Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID

Abstract

General transcription factor TFIID is a key component of RNA polymerase II transcription initiation. Human TFIID is a megadalton-sized complex comprising TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs). TBP binds to core promoter DNA, recognizing the TATA-box. We identified a ternary complex formed by TBP and the histone fold (HF) domain-containing TFIID subunits TAF11 and TAF13. We demonstrate that TAF11/TAF13 competes for TBP binding with TATA-box DNA, and also with the N-terminal domain of TAF1 previously implicated in TATA-box mimicry. In an integrative approach combining crystal coordinates, biochemical analyses and data from cross-linking mass-spectrometry (CLMS), we determine the architecture of the TAF11/TAF13/TBP complex, revealing TAF11/TAF13 interaction with the DNA binding surface of TBP. We identify a highly conserved C-terminal TBP-interaction domain (CTID) in TAF13, which is essential for supporting cell growth. Our results thus have implications for cellular TFIID assembly and suggest a novel regulatory state for TFIID function.

Autoren

Kapil Gupta
Aleksandra A Watson
Tiago Baptista
Elisabeth Scheer
Anna L Chambers
Christine Koehler
Juan Zou
Ima Obong-Ebong
Eaazhisai Kandiah
Arturo Temblador
Adam Round
Eric Forest
Petr Man
Christoph Bieniossek
Ernest D Laue
Edward A Lemke
Juri Rappsilber
Carol V Robinson
Didier Devys
Làszlò Tora
Imre Berger

DOI

10.7554/elife.30395

eISSN

2050-084X

Zeitschrift

eLife

Sprache

en

Online publication date

2017

Status

Published online

Herausgeber

eLife Sciences Publications, Ltd

Herausgeber URL

http://dx.doi.org/10.7554/elife.30395

Datum der Datenerfassung

2023

Titel

Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID

Ausgabe der Zeitschrift

6

Datenquelle: Crossref

Abstract

General transcription factor TFIID is a key component of RNA polymerase II transcription initiation. Human TFIID is a megadalton-sized complex comprising TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs). TBP binds to core promoter DNA, recognizing the TATA-box. We identified a ternary complex formed by TBP and the histone fold (HF) domain-containing TFIID subunits TAF11 and TAF13. We demonstrate that TAF11/TAF13 competes for TBP binding with TATA-box DNA, and also with the N-terminal domain of TAF1 previously implicated in TATA-box mimicry. In an integrative approach combining crystal coordinates, biochemical analyses and data from cross-linking mass-spectrometry (CLMS), we determine the architecture of the TAF11/TAF13/TBP complex, revealing TAF11/TAF13 interaction with the DNA binding surface of TBP. We identify a highly conserved C-terminal TBP-interaction domain (CTID) in TAF13, which is essential for supporting cell growth. Our results thus have implications for cellular TFIID assembly and suggest a novel regulatory state for TFIID function.

Addresses

BrisSynBio Centre, The School of Biochemistry, Faculty of Biomedical Sciences, University of Bristol, Bristol, United Kingdom.

Autoren

Kapil Gupta
Aleksandra A Watson
Tiago Baptista
Elisabeth Scheer
Anna L Chambers
Christine Koehler
Juan Zou
Ima Obong-Ebong
Eaazhisai Kandiah
Arturo Temblador
Adam Round
Eric Forest
Petr Man
Christoph Bieniossek
Ernest D Laue
Edward A Lemke
Juri Rappsilber
Carol V Robinson
Didier Devys
Làszlò Tora
Imre Berger

DOI

10.7554/elife.30395

eISSN

2050-084X

Externe Identifier

PubMed Identifier: 29111974
PubMed Central ID: PMC5690282

Funding acknowledgements

Wellcome Trust: 108504
Cancer Research UK: 17506
European Research Council: 340551
Wellcome Trust: Senior Research Fellowship 10313
Wellcome Trust: 103139/Z/13/Z
Biotechnology and Biological Sciences Research Council: BB/L01386X/1
Wellcome Trust: 10313
Agence Nationale de la Recherche: ANR-13-BSV8-0021-03
European Research Council: ERC-2013-340551
Baden-Württemberg Stiftung:
Research Councils UK:
Wellcome Trust: 092076
Wellcome Trust: 106115/Z/14/Z
Wellcome Trust:
Wellcome Trust: 103139

