Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism

F. Hatanaka; C. Matsubara; J. Myung; T. Yoritaka; N. Kamimura; S. Tsutsumi; A. Kanai; Y. Suzuki; P. Sassone-Corsi; H. Aburatani; S. Sugano; T. Takumi

doi:10.1128/MCB.00781-10

Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism

F. Hatanaka, C. Matsubara, J. Myung, T. Yoritaka, N. Kamimura, S. Tsutsumi, A. Kanai, Y. Suzuki, P. Sassone-Corsi, H. Aburatani, S. Sugano, T. Takumi

Research output: Contribution to journal › Article › peer-review

114 Citations (Scopus)

Abstract

Circadian rhythms are common to most organisms and govern much of homeostasis and physiology. Since a significant fraction of the mammalian genome is controlled by the clock machinery, understanding the genome-wide signaling and epigenetic basis of circadian gene expression is essential. BMAL1 is a critical circadian transcription factor that regulates genes via E-box elements in their promoters. We used multiple high-throughput approaches, including chromatin immunoprecipitation-based systematic analyses and DNA microarrays combined with bioinformatics, to generate genome-wide profiles of BMAL1 target genes. We reveal that, in addition to E-boxes, the CCAATG element contributes to elicit robust circadian expression. BMAL1 occupancy is found in more than 150 sites, including all known clock genes. Importantly, a significant proportion of BMAL1 targets include genes that encode central regulators of metabolic processes. The database generated in this study constitutes a useful resource to decipher the network of circadian gene control and its intimate links with several fundamental physiological functions. © 2010, American Society for Microbiology.

Original language	English
Pages (from-to)	5636-5648
Number of pages	13
Journal	Molecular and Cellular Biology
Volume	30
Issue number	24
DOIs	https://doi.org/10.1128/MCB.00781-10
Publication status	Published - 2010

Keywords

transcription factor ARNTL
animal
article
Bagg albino mouse
biological rhythm
biology
cell line
chromatin immunoprecipitation
circadian rhythm
energy metabolism
gene expression profiling
gene expression regulation
genetics
genome
high throughput screening
male
metabolism
methodology
microarray analysis
mouse
mouse mutant
physiology
Animals
ARNTL Transcription Factors
Biological Clocks
Cell Line
Chromatin Immunoprecipitation
Circadian Rhythm
Computational Biology
Energy Metabolism
Gene Expression Profiling
Gene Expression Regulation
Genome
High-Throughput Screening Assays
Male
Mice
Mice, Inbred BALB C
Mice, Knockout
Microarray Analysis

Access to Document

10.1128/MCB.00781-10

https://www.scopus.com/inward/record.uri?eid=2-s2.0-79952255290&doi=10.1128%2fMCB.00781-10&partnerID=40&md5=c0ff91f9468888802abd29634675d7c1

Cite this

@article{51cf45cdc0fa4e98a222eebfa3edc9af,

title = "Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism",

abstract = "Circadian rhythms are common to most organisms and govern much of homeostasis and physiology. Since a significant fraction of the mammalian genome is controlled by the clock machinery, understanding the genome-wide signaling and epigenetic basis of circadian gene expression is essential. BMAL1 is a critical circadian transcription factor that regulates genes via E-box elements in their promoters. We used multiple high-throughput approaches, including chromatin immunoprecipitation-based systematic analyses and DNA microarrays combined with bioinformatics, to generate genome-wide profiles of BMAL1 target genes. We reveal that, in addition to E-boxes, the CCAATG element contributes to elicit robust circadian expression. BMAL1 occupancy is found in more than 150 sites, including all known clock genes. Importantly, a significant proportion of BMAL1 targets include genes that encode central regulators of metabolic processes. The database generated in this study constitutes a useful resource to decipher the network of circadian gene control and its intimate links with several fundamental physiological functions. {\textcopyright} 2010, American Society for Microbiology.",

keywords = "transcription factor ARNTL, animal, article, Bagg albino mouse, biological rhythm, biology, cell line, chromatin immunoprecipitation, circadian rhythm, energy metabolism, gene expression profiling, gene expression regulation, genetics, genome, high throughput screening, male, metabolism, methodology, microarray analysis, mouse, mouse mutant, physiology, Animals, ARNTL Transcription Factors, Biological Clocks, Cell Line, Chromatin Immunoprecipitation, Circadian Rhythm, Computational Biology, Energy Metabolism, Gene Expression Profiling, Gene Expression Regulation, Genome, High-Throughput Screening Assays, Male, Mice, Mice, Inbred BALB C, Mice, Knockout, Microarray Analysis",

