IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-24624-5.html
   My bibliography  Save this article

Extensive transcriptional and chromatin changes underlie astrocyte maturation in vivo and in culture

Author

Listed:
  • Michael Lattke

    (The Francis Crick Institute)

  • Robert Goldstone

    (The Francis Crick Institute)

  • James K. Ellis

    (The Francis Crick Institute)

  • Stefan Boeing

    (The Francis Crick Institute
    The Francis Crick Institute)

  • Jerónimo Jurado-Arjona

    (King’s College London)

  • Nicolás Marichal

    (King’s College London)

  • James I. MacRae

    (The Francis Crick Institute)

  • Benedikt Berninger

    (King’s College London
    King’s College London
    University Medical Center of the Johannes Gutenberg University Mainz
    The Francis Crick Institute)

  • Francois Guillemot

    (The Francis Crick Institute)

Abstract

Astrocytes have essential functions in brain homeostasis that are established late in differentiation, but the mechanisms underlying the functional maturation of astrocytes are not well understood. Here we identify extensive transcriptional changes that occur during murine astrocyte maturation in vivo that are accompanied by chromatin remodelling at enhancer elements. Investigating astrocyte maturation in a cell culture model revealed that in vitro-differentiated astrocytes lack expression of many mature astrocyte-specific genes, including genes for the transcription factors Rorb, Dbx2, Lhx2 and Fezf2. Forced expression of these factors in vitro induces distinct sets of mature astrocyte-specific transcripts. Culturing astrocytes in a three-dimensional matrix containing FGF2 induces expression of Rorb, Dbx2 and Lhx2 and improves astrocyte maturity based on transcriptional and chromatin profiles. Therefore, extrinsic signals orchestrate the expression of multiple intrinsic regulators, which in turn induce in a modular manner the transcriptional and chromatin changes underlying astrocyte maturation.

Suggested Citation

  • Michael Lattke & Robert Goldstone & James K. Ellis & Stefan Boeing & Jerónimo Jurado-Arjona & Nicolás Marichal & James I. MacRae & Benedikt Berninger & Francois Guillemot, 2021. "Extensive transcriptional and chromatin changes underlie astrocyte maturation in vivo and in culture," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-24624-5
    DOI: 10.1038/s41467-021-24624-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-24624-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-24624-5?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. Michael Lawrence & Wolfgang Huber & Hervé Pagès & Patrick Aboyoun & Marc Carlson & Robert Gentleman & Martin T Morgan & Vincent J Carey, 2013. "Software for Computing and Annotating Genomic Ranges," PLOS Computational Biology, Public Library of Science, vol. 9(8), pages 1-10, August.
    2. Woo-Ping Ge & Atsushi Miyawaki & Fred H. Gage & Yuh Nung Jan & Lily Yeh Jan, 2012. "Local generation of glia is a major astrocyte source in postnatal cortex," Nature, Nature, vol. 484(7394), pages 376-380, April.
    3. Gil Ron & Yuval Globerson & Dror Moran & Tommy Kaplan, 2017. "Promoter-enhancer interactions identified from Hi-C data using probabilistic models and hierarchical topological domains," Nature Communications, Nature, vol. 8(1), pages 1-12, December.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Yi Huang & Anyongqi Wang & Wenjiang Zhou & Baoguo Li & Linshan Zhang & Agata M. Rudolf & Zengguang Jin & Catherine Hambly & Guanlin Wang & John R. Speakman, 2024. "Maternal dietary fat during lactation shapes single nucleus transcriptomic profile of postnatal offspring hypothalamus in a sexually dimorphic manner in mice," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    2. Michael R. Williamson & Stephanie P. Le & Ronald L. Franzen & Nicole A. Donlan & Jill L. Rosow & Mathilda S. Nicot-Cartsonis & Alexis Cervantes & Benjamin Deneen & Andrew K. Dunn & Theresa A. Jones & , 2023. "Subventricular zone cytogenesis provides trophic support for neural repair in a mouse model of stroke," Nature Communications, Nature, vol. 14(1), pages 1-18, December.

