IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38797-8.html
   My bibliography  Save this article

LIS1 RNA-binding orchestrates the mechanosensitive properties of embryonic stem cells in AGO2-dependent and independent ways

Author

Listed:
  • Aditya Kshirsagar

    (Weizmann Institute of Science)

  • Svetlana Maslov Doroshev

    (Weizmann Institute of Science)

  • Anna Gorelik

    (Weizmann Institute of Science)

  • Tsviya Olender

    (Weizmann Institute of Science)

  • Tamar Sapir

    (Weizmann Institute of Science)

  • Daisuke Tsuboi

    (Fujita Health University)

  • Irit Rosenhek-Goldian

    (Weizmann Institute of Science)

  • Sergey Malitsky

    (Weizmann Institute of Science)

  • Maxim Itkin

    (Weizmann Institute of Science)

  • Amir Argoetti

    (Technion-Israel Institute of Technology)

  • Yael Mandel-Gutfreund

    (Technion-Israel Institute of Technology)

  • Sidney R. Cohen

    (Weizmann Institute of Science)

  • Jacob H. Hanna

    (Weizmann Institute of Science)

  • Igor Ulitsky

    (Weizmann Institute of Science)

  • Kozo Kaibuchi

    (Fujita Health University)

  • Orly Reiner

    (Weizmann Institute of Science)

Abstract

Lissencephaly-1 (LIS1) is associated with neurodevelopmental diseases and is known to regulate the molecular motor cytoplasmic dynein activity. Here we show that LIS1 is essential for the viability of mouse embryonic stem cells (mESCs), and it governs the physical properties of these cells. LIS1 dosage substantially affects gene expression, and we uncovered an unexpected interaction of LIS1 with RNA and RNA-binding proteins, most prominently the Argonaute complex. We demonstrate that LIS1 overexpression partially rescued the extracellular matrix (ECM) expression and mechanosensitive genes conferring stiffness to Argonaute null mESCs. Collectively, our data transforms the current perspective on the roles of LIS1 in post-transcriptional regulation underlying development and mechanosensitive processes.