Open access

true

ISSN

2050-084X

Zeitschrift

eLife

Schlüsselwörter

Humans
TATA-Binding Protein Associated Factors
TATA-Box Binding Protein
Transcription Factor TFIID
DNA
Crystallography, X-Ray
Protein Interaction Mapping
Protein Conformation
Protein Binding
Histone Acetyltransferases
Mass Spectrometry
Promoter Regions, Genetic

Sprache

eng

Medium

Electronic

Online publication date

2017

Open access status

Open Access

Paginierung

e30395

Datum der Veröffentlichung

2017

Status

Published

Publisher licence

CC BY

Datum der Datenerfassung

2017

Titel

Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID.

Sub types

Research Support, Non-U.S. Gov't
research-article
Journal Article

Ausgabe der Zeitschrift

6

Files

https://europepmc.org/articles/PMC5690282?pdf=render

Datenquelle: Europe PubMed Central

Abstract

General transcription factor TFIID is a key component of RNA polymerase II transcription initiation. Human TFIID is a megadalton-sized complex comprising TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs). TBP binds to core promoter DNA, recognizing the TATA-box. We identified a ternary complex formed by TBP and the histone fold (HF) domain-containing TFIID subunits TAF11 and TAF13. We demonstrate that TAF11/TAF13 competes for TBP binding with TATA-box DNA, and also with the N-terminal domain of TAF1 previously implicated in TATA-box mimicry. In an integrative approach combining crystal coordinates, biochemical analyses and data from cross-linking mass-spectrometry (CLMS), we determine the architecture of the TAF11/TAF13/TBP complex, revealing TAF11/TAF13 interaction with the DNA binding surface of TBP. We identify a highly conserved C-terminal TBP-interaction domain (CTID) in TAF13, which is essential for supporting cell growth. Our results thus have implications for cellular TFIID assembly and suggest a novel regulatory state for TFIID function.

Date of acceptance

2017

Autoren

Kapil Gupta
Aleksandra A Watson
Tiago Baptista
Elisabeth Scheer
Anna L Chambers
Christine Koehler
Juan Zou
Ima Obong-Ebong
Eaazhisai Kandiah
Arturo Temblador
Adam Round
Eric Forest
Petr Man
Christoph Bieniossek
Ernest D Laue
Edward A Lemke
Juri Rappsilber
Carol V Robinson
Didier Devys
Làszlò Tora
Imre Berger

Autoren-URL

https://www.ncbi.nlm.nih.gov/pubmed/29111974

DOI

10.7554/eLife.30395

eISSN

2050-084X

Externe Identifier

PubMed Central ID: PMC5690282

Funding acknowledgements

Biotechnology and Biological Sciences Research Council: BB/L01386X/1
Cancer Research UK: 17506
Wellcome Trust: 103139/Z/13/Z
Wellcome Trust: 10313
European Research Council: 340551
Wellcome Trust: 108504
Wellcome Trust: 092076
Wellcome Trust: 103139
Wellcome Trust:

Zeitschrift

Elife

Schlüsselwörter

S. cerevisiae
TBP associated factors
TFIID
biochemistry
biophysics
core promoter DNA
gene regulation
histone fold domain
human
structural biology
transcription factors
Crystallography, X-Ray
DNA
Histone Acetyltransferases
Humans
Mass Spectrometry
Promoter Regions, Genetic
Protein Binding
Protein Conformation
Protein Interaction Mapping
TATA-Binding Protein Associated Factors
TATA-Box Binding Protein
Transcription Factor TFIID

Sprache

eng

Country

England

PII

30395

Datum der Veröffentlichung

2017

Status

Published online

Datum, an dem der Datensatz öffentlich gemacht wurde

2018

Titel

Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID.

Sub types

Journal Article
Research Support, Non-U.S. Gov't

Ausgabe der Zeitschrift

6

Datenquelle: PubMed

Architecture of TAF11/TAF13/TBP complex suggests novel regulation properties of general transcription factor TFIID

Files

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