Cited by 121Genomics and Chromatin DynamicsChromatin Remodeling and CancerPeroxisome Proliferator-Activated Receptors

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Transcription factor assisted loading and enhancer dynamics dictate the hepatic fasting response

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Goldstein, Ido, Baek, Songjoon, Presman, Diego M., Paakinaho, Ville, Swinstead, Erin E., Hager, Gordon L.·2017·Genome Research

DOI 10.1101/gr.212175.116PMC PMC5340970

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Abstract

Fasting elicits transcriptional programs in hepatocytes leading to glucose and ketone production. This transcriptional program is regulated by many transcription factors (TFs). To understand how this complex network regulates the metabolic response to fasting, we aimed at isolating the enhancers and TFs dictating it. Measuring chromatin accessibility revealed that fasting massively reorganizes liver chromatin, exposing numerous fasting-induced enhancers. By utilizing computational methods in combination with dissecting enhancer features and TF cistromes, we implicated four key TFs regulating the fasting response: glucocorticoid receptor (GR), cAMP responsive element binding protein 1 (CREB1), peroxisome proliferator activated receptor alpha (PPARA), and CCAAT/enhancer binding protein beta (CEBPB). These TFs regulate fuel production by two distinctly operating modules, each controlling a separate metabolic pathway. The gluconeogenic module operates through assisted loading, whereby GR doubles the number of sites occupied by CREB1 as well as enhances CREB1 binding intensity and increases accessibility of CREB1 binding sites. Importantly, this GR-assisted CREB1 binding was enhancer-selective and did not affect all CREB1-bound enhancers. Single-molecule tracking revealed that GR increases the number and DNA residence time of a portion of chromatin-bound CREB1 molecules. These events collectively result in rapid synergistic gene expression and higher hepatic glucose production. Conversely, the ketogenic module operates via a GR-induced TF cascade, whereby PPARA levels are increased following GR activation, facilitating gradual enhancer maturation next to PPARA target genes and delayed ketogenic gene expression. Our findings reveal a complex network of enhancers and TFs that dynamically cooperate to restore homeostasis upon fasting.

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Authors: Goldstein, I., Baek, S., Presman, D. M., Paakinaho, V., Swinstead, E. E., & Hager, G. L.
Affiliations: National Institutes of Health (US)
ORCID: Goldstein, Ido
Baek, Songjoon
Presman, Diego M.
Paakinaho, Ville
Hager, Gordon L.
Venue: Genome Research
Publisher: Cold Spring Harbor Laboratory
Published: 2016-12-28
Volume: 27
Issue: 3
Pages: 427-439
ISSN: 1088-9051 (ISSN-L)
1549-5469
DOI: 10.1101/gr.212175.116
PMC: PMC5340970
OpenAlex: W2566710076
Cited by: 121
References: 51
Citations by year: 2026: 11 · 2025: 9 · 2024: 17 · 2023: 16 · 2022: 15 · 2021: 13 · 2020: 14 · 2019: 11 · 2018: 6 · 2017: 9
Type: posted content
Language: en
Open access: hybrid
doi.org
Licence: cc-by-nc
Locations: Genome Research (publishedVersion, cc-by-nc)
Europe PMC (PubMed Central) (publishedVersion, cc-by-nc)
PubMed Central (publishedVersion, cc-by-nc)
PubMed (publishedVersion)
Americanae (AECID Library) (submittedVersion, cc-by-nc-sa)
HighWire Press Open Archive (submittedVersion)
LA Referencia (Red Federada de Repositorios Institucionales de Publicaciones Científicas) (submittedVersion, cc-by-nc-sa)
Funders: National Institutes of Health
National Cancer Institute
Center for Cancer Research
Sigrid Jusélius Foundation
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Peroxisome Proliferator-Activated Receptors
Keywords: fasting response, hepatic glucose production, ketogenesis, transcription factors, enhancer dynamics, chromatin accessibility, glucocorticoid receptor, CREB1, PPARα, CEBPB, single-molecule tracking, hepatic metabolism
MeSH terms: Animals, Binding Sites, Chromatin, Enhancer Elements, Genetic, Fasting, Glucose, Ketones, Male, Mice, Inbred C57BL, Receptors, Glucocorticoid, Transcriptional Activation, Cyclic AMP Response Element-Binding Protein, Hepatocytes, CCAAT-Enhancer-Binding Protein-beta, Chromatin Assembly and Disassembly, PPAR alpha, Mice

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Transcription factor assisted loading and enhancer dynamics dictate the hepatic fasting response

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