author = "F. Hatanaka and C. Matsubara and J. Myung and T. Yoritaka and N. Kamimura and S. Tsutsumi and A. Kanai and Y. Suzuki and P. Sassone-Corsi and H. Aburatani and S. Sugano and T. Takumi",

note = "引用次數:61 Export Date: 18 September 2018 CODEN: MCEBD 通訊地址: Takumi, T.; Laboratory of Integrative Bioscience, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami, Hiroshima 734-8553, Japan; 電子郵件: takumi@hiroshima-u.ac.jp 化學物質/CAS: ARNTL Transcription Factors 參考文獻: Akashi, M., Ichise, T., Mamine, T., Takumi, T., Molecular mechanism of cell-autonomous circadian gene expression of Period2, a crucial regulator of the mammalian circadian clock (2006) Mol. Biol. Cell, 17, pp. 555-565; Akashi, M., Takumi, T., The orphan nuclear receptor ROR regulates circadian transcription of the mammalian core-clock Bmal1 (2005) Nat. Struct. Mol. Biol., 12, pp. 441-448; Akhtar, R.A., Reddy, A.B., Maywood, E.S., Clayton, J.D., King, V.M., Smith, A.G., Gant, T.W., Kyriacou, C.P., Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus (2002) Curr. Biol., 12, pp. 540-550; Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Zhao, K., High-resolution profiling of histone methylations in the human genome (2007) Cell, 129, pp. 823-837; Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L.A., Hogenesch, J.B., Simon, M.C., Bradfield, C.A., Mop3 is an essential component of the master circadian pacemaker in mammals (2000) Cell, 103, pp. 1009-1017; Canaple, L., Rambaud, J., Dkhissi-Benyahya, O., Rayet, B., Tan, N.S., Michalik, L., Delaunay, F., Laudet, V., Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferatoractivated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock (2006) Mol. Endocrinol., 20, pp. 1715-1727; Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V.B., Wong, E., Ng, H.H., Integration of external signaling pathways with the core transcriptional network in embryonic stem cells (2008) Cell, 133, pp. 1106-1117; Doi, M., Hirayama, J., Sassone-Corsi, P., Circadian regulator CLOCK is a histone acetyltransferase (2006) Cell, 125, pp. 497-508; Duffield, G.E., Best, J.D., Meurers, B.H., Bittner, A., Loros, J.J., Dunlap, J.C., Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells (2002) Curr. Biol., 12, pp. 551-557; Eckel-Mahan, K., Sassone-Corsi, P., Metabolism control by the circadian clock and vice versa (2009) Nat. Struct. Mol. Biol., 16, pp. 462-467; Gekakis, N., Staknis, D., Nguyen, H.B., Davis, F.C., Wilsbacher, L.D., King, D.P., Takahashi, J.S., Weitz, C.J., Role of the CLOCK protein in the mammalian circadian mechanism (1998) Science, 280, pp. 1564-1569; Green, C.B., Takahashi, J.S., Bass, J., The meter of metabolism (2008) Cell, 134, pp. 728-742; Hastings, M.H., Reddy, A.B., Maywood, E.S., A clockwork web: circadian timing in brain and periphery, in health and disease (2003) Nat. Rev. Neurosci., 4, pp. 649-661; Johnson, D.S., Li, W., Gordon, D.B., Bhattacharjee, A., Curry, B., Ghosh, J., Brizuela, L., Liu, X.S., Systematic evaluation of variability in ChIP-chip experiments using predefined DNA targets (2008) Genome Res., 18, pp. 393-403; Johnson, D.S., Mortazavi, A., Myers, R.M., Wold, B., Genomewide mapping of in vivo protein-DNA interactions (2007) Science, 316, pp. 1497-1502; Johnson, W.E., Li, W., Meyer, C.A., Gottardo, R., Carroll, J.S., Brown, M., Liu, X.S., Model-based analysis of tiling-arrays for ChIP-chip (2006) Proc. Natl. Acad. Sci. U. S. A., 103, pp. 