Home LiteratureArticle Details
PMID: 19940241 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

Time of feeding and the intrinsic circadian clock drive rhythms in hepatic gene expression.

Vollmers C, Gill S, DiTacchio L, Pulivarthy SR, Le HD, Panda S

Abstract

In mammals, the circadian oscillator generates approximately 24-h rhythms in feeding behavior, even under constant environmental conditions. Livers of mice held under constant darkness exhibit circadian rhythm in abundance in up to 15% of expressed transcripts. Therefore, oscillations in hepatic transcripts could be driven by rhythmic food intake or sustained by the hepatic circadian oscillator, or a combination of both. To address this question, we used distinct feeding and fasting paradigms on wild-type (WT) and circadian clock-deficient mice. We monitored temporal patterns of feeding and hepatic transcription. Both food availability and the temporal pattern of feeding determined the repertoire, phase, and amplitude of the circadian transcriptome in WT liver. In the absence of feeding, only a small subset of transcripts continued to express circadian patterns. Conversely, temporally restricted feeding restored rhythmic transcription of hundreds of genes in oscillator-deficient mouse liver. Our findings show that both temporal pattern of food intake and the circadian clock drive rhythmic transcription, thereby highlighting temporal regulation of hepatic transcription as an emergent property of the circadian system.

MeSH Terms
Animals Circadian Rhythm/genetics Eating/genetics Gene Expression Profiling Gene Expression Regulation Liver/metabolism Male Mice Mice, Inbred C57BL RNA, Messenger/analysis Time Factors
Chemicals
RNA, Messenger
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Vollmers Christopher
Regulatory Biology Laboratory, Salk Institute for Biological Studies, 10010 North Torrey Pines Road, La Jolla, CA 92037, USA.
Gill Shubhroz
DiTacchio Luciano
Pulivarthy Sandhya R
Le Hiep D
Panda Satchidananda
References (40)
40 references, click to expand
  1. Impact of behavior on central and peripheral circadian clocks in the common vole Microtus arvalis, a mammal with ultradian rhythms.
    Proc Natl Acad Sci U S A. 2006 Feb 28;103(9):3393-8 PMID: 16481616
  2. Transcriptional regulation by the phosphorylation-dependent factor CREB.
    Nat Rev Mol Cell Biol. 2001 Aug;2(8):599-609 PMID: 11483993
  3. The transcriptomic signature of fasting murine liver.
    BMC Genomics. 2008 Nov 06;9:528 PMID: 18990241
  4. The circadian system in higher plants.
    Annu Rev Plant Biol. 2009;60:357-77 PMID: 19575587
  5. Combined analysis of oligonucleotide microarray data from transgenic and knockout mice identifies direct SREBP target genes.
    Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12027-32 PMID: 14512514
  6. Entrainment of the circadian clock in the liver by feeding.
    Science. 2001 Jan 19;291(5503):490-3 PMID: 11161204
  7. Restricted feeding uncouples circadian oscillators in peripheral tissues from the central pacemaker in the suprachiasmatic nucleus.
    Genes Dev. 2000 Dec 1;14(23):2950-61 PMID: 11114885
  8. Genome-wide analysis of CREB target genes reveals a core promoter requirement for cAMP responsiveness.
    Mol Cell. 2003 Apr;11(4):1101-8 PMID: 12718894
  9. High-resolution time course analysis of gene expression from pituitary.
    Cold Spring Harb Symp Quant Biol. 2007;72:381-6 PMID: 18419295
  10. Characterization of motifs which are critical for activity of the cyclic AMP-responsive transcription factor CREB.
    Mol Cell Biol. 1991 Mar;11(3):1306-12 PMID: 1671708
  11. Entrainment to feeding but not to light: circadian phenotype of VPAC2 receptor-null mice.
    J Neurosci. 2007 Apr 18;27(16):4351-8 PMID: 17442819
  12. BMAL1 and CLOCK, two essential components of the circadian clock, are involved in glucose homeostasis.
    PLoS Biol. 2004 Nov;2(11):e377 PMID: 15523558
  13. Effects of fasting and re-feeding on the expression of Dec1, Per1, and other clock-related genes.
    J Biochem. 2006 Sep;140(3):401-8 PMID: 16873396
  14. Regulation of histone methylation by demethylimination and demethylation.
