IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-40743-7.html
   My bibliography  Save this article

LINE-1 regulates cortical development by acting as long non-coding RNAs

Author

Listed:
  • Damiano Mangoni

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Alessandro Simi

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Pierre Lau

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Alexandros Armaos

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Federico Ansaloni

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Azzurra Codino

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Devid Damiani

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Lavinia Floreani

    (Area of Neuroscience, International School for Advanced Studies (SISSA))

  • Valerio Carlo

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Diego Vozzi

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Francesca Persichetti

    (University of Piemonte Orientale (UPO))

  • Claudio Santoro

    (University of Piemonte Orientale (UPO))

  • Luca Pandolfini

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Gian Gaetano Tartaglia

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

  • Remo Sanges

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT)
    Area of Neuroscience, International School for Advanced Studies (SISSA))

  • Stefano Gustincich

    (Central RNA Laboratory, Istituto Italiano di Tecnologia (IIT))

Abstract

Long Interspersed Nuclear Elements-1s (L1s) are transposable elements that constitute most of the genome’s transcriptional output yet have still largely unknown functions. Here we show that L1s are required for proper mouse brain corticogenesis operating as regulatory long non-coding RNAs. They contribute to the regulation of the balance between neuronal progenitors and differentiation, the migration of post-mitotic neurons and the proportions of different cell types. In cortical cultured neurons, L1 RNAs are mainly associated to chromatin and interact with the Polycomb Repressive Complex 2 (PRC2) protein subunits enhancer of Zeste homolog 2 (Ezh2) and suppressor of zeste 12 (Suz12). L1 RNA silencing influences PRC2’s ability to bind a portion of its targets and the deposition of tri-methylated histone H3 (H3K27me3) marks. Our results position L1 RNAs as crucial signalling hubs for genome-wide chromatin remodelling, enabling the fine-tuning of gene expression during brain development and evolution.

Suggested Citation

  • Damiano Mangoni & Alessandro Simi & Pierre Lau & Alexandros Armaos & Federico Ansaloni & Azzurra Codino & Devid Damiani & Lavinia Floreani & Valerio Carlo & Diego Vozzi & Francesca Persichetti & Claud, 2023. "LINE-1 regulates cortical development by acting as long non-coding RNAs," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40743-7
    DOI: 10.1038/s41467-023-40743-7
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-40743-7
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-023-40743-7?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. Alysson R. Muotri & Vi T. Chu & Maria C. N. Marchetto & Wei Deng & John V. Moran & Fred H. Gage, 2005. "Somatic mosaicism in neuronal precursor cells mediated by L1 retrotransposition," Nature, Nature, vol. 435(7044), pages 903-910, June.
    2. Lipin Loo & Jeremy M. Simon & Lei Xing & Eric S. McCoy & Jesse K. Niehaus & Jiami Guo & E. S. Anton & Mark J. Zylka, 2019. "Single-cell transcriptomic analysis of mouse neocortical development," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    3. Laurie A. Boyer & Kathrin Plath & Julia Zeitlinger & Tobias Brambrink & Lea A. Medeiros & Tong Ihn Lee & Stuart S. Levine & Marius Wernig & Adriana Tajonar & Mridula K. Ray & George W. Bell & Arie P. , 2006. "Polycomb complexes repress developmental regulators in murine embryonic stem cells," Nature, Nature, vol. 441(7091), pages 349-353, May.
    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. Marco D. Carpenter & Delaney K. Fischer & Shuo Zhang & Allison M. Bond & Kyle S. Czarnecki & Morgan T. Woolf & Hongjun Song & Elizabeth A. Heller, 2022. "Cell-type specific profiling of histone post-translational modifications in the adult mouse striatum," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    2. Shijia Zhu & Guohua Wang & Bo Liu & Yadong Wang, 2013. "Modeling Exon Expression Using Histone Modifications," PLOS ONE, Public Library of Science, vol. 8(6), pages 1-15, June.
    3. Jacob Bergstedt & Sadoune Ait Kaci Azzou & Kristin Tsuo & Anthony Jaquaniello & Alejandra Urrutia & Maxime Rotival & David T. S. Lin & Julia L. MacIsaac & Michael S. Kobor & Matthew L. Albert & Darrag, 2022. "The immune factors driving DNA methylation variation in human blood," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    4. C. W. Ryan & S. L. Regan & E. F. Mills & B. T. McGrath & E. Gong & Y. T. Lai & J. B. Sheingold & K. Patel & T. Horowitz & A. Moccia & Y. C. Tsan & A. Srivastava & S. L. Bielas, 2024. "RING1 missense variants reveal sensitivity of DNA damage repair to H2A monoubiquitination dosage during neurogenesis," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Chen Sun & Kunal Kathuria & Sarah B. Emery & ByungJun Kim & Ian E. Burbulis & Joo Heon Shin & Daniel R. Weinberger & John V. Moran & Jeffrey M. Kidd & Ryan E. Mills & Michael J. McConnell, 2024. "Mapping recurrent mosaic copy number variation in human neurons," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    6. Natalia Benetti & Quentin Gouil & Andres Tapia del Fierro & Tamara Beck & Kelsey Breslin & Andrew Keniry & Edwina McGlinn & Marnie E. Blewitt, 2022. "Maternal SMCHD1 regulates Hox gene expression and patterning in the mouse embryo," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. Bert I. Crawford & Mary Jo Talley & Joshua Russman & James Riddle & Sabrina Torres & Troy Williams & Michelle S. Longworth, 2024. "Condensin-mediated restriction of retrotransposable elements facilitates brain development in Drosophila melanogaster," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    8. M S Vijayabaskar & Debbie K Goode & Nadine Obier & Monika Lichtinger & Amber M L Emmett & Fatin N Zainul Abidin & Nisar Shar & Rebecca Hannah & Salam A Assi & Michael Lie-A-Ling & Berthold Gottgens & , 2019. "Identification of gene specific cis-regulatory elements during differentiation of mouse embryonic stem cells: An integrative approach using high-throughput datasets," PLOS Computational Biology, Public Library of Science, vol. 15(11), pages 1-29, November.
    9. Tara N. Yankee & Sungryong Oh & Emma Wentworth Winchester & Andrea Wilderman & Kelsey Robinson & Tia Gordon & Jill A. Rosenfeld & Jennifer VanOudenhove & Daryl A. Scott & Elizabeth J. Leslie & Justin , 2023. "Integrative analysis of transcriptome dynamics during human craniofacial development identifies candidate disease genes," Nature Communications, Nature, vol. 14(1), pages 1-23, December.
    10. Fiona G G Nielsen & Kasper Galschiøt Markus & Rune Møllegaard Friborg & Lene Monrad Favrholdt & Hendrik G Stunnenberg & Martijn Huynen, 2012. "CATCHprofiles: Clustering and Alignment Tool for ChIP Profiles," PLOS ONE, Public Library of Science, vol. 7(1), pages 1-8, January.

    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_s41467-023-40743-7. 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.