High-resolution and high-accuracy topographic and transcriptional maps of the nucleosome barrier.

E. coli epigenetic modifications high-resolution optical tweezers histone ubiquitination histone variant H2A.Z human molecular biophysics nucleosome transcription structural biology transcription regulation xenopus

Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
31 07 2019
Historique:
received: 08 05 2019
accepted: 30 07 2019
pubmed: 1 8 2019
medline: 31 1 2020
entrez: 1 8 2019
Statut: epublish

Résumé

Nucleosomes represent mechanical and energetic barriers that RNA Polymerase II (Pol II) must overcome during transcription. A high-resolution description of the barrier topography, its modulation by epigenetic modifications, and their effects on Pol II nucleosome crossing dynamics, is still missing. Here, we obtain topographic and transcriptional (Pol II residence time) maps of canonical, H2A.Z, and monoubiquitinated H2B (uH2B) nucleosomes at near base-pair resolution and accuracy. Pol II crossing dynamics are complex, displaying pauses at specific loci, backtracking, and nucleosome hopping between wrapped states. While H2A.Z widens the barrier, uH2B heightens it, and both modifications greatly lengthen Pol II crossing time. Using the dwell times of Pol II at each nucleosomal position we extract the energetics of the barrier. The orthogonal barrier modifications of H2A.Z and uH2B, and their effects on Pol II dynamics rationalize their observed enrichment in +1 nucleosomes and suggest a mechanism for selective control of gene expression.

Identifiants

pubmed: 31364986
doi: 10.7554/eLife.48281
pii: 48281
pmc: PMC6744274
doi:
pii:

Substances chimiques

Histones 0
Nucleosomes 0
RNA Polymerase II EC 2.7.7.-

Banques de données

Dryad
['10.5061/dryad.8sb6h8n']

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NIGMS NIH HHS
ID : R01GM098401
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM098401
Pays : United States
Organisme : Alfred P. Sloan Foundation
ID : FG-2018-10394
Pays : International
Organisme : NIGMS NIH HHS
ID : R01 GM032543
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM097260
Pays : United States
Organisme : Burroughs Wellcome Fund
ID : Collaborative Research Travel Grant
Pays : International
Organisme : NIGMS NIH HHS
ID : R01 GM097260
Pays : United States
Organisme : Basic Energy Sciences
ID : Nanomachine Program under Contract DE-AC02-05CH11231
Pays : International
Organisme : NIGMS NIH HHS
ID : R01GM071552
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01 GM071552
Pays : United States
Organisme : NIGMS NIH HHS
ID : R01GM032543
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

© 2019, Chen et al.