Suggested Citation

  • Aditya Kshirsagar & Svetlana Maslov Doroshev & Anna Gorelik & Tsviya Olender & Tamar Sapir & Daisuke Tsuboi & Irit Rosenhek-Goldian & Sergey Malitsky & Maxim Itkin & Amir Argoetti & Yael Mandel-Gutfre, 2023. "LIS1 RNA-binding orchestrates the mechanosensitive properties of embryonic stem cells in AGO2-dependent and independent ways," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38797-8
    DOI: 10.1038/s41467-023-38797-8
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38797-8
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-38797-8?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. Yoach Rais & Asaf Zviran & Shay Geula & Ohad Gafni & Elad Chomsky & Sergey Viukov & Abed AlFatah Mansour & Inbal Caspi & Vladislav Krupalnik & Mirie Zerbib & Itay Maza & Nofar Mor & Dror Baran & Leehe, 2013. "Deterministic direct reprogramming of somatic cells to pluripotency," Nature, Nature, vol. 502(7469), pages 65-70, October.
    2. Liang Zheng & Simone Cardaci & Livnat Jerby & Elaine D. MacKenzie & Marco Sciacovelli & T. Isaac Johnson & Edoardo Gaude & Ayala King & Joshua D. G. Leach & RuAngelie Edrada-Ebel & Ann Hedley & Nichol, 2015. "Fumarate induces redox-dependent senescence by modifying glutathione metabolism," Nature Communications, Nature, vol. 6(1), pages 1-12, May.
    3. Eric L. Nostrand & Peter Freese & Gabriel A. Pratt & Xiaofeng Wang & Xintao Wei & Rui Xiao & Steven M. Blue & Jia-Yu Chen & Neal A. L. Cody & Daniel Dominguez & Sara Olson & Balaji Sundararaman & Liju, 2020. "A large-scale binding and functional map of human RNA-binding proteins," Nature, Nature, vol. 583(7818), pages 711-719, July.
    4. Davor Lessel & Daniela M. Zeitler & Margot R. F. Reijnders & Andriy Kazantsev & Fatemeh Hassani Nia & Alexander Bartholomäus & Victoria Martens & Astrid Bruckmann & Veronika Graus & Allyn McConkie-Ros, 2020. "Germline AGO2 mutations impair RNA interference and human neurological development," Nature Communications, Nature, vol. 11(1), pages 1-14, December.
    5. Mette Bentsen & Philipp Goymann & Hendrik Schultheis & Kathrin Klee & Anastasiia Petrova & René Wiegandt & Annika Fust & Jens Preussner & Carsten Kuenne & Thomas Braun & Johnny Kim & Mario Looso, 2020. "ATAC-seq footprinting unravels kinetics of transcription factor binding during zygotic genome activation," Nature Communications, Nature, vol. 11(1), pages 1-11, December.
    6. Ohad Gafni & Leehee Weinberger & Abed AlFatah Mansour & Yair S. Manor & Elad Chomsky & Dalit Ben-Yosef & Yael Kalma & Sergey Viukov & Itay Maza & Asaf Zviran & Yoach Rais & Zohar Shipony & Zohar Mukam, 2013. "Derivation of novel human ground state naive pluripotent stem cells," Nature, Nature, vol. 504(7479), pages 282-286, December.
    7. Barry Slaff & Caleb M. Radens & Paul Jewell & Anupama Jha & Nicholas F. Lahens & Gregory R. Grant & Andrei Thomas-Tikhonenko & Kristen W. Lynch & Yoseph Barash, 2021. "MOCCASIN: a method for correcting for known and unknown confounders in RNA splicing analysis," Nature Communications, Nature, vol. 12(1), pages 1-9, December.
    8. Amol Panhale & Florian M. Richter & Fidel Ramírez & Maria Shvedunova & Thomas Manke & Gerhard Mittler & Asifa Akhtar, 2019. "CAPRI enables comparison of evolutionarily conserved RNA interacting regions," Nature Communications, Nature, vol. 10(1), pages 1-22, 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. Anna Knörlein & Chris P. Sarnowski & Tebbe Vries & Moritz Stoltz & Michael Götze & Ruedi Aebersold & Frédéric H.-T. Allain & Alexander Leitner & Jonathan Hall, 2022. "Nucleotide-amino acid π-stacking interactions initiate photo cross-linking in RNA-protein complexes," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Jorge Vaquero-Garcia & Joseph K. Aicher & San Jewell & Matthew R. Gazzara & Caleb M. Radens & Anupama Jha & Scott S. Norton & Nicholas F. Lahens & Gregory R. Grant & Yoseph Barash, 2023. "RNA splicing analysis using heterogeneous and large RNA-seq datasets," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Denis Torre & Nancy J. Francoeur & Yael Kalma & Ilana Gross Carmel & Betsaida S. Melo & Gintaras Deikus & Kimaada Allette & Ron Flohr & Maya Fridrikh & Konstantinos Vlachos & Kent Madrid & Hardik Shah, 2023. "Isoform-resolved transcriptome of the human preimplantation embryo," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    4. Matvei Khoroshkin & Andrey Buyan & Martin Dodel & Albertas Navickas & Johnny Yu & Fathima Trejo & Anthony Doty & Rithvik Baratam & Shaopu Zhou & Sean B. Lee & Tanvi Joshi & Kristle Garcia & Benedict C, 2024. "Systematic identification of post-transcriptional regulatory modules," Nature Communications, Nature, vol. 15(1), pages 1-21, December.
