Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules

Simon Trowitzsch; Cristina Viola; Elisabeth  Scheer; Sascha Conic; Virginie Chavant; Marjorie Fournier; Gabor Papai; Ima-Obong Ebong; Christiane Schaffitzel; Juan  Zou; Matthias Haffke; Juri Rappsilber; Carol V. Robinson; Patrick Schultz; Laszlo Tora; Imre Berger

doi:10.1038/ncomms7011

Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules

Simon Trowitzsch, Cristina Viola, Elisabeth Scheer, Sascha Conic, Virginie Chavant, Marjorie Fournier, Gabor Papai, Ima-Obong Ebong, Christiane Schaffitzel, Juan Zou, Matthias Haffke, Juri Rappsilber, Carol V. Robinson, Patrick Schultz, Laszlo Tora, Imre Berger

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Abstract

General transcription factor TFIID is a cornerstone of RNA polymerase II transcription initiation in eukaryotic cells. How human TFIID-a megadalton-sized multiprotein complex composed of the TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs)-assembles into a functional transcription factor is poorly understood. Here we describe a heterotrimeric TFIID subcomplex consisting of the TAF2, TAF8 and TAF10 proteins, which assembles in the cytoplasm. Using native mass spectrometry, we define the interactions between the TAFs and uncover a central role for TAF8 in nucleating the complex. X-ray crystallography reveals a non-canonical arrangement of the TAF8-TAF10 histone fold domains. TAF2 binds to multiple motifs within the TAF8 C-terminal region, and these interactions dictate TAF2 incorporation into a core-TFIID complex that exists in the nucleus. Our results provide evidence for a stepwise assembly pathway of nuclear holo-TFIID, regulated by nuclear import of preformed cytoplasmic submodules.

Original language	English
Article number	6011
Number of pages	14
Journal	Nature Communications
Volume	6
DOIs	https://doi.org/10.1038/ncomms7011
Publication status	Published - 14 Jan 2015

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This is the final published version of the article (version of record). It first appeared online via Nature at http://www.nature.com/ncomms/2015/150114/ncomms7011/full/ncomms7011.html. Please refer to any applicable terms of use of the publisher.
Final published version, 2.88 MBLicence: CC BY

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Professor Imre Berger
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- School of Biochemistry - Professor of Biochemistry
- Infection and Immunity
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Trowitzsch, S., Viola, C., Scheer, E., Conic, S., Chavant, V., Fournier, M., Papai, G., Ebong, I.-O., Schaffitzel, C., Zou, J., Haffke, M., Rappsilber, J., Robinson, C. V., Schultz, P., Tora, L., & Berger, I. (2015). Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules. Nature Communications, 6, Article 6011. https://doi.org/10.1038/ncomms7011

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title = "Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules",

abstract = "General transcription factor TFIID is a cornerstone of RNA polymerase II transcription initiation in eukaryotic cells. How human TFIID-a megadalton-sized multiprotein complex composed of the TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs)-assembles into a functional transcription factor is poorly understood. Here we describe a heterotrimeric TFIID subcomplex consisting of the TAF2, TAF8 and TAF10 proteins, which assembles in the cytoplasm. Using native mass spectrometry, we define the interactions between the TAFs and uncover a central role for TAF8 in nucleating the complex. X-ray crystallography reveals a non-canonical arrangement of the TAF8-TAF10 histone fold domains. TAF2 binds to multiple motifs within the TAF8 C-terminal region, and these interactions dictate TAF2 incorporation into a core-TFIID complex that exists in the nucleus. Our results provide evidence for a stepwise assembly pathway of nuclear holo-TFIID, regulated by nuclear import of preformed cytoplasmic submodules.",

author = "Simon Trowitzsch and Cristina Viola and Elisabeth Scheer and Sascha Conic and Virginie Chavant and Marjorie Fournier and Gabor Papai and Ima-Obong Ebong and Christiane Schaffitzel and Juan Zou and Matthias Haffke and Juri Rappsilber and Robinson, {Carol V.} and Patrick Schultz and Laszlo Tora and Imre Berger",

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doi = "10.1038/ncomms7011",

language = "English",

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Trowitzsch, S, Viola, C, Scheer, E, Conic, S, Chavant, V, Fournier, M, Papai, G, Ebong, I-O, Schaffitzel, C, Zou, J, Haffke, M, Rappsilber, J, Robinson, CV, Schultz, P, Tora, L & Berger, I 2015, 'Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules', Nature Communications, vol. 6, 6011. https://doi.org/10.1038/ncomms7011

TY - JOUR

T1 - Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules

AU - Trowitzsch, Simon

AU - Viola, Cristina

AU - Scheer, Elisabeth

AU - Conic, Sascha

AU - Chavant, Virginie

AU - Fournier, Marjorie

AU - Papai, Gabor

AU - Ebong, Ima-Obong

AU - Schaffitzel, Christiane

AU - Zou, Juan

AU - Haffke, Matthias

AU - Rappsilber, Juri

AU - Robinson, Carol V.

AU - Schultz, Patrick

AU - Tora, Laszlo

AU - Berger, Imre

PY - 2015/1/14

Y1 - 2015/1/14

N2 - General transcription factor TFIID is a cornerstone of RNA polymerase II transcription initiation in eukaryotic cells. How human TFIID-a megadalton-sized multiprotein complex composed of the TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs)-assembles into a functional transcription factor is poorly understood. Here we describe a heterotrimeric TFIID subcomplex consisting of the TAF2, TAF8 and TAF10 proteins, which assembles in the cytoplasm. Using native mass spectrometry, we define the interactions between the TAFs and uncover a central role for TAF8 in nucleating the complex. X-ray crystallography reveals a non-canonical arrangement of the TAF8-TAF10 histone fold domains. TAF2 binds to multiple motifs within the TAF8 C-terminal region, and these interactions dictate TAF2 incorporation into a core-TFIID complex that exists in the nucleus. Our results provide evidence for a stepwise assembly pathway of nuclear holo-TFIID, regulated by nuclear import of preformed cytoplasmic submodules.

AB - General transcription factor TFIID is a cornerstone of RNA polymerase II transcription initiation in eukaryotic cells. How human TFIID-a megadalton-sized multiprotein complex composed of the TATA-binding protein (TBP) and 13 TBP-associated factors (TAFs)-assembles into a functional transcription factor is poorly understood. Here we describe a heterotrimeric TFIID subcomplex consisting of the TAF2, TAF8 and TAF10 proteins, which assembles in the cytoplasm. Using native mass spectrometry, we define the interactions between the TAFs and uncover a central role for TAF8 in nucleating the complex. X-ray crystallography reveals a non-canonical arrangement of the TAF8-TAF10 histone fold domains. TAF2 binds to multiple motifs within the TAF8 C-terminal region, and these interactions dictate TAF2 incorporation into a core-TFIID complex that exists in the nucleus. Our results provide evidence for a stepwise assembly pathway of nuclear holo-TFIID, regulated by nuclear import of preformed cytoplasmic submodules.

U2 - 10.1038/ncomms7011

DO - 10.1038/ncomms7011

M3 - Article (Academic Journal)

C2 - 25586196

SN - 2041-1723

VL - 6

JO - Nature Communications

JF - Nature Communications

M1 - 6011

ER -

Cytoplasmic TAF2-TAF8-TAF10 complex provides evidence for nuclear holo-TFIID assembly from preformed submodules

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