TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage

Changwei Yu; Nevena Cvetesic; Vincent Hisler; Kapil Gupta; Tao Ye; Emese Gazdag; Luc Negroni; Petra Hajkova; Imre Berger; Boris Lenhard; Ferenc Müller; Stéphane D. Vincent; László Tora

doi:10.1038/s41467-020-20239-4

TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage

Changwei Yu, Nevena Cvetesic, Vincent Hisler, Kapil Gupta, Tao Ye, Emese Gazdag, Luc Negroni, Petra Hajkova, Imre Berger, Boris Lenhard, Ferenc Müller, Stéphane D. Vincent^*, László Tora

^*Corresponding author for this work

Cancer and Genomic Sciences

Research output: Contribution to journal › Article › peer-review

5 Citations (Scopus)

Abstract

During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence. During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. We show that in oocytes TBPL2 does not assemble into a canonical TFIID complex. Our transcript analyses demonstrate that TBPL2 mediates transcription of oocyte-expressed genes, including mRNA survey genes, as well as specific endogenous retroviral elements. Transcription start site (TSS) mapping indicates that TBPL2 has a strong preference for TATA-like motif in core promoters driving sharp TSS selection, in contrast with canonical TBP/TFIID-driven TATA-less promoters that have broader TSS architecture. Thus, we show a role for the TBPL2/TFIIA complex in the establishment of the oocyte transcriptome by using a specific TSS recognition code.

Original language	English
Article number	6439
Journal	Nature Communications
Volume	11
Issue number	1
DOIs	https://doi.org/10.1038/s41467-020-20239-4
Publication status	Published - Dec 2020

Bibliographical note

Funding Information:
We thank D. Singer and A. Gegonne for the gift of the Taf7flox mouse line and H. Stunnenberg for TFIIA antibodies. We would also like to thank D. Devys for critically reading the manuscript, all members of the Tora lab for thoughtful discussions and suggestions throughout the course of the work. We are grateful to I. Kukhtevich, M. Borsos, M.E. Torres Padilla, T. Gupta, L. Casini, G. Barzaghi and A. Krebs for help in preliminary experiments, and A.H.F.M. Peters for suggestions on the analysis of the retrotransposon data. We thank C. Hérouard and M. Jung from the GenomEAST platform for library preparation and preliminary analyses, P. Eberling for peptide synthesis, F. Ruffenach for proteomic analyses, G. Duval for polyclonal antibody generation, the histology platform, the IGBMC cell culture facility and S. Falcone, M. Poirot and F. Memedov of the IGBMC animal facility for animal care taking. This work was supported by funds from CNRS, INSERM, and Strasbourg University. This study was also supported by the European Research Council (ERC) Advanced grant (ERC-2013-340551, Birtoaction) (to LT) and grant ANR-10-LABX-0030-INRT and a French State fund managed by the Agence Nationale de la Recherche under the frame program Investissements d’Avenir ANR-10-IDEX-0002-02 (to IGBMC). IB and FM acknowledge support by Wellcome Trust Senior Investigator awards (106115/Z/14/Z and 106955/Z/ 15/Z, respectively).

Publisher Copyright:
© 2020, The Author(s).

ASJC Scopus subject areas

Chemistry(all)
Biochemistry, Genetics and Molecular Biology(all)
Physics and Astronomy(all)

Access to Document

10.1038/s41467-020-20239-4

Cite this

@article{ee4d795fe4704750a544b88a8cd1e422,

title = "TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage",

abstract = "During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence. During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. We show that in oocytes TBPL2 does not assemble into a canonical TFIID complex. Our transcript analyses demonstrate that TBPL2 mediates transcription of oocyte-expressed genes, including mRNA survey genes, as well as specific endogenous retroviral elements. Transcription start site (TSS) mapping indicates that TBPL2 has a strong preference for TATA-like motif in core promoters driving sharp TSS selection, in contrast with canonical TBP/TFIID-driven TATA-less promoters that have broader TSS architecture. Thus, we show a role for the TBPL2/TFIIA complex in the establishment of the oocyte transcriptome by using a specific TSS recognition code.",

author = "Changwei Yu and Nevena Cvetesic and Vincent Hisler and Kapil Gupta and Tao Ye and Emese Gazdag and Luc Negroni and Petra Hajkova and Imre Berger and Boris Lenhard and Ferenc M{\"u}ller and Vincent, {St{\'e}phane D.} and L{\'a}szl{\'o} Tora",

