IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-33433-3.html
   My bibliography  Save this article

The transcriptional coactivator RUVBL2 regulates Pol II clustering with diverse transcription factors

Author

Listed:
  • Hui Wang

    (Peking University
    Chengdu Medical College)

  • Boyuan Li

    (Peking University)

  • Linyu Zuo

    (Peking University)

  • Bo Wang

    (Peking University)

  • Yan Yan

    (Tsinghua University
    Tsinghua University)

  • Kai Tian

    (Peking University)

  • Rong Zhou

    (Peking University)

  • Chenlu Wang

    (Peking University)

  • Xizi Chen

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, Shanghai Medical College of Fudan University)

  • Yongpeng Jiang

    (Peking University)

  • Haonan Zheng

    (Peking University)

  • Fangfei Qin

    (Peking University)

  • Bin Zhang

    (University of Rochester Medical Center)

  • Yang Yu

    (Chinese Academy of Sciences)

  • Chao-Pei Liu

    (Chinese Academy of Sciences)

  • Yanhui Xu

    (Fudan University Shanghai Cancer Center, Institutes of Biomedical Sciences, Shanghai Medical College of Fudan University)

  • Juntao Gao

    (Tsinghua University
    Tsinghua University)

  • Zhi Qi

    (Peking University)

  • Wulan Deng

    (Peking University)

  • Xiong Ji

    (Peking University)

Abstract

RNA polymerase II (Pol II) apparatuses are compartmentalized into transcriptional clusters. Whether protein factors control these clusters remains unknown. In this study, we find that the ATPase-associated with diverse cellular activities (AAA + ) ATPase RUVBL2 co-occupies promoters with Pol II and various transcription factors. RUVBL2 interacts with unphosphorylated Pol II in chromatin to promote RPB1 carboxy-terminal domain (CTD) clustering and transcription initiation. Rapid depletion of RUVBL2 leads to a decrease in the number of Pol II clusters and inhibits nascent RNA synthesis, and tethering RUVBL2 to an active promoter enhances Pol II clustering at the promoter. We also identify target genes that are directly linked to the RUVBL2-Pol II axis. Many of these genes are hallmarks of cancers and encode proteins with diverse cellular functions. Our results demonstrate an emerging activity for RUVBL2 in regulating Pol II cluster formation in the nucleus.

