IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-42345-9.html
   My bibliography  Save this article

A DEAD-box helicase drives the partitioning of a pro-differentiation NAB protein into nuclear foci

Author

Listed:
  • Akiko Doi

    (Massachusetts Institute of Technology)

  • Gianmarco D. Suarez

    (Massachusetts Institute of Technology)

  • Rita Droste

    (Massachusetts Institute of Technology)

  • H. Robert Horvitz

    (Massachusetts Institute of Technology)

Abstract

How cells regulate gene expression in a precise spatiotemporal manner during organismal development is a fundamental question in biology. Although the role of transcriptional condensates in gene regulation has been established, little is known about the function and regulation of these molecular assemblies in the context of animal development and physiology. Here we show that the evolutionarily conserved DEAD-box helicase DDX-23 controls cell fate in Caenorhabditis elegans by binding to and facilitating the condensation of MAB-10, the C. elegans homolog of mammalian NGFI-A-binding (NAB) protein. MAB-10 is a transcriptional cofactor that functions with the early growth response (EGR) protein LIN-29 to regulate the transcription of genes required for exiting the cell cycle, terminal differentiation, and the larval-to-adult transition. We suggest that DEAD-box helicase proteins function more generally during animal development to control the condensation of NAB proteins important in cell identity and that this mechanism is evolutionarily conserved. In mammals, such a mechanism might underlie terminal cell differentiation and when dysregulated might promote cancerous growth.

Suggested Citation

  • Akiko Doi & Gianmarco D. Suarez & Rita Droste & H. Robert Horvitz, 2023. "A DEAD-box helicase drives the partitioning of a pro-differentiation NAB protein into nuclear foci," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-42345-9
    DOI: 10.1038/s41467-023-42345-9
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-42345-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-42345-9?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. Nicholas Treen & Shunsuke F. Shimobayashi & Jorine Eeftens & Clifford P. Brangwynne & Michael Levine, 2021. "Properties of repression condensates in living Ciona embryos," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    2. 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.
    3. Brenda J. Reinhart & Frank J. Slack & Michael Basson & Amy E. Pasquinelli & Jill C. Bettinger & Ann E. Rougvie & H. Robert Horvitz & Gary Ruvkun, 2000. "The 21-nucleotide let-7 RNA regulates developmental timing in Caenorhabditis elegans," Nature, Nature, vol. 403(6772), pages 901-906, February.
    4. Amy R. Strom & Alexander V. Emelyanov & Mustafa Mir & Dmitry V. Fyodorov & Xavier Darzacq & Gary H. Karpen, 2017. "Phase separation drives heterochromatin domain formation," Nature, Nature, vol. 547(7662), pages 241-245, July.
    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. 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.
    2. 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.
    3. 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.
    4. Ting Peng & Yingping Hou & Haowei Meng & Yong Cao & Xiaotian Wang & Lumeng Jia & Qing Chen & Yang Zheng & Yujie Sun & Hebing Chen & Tingting Li & Cheng Li, 2023. "Mapping nucleolus-associated chromatin interactions using nucleolus Hi-C reveals pattern of heterochromatin interactions," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    5. Jorine M. Eeftens & Manya Kapoor & Davide Michieletto & Clifford P. Brangwynne, 2021. "Polycomb condensates can promote epigenetic marks but are not required for sustained chromatin compaction," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    6. 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.
    7. Catherine Naughton & Covadonga Huidobro & Claudia R. Catacchio & Adam Buckle & Graeme R. Grimes & Ryu-Suke Nozawa & Stefania Purgato & Mariano Rocchi & Nick Gilbert, 2022. "Human centromere repositioning activates transcription and opens chromatin fibre structure," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    8. 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.
    9. 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.
    10. 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.
    11. 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.
    12. Yohan Lee & Sujin Park & Feng Yuan & Carl C. Hayden & Liping Wang & Eileen M. Lafer & Siyoung Q. Choi & Jeanne C. Stachowiak, 2023. "Transmembrane coupling of liquid-like protein condensates," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    13. 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.
    14. Lidice González & Daniel Kolbin & Christian Trahan & Célia Jeronimo & François Robert & Marlene Oeffinger & Kerry Bloom & Stephen W. Michnick, 2023. "Adaptive partitioning of a gene locus to the nuclear envelope in Saccharomyces cerevisiae is driven by polymer-polymer phase separation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    15. Lennart Enders & Marton Siklos & Jan Borggräfe & Stefan Gaussmann & Anna Koren & Monika Malik & Tatjana Tomek & Michael Schuster & Jiří Reiniš & Elisa Hahn & Andrea Rukavina & Andreas Reicher & Tamara, 2023. "Pharmacological perturbation of the phase-separating protein SMNDC1," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    16. Juan Roa & Miguel Ruiz-Cruz & Francisco Ruiz-Pino & Rocio Onieva & Maria J. Vazquez & Maria J. Sanchez-Tapia & Jose M. Ruiz-Rodriguez & Veronica Sobrino & Alexia Barroso & Violeta Heras & Inmaculada V, 2022. "Dicer ablation in Kiss1 neurons impairs puberty and fertility preferentially in female mice," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    17. 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.
    18. 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.
    19. Tengfei Wang & Shuxiang Shi & Yuanyuan Shi & Peipei Jiang & Ganlu Hu & Qinying Ye & Zhan Shi & Kexin Yu & Chenguang Wang & Guoping Fan & Suwen Zhao & Hanhui Ma & Alex C. Y. Chang & Zhi Li & Qian Bian , 2023. "Chemical-induced phase transition and global conformational reorganization of chromatin," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    20. Shuang Hou & Jiaojiao Hu & Zhaowei Yu & Dan Li & Cong Liu & Yong Zhang, 2024. "Machine learning predictor PSPire screens for phase-separating proteins lacking intrinsically disordered regions," Nature Communications, Nature, vol. 15(1), pages 1-13, 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:14:y:2023:i:1:d:10.1038_s41467-023-42345-9. 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.