    Nat Rev Mol Cell Biol. 2007 Apr;8(4):307-18 PMID: 17342184
  15. Sirtuins as potential targets for metabolic syndrome.
    Nature. 2006 Dec 14;444(7121):868-74 PMID: 17167475
  16. A serum shock induces circadian gene expression in mammalian tissue culture cells.
    Cell. 1998 Jun 12;93(6):929-37 PMID: 9635423
  17. Bimodal regulation of mPeriod promoters by CREB-dependent signaling and CLOCK/BMAL1 activity.
    Proc Natl Acad Sci U S A. 2002 May 28;99(11):7728-33 PMID: 12032351
  18. A fasting inducible switch modulates gluconeogenesis via activator/coactivator exchange.
    Nature. 2008 Nov 13;456(7219):269-73 PMID: 18849969
  19. Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.
    Science. 2000 Dec 15;290(5499):2110-3 PMID: 11118138
  20. System-driven and oscillator-dependent circadian transcription in mice with a conditionally active liver clock.
    PLoS Biol. 2007 Feb;5(2):e34 PMID: 17298173
  21. Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development.
    Genome Biol. 2008;9(8):R130 PMID: 18710561
  22. Genetics of the mammalian circadian system: Photic entrainment, circadian pacemaker mechanisms, and posttranslational regulation.
    Annu Rev Genet. 2000;34:533-562 PMID: 11092838
  23. Mammalian circadian biology: elucidating genome-wide levels of temporal organization.
    Annu Rev Genomics Hum Genet. 2004;5:407-41 PMID: 15485355
  24. Circadian and CLOCK-controlled regulation of the mouse transcriptome and cell proliferation.
    Proc Natl Acad Sci U S A. 2007 Feb 27;104(9):3342-7 PMID: 17360649
  25. Obesity and metabolic syndrome in circadian Clock mutant mice.
    Science. 2005 May 13;308(5724):1043-5 PMID: 15845877
  26. Physiological significance of a peripheral tissue circadian clock.
    Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15172-7 PMID: 18779586
  27. Coordination of circadian timing in mammals.
    Nature. 2002 Aug 29;418(6901):935-41 PMID: 12198538
  28. Differential display of DNA-binding proteins reveals heat-shock factor 1 as a circadian transcription factor.
    Genes Dev. 2008 Feb 1;22(3):331-45 PMID: 18245447
  29. ATP-citrate lyase links cellular metabolism to histone acetylation.
    Science. 2009 May 22;324(5930):1076-80 PMID: 19461003
  30. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  31. Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A.
    Mol Cell Biol. 1993 Aug;13(8):4852-9 PMID: 8336722
  32. Circadian gene expression is resilient to large fluctuations in overall transcription rates.
    EMBO J. 2009 Jan 21;28(2):123-34 PMID: 19078963
  33. High-fat diet disrupts behavioral and molecular circadian rhythms in mice.
    Cell Metab. 2007 Nov;6(5):414-21 PMID: 17983587
  34. Coordinated transcription of key pathways in the mouse by the circadian clock.
    Cell. 2002 May 3;109(3):307-20 PMID: 12015981
  35. FoxO1 regulates multiple metabolic pathways in the liver: effects on gluconeogenic, glycolytic, and lipogenic gene expression.
    J Biol Chem. 2006 Apr 14;281(15):10105-17 PMID: 16492665
  36. Mechanism of activation of protein kinase B by insulin and IGF-1.
    EMBO J. 1996 Dec 2;15(23):6541-51 PMID: 8978681
  37. Harmonics of circadian gene transcription in mammals.
    PLoS Genet. 2009 Apr;5(4):e1000442 PMID: 19343201
  38. DNA microarray time series analysis: automated statistical assessment of circadian rhythms in gene expression patterning.
    Methods Enzymol. 2004;383:149-66 PMID: 15063650
  39. Genome-wide expression analysis of mouse liver reveals CLOCK-regulated circadian output genes.
    J Biol Chem. 2003 Oct 17;278(42):41519-27 PMID: 12865428
  40. The suprachiasmatic nucleus controls the daily variation of plasma glucose via the autonomic output to the liver: are the clock genes involved?
    Eur J Neurosci. 2005 Nov;22(10):2531-40 PMID: 16307595
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-12-15
Epub
2009-00-25
Pages
21453-8
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2795502
Subset
IM
Grants
NIGMS NIH HHS · F32 GM082083 · United States
NEI NIH HHS · R01 EY016807 · United States
NEI NIH HHS · EY016807 · United States
NIGMS NIH HHS · 1F32GM082083-01 · United States
Databases
GEO
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com