12457-12462; Kim, T.H., Ren, B., Genome-wide analysis of protein-DNA interactions (2006) Annu. Rev. Genomics Hum. Genet., 7, pp. 81-102; Kumaki, Y., Ukai-Tadenuma, M., Uno, K.D., Nishio, J., Masumoto, K.H., Nagano, M., Komori, T., Ueda, H.R., Analysis and synthesis of high-amplitude Cis-elements in the mammalian circadian clock (2008) Proc. Natl. Acad. Sci. U. S. A., 105, pp. 14946-14951; Le Martelot, G., Claudel, T., Gatfield, D., Schaad, O., Kornmann, B., Sasso, G.L., Moschetta, A., Schibler, U., REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis (2009) PLoS Biol., 7, pp. e1000181; Liu, A.C., Lewis, W.G., Kay, S.A., Mammalian circadian signaling networks and therapeutic targets (2007) Nat. Chem. Biol., 3, pp. 630-639; Mitchell, P.J., Tjian, R., Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins (1989) Science, 245, pp. 371-378; Nakahata, Y., Akashi, M., Trcka, D., Yasuda, A., Takumi, T., The in vitro real-time oscillation monitoring system identifies potential entrainment factors for circadian clocks (2006) BMC Mol. Biol., 7, p. 5; Nakahata, Y., Grimaldi, B., Sahar, S., Hirayama, J., Sassone-Corsi, P., Signaling to the circadian clock: plasticity by chromatin remodeling (2007) Curr. Opin. Cell Biol., 19, pp. 230-237; Nakahata, Y., Yoshida, M., Takano, A., Soma, H., Yamamoto, T., Yasuda, A., Nakatsu, T., Takumi, T., A direct repeat of E-box-like elements is required for cell-autonomous circadian rhythm of clock genes (2008) BMC Mol. Biol., 9, p. 1; Nakatani, J., Tamada, K., Hatanaka, F., Ise, S., Ohta, H., Inoue, K., Tomonaga, S., Takumi, T., Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism (2009) Cell, 137, pp. 1235-1246; Panda, S., Antoch, M.P., Miller, B.H., Su, A.I., Schook, A.B., Straume, M., Schultz, P.G., Hogenesch, J.B., Coordinated transcription of key pathways in the mouse by the circadian clock (2002) Cell, 109, pp. 307-320; Pendergast, J.S., Nakamura, W., Friday, R.C., Hatanaka, F., Takumi, T., Yamazaki, S., Robust food anticipatory activity in BMAL1-deficient mice (2009) PLoS One, 4, pp. e4860; Porterfield, V.M., Piontkivska, H., Mintz, E.M., Identification of novel light-induced genes in the suprachiasmatic nucleus (2007) BMC Neurosci., 8, p. 98; 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 (2002) Cell, 110, pp. 251-260; Ptitsyn, A.A., Zvonic, S., Conrad, S.A., Scott, L.K., Mynatt, R.L., Gimble, J.M., Circadian clocks are resounding in peripheral tissues (2006) PLoS Comput. Biol., 2, pp. e16; Reppert, S.M., Weaver, D.R., Coordination of circadian timing in mammals (2002) Nature, 418, pp. 935-941; Ripperger, J.A., Schibler, U., Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions (2006) Nat. Genet., 38, pp. 369-374; Robertson, G., Hirst, M., Bainbridge, M., Bilenky, M., Zhao, Y., Zeng, T., Euskirchen, G., Jones, S., Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing (2007) Nat. Methods, 4, pp. 651-657; 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 (2004) PLoS Biol., 2, pp. e377; Sahar, S., Sassone-Corsi, P., Metabolism and cancer: the circadian clock connection (2009) Nat. Rev. Cancer, 9, pp. 886-896; Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., Mcnamara, P., Naik, K.A., Hogenesch, J.B., A functional genomics strategy reveals Rora as a component of the mammalian circadian clock (2004) Neuron, 43, pp. 527-537; Schibler, U., Sassone-Corsi, P., A web of circadian pacemakers (2002) Cell, 111, pp. 