Suggested Citation

  • Hui Wang & Boyuan Li & Linyu Zuo & Bo Wang & Yan Yan & Kai Tian & Rong Zhou & Chenlu Wang & Xizi Chen & Yongpeng Jiang & Haonan Zheng & Fangfei Qin & Bin Zhang & Yang Yu & Chao-Pei Liu & Yanhui Xu & J, 2022. "The transcriptional coactivator RUVBL2 regulates Pol II clustering with diverse transcription factors," Nature Communications, Nature, vol. 13(1), pages 1-26, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33433-3
    DOI: 10.1038/s41467-022-33433-3
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-33433-3
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-33433-3?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. Ralph Stadhouders & Guillaume J. Filion & Thomas Graf, 2019. "Transcription factors and 3D genome conformation in cell-fate decisions," Nature, Nature, vol. 569(7756), pages 345-354, May.
    2. Charles H. Li & Eliot L. Coffey & Alessandra Dall’Agnese & Nancy M. Hannett & Xin Tang & Jonathan E. Henninger & Jesse M. Platt & Ozgur Oksuz & Alicia V. Zamudio & Lena K. Afeyan & Jurian Schuijers & , 2020. "MeCP2 links heterochromatin condensates and neurodevelopmental disease," Nature, Nature, vol. 586(7829), pages 440-444, October.
    3. Linyu Zuo & Guanwei Zhang & Matthew Massett & Jun Cheng & Zicong Guo & Liang Wang & Yifei Gao & Ru Li & Xu Huang & Pilong Li & Zhi Qi, 2021. "Loci-specific phase separation of FET fusion oncoproteins promotes gene transcription," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    4. Huasong Lu & Dan Yu & Anders S. Hansen & Sourav Ganguly & Rongdiao Liu & Alec Heckert & Xavier Darzacq & Qiang Zhou, 2018. "Phase-separation mechanism for C-terminal hyperphosphorylation of RNA polymerase II," Nature, Nature, vol. 558(7709), pages 318-323, June.
    5. Philippe Cloutier & Christian Poitras & Mathieu Durand & Omid Hekmat & Émilie Fiola-Masson & Annie Bouchard & Denis Faubert & Benoit Chabot & Benoit Coulombe, 2017. "R2TP/Prefoldin-like component RUVBL1/RUVBL2 directly interacts with ZNHIT2 to regulate assembly of U5 small nuclear ribonucleoprotein," Nature Communications, Nature, vol. 8(1), pages 1-14, August.
    6. Yang Eric Guo & John C. Manteiga & Jonathan E. Henninger & Benjamin R. Sabari & Alessandra Dall’Agnese & Nancy M. Hannett & Jan-Hendrik Spille & Lena K. Afeyan & Alicia V. Zamudio & Krishna Shrinivas , 2019. "Pol II phosphorylation regulates a switch between transcriptional and splicing condensates," Nature, Nature, vol. 572(7770), pages 543-548, August.
    7. Patrick Cramer, 2019. "Organization and regulation of gene transcription," Nature, Nature, vol. 573(7772), pages 45-54, September.
    8. Jung Hwa Kim & Bogyou Kim & Ling Cai & Hee June Choi & Kenneth A. Ohgi & Chris Tran & Charlie Chen & Chin Ha Chung & Otmar Huber & David W. Rose & Charles L. Sawyers & Michael G. Rosenfeld & Sung Hee , 2005. "Transcriptional regulation of a metastasis suppressor gene by Tip60 and β-catenin complexes," Nature, Nature, vol. 434(7035), pages 921-926, April.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Marta Vicioso-Mantis & Raquel Fueyo & Claudia Navarro & Sara Cruz-Molina & Wilfred F. J. Ijcken & Elena Rebollo & Álvaro Rada-Iglesias & Marian A. Martínez-Balbás, 2022. "JMJD3 intrinsically disordered region links the 3D-genome structure to TGFβ-dependent transcription activation," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    2. David Flores-Solis & Irina P. Lushpinskaia & Anton A. Polyansky & Arya Changiarath & Marc Boehning & Milana Mirkovic & James Walshe & Lisa M. Pietrek & Patrick Cramer & Lukas S. Stelzl & Bojan Zagrovi, 2023. "Driving forces behind phase separation of the carboxy-terminal domain of RNA polymerase II," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    3. Baolei Yuan & Xuan Zhou & Keiichiro Suzuki & Gerardo Ramos-Mandujano & Mengge Wang & Muhammad Tehseen & Lorena V. Cortés-Medina & James J. Moresco & Sarah Dunn & Reyna Hernandez-Benitez & Tomoaki Hish, 2022. "Wiskott-Aldrich syndrome protein forms nuclear condensates and regulates alternative splicing," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    4. Hiroaki Ohishi & Seiru Shimada & Satoshi Uchino & Jieru Li & Yuko Sato & Manabu Shintani & Hitoshi Owada & Yasuyuki Ohkawa & Alexandros Pertsinidis & Takashi Yamamoto & Hiroshi Kimura & Hiroshi Ochiai, 2022. "STREAMING-tag system reveals spatiotemporal relationships between transcriptional regulatory factors and transcriptional activity," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    5. Lisa-Marie Appel & Vedran Franke & Melania Bruno & Irina Grishkovskaya & Aiste Kasiliauskaite & Tanja Kaufmann & Ursula E. Schoeberl & Martin G. Puchinger & Sebastian Kostrhon & Carmen Ebenwaldner & M, 2021. "PHF3 regulates neuronal gene expression through the Pol II CTD reader domain SPOC," Nature Communications, Nature, vol. 12(1), pages 1-24, December.
