Cargando…

MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation

The MYC oncoprotein binds to promoter-proximal regions of virtually all transcribed genes and enhances RNA polymerase II (Pol II) function, but its precise mode of action is poorly understood. Using mass spectrometry of both MYC and Pol II complexes, we show here that MYC controls the assembly of Po...

Descripción completa

Detalles Bibliográficos
Autores principales: Baluapuri, Apoorva, Hofstetter, Julia, Dudvarski Stankovic, Nevenka, Endres, Theresa, Bhandare, Pranjali, Vos, Seychelle Monique, Adhikari, Bikash, Schwarz, Jessica Denise, Narain, Ashwin, Vogt, Markus, Wang, Shuang-Yan, Düster, Robert, Jung, Lisa Anna, Vanselow, Jens Thorsten, Wiegering, Armin, Geyer, Matthias, Maric, Hans Michael, Gallant, Peter, Walz, Susanne, Schlosser, Andreas, Cramer, Patrick, Eilers, Martin, Wolf, Elmar
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Cell Press 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527870/
https://www.ncbi.nlm.nih.gov/pubmed/30928206
http://dx.doi.org/10.1016/j.molcel.2019.02.031
_version_ 1783420102047170560
author Baluapuri, Apoorva
Hofstetter, Julia
Dudvarski Stankovic, Nevenka
Endres, Theresa
Bhandare, Pranjali
Vos, Seychelle Monique
Adhikari, Bikash
Schwarz, Jessica Denise
Narain, Ashwin
Vogt, Markus
Wang, Shuang-Yan
Düster, Robert
Jung, Lisa Anna
Vanselow, Jens Thorsten
Wiegering, Armin
Geyer, Matthias
Maric, Hans Michael
Gallant, Peter
Walz, Susanne
Schlosser, Andreas
Cramer, Patrick
Eilers, Martin
Wolf, Elmar
author_facet Baluapuri, Apoorva
Hofstetter, Julia
Dudvarski Stankovic, Nevenka
Endres, Theresa
Bhandare, Pranjali
Vos, Seychelle Monique
Adhikari, Bikash
Schwarz, Jessica Denise
Narain, Ashwin
Vogt, Markus
Wang, Shuang-Yan
Düster, Robert
Jung, Lisa Anna
Vanselow, Jens Thorsten
Wiegering, Armin
Geyer, Matthias
Maric, Hans Michael
Gallant, Peter
Walz, Susanne
Schlosser, Andreas
Cramer, Patrick
Eilers, Martin
Wolf, Elmar
author_sort Baluapuri, Apoorva
collection PubMed
description The MYC oncoprotein binds to promoter-proximal regions of virtually all transcribed genes and enhances RNA polymerase II (Pol II) function, but its precise mode of action is poorly understood. Using mass spectrometry of both MYC and Pol II complexes, we show here that MYC controls the assembly of Pol II with a small set of transcription elongation factors that includes SPT5, a subunit of the elongation factor DSIF. MYC directly binds SPT5, recruits SPT5 to promoters, and enables the CDK7-dependent transfer of SPT5 onto Pol II. Consistent with known functions of SPT5, MYC is required for fast and processive transcription elongation. Intriguingly, the high levels of MYC that are expressed in tumors sequester SPT5 into non-functional complexes, thereby decreasing the expression of growth-suppressive genes. Altogether, these results argue that MYC controls the productive assembly of processive Pol II elongation complexes and provide insight into how oncogenic levels of MYC permit uncontrolled cellular growth.
format Online
Article
Text
id pubmed-6527870
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher Cell Press
record_format MEDLINE/PubMed
spelling pubmed-65278702019-05-28 MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation Baluapuri, Apoorva Hofstetter, Julia Dudvarski Stankovic, Nevenka Endres, Theresa Bhandare, Pranjali Vos, Seychelle Monique Adhikari, Bikash Schwarz, Jessica Denise Narain, Ashwin Vogt, Markus Wang, Shuang-Yan Düster, Robert Jung, Lisa Anna Vanselow, Jens Thorsten Wiegering, Armin Geyer, Matthias Maric, Hans Michael Gallant, Peter Walz, Susanne Schlosser, Andreas Cramer, Patrick Eilers, Martin Wolf, Elmar Mol Cell Article The MYC oncoprotein binds to promoter-proximal regions of virtually all transcribed genes and enhances RNA polymerase II (Pol II) function, but its precise mode of action is poorly understood. Using mass spectrometry of both MYC and Pol II complexes, we show here that MYC controls the assembly of Pol II with a small set of transcription elongation factors that includes SPT5, a subunit of the elongation factor DSIF. MYC directly binds SPT5, recruits SPT5 to promoters, and enables the CDK7-dependent transfer of SPT5 onto Pol II. Consistent with known functions of SPT5, MYC is required for fast and processive transcription elongation. Intriguingly, the high levels of MYC that are expressed in tumors sequester SPT5 into non-functional complexes, thereby decreasing the expression of growth-suppressive genes. Altogether, these results argue that MYC controls the productive assembly of processive Pol II elongation complexes and provide insight into how oncogenic levels of MYC permit uncontrolled cellular growth. Cell Press 2019-05-16 /pmc/articles/PMC6527870/ /pubmed/30928206 http://dx.doi.org/10.1016/j.molcel.2019.02.031 Text en © 2019 The Author(s) http://creativecommons.org/licenses/by/4.0/ This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Baluapuri, Apoorva
Hofstetter, Julia
Dudvarski Stankovic, Nevenka
Endres, Theresa
Bhandare, Pranjali
Vos, Seychelle Monique
Adhikari, Bikash
Schwarz, Jessica Denise
Narain, Ashwin
Vogt, Markus
Wang, Shuang-Yan
Düster, Robert
Jung, Lisa Anna
Vanselow, Jens Thorsten
Wiegering, Armin
Geyer, Matthias
Maric, Hans Michael
Gallant, Peter
Walz, Susanne
Schlosser, Andreas
Cramer, Patrick
Eilers, Martin
Wolf, Elmar
MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title_full MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title_fullStr MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title_full_unstemmed MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title_short MYC Recruits SPT5 to RNA Polymerase II to Promote Processive Transcription Elongation
title_sort myc recruits spt5 to rna polymerase ii to promote processive transcription elongation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6527870/
https://www.ncbi.nlm.nih.gov/pubmed/30928206
http://dx.doi.org/10.1016/j.molcel.2019.02.031
work_keys_str_mv AT baluapuriapoorva mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT hofstetterjulia mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT dudvarskistankovicnevenka mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT endrestheresa mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT bhandarepranjali mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT vosseychellemonique mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT adhikaribikash mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT schwarzjessicadenise mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT narainashwin mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT vogtmarkus mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT wangshuangyan mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT dusterrobert mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT junglisaanna mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT vanselowjensthorsten mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT wiegeringarmin mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT geyermatthias mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT marichansmichael mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT gallantpeter mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT walzsusanne mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT schlosserandreas mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT cramerpatrick mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT eilersmartin mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation
AT wolfelmar mycrecruitsspt5tornapolymeraseiitopromoteprocessivetranscriptionelongation