919-922; Storch, K.F., Lipan, O., Leykin, I., Viswanathan, N., Davis, F.C., Wong, W.H., Weitz, C.J., Extensive and divergent circadian gene expression in liver and heart (2002) Nature, 417, pp. 78-83; Storch, K.F., Paz, C., Signorovitch, J., Raviola, E., Pawlyk, B., Li, T., Weitz, C.J., Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information (2007) Cell, 130, pp. 730-741; 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 (2008) Nat. Rev. Genet., 9, pp. 764-775; Tamaru, T., Isojima, Y., van der Horst, G.T., Takei, K., Nagai, K., Takamatsu, K., Nucleocytoplasmic shuttling and phosphorylation of BMAL1 are regulated by circadian clock in cultured fibroblasts (2003) Genes Cells, 8, pp. 973-983; Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M., Sassone-Corsi, P., Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 7728-7733; Tsuchihara, K., Suzuki, Y., Wakaguri, H., Irie, T., Tanimoto, K., Hashimoto, S., Matsushima, K., Sugano, S., Massive transcriptional start site analysis of human genes in hypoxia cells (2009) Nucleic Acids Res., 37, pp. 2249-2263; Tu, B.P., Mcknight, S.L., Metabolic cycles as an underlying basis of biological oscillations (2006) Nat. Rev. Mol. Cell. Biol., 7, pp. 696-701; Turek, F.W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., Mcdearmon, E., Laposky, A., Bass, J., Obesity and metabolic syndrome in circadian Clock mutant mice (2005) Science, 308, pp. 1043-1045; Ueda, H.R., Chen, W., Adachi, A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Hashimoto, S., A transcription factor response element for gene expression during circadian night (2002) Nature, 418, pp. 534-539; Ueda, H.R., Hayashi, S., Chen, W., Sano, M., Machida, M., Shigeyoshi, Y., Iino, M., Hashimoto, S., System-level identification of transcriptional circuits underlying mammalian circadian clocks (2005) Nat. Genet., 37, pp. 187-192; Watanabe, Y., Inoue, K., Okuyama-Yamamoto, A., Nakai, N., Nakatani, J., Nibu, K., Sato, N., Takumi, T., Fezf1 is required for penetration of the basal lamina by olfactory axons to promote olfactory development (2009) J. Comp. Neurol., 515, pp. 565-584; Wendt, K.S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Peters, J.M., Cohesin mediates transcriptional insulation by CCCTC-binding factor (2008) Nature, 451, pp. 796-801; Wijnen, H., Young, M.W., Interplay of circadian clocks and metabolic rhythms (2006) Annu. Rev. Genet., 40, pp. 409-448; Yamada, R., Ueda, H.R., Microarrays: statistical methods for circadian rhythms (2007) Methods Mol. Biol., 362, pp. 245-264; Yamamoto, T., Nakahata, Y., Soma, H., Akashi, M., Mamine, T., Takumi, T., Transcriptional oscillation of canonical clock genes in mouse peripheral tissues (2004) BMC Mol. Biol., 5, p. 18; Yang, X., Downes, M., Yu, R.T., Bookout, A.L., He, W., Straume, M., Mangelsdorf, D.J., Evans, R.M., Nuclear receptor expression links the circadian clock to metabolism (2006) Cell, 126, pp. 801-810; Yin, L., Wu, N., Curtin, J.C., Qatanani, M., Szwergold, N.R., Reid, R.A., Waitt, G.M., Lazar, M.A., Rev-erb, a heme sensor that coordinates metabolic and circadian pathways (2007) Science, 318, pp. 1786-1789; Yoo, S.H., Ko, C.H., Lowrey, P.L., Buhr, E.D., Song, E.J., Chang, S., Yoo, O.J., Takahashi, J.S., A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 2608-2613; Zhang, X., Odom, D.T., Koo, S.H., Conkright, M.D., Canettieri, G., Best, J., Chen, H., Montminy, M., Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 4459-4464",