Déclaration de conflit d'intérêts

ZC, RG, AB, AL, AS, CD, CK, EK, TY, CB No competing interests declared

Références

Genes Dev. 2011 Nov 1;25(21):2254-65
pubmed: 22056671
Mol Cell. 2014 Mar 6;53(5):819-30
pubmed: 24606920
Sci Adv. 2015 Aug 7;1(7):
pubmed: 26269799
Methods Enzymol. 2004;375:23-44
pubmed: 14870657
Nat Methods. 2011 Apr;8(4):335-40
pubmed: 21336286
Mol Cell. 2002 Mar;9(3):541-52
pubmed: 11931762
Cell. 2012 Nov 9;151(4):738-749
pubmed: 23141536
Nat Commun. 2018 Dec 21;9(1):5432
pubmed: 30575770
Elife. 2019 Jul 31;8:
pubmed: 31364986
Structure. 2008 Feb;16(2):166-79
pubmed: 18275809
Nucleic Acids Res. 2012 Nov;40(21):10719-41
pubmed: 23002134
Methods Mol Biol. 2017;1486:183-256
pubmed: 27844430
Cell. 2015 Mar 12;160(6):1135-44
pubmed: 25768909
Proc Natl Acad Sci U S A. 2018 Feb 06;115(6):1286-1291
pubmed: 29351994
Nat Commun. 2013;4:2579
pubmed: 24113677
Biophys J. 1997 Mar;72(3):1335-46
pubmed: 9138579
Science. 1996 Feb 9;271(5250):795-9
pubmed: 8628994
Mol Cell Biol. 2011 May;31(9):1848-60
pubmed: 21357739
J Mol Biol. 1999 Jan 8;285(1):245-57
pubmed: 9878403
Cell. 2006 Jun 16;125(6):1083-94
pubmed: 16777599
Mol Cell. 2007 Jul 20;27(2):275-88
pubmed: 17643376
Science. 2018 Nov 2;362(6414):595-598
pubmed: 30287617
Nat Commun. 2018 Jul 26;9(1):2930
pubmed: 30050038
Nat Struct Mol Biol. 2009 Feb;16(2):124-9
pubmed: 19136959
Nat Commun. 2016 Sep 22;7:12958
pubmed: 27653784
Mol Cell. 2017 Dec 21;68(6):1038-1053.e4
pubmed: 29225036
Anal Biochem. 2016 Mar 1;496:71-5
pubmed: 26706802
Mol Cell. 2018 Jul 19;71(2):284-293.e4
pubmed: 30029006
Cell. 2005 Oct 21;123(2):219-31
pubmed: 16239141
Science. 1994 Sep 9;265(5178):1599-600
pubmed: 8079175
Methods Enzymol. 2003;370:138-55
pubmed: 14712640
Mol Cell Biol. 2003 Nov;23(22):8323-33
pubmed: 14585989
Proc Natl Acad Sci U S A. 2013 May 7;110(19):7654-9
pubmed: 23610384
Proc Natl Acad Sci U S A. 2006 Oct 24;103(43):15871-6
pubmed: 17043216
Nat Struct Mol Biol. 2018 Jan;25(1):101-108
pubmed: 29323273
Proc Natl Acad Sci U S A. 2016 Nov 8;113(45):12733-12738
pubmed: 27791062
Nat Genet. 2017 Jul;49(7):1045-1051
pubmed: 28504701
Nature. 1999 Jun 17;399(6737):694-7
pubmed: 10385122
Science. 2003 Aug 22;301(5636):1090-3
pubmed: 12934006
Proc Natl Acad Sci U S A. 2009 Sep 29;106(39):16686-91
pubmed: 19805358
Nucleic Acids Res. 2014 Jul;42(13):8767-76
pubmed: 24990379
Phys Rev E Stat Nonlin Soft Matter Phys. 2012 Jul;86(1 Pt 1):011906
pubmed: 23005451
Biophys J. 1999 Jan;76(1 Pt 1):409-13
pubmed: 9876152
J Mol Biol. 1998 Feb 13;276(1):19-42
pubmed: 9514715
Science. 2009 Jul 31;325(5940):626-8
pubmed: 19644123
Cell. 2010 Jan 22;140(2):183-95
pubmed: 20141833
Science. 2019 Feb 15;363(6428):744-747
pubmed: 30733384
Mol Cell. 2006 Nov 3;24(3):469-79
pubmed: 17081995
Nature. 1997 Sep 18;389(6648):251-60
pubmed: 9305837
Methods. 2014 Dec;70(2-3):134-8
pubmed: 25063569
Elife. 2013 Sep 24;2:e00971
pubmed: 24066225
Science. 1992 Nov 13;258(5085):1122-6
pubmed: 1439819
Cold Spring Harb Protoc. 2009 Oct;2009(10):pdb.top60
pubmed: 20147062
Trends Biochem Sci. 2014 Dec;39(12):577-86
pubmed: 25455758
Cell. 2014 Dec 4;159(6):1377-88
pubmed: 25480300
Biophys J. 2009 Oct 21;97(8):2128-36
pubmed: 19843445
J Biol Chem. 2004 Jun 4;279(23):24274-82
pubmed: 15020582

Auteurs

Zhijie Chen (Z)

Institute for Quantitative Biosciences-QB3, University of California, Berkeley, Berkeley, United States.
Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States.

Ronen Gabizon (R)

Institute for Quantitative Biosciences-QB3, University of California, Berkeley, Berkeley, United States.

Aidan I Brown (AI)

Department of Physics, University of California, San Diego, San Diego, United States.

Antony Lee (A)

Department of Physics, University of California, Berkeley, Berkeley, United States.

Aixin Song (A)

Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, United States.

César Díaz-Celis (C)

Institute for Quantitative Biosciences-QB3, University of California, Berkeley, Berkeley, United States.
Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States.

Craig D Kaplan (CD)

Department of Biological Sciences, University of Pittsburgh, Pittsburgh, United States.

Elena F Koslover (EF)

Department of Physics, University of California, San Diego, San Diego, United States.

Tingting Yao (T)

Department of Biochemistry and Molecular Biology, Colorado State University, Fort Collins, United States.

Carlos Bustamante (C)

Institute for Quantitative Biosciences-QB3, University of California, Berkeley, Berkeley, United States.
Howard Hughes Medical Institute, University of California, Berkeley, Berkeley, United States.
Department of Physics, University of California, Berkeley, Berkeley, United States.
Jason L Choy Laboratory of Single-Molecule Biophysics, University of California, Berkeley, Berkeley, United States.
Biophysics Graduate Group, University of California, Berkeley, Berkeley, United States.
Department of Molecular & Cell Biology, University of California, Berkeley, Berkeley, United States.
Department of Chemistry, University of California, Berkeley, Berkeley, United States.
Kavli Energy Nanoscience Institute, University of California, Berkeley, Berkeley, United States.

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