Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions

Erin E Swinstead, Tina B Miranda, Ville Paakinaho, Songjoon Baek, Ido Goldstein, Mary Hawkins, Tatiana S Karpova, David Ball, Davide Mazza, Luke D Lavis, Jonathan B Grimm, Tatsuya Morisaki, Lars Grøntved, Diego M Presman, Gordon L Hager

Research output: Contribution to journalJournal articleResearchpeer-review

Abstract

The estrogen receptor (ER), glucocorticoid receptor (GR), and forkhead box protein 1 (FoxA1) are significant factors in breast cancer progression. FoxA1 has been implicated in establishing ER-binding patterns though its unique ability to serve as a pioneer factor. However, the molecular interplay between ER, GR, and FoxA1 requires further investigation. Here we show that ER and GR both have the ability to alter the genomic distribution of the FoxA1 pioneer factor. Single-molecule tracking experiments in live cells reveal a highly dynamic interaction of FoxA1 with chromatin in vivo. Furthermore, the FoxA1 factor is not associated with detectable footprints at its binding sites throughout the genome. These findings support a model wherein interactions between transcription factors and pioneer factors are highly dynamic. Moreover, at a subset of genomic sites, the role of pioneer can be reversed, with the steroid receptors serving to enhance binding of FoxA1.

Original languageEnglish
JournalCell
Volume165
Issue number3
Pages (from-to)593-605
ISSN0092-8674
DOIs
Publication statusPublished - 21. Apr 2016
Externally publishedYes

Fingerprint

Steroid Receptors
Estrogen Receptors
Chromatin
Glucocorticoid Receptors
Forkhead Transcription Factors
Transcription Factors
Genes
Binding Sites
Molecules
Experiments

Keywords

  • Journal Article

Cite this

Swinstead, E. E., Miranda, T. B., Paakinaho, V., Baek, S., Goldstein, I., Hawkins, M., ... Hager, G. L. (2016). Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. Cell, 165(3), 593-605. https://doi.org/10.1016/j.cell.2016.02.067
Swinstead, Erin E ; Miranda, Tina B ; Paakinaho, Ville ; Baek, Songjoon ; Goldstein, Ido ; Hawkins, Mary ; Karpova, Tatiana S ; Ball, David ; Mazza, Davide ; Lavis, Luke D ; Grimm, Jonathan B ; Morisaki, Tatsuya ; Grøntved, Lars ; Presman, Diego M ; Hager, Gordon L. / Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. In: Cell. 2016 ; Vol. 165, No. 3. pp. 593-605.
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abstract = "The estrogen receptor (ER), glucocorticoid receptor (GR), and forkhead box protein 1 (FoxA1) are significant factors in breast cancer progression. FoxA1 has been implicated in establishing ER-binding patterns though its unique ability to serve as a pioneer factor. However, the molecular interplay between ER, GR, and FoxA1 requires further investigation. Here we show that ER and GR both have the ability to alter the genomic distribution of the FoxA1 pioneer factor. Single-molecule tracking experiments in live cells reveal a highly dynamic interaction of FoxA1 with chromatin in vivo. Furthermore, the FoxA1 factor is not associated with detectable footprints at its binding sites throughout the genome. These findings support a model wherein interactions between transcription factors and pioneer factors are highly dynamic. Moreover, at a subset of genomic sites, the role of pioneer can be reversed, with the steroid receptors serving to enhance binding of FoxA1.",
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Swinstead, EE, Miranda, TB, Paakinaho, V, Baek, S, Goldstein, I, Hawkins, M, Karpova, TS, Ball, D, Mazza, D, Lavis, LD, Grimm, JB, Morisaki, T, Grøntved, L, Presman, DM & Hager, GL 2016, 'Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions', Cell, vol. 165, no. 3, pp. 593-605. https://doi.org/10.1016/j.cell.2016.02.067

Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. / Swinstead, Erin E; Miranda, Tina B; Paakinaho, Ville; Baek, Songjoon; Goldstein, Ido; Hawkins, Mary; Karpova, Tatiana S; Ball, David; Mazza, Davide; Lavis, Luke D; Grimm, Jonathan B; Morisaki, Tatsuya; Grøntved, Lars; Presman, Diego M; Hager, Gordon L.

In: Cell, Vol. 165, No. 3, 21.04.2016, p. 593-605.

Research output: Contribution to journalJournal articleResearchpeer-review

TY - JOUR

T1 - Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions

AU - Swinstead, Erin E

AU - Miranda, Tina B

AU - Paakinaho, Ville

AU - Baek, Songjoon

AU - Goldstein, Ido

AU - Hawkins, Mary

AU - Karpova, Tatiana S

AU - Ball, David

AU - Mazza, Davide

AU - Lavis, Luke D

AU - Grimm, Jonathan B

AU - Morisaki, Tatsuya

AU - Grøntved, Lars

AU - Presman, Diego M

AU - Hager, Gordon L

N1 - Copyright © 2016 Elsevier Inc. All rights reserved.

PY - 2016/4/21

Y1 - 2016/4/21

N2 - The estrogen receptor (ER), glucocorticoid receptor (GR), and forkhead box protein 1 (FoxA1) are significant factors in breast cancer progression. FoxA1 has been implicated in establishing ER-binding patterns though its unique ability to serve as a pioneer factor. However, the molecular interplay between ER, GR, and FoxA1 requires further investigation. Here we show that ER and GR both have the ability to alter the genomic distribution of the FoxA1 pioneer factor. Single-molecule tracking experiments in live cells reveal a highly dynamic interaction of FoxA1 with chromatin in vivo. Furthermore, the FoxA1 factor is not associated with detectable footprints at its binding sites throughout the genome. These findings support a model wherein interactions between transcription factors and pioneer factors are highly dynamic. Moreover, at a subset of genomic sites, the role of pioneer can be reversed, with the steroid receptors serving to enhance binding of FoxA1.

AB - The estrogen receptor (ER), glucocorticoid receptor (GR), and forkhead box protein 1 (FoxA1) are significant factors in breast cancer progression. FoxA1 has been implicated in establishing ER-binding patterns though its unique ability to serve as a pioneer factor. However, the molecular interplay between ER, GR, and FoxA1 requires further investigation. Here we show that ER and GR both have the ability to alter the genomic distribution of the FoxA1 pioneer factor. Single-molecule tracking experiments in live cells reveal a highly dynamic interaction of FoxA1 with chromatin in vivo. Furthermore, the FoxA1 factor is not associated with detectable footprints at its binding sites throughout the genome. These findings support a model wherein interactions between transcription factors and pioneer factors are highly dynamic. Moreover, at a subset of genomic sites, the role of pioneer can be reversed, with the steroid receptors serving to enhance binding of FoxA1.

KW - Journal Article

U2 - 10.1016/j.cell.2016.02.067

DO - 10.1016/j.cell.2016.02.067

M3 - Journal article

C2 - 27062924

VL - 165

SP - 593

EP - 605

JO - Cell

JF - Cell

SN - 0092-8674

IS - 3

ER -

Swinstead EE, Miranda TB, Paakinaho V, Baek S, Goldstein I, Hawkins M et al. Steroid receptors reprogram FoxA1 occupancy through dynamic chromatin transitions. Cell. 2016 Apr 21;165(3):593-605. https://doi.org/10.1016/j.cell.2016.02.067