year = "2010",

doi = "10.1128/MCB.00781-10",

language = "English",

volume = "30",

pages = "5636--5648",

journal = "Molecular and Cellular Biology",

issn = "0270-7306",

publisher = "American Society for Microbiology",

number = "24",

}

TY - JOUR

T1 - Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism

AU - Hatanaka, F.

AU - Matsubara, C.

AU - Myung, J.

AU - Yoritaka, T.

AU - Kamimura, N.

AU - Tsutsumi, S.

AU - Kanai, A.

AU - Suzuki, Y.

AU - Sassone-Corsi, P.

AU - Aburatani, H.

AU - Sugano, S.

AU - Takumi, T.

N1 - 引用次數:61 Export Date: 18 September 2018 CODEN: MCEBD 通訊地址: Takumi, T.; Laboratory of Integrative Bioscience, Graduate School of Biomedical Sciences, Hiroshima University, 1-2-3 Kasumi, Minami, Hiroshima 734-8553, Japan; 電子郵件: takumi@hiroshima-u.ac.jp 化學物質/CAS: ARNTL Transcription Factors 參考文獻: Akashi, M., Ichise, T., Mamine, T., Takumi, T., Molecular mechanism of cell-autonomous circadian gene expression of Period2, a crucial regulator of the mammalian circadian clock (2006) Mol. Biol. Cell, 17, pp. 555-565; Akashi, M., Takumi, T., The orphan nuclear receptor ROR regulates circadian transcription of the mammalian core-clock Bmal1 (2005) Nat. Struct. Mol. Biol., 12, pp. 441-448; Akhtar, R.A., Reddy, A.B., Maywood, E.S., Clayton, J.D., King, V.M., Smith, A.G., Gant, T.W., Kyriacou, C.P., Circadian cycling of the mouse liver transcriptome, as revealed by cDNA microarray, is driven by the suprachiasmatic nucleus (2002) Curr. Biol., 12, pp. 540-550; Barski, A., Cuddapah, S., Cui, K., Roh, T.Y., Schones, D.E., Wang, Z., Wei, G., Zhao, K., High-resolution profiling of histone methylations in the human genome (2007) Cell, 129, pp. 823-837; Bunger, M.K., Wilsbacher, L.D., Moran, S.M., Clendenin, C., Radcliffe, L.A., Hogenesch, J.B., Simon, M.C., Bradfield, C.A., Mop3 is an essential component of the master circadian pacemaker in mammals (2000) Cell, 103, pp. 1009-1017; Canaple, L., Rambaud, J., Dkhissi-Benyahya, O., Rayet, B., Tan, N.S., Michalik, L., Delaunay, F., Laudet, V., Reciprocal regulation of brain and muscle Arnt-like protein 1 and peroxisome proliferatoractivated receptor alpha defines a novel positive feedback loop in the rodent liver circadian clock (2006) Mol. Endocrinol., 20, pp. 1715-1727; Chen, X., Xu, H., Yuan, P., Fang, F., Huss, M., Vega, V.B., Wong, E., Ng, H.H., Integration of external signaling pathways with the core transcriptional network in embryonic stem cells (2008) Cell, 133, pp. 1106-1117; Doi, M., Hirayama, J., Sassone-Corsi, P., Circadian regulator CLOCK is a histone acetyltransferase (2006) Cell, 125, pp. 497-508; Duffield, G.E., Best, J.D., Meurers, B.H., Bittner, A., Loros, J.J., Dunlap, J.C., Circadian programs of transcriptional activation, signaling, and protein turnover revealed by microarray analysis of mammalian cells (2002) Curr. Biol., 12, pp. 551-557; Eckel-Mahan, K., Sassone-Corsi, P., Metabolism control by the circadian clock and vice versa (2009) Nat. Struct. Mol. Biol., 16, pp. 462-467; Gekakis, N., Staknis, D., Nguyen, H.B., Davis, F.C., Wilsbacher, L.D., King, D.P., Takahashi, J.S., Weitz, C.J., Role of the CLOCK protein in the mammalian circadian mechanism (1998) Science, 280, pp. 1564-1569; Green, C.B., Takahashi, J.S., Bass, J., The meter of metabolism (2008) Cell, 134, pp. 728-742; Hastings, M.H., Reddy, A.B., Maywood, E.S., A clockwork web: circadian timing in brain and periphery, in health and disease (2003) Nat. Rev. Neurosci., 4, pp. 649-661; Johnson, D.S., Li, W., Gordon, D.B., Bhattacharjee, A., Curry, B., Ghosh, J., Brizuela, L., Liu, X.S., Systematic evaluation of variability in ChIP-chip experiments using predefined DNA targets (2008) Genome Res., 18, pp. 393-403; Johnson, D.S., Mortazavi, A., Myers, R.M., Wold, B., Genomewide mapping of in vivo protein-DNA