    5. Haofan Sun & Bin Fu & Xiaohong Qian & Ping Xu & Weijie Qin, 2024. "Nuclear and cytoplasmic specific RNA binding proteome enrichment and its changes upon ferroptosis induction," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Johanna Luige & Alexandros Armaos & Gian Gaetano Tartaglia & Ulf Andersson Vang Ørom, 2024. "Predicting nuclear G-quadruplex RNA-binding proteins with roles in transcription and phase separation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Oliver J. Ziff & Jacob Neeves & Jamie Mitchell & Giulia Tyzack & Carlos Martinez-Ruiz & Raphaelle Luisier & Anob M. Chakrabarti & Nicholas McGranahan & Kevin Litchfield & Simon J. Boulton & Ammar Al-C, 2023. "Integrated transcriptome landscape of ALS identifies genome instability linked to TDP-43 pathology," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    8. Zili Song & Shuang Zhou & Hongjiao Zhang & Nancy P. Keller & Berl R. Oakley & Xiao Liu & Wen-Bing Yin, 2023. "Fungal secondary metabolism is governed by an RNA-binding protein CsdA/RsdA complex," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    9. Wei Hu & Yangjun Wu & Qili Shi & Jingni Wu & Deping Kong & Xiaohua Wu & Xianghuo He & Teng Liu & Shengli Li, 2022. "Systematic characterization of cancer transcriptome at transcript resolution," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    10. David Wang & Mathieu Quesnel-Vallieres & San Jewell & Moein Elzubeir & Kristen Lynch & Andrei Thomas-Tikhonenko & Yoseph Barash, 2023. "A Bayesian model for unsupervised detection of RNA splicing based subtypes in cancers," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    11. Tao Zhu & Chunjiao Xia & Ranran Yu & Xinkai Zhou & Xingbing Xu & Lin Wang & Zhanxiang Zong & Junjiao Yang & Yinmeng Liu & Luchang Ming & Yuxin You & Dijun Chen & Weibo Xie, 2024. "Comprehensive mapping and modelling of the rice regulome landscape unveils the regulatory architecture underlying complex traits," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    12. Haoran Zhu & Yuning Yang & Yunhe Wang & Fuzhou Wang & Yujian Huang & Yi Chang & Ka-chun Wong & Xiangtao Li, 2023. "Dynamic characterization and interpretation for protein-RNA interactions across diverse cellular conditions using HDRNet," Nature Communications, Nature, vol. 14(1), pages 1-22, December.
    13. Huijuan Feng & Xiang-Jun Lu & Suvrajit Maji & Linxi Liu & Dmytro Ustianenko & Noam D. Rudnick & Chaolin Zhang, 2024. "Structure-based prediction and characterization of photo-crosslinking in native protein–RNA complexes," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    14. Jian Han & Omer An & Xi Ren & Yangyang Song & Sze Jing Tang & Haoqing Shen & Xinyu Ke & Vanessa Hui En Ng & Daryl Jin Tai Tay & Hui Qing Tan & Dennis Kappei & Henry Yang & Leilei Chen, 2022. "Multilayered control of splicing regulatory networks by DAP3 leads to widespread alternative splicing changes in cancer," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    15. Zhenhui Zhong & Yafei Wang & Ming Wang & Fan Yang & Quentin Angelo Thomas & Yan Xue & Yaxin Zhang & Wanlu Liu & Yasaman Jami-Alahmadi & Linhao Xu & Suhua Feng & Sebastian Marquardt & James A. Wohlschl, 2022. "Histone chaperone ASF1 mediates H3.3-H4 deposition in Arabidopsis," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    16. Dhurjhoti Saha & Solomon Hailu & Arjan Hada & Junwoo Lee & Jie Luo & Jeff A. Ranish & Yuan-chi Lin & Kyle Feola & Jim Persinger & Abhinav Jain & Bin Liu & Yue Lu & Payel Sen & Blaine Bartholomew, 2023. "The AT-hook is an evolutionarily conserved auto-regulatory domain of SWI/SNF required for cell lineage priming," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Joyce J. Thompson & Daniel J. Lee & Apratim Mitra & Sarah Frail & Ryan K. Dale & Pedro P. Rocha, 2022. "Extensive co-binding and rapid redistribution of NANOG and GATA6 during emergence of divergent lineages," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    18. Xinzhi Li & Kaixin Ding & Xueying Li & Bingchuan Yuan & Yuqin Wang & Zhicheng Yao & Shuaikang Wang & He Huang & Bolin Xu & Liwei Xie & Tuo Deng & Xiao-wei Chen & Zheng Chen, 2022. "Deficiency of WTAP in hepatocytes induces lipoatrophy and non-alcoholic steatohepatitis (NASH)," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    19. Marissa Cloutier & Surinder Kumar & Emily Buttigieg & Laura Keller & Brandon Lee & Aaron Williams & Sandra Mojica-Perez & Indri Erliandri & Andre Monteiro Da Rocha & Kenneth Cadigan & Gary D. Smith & , 2022. "Preventing erosion of X-chromosome inactivation in human embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-18, December.
    20. Stefano Suzzi & Tommaso Croese & Adi Ravid & Or Gold & Abbe R. Clark & Sedi Medina & Daniel Kitsberg & Miriam Adam & Katherine A. Vernon & Eva Kohnert & Inbar Shapira & Sergey Malitsky & Maxim Itkin &, 2023. "N-acetylneuraminic acid links immune exhaustion and accelerated memory deficit in diet-induced obese Alzheimer’s disease mouse model," Nature Communications, Nature, vol. 14(1), pages 1-19, 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_s41467-023-38797-8. 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.