Basic helix-loop-helix pioneer factors interact with the histone octamer to invade nucleosomes and generate nucleosome-depleted regions.

Nucleosomes / genetics Histones / metabolism Saccharomyces cerevisiae / genetics Chromatin / metabolism Transcription Factors / genetics Saccharomyces cerevisiae Proteins / genetics Basic Helix-Loop-Helix Leucine Zipper Transcription Factors / genetics
chromatin biology cryoelectron microscopy single-particle analysis dissociation rate compensation mechanism gene regulation nucleosome-depleted regions pioneer transcription factors single-molecule measurement

Journal

Molecular cell
ISSN: 1097-4164
Titre abrégé: Mol Cell
Pays: United States
ID NLM: 9802571

Informations de publication

Date de publication:
20 04 2023
Historique:
received: 09 08 2022
revised: 13 01 2023
accepted: 06 03 2023
pmc-release: 20 04 2024
medline: 25 4 2023
pubmed: 31 3 2023
entrez: 30 3 2023
Statut: ppublish

Résumé

Nucleosomes drastically limit transcription factor (TF) occupancy, while pioneer transcription factors (PFs) somehow circumvent this nucleosome barrier. In this study, we compare nucleosome binding of two conserved S. cerevisiae basic helix-loop-helix (bHLH) TFs, Cbf1 and Pho4. A cryo-EM structure of Cbf1 in complex with the nucleosome reveals that the Cbf1 HLH region can electrostatically interact with exposed histone residues within a partially unwrapped nucleosome. Single-molecule fluorescence studies show that the Cbf1 HLH region facilitates efficient nucleosome invasion by slowing its dissociation rate relative to DNA through interactions with histones, whereas the Pho4 HLH region does not. In vivo studies show that this enhanced binding provided by the Cbf1 HLH region enables nucleosome invasion and ensuing repositioning. These structural, single-molecule, and in vivo studies reveal the mechanistic basis of dissociation rate compensation by PFs and how this translates to facilitating chromatin opening inside cells.

Identifiants

DOI: 10.1016/j.molcel.2023.03.006 PMID: 36996811 PMC: PMC10182836
pubmed: 36996811
pii: S1097-2765(23)00163-6
doi: 10.1016/j.molcel.2023.03.006
pmc: PMC10182836
mid: NIHMS1895324
pii:
doi:

Substances chimiques

Nucleosomes 0
Histones 0
Chromatin 0
Transcription Factors 0
CBF1 protein, S cerevisiae 0
Saccharomyces cerevisiae Proteins 0
Basic Helix-Loop-Helix Leucine Zipper Transcription Factors 0

Types de publication

Journal Article Research Support, U.S. Gov't, Non-P.H.S. Research Support, Non-U.S. Gov't Research Support, N.I.H., Extramural

Langues

eng

Sous-ensembles de citation

IM

Pagination

1251-1263.e6

Subventions

Organisme : NIGMS NIH HHS
ID : R35 GM139564
Pays : United States
Organisme : NIGMS NIH HHS
ID : T32 GM086252
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM121858
Pays : United States
Organisme : NIH HHS
ID : S10 OD026822
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM127034
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM131626
Pays : United States
Organisme : NIGMS NIH HHS
ID : U24 GM129547
Pays : United States
Organisme : NCI NIH HHS
ID : P30 CA016058
Pays : United States
Organisme : NIGMS NIH HHS
ID : R35 GM139654
Pays : United States

Informations de copyright

Copyright © 2023. Published by Elsevier Inc.

Déclaration de conflit d'intérêts

Declaration of interests The authors declare no competing interests.

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Auteurs

Benjamin T Donovan (BT)

Biophysics Graduate Program, The Ohio State University, Columbus, OH 43210, USA.

Hengye Chen (H)

Department of Biochemistry and Molecular Biology, Center for Eukaryotic Gene Regulation, The Pennsylvania State University, University Park, PA 16802, USA.

Priit Eek (P)

Department of Biochemistry and Molecular Biology, Center for Eukaryotic Gene Regulation, The Pennsylvania State University, University Park, PA 16802, USA.

Zhiyuan Meng (Z)

Biophysics Graduate Program, The Ohio State University, Columbus, OH 43210, USA.

Caroline Jipa (C)

Department of Physics, The Ohio State University, Columbus, OH 43210, USA.

Song Tan (S)

Department of Biochemistry and Molecular Biology, Center for Eukaryotic Gene Regulation, The Pennsylvania State University, University Park, PA 16802, USA; Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA 16802, USA. Electronic address: sxt30@psu.edu.

Lu Bai (L)

Department of Biochemistry and Molecular Biology, Center for Eukaryotic Gene Regulation, The Pennsylvania State University, University Park, PA 16802, USA; Department of Physics, The Pennsylvania State University, University Park, PA 16802, USA. Electronic address: lub15@psu.edu.

Michael G Poirier (MG)

Biophysics Graduate Program, The Ohio State University, Columbus, OH 43210, USA; Department of Physics, The Ohio State University, Columbus, OH 43210, USA; Department of Chemistry & Biochemistry, The Ohio State University, Columbus, OH 43210, USA. Electronic address: poirier.18@osu.edu.

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Classifications MeSH

questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Nucléosomes › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Nucléoprotéines › Histone › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Eucaryotes › Champignons › Levures › Saccharomyces › Saccharomyces cerevisiae › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Phénomènes génétiques › Structures génétiques › Structures de chromosome › Chromatine › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines fongiques › Protéines de Saccharomyces cerevisiae › Basic helix-loop-helix pioneer factors...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription à motif basique et à glissière à leucines › Facteurs de transcription à motifs basiques hélice-boucle-hélice et à glissière à leucines › Basic helix-loop-helix pioneer factors...