interactions (2007) Science, 316, pp. 1497-1502; Johnson, W.E., Li, W., Meyer, C.A., Gottardo, R., Carroll, J.S., Brown, M., Liu, X.S., Model-based analysis of tiling-arrays for ChIP-chip (2006) Proc. Natl. Acad. Sci. U. S. A., 103, pp. 12457-12462; Kim, T.H., Ren, B., Genome-wide analysis of protein-DNA interactions (2006) Annu. Rev. Genomics Hum. Genet., 7, pp. 81-102; Kumaki, Y., Ukai-Tadenuma, M., Uno, K.D., Nishio, J., Masumoto, K.H., Nagano, M., Komori, T., Ueda, H.R., Analysis and synthesis of high-amplitude Cis-elements in the mammalian circadian clock (2008) Proc. Natl. Acad. Sci. U. S. A., 105, pp. 14946-14951; Le Martelot, G., Claudel, T., Gatfield, D., Schaad, O., Kornmann, B., Sasso, G.L., Moschetta, A., Schibler, U., REV-ERBalpha participates in circadian SREBP signaling and bile acid homeostasis (2009) PLoS Biol., 7, pp. e1000181; Liu, A.C., Lewis, W.G., Kay, S.A., Mammalian circadian signaling networks and therapeutic targets (2007) Nat. Chem. Biol., 3, pp. 630-639; Mitchell, P.J., Tjian, R., Transcriptional regulation in mammalian cells by sequence-specific DNA binding proteins (1989) Science, 245, pp. 371-378; Nakahata, Y., Akashi, M., Trcka, D., Yasuda, A., Takumi, T., The in vitro real-time oscillation monitoring system identifies potential entrainment factors for circadian clocks (2006) BMC Mol. Biol., 7, p. 5; Nakahata, Y., Grimaldi, B., Sahar, S., Hirayama, J., Sassone-Corsi, P., Signaling to the circadian clock: plasticity by chromatin remodeling (2007) Curr. Opin. Cell Biol., 19, pp. 230-237; Nakahata, Y., Yoshida, M., Takano, A., Soma, H., Yamamoto, T., Yasuda, A., Nakatsu, T., Takumi, T., A direct repeat of E-box-like elements is required for cell-autonomous circadian rhythm of clock genes (2008) BMC Mol. Biol., 9, p. 1; Nakatani, J., Tamada, K., Hatanaka, F., Ise, S., Ohta, H., Inoue, K., Tomonaga, S., Takumi, T., Abnormal behavior in a chromosome-engineered mouse model for human 15q11-13 duplication seen in autism (2009) Cell, 137, pp. 1235-1246; Panda, S., Antoch, M.P., Miller, B.H., Su, A.I., Schook, A.B., Straume, M., Schultz, P.G., Hogenesch, J.B., Coordinated transcription of key pathways in the mouse by the circadian clock (2002) Cell, 109, pp. 307-320; Pendergast, J.S., Nakamura, W., Friday, R.C., Hatanaka, F., Takumi, T., Yamazaki, S., Robust food anticipatory activity in BMAL1-deficient mice (2009) PLoS One, 4, pp. e4860; Porterfield, V.M., Piontkivska, H., Mintz, E.M., Identification of novel light-induced genes in the suprachiasmatic nucleus (2007) BMC Neurosci., 8, p. 98; 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 (2002) Cell, 110, pp. 251-260; Ptitsyn, A.A., Zvonic, S., Conrad, S.A., Scott, L.K., Mynatt, R.L., Gimble, J.M., Circadian clocks are resounding in peripheral tissues (2006) PLoS Comput. Biol., 2, pp. e16; Reppert, S.M., Weaver, D.R., Coordination of circadian timing in mammals (2002) Nature, 418, pp. 935-941; Ripperger, J.A., Schibler, U., Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions (2006) Nat. Genet., 38, pp. 369-374; Robertson, G., Hirst, M., Bainbridge, M., Bilenky, M., Zhao, Y., Zeng, T., Euskirchen, G., Jones, S., Genome-wide profiles of STAT1 DNA association using chromatin immunoprecipitation and massively parallel sequencing (2007) Nat. Methods, 4, pp. 651-657; 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 (2004) PLoS Biol., 2, pp. e377; Sahar, S., Sassone-Corsi, P., Metabolism and cancer: the circadian clock connection (2009) Nat. Rev. Cancer, 9, pp. 886-896; Sato, T.K., Panda, S., Miraglia, L.J., Reyes, T.M., Rudic, R.D., Mcnamara, P., Naik, K.A., Hogenesch, J.B., A functional genomics strategy reveals Rora as a component of the mammalian circadian clock (2004) Neuron, 43, pp. 527-537; Schibler, U., Sassone-Corsi, P., A web of circadian pacemakers (2002) Cell, 111, pp. 919-922; Storch, K.F., Lipan, O., Leykin, I., Viswanathan, N., Davis, F.C., Wong, W.H., Weitz, C.J., Extensive and divergent circadian gene expression in liver and heart (2002) Nature, 417, pp. 78-83; Storch, K.F., Paz, C., Signorovitch, J., Raviola, E., Pawlyk, B., Li, T., Weitz, C.J., Intrinsic circadian clock of the mammalian retina: importance for retinal processing of visual information (2007) Cell, 130, pp. 730-741; 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 (2008) Nat. Rev. Genet., 9, pp. 764-775; Tamaru, T., Isojima, Y., van der Horst, G.T., Takei, K., Nagai, K., Takamatsu, K., Nucleocytoplasmic shuttling and phosphorylation of BMAL1 are regulated by circadian clock in cultured fibroblasts (2003) Genes Cells, 8, pp. 973-983; Travnickova-Bendova, Z., Cermakian, N., Reppert, S.M., Sassone-Corsi, P., Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity (2002) Proc. Natl. Acad. Sci. U. S. A., 99, pp. 7728-7733; Tsuchihara, K., Suzuki, Y., Wakaguri, H., Irie, T., Tanimoto, K., Hashimoto, S., Matsushima, K., Sugano, S., Massive transcriptional start site analysis of human genes in hypoxia cells (2009) Nucleic Acids Res., 37, pp. 2249-2263; Tu, B.P., Mcknight, S.L., Metabolic cycles as an underlying basis of biological oscillations (2006) Nat. Rev. Mol. Cell. Biol., 7, pp. 696-701; Turek, F.W., Joshu, C., Kohsaka, A., Lin, E., Ivanova, G., Mcdearmon, E., Laposky, A., Bass, J., Obesity and metabolic syndrome in circadian Clock mutant mice (2005) Science, 308, pp. 1043-1045; Ueda, H.R., Chen, W., Adachi, A., Wakamatsu, H., Hayashi, S., Takasugi, T., Nagano, M., Hashimoto, S., A transcription factor response element for gene expression during circadian night (2002) Nature, 418, pp. 534-539; Ueda, H.R., Hayashi, S., Chen, W., Sano, M., Machida, M., Shigeyoshi, Y., Iino, M., Hashimoto, S., System-level identification of transcriptional circuits underlying mammalian circadian clocks (2005) Nat. Genet., 37, pp. 187-192; Watanabe, Y., Inoue, K., Okuyama-Yamamoto, A., Nakai, N., Nakatani, J., Nibu, K., Sato, N., Takumi, T., Fezf1 is required for penetration of the basal lamina by olfactory axons to promote olfactory development (2009) J. Comp. Neurol., 515, pp. 565-584; Wendt, K.S., Yoshida, K., Itoh, T., Bando, M., Koch, B., Schirghuber, E., Tsutsumi, S., Peters, J.M., Cohesin mediates transcriptional insulation by CCCTC-binding factor (2008) Nature, 451, pp. 796-801; Wijnen, H., Young, M.W., Interplay of circadian clocks and metabolic rhythms (2006) Annu. Rev. Genet., 40, pp. 409-448; Yamada, R., Ueda, H.R., Microarrays: statistical methods for circadian rhythms (2007) Methods Mol. Biol., 362, pp. 245-264; Yamamoto, T., Nakahata, Y., Soma, H., Akashi, M., Mamine, T., Takumi, T., Transcriptional oscillation of canonical clock genes in mouse peripheral tissues (2004) BMC Mol. Biol., 5, p. 18; Yang, X., Downes, M., Yu, R.T., Bookout, A.L., He, W., Straume, M., Mangelsdorf, D.J., Evans, R.M., Nuclear receptor expression links the circadian clock to metabolism (2006) Cell, 126, pp. 801-810; Yin, L., Wu, N., Curtin, J.C., Qatanani, M., Szwergold, N.R., Reid, R.A., Waitt, G.M., Lazar, M.A., Rev-erb, a heme sensor that coordinates metabolic and circadian pathways (2007) Science, 318, pp. 1786-1789; Yoo, S.H., Ko, C.H., Lowrey, P.L., Buhr, E.D., Song, E.J., Chang, S., Yoo, O.J., Takahashi, J.S., A noncanonical E-box enhancer drives mouse Period2 circadian oscillations in vivo (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 2608-2613; Zhang, X., Odom, D.T., Koo, S.H., Conkright, M.D., Canettieri, G., Best, J., Chen, H., Montminy, M., Genome-wide analysis of cAMP-response element binding protein occupancy, phosphorylation, and target gene activation in human tissues (2005) Proc. Natl. Acad. Sci. U. S. A., 102, pp. 4459-4464

