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 journalArticle

73 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 languageEnglish
Pages (from-to)5636-5648
Number of pages13
JournalMolecular and Cellular Biology
Volume30
Issue number24
DOIs
Publication statusPublished - 2010

Fingerprint

ARNTL Transcription Factors
E-Box Elements
Genome
Genes
Gene Regulatory Networks
Chromatin Immunoprecipitation
Circadian Rhythm
Microbiology
Oligonucleotide Array Sequence Analysis
Computational Biology
Epigenomics
Homeostasis
Transcription Factors
Databases
Gene Expression

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

Cite this

Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. / Hatanaka, F.; Matsubara, C.; Myung, J.; Yoritaka, T.; Kamimura, N.; Tsutsumi, S.; Kanai, A.; Suzuki, Y.; Sassone-Corsi, P.; Aburatani, H.; Sugano, S.; Takumi, T.

In: Molecular and Cellular Biology, Vol. 30, No. 24, 2010, p. 5636-5648.

Research output: Contribution to journalArticle

Hatanaka, F, Matsubara, C, Myung, J, Yoritaka, T, Kamimura, N, Tsutsumi, S, Kanai, A, Suzuki, Y, Sassone-Corsi, P, Aburatani, H, Sugano, S & Takumi, T 2010, 'Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism', Molecular and Cellular Biology, vol. 30, no. 24, pp. 5636-5648. https://doi.org/10.1128/MCB.00781-10
Hatanaka, F. ; Matsubara, C. ; Myung, J. ; Yoritaka, T. ; Kamimura, N. ; Tsutsumi, S. ; Kanai, A. ; Suzuki, Y. ; Sassone-Corsi, P. ; Aburatani, H. ; Sugano, S. ; Takumi, T. / Genome-wide profiling of the core clock protein BMAL1 targets reveals a strict relationship with metabolism. In: Molecular and Cellular Biology. 2010 ; Vol. 30, No. 24. pp. 5636-5648.
@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. {\circledC} 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. 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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. 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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

VL - 30

SP - 5636

EP - 5648

JO - Molecular and Cellular Biology

JF - Molecular and Cellular Biology

SN - 0270-7306

IS - 24

ER -