note = "Funding Information: We thank D. Singer and A. Gegonne for the gift of the Taf7flox mouse line and H. Stunnenberg for TFIIA antibodies. We would also like to thank D. Devys for critically reading the manuscript, all members of the Tora lab for thoughtful discussions and suggestions throughout the course of the work. We are grateful to I. Kukhtevich, M. Borsos, M.E. Torres Padilla, T. Gupta, L. Casini, G. Barzaghi and A. Krebs for help in preliminary experiments, and A.H.F.M. Peters for suggestions on the analysis of the retrotransposon data. We thank C. H{\'e}rouard and M. Jung from the GenomEAST platform for library preparation and preliminary analyses, P. Eberling for peptide synthesis, F. Ruffenach for proteomic analyses, G. Duval for polyclonal antibody generation, the histology platform, the IGBMC cell culture facility and S. Falcone, M. Poirot and F. Memedov of the IGBMC animal facility for animal care taking. This work was supported by funds from CNRS, INSERM, and Strasbourg University. This study was also supported by the European Research Council (ERC) Advanced grant (ERC-2013-340551, Birtoaction) (to LT) and grant ANR-10-LABX-0030-INRT and a French State fund managed by the Agence Nationale de la Recherche under the frame program Investissements d{\textquoteright}Avenir ANR-10-IDEX-0002-02 (to IGBMC). IB and FM acknowledge support by Wellcome Trust Senior Investigator awards (106115/Z/14/Z and 106955/Z/ 15/Z, respectively). Publisher Copyright: {\textcopyright} 2020, The Author(s).",

year = "2020",

month = dec,

doi = "10.1038/s41467-020-20239-4",

language = "English",

volume = "11",

journal = "Nature Communications",

issn = "2041-1723",

publisher = "Springer",

number = "1",

}

TY - JOUR

T1 - TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage

AU - Yu, Changwei

AU - Cvetesic, Nevena

AU - Hisler, Vincent

AU - Gupta, Kapil

AU - Ye, Tao

AU - Gazdag, Emese

AU - Negroni, Luc

AU - Hajkova, Petra

AU - Berger, Imre

AU - Lenhard, Boris

AU - Müller, Ferenc

AU - Vincent, Stéphane D.

AU - Tora, László

N1 - Funding Information: We thank D. Singer and A. Gegonne for the gift of the Taf7flox mouse line and H. Stunnenberg for TFIIA antibodies. We would also like to thank D. Devys for critically reading the manuscript, all members of the Tora lab for thoughtful discussions and suggestions throughout the course of the work. We are grateful to I. Kukhtevich, M. Borsos, M.E. Torres Padilla, T. Gupta, L. Casini, G. Barzaghi and A. Krebs for help in preliminary experiments, and A.H.F.M. Peters for suggestions on the analysis of the retrotransposon data. We thank C. Hérouard and M. Jung from the GenomEAST platform for library preparation and preliminary analyses, P. Eberling for peptide synthesis, F. Ruffenach for proteomic analyses, G. Duval for polyclonal antibody generation, the histology platform, the IGBMC cell culture facility and S. Falcone, M. Poirot and F. Memedov of the IGBMC animal facility for animal care taking. This work was supported by funds from CNRS, INSERM, and Strasbourg University. This study was also supported by the European Research Council (ERC) Advanced grant (ERC-2013-340551, Birtoaction) (to LT) and grant ANR-10-LABX-0030-INRT and a French State fund managed by the Agence Nationale de la Recherche under the frame program Investissements d’Avenir ANR-10-IDEX-0002-02 (to IGBMC). IB and FM acknowledge support by Wellcome Trust Senior Investigator awards (106115/Z/14/Z and 106955/Z/ 15/Z, respectively). Publisher Copyright: © 2020, The Author(s).

PY - 2020/12

Y1 - 2020/12

N2 - During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence. During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. We show that in oocytes TBPL2 does not assemble into a canonical TFIID complex. Our transcript analyses demonstrate that TBPL2 mediates transcription of oocyte-expressed genes, including mRNA survey genes, as well as specific endogenous retroviral elements. Transcription start site (TSS) mapping indicates that TBPL2 has a strong preference for TATA-like motif in core promoters driving sharp TSS selection, in contrast with canonical TBP/TFIID-driven TATA-less promoters that have broader TSS architecture. Thus, we show a role for the TBPL2/TFIIA complex in the establishment of the oocyte transcriptome by using a specific TSS recognition code.

AB - During oocyte growth, transcription is required to create RNA and protein reserves to achieve maternal competence. During this period, the general transcription factor TATA binding protein (TBP) is replaced by its paralogue, TBPL2 (TBP2 or TRF3), which is essential for RNA polymerase II transcription. We show that in oocytes TBPL2 does not assemble into a canonical TFIID complex. Our transcript analyses demonstrate that TBPL2 mediates transcription of oocyte-expressed genes, including mRNA survey genes, as well as specific endogenous retroviral elements. Transcription start site (TSS) mapping indicates that TBPL2 has a strong preference for TATA-like motif in core promoters driving sharp TSS selection, in contrast with canonical TBP/TFIID-driven TATA-less promoters that have broader TSS architecture. Thus, we show a role for the TBPL2/TFIIA complex in the establishment of the oocyte transcriptome by using a specific TSS recognition code.

UR - http://www.scopus.com/inward/record.url?scp=85097935914&partnerID=8YFLogxK

U2 - 10.1038/s41467-020-20239-4

DO - 10.1038/s41467-020-20239-4

M3 - Article

C2 - 33353944

AN - SCOPUS:85097935914

SN - 2041-1723

VL - 11

JO - Nature Communications

JF - Nature Communications

IS - 1

M1 - 6439

ER -

TBPL2/TFIIA complex establishes the maternal transcriptome through oocyte-specific promoter usage

Abstract

Bibliographical note

ASJC Scopus subject areas

Access to Document

Fingerprint

Cite this