis of circadian liver gene expression by ADDER, a highly sensitive method for the display of differentially expressed mRNAs. Nucleic Acids Res. 2001; 29(11):E51-1. PMC: 55721. DOI: 10.1093/nar/29.11.e51. View

Yan L, Christians E, Liu L, Xiao X, Sohal R, Benjamin I . Mouse heat shock transcription factor 1 deficiency alters cardiac redox homeostasis and increases mitochondrial oxidative damage. EMBO J. 2002; 21(19):5164-72. PMC: 129050. DOI: 10.1093/emboj/cdf528. View

10.

Ripperger J, Shearman L, Reppert S, Schibler U . CLOCK, an essential pacemaker component, controls expression of the circadian transcription factor DBP. Genes Dev. 2000; 14(6):679-89. PMC: 316463. View

11.

Yamazaki S, Numano R, Abe M, Hida A, Takahashi R, Ueda M . Resetting central and peripheral circadian oscillators in transgenic rats. Science. 2000; 288(5466):682-5. DOI: 10.1126/science.288.5466.682. View

12.

Hardin P . Essential and expendable features of the circadian timekeeping mechanism. Curr Opin Neurobiol. 2006; 16(6):686-92. DOI: 10.1016/j.conb.2006.09.001. View

13.

Holmberg C, Hietakangas V, Mikhailov A, Rantanen J, Kallio M, Meinander A . Phosphorylation of serine 230 promotes inducible transcriptional activity of heat shock factor 1. EMBO J. 2001; 20(14):3800-10. PMC: 125548. DOI: 10.1093/emboj/20.14.3800. View

14.

Fonjallaz P, Ossipow V, Wanner G, Schibler U . The two PAR leucine zipper proteins, TEF and DBP, display similar circadian and tissue-specific expression, but have different target promoter preferences. EMBO J. 1996; 15(2):351-62. PMC: 449950. View

15.

Ripperger J, Schibler U . Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions. Nat Genet. 2006; 38(3):369-74. DOI: 10.1038/ng1738. View

16.

Brenner S, Johnson M, Bridgham J, Golda G, Lloyd D, Johnson D . Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol. 2000; 18(6):630-4. DOI: 10.1038/76469. View

17.

Balsalobre A, Damiola F, Schibler U . A serum shock induces circadian gene expression in mammalian tissue culture cells. Cell. 1998; 93(6):929-37. DOI: 10.1016/s0092-8674(00)81199-x. View

18.

Preitner N, Damiola F, Lopez-Molina L, Zakany J, Duboule D, Albrecht U . The orphan nuclear receptor REV-ERBalpha controls circadian transcription within the positive limb of the mammalian circadian oscillator. Cell. 2002; 110(2):251-60. DOI: 10.1016/s0092-8674(02)00825-5. View

19.

Reddy A, Karp N, Maywood E, Sage E, Deery M, ONeill J . Circadian orchestration of the hepatic proteome. Curr Biol. 2006; 16(11):1107-15. DOI: 10.1016/j.cub.2006.04.026. View

20.

Munoz E, Brewer M, Baler R . Modulation of BMAL/CLOCK/E-Box complex activity by a CT-rich cis-acting element. Mol Cell Endocrinol. 2006; 252(1-2):74-81. DOI: 10.1016/j.mce.2006.03.007. View