    6. Jiegen Wu & Baoqiang Chen & Yadi Liu & Liang Ma & Wen Huang & Yihan Lin, 2022. "Modulating gene regulation function by chemically controlled transcription factor clustering," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    7. Halima H. Schede & Pradeep Natarajan & Arup K. Chakraborty & Krishna Shrinivas, 2023. "A model for organization and regulation of nuclear condensates by gene activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. Maria A. Missinato & Sean Murphy & Michaela Lynott & Michael S. Yu & Anaïs Kervadec & Yu-Ling Chang & Suraj Kannan & Mafalda Loreti & Christopher Lee & Prashila Amatya & Hiroshi Tanaka & Chun-Teng Hua, 2023. "Conserved transcription factors promote cell fate stability and restrict reprogramming potential in differentiated cells," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    9. Min Lee & Hyungseok C. Moon & Hyeonjeong Jeong & Dong Wook Kim & Hye Yoon Park & Yongdae Shin, 2024. "Optogenetic control of mRNA condensation reveals an intimate link between condensate material properties and functions," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    10. Mitsuaki Fujimoto & Ryosuke Takii & Masaki Matsumoto & Mariko Okada & Keiich I. Nakayama & Ryuichiro Nakato & Katsunori Fujiki & Katsuhiko Shirahige & Akira Nakai, 2022. "HSF1 phosphorylation establishes an active chromatin state via the TRRAP–TIP60 complex and promotes tumorigenesis," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    11. Sarah M. Lloyd & Daniel B. Leon & Mari O. Brady & Deborah Rodriguez & Madison P. McReynolds & Junghun Kweon & Amy E. Neely & Laura A. Blumensaadt & Patric J. Ho & Xiaomin Bao, 2022. "CDK9 activity switch associated with AFF1 and HEXIM1 controls differentiation initiation from epidermal progenitors," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    12. Mina Farag & Wade M. Borcherds & Anne Bremer & Tanja Mittag & Rohit V. Pappu, 2023. "Phase separation of protein mixtures is driven by the interplay of homotypic and heterotypic interactions," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    13. Fadi J. Najm & Peter DeWeirdt & Molly M. Moore & Samantha M. Bevill & Chadi A. El Farran & Kevin A. Macias & Mudra Hegde & Amanda L. Waterbury & Brian B. Liau & Peter Galen & John G. Doench & Bradley , 2023. "Chromatin complex dependencies reveal targeting opportunities in leukemia," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    14. Weiliang Mo & Junchuan Zhang & Li Zhang & Zhenming Yang & Liang Yang & Nan Yao & Yong Xiao & Tianhong Li & Yaxing Li & Guangmei Zhang & Mingdi Bian & Xinglin Du & Zecheng Zuo, 2022. "Arabidopsis cryptochrome 2 forms photobodies with TCP22 under blue light and regulates the circadian clock," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    15. Claire Marchal & Nivedita Singh & Zachary Batz & Jayshree Advani & Catherine Jaeger & Ximena Corso-Díaz & Anand Swaroop, 2022. "High-resolution genome topology of human retina uncovers super enhancer-promoter interactions at tissue-specific and multifactorial disease loci," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    16. Tomas Zelenka & Antonios Klonizakis & Despina Tsoukatou & Dionysios-Alexandros Papamatheakis & Sören Franzenburg & Petros Tzerpos & Ioannis-Rafail Tzonevrakis & George Papadogkonas & Manouela Kapsetak, 2022. "The 3D enhancer network of the developing T cell genome is shaped by SATB1," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    17. Ines H. Kaltheuner & Kanchan Anand & Jonas Moecking & Robert Düster & Jinhua Wang & Nathanael S. Gray & Matthias Geyer, 2021. "Abemaciclib is a potent inhibitor of DYRK1A and HIP kinases involved in transcriptional regulation," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
    18. Mattia Zaghi & Federica Banfi & Luca Massimino & Monica Volpin & Edoardo Bellini & Simone Brusco & Ivan Merelli & Cristiana Barone & Michela Bruni & Linda Bossini & Luigi Antonio Lamparelli & Laura Pi, 2023. "Balanced SET levels favor the correct enhancer repertoire during cell fate acquisition," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    19. Wen Jun Xie & Yifeng Qi & Bin Zhang, 2020. "Characterizing chromatin folding coordinate and landscape with deep learning," PLOS Computational Biology, Public Library of Science, vol. 16(9), pages 1-19, September.
    20. Ziad Ibrahim & Tao Wang & Olivier Destaing & Nicola Salvi & Naghmeh Hoghoughi & Clovis Chabert & Alexandra Rusu & Jinjun Gao & Leonardo Feletto & Nicolas Reynoird & Thomas Schalch & Yingming Zhao & Ma, 2022. "Structural insights into p300 regulation and acetylation-dependent genome organisation," Nature Communications, Nature, vol. 13(1), pages 1-23, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-33433-3. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.