PY - 2010

Y1 - 2010

N2 - Circadian rhythms are common to most organisms and govern much of homeostasis and physiology. Since a significant fraction of the mammalian genome is controlled by the clock machinery, understanding the genome-wide signaling and epigenetic basis of circadian gene expression is essential. BMAL1 is a critical circadian transcription factor that regulates genes via E-box elements in their promoters. We used multiple high-throughput approaches, including chromatin immunoprecipitation-based systematic analyses and DNA microarrays combined with bioinformatics, to generate genome-wide profiles of BMAL1 target genes. We reveal that, in addition to E-boxes, the CCAATG element contributes to elicit robust circadian expression. BMAL1 occupancy is found in more than 150 sites, including all known clock genes. Importantly, a significant proportion of BMAL1 targets include genes that encode central regulators of metabolic processes. The database generated in this study constitutes a useful resource to decipher the network of circadian gene control and its intimate links with several fundamental physiological functions. © 2010, American Society for Microbiology.

AB - Circadian rhythms are common to most organisms and govern much of homeostasis and physiology. Since a significant fraction of the mammalian genome is controlled by the clock machinery, understanding the genome-wide signaling and epigenetic basis of circadian gene expression is essential. BMAL1 is a critical circadian transcription factor that regulates genes via E-box elements in their promoters. We used multiple high-throughput approaches, including chromatin immunoprecipitation-based systematic analyses and DNA microarrays combined with bioinformatics, to generate genome-wide profiles of BMAL1 target genes. We reveal that, in addition to E-boxes, the CCAATG element contributes to elicit robust circadian expression. BMAL1 occupancy is found in more than 150 sites, including all known clock genes. Importantly, a significant proportion of BMAL1 targets include genes that encode central regulators of metabolic processes. The database generated in this study constitutes a useful resource to decipher the network of circadian gene control and its intimate links with several fundamental physiological functions. © 2010, American Society for Microbiology.

KW - transcription factor ARNTL

KW - animal

KW - article

KW - Bagg albino mouse

KW - biological rhythm

KW - biology

KW - cell line

KW - chromatin immunoprecipitation

KW - circadian rhythm

KW - energy metabolism

KW - gene expression profiling

KW - gene expression regulation

KW - genetics

KW - genome

KW - high throughput screening

KW - male

KW - metabolism

KW - methodology

KW - microarray analysis

KW - mouse

KW - mouse mutant

KW - physiology

KW - Animals

KW - ARNTL Transcription Factors

KW - Biological Clocks

KW - Cell Line

KW - Chromatin Immunoprecipitation

KW - Circadian Rhythm

KW - Computational Biology

KW - Energy Metabolism

KW - Gene Expression Profiling

KW - Gene Expression Regulation

KW - Genome

KW - High-Throughput Screening Assays

KW - Male

KW - Mice

KW - Mice, Inbred BALB C

KW - Mice, Knockout

KW - Microarray Analysis

U2 - 10.1128/MCB.00781-10

DO - 10.1128/MCB.00781-10

M3 - Article

SN - 0270-7306

VL - 30

SP - 5636

EP - 5648

JO - Molecular and Cellular Biology

JF - Molecular and Cellular Biology

IS - 24

ER -

Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism

Abstract

Keywords

Access to Document

Fingerprint

Cite this