IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v15y2024i1d10.1038_s41467-024-48580-y.html
   My bibliography  Save this article

Nuclear actin structure regulates chromatin accessibility

Author

Listed:
  • Buer Sen

    (University of North Carolina)

  • Zhihui Xie

    (University of North Carolina)

  • Michelle D. Thomas

    (University of North Carolina at Chapel Hill)

  • Samantha G. Pattenden

    (University of North Carolina at Chapel Hill)

  • Sean Howard

    (Boise State University)

  • Cody McGrath

    (University of North Carolina)

  • Maya Styner

    (University of North Carolina)

  • Gunes Uzer

    (Boise State University)

  • Terrence S. Furey

    (University of North Carolina at Chapel Hill)

  • Janet Rubin

    (University of North Carolina)

Abstract

Polymerized β-actin may provide a structural basis for chromatin accessibility and actin transport into the nucleus can guide mesenchymal stem cell (MSC) differentiation. Using MSC, we show that using CK666 to inhibit Arp2/3 directed secondary actin branching results in decreased nuclear actin structure, and significantly alters chromatin access measured with ATACseq at 24 h. The ATAC-seq results due to CK666 are distinct from those caused by cytochalasin D (CytoD), which enhances nuclear actin structure. In addition, nuclear visualization shows Arp2/3 inhibition decreases pericentric H3K9me3 marks. CytoD, alternatively, induces redistribution of H3K27me3 marks centrally. Such alterations in chromatin landscape are consistent with differential gene expression associated with distinctive differentiation patterns. Further, knockdown of the non-enzymatic monomeric actin binding protein, Arp4, leads to extensive chromatin unpacking, but only a modest increase in transcription, indicating an active role for actin-Arp4 in transcription. These data indicate that dynamic actin remodeling can regulate chromatin interactions.

Suggested Citation

  • Buer Sen & Zhihui Xie & Michelle D. Thomas & Samantha G. Pattenden & Sean Howard & Cody McGrath & Maya Styner & Gunes Uzer & Terrence S. Furey & Janet Rubin, 2024. "Nuclear actin structure regulates chromatin accessibility," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48580-y
    DOI: 10.1038/s41467-024-48580-y
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-024-48580-y
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-024-48580-y?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. Maud Debaugnies & Sara Rodríguez-Acebes & Jeremy Blondeau & Marie-Astrid Parent & Manuel Zocco & Yura Song & Viviane Maertelaer & Virginie Moers & Mathilde Latil & Christine Dubois & Katia Coulonval &, 2023. "RHOJ controls EMT-associated resistance to chemotherapy," Nature, Nature, vol. 616(7955), pages 168-175, April.
    2. 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.
    3. Ying Wang & Alice Sherrard & Bing Zhao & Michael Melak & Jonathan Trautwein & Eva-Maria Kleinschnitz & Nikolaos Tsopoulidis & Oliver T. Fackler & Carsten Schwan & Robert Grosse, 2019. "GPCR-induced calcium transients trigger nuclear actin assembly for chromatin dynamics," Nature Communications, Nature, vol. 10(1), pages 1-9, December.
    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. Yifeng Qi & Bin Zhang, 2021. "Chromatin network retards nucleoli coalescence," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. 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.
    3. 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.
    4. Guillermo A. Orsi & Maxime M. C. Tortora & Béatrice Horard & Dominique Baas & Jean-Philippe Kleman & Jonas Bucevičius & Gražvydas Lukinavičius & Daniel Jost & Benjamin Loppin, 2023. "Biophysical ordering transitions underlie genome 3D re-organization during cricket spermiogenesis," Nature Communications, Nature, vol. 14(1), pages 1-16, 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. Hye Ji Cha & Özgün Uyan & Yan Kai & Tianxin Liu & Qian Zhu & Zuzana Tothova & Giovanni A. Botten & Jian Xu & Guo-Cheng Yuan & Job Dekker & Stuart H. Orkin, 2021. "Inner nuclear protein Matrin-3 coordinates cell differentiation by stabilizing chromatin architecture," Nature Communications, Nature, vol. 12(1), pages 1-19, December.
    7. Taehyun Kim & Jaeyoon Yoo & Sungho Do & Dong Soo Hwang & YongKeun Park & Yongdae Shin, 2023. "RNA-mediated demixing transition of low-density condensates," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    8. 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.
    9. Naohiro Kuwayama & Tomoya Kujirai & Yusuke Kishi & Rina Hirano & Kenta Echigoya & Lingyan Fang & Sugiko Watanabe & Mitsuyoshi Nakao & Yutaka Suzuki & Kei-ichiro Ishiguro & Hitoshi Kurumizaka & Yukiko , 2023. "HMGA2 directly mediates chromatin condensation in association with neuronal fate regulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    10. 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.
    11. Pan Jia & Xiang Li & Xuelei Wang & Liangjiao Yao & Yingying Xu & Yu Hu & Wenwen Xu & Zhe He & Qifan Zhao & Yicong Deng & Yi Zang & Meiyu Zhang & Yan Zhang & Jun Qin & Wei Lu, 2021. "ZMYND8 mediated liquid condensates spatiotemporally decommission the latent super-enhancers during macrophage polarization," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    12. 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.
    13. 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.
    14. Adel Al Jord & Gaëlle Letort & Soline Chanet & Feng-Ching Tsai & Christophe Antoniewski & Adrien Eichmuller & Christelle Da Silva & Jean-René Huynh & Nir S. Gov & Raphaël Voituriez & Marie-Émilie Terr, 2022. "Cytoplasmic forces functionally reorganize nuclear condensates in oocytes," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    15. Simon M Lichtinger & Adiran Garaizar & Rosana Collepardo-Guevara & Aleks Reinhardt, 2021. "Targeted modulation of protein liquid–liquid phase separation by evolution of amino-acid sequence," PLOS Computational Biology, Public Library of Science, vol. 17(8), pages 1-28, August.
    16. Clara Lopes Novo & Emily V. Wong & Colin Hockings & Chetan Poudel & Eleanor Sheekey & Meike Wiese & Hanneke Okkenhaug & Simon J. Boulton & Srinjan Basu & Simon Walker & Gabriele S. Kaminski Schierle &, 2022. "Satellite repeat transcripts modulate heterochromatin condensates and safeguard chromosome stability in mouse embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    17. Xiaowen Lyu & M. Jordan Rowley & Michael J. Kulik & Stephen Dalton & Victor G. Corces, 2023. "Regulation of CTCF loop formation during pancreatic cell differentiation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    18. 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.
    19. Maria Dilia Palumbieri & Chiara Merigliano & Daniel González-Acosta & Danina Kuster & Jana Krietsch & Henriette Stoy & Thomas Känel & Svenja Ulferts & Bettina Welter & Joël Frey & Cyril Doerdelmann & , 2023. "Nuclear actin polymerization rapidly mediates replication fork remodeling upon stress by limiting PrimPol activity," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    20. 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.

    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:15:y:2024:i:1:d:10.1038_s41467-024-48580-y. 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.