    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. Poonam Dhillon & Kelly Ann Mulholland & Hailong Hu & Jihwan Park & Xin Sheng & Amin Abedini & Hongbo Liu & Allison Vassalotti & Junnan Wu & Katalin Susztak, 2023. "Increased levels of endogenous retroviruses trigger fibroinflammation and play a role in kidney disease development," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Andreas Herchenröther & Stefanie Gossen & Tobias Friedrich & Alexander Reim & Nadine Daus & Felix Diegmüller & Jörg Leers & Hakimeh Moghaddas Sani & Sarah Gerstner & Leah Schwarz & Inga Stellmacher & , 2023. "The H2A.Z and NuRD associated protein HMG20A controls early head and heart developmental transcription programs," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    3. Teresa Maria Rosaria Noviello & Anna Maria Giacomo & Francesca Pia Caruso & Alessia Covre & Roberta Mortarini & Giovanni Scala & Maria Claudia Costa & Sandra Coral & Wolf H. Fridman & Catherine Sautès, 2023. "Guadecitabine plus ipilimumab in unresectable melanoma: five-year follow-up and integrated multi-omic analysis in the phase 1b NIBIT-M4 trial," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    4. Tiago C. Luis & Nikolaos Barkas & Joana Carrelha & Alice Giustacchini & Stefania Mazzi & Ruggiero Norfo & Bishan Wu & Affaf Aliouat & Jose A. Guerrero & Alba Rodriguez-Meira & Tiphaine Bouriez-Jones &, 2023. "Perivascular niche cells sense thrombocytopenia and activate hematopoietic stem cells in an IL-1 dependent manner," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    5. Michael R. Kelly & Kamila Wisniewska & Matthew J. Regner & Michael W. Lewis & Andrea A. Perreault & Eric S. Davis & Douglas H. Phanstiel & Joel S. Parker & Hector L. Franco, 2022. "A multi-omic dissection of super-enhancer driven oncogenic gene expression programs in ovarian cancer," Nature Communications, Nature, vol. 13(1), pages 1-22, December.
    6. Zachary A. Hing & Janek S. Walker & Ethan C. Whipp & Lindsey Brinton & Matthew Cannon & Pu Zhang & Steven Sher & Casey B. Cempre & Fiona Brown & Porsha L. Smith & Claudio Agostinelli & Stefano A. Pile, 2023. "Dysregulation of PRMT5 in chronic lymphocytic leukemia promotes progression with high risk of Richter’s transformation," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    7. Brian M. Schilder & Alan E. Murphy & Nathan G. Skene, 2024. "rworkflows: automating reproducible practices for the R community," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    8. Jose V Die & Ransom L Baldwin & Lisa J Rowland & Robert Li & Sunghee Oh & Congjun Li & Erin E Connor & Maria-Jose Ranilla, 2017. "Selection of internal reference genes for normalization of reverse transcription quantitative polymerase chain reaction (RT-qPCR) analysis in the rumen epithelium," PLOS ONE, Public Library of Science, vol. 12(2), pages 1-13, February.
    9. Maja Olecka & Alena Bömmel & Lena Best & Madlen Haase & Silke Foerste & Konstantin Riege & Thomas Dost & Stefano Flor & Otto W. Witte & Sören Franzenburg & Marco Groth & Björn Eyss & Christoph Kaleta , 2024. "Nonlinear DNA methylation trajectories in aging male mice," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    10. 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.
    11. Daniela Klaproth-Andrade & Johannes Hingerl & Yanik Bruns & Nicholas H. Smith & Jakob Träuble & Mathias Wilhelm & Julien Gagneur, 2024. "Deep learning-driven fragment ion series classification enables highly precise and sensitive de novo peptide sequencing," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    12. Ihab Ansari & Llorenç Solé-Boldo & Meshi Ridnik & Julian Gutekunst & Oliver Gilliam & Maria Korshko & Timur Liwinski & Birgit Jickeli & Noa Weinberg-Corem & Michal Shoshkes-Carmel & Eli Pikarsky & Era, 2023. "TET2 and TET3 loss disrupts small intestine differentiation and homeostasis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Maritere Uriostegui-Arcos & Steven T. Mick & Zhuo Shi & Rufuto Rahman & Ana Fiszbein, 2023. "Splicing activates transcription from weak promoters upstream of alternative exons," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    14. Yue Yuan & Qiang Huo & Ziru Zhang & Qun Wang & Juanxia Wang & Shuaikang Chang & Peng Cai & Karen M. Song & David W. Galbraith & Weixiao Zhang & Long Huang & Rentao Song & Zeyang Ma, 2024. "Decoding the gene regulatory network of endosperm differentiation in maize," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    15. François Serra & Andrea Nieto-Aliseda & Lucía Fanlo-Escudero & Llorenç Rovirosa & Mónica Cabrera-Pasadas & Aleksey Lazarenkov & Blanca Urmeneta & Alvaro Alcalde-Merino & Emanuele M. Nola & Andrei L. O, 2024. "p53 rapidly restructures 3D chromatin organization to trigger a transcriptional response," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    16. Jacques Serizay & Cyril Matthey-Doret & Amaury Bignaud & Lyam Baudry & Romain Koszul, 2024. "Orchestrating chromosome conformation capture analysis with Bioconductor," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    17. Seppe Goovaerts & Hanne Hoskens & Ryan J. Eller & Noah Herrick & Anthony M. Musolf & Cristina M. Justice & Meng Yuan & Sahin Naqvi & Myoung Keun Lee & Dirk Vandermeulen & Heather L. Szabo-Rogers & Pau, 2023. "Joint multi-ancestry and admixed GWAS reveals the complex genetics behind human cranial vault shape," Nature Communications, Nature, vol. 14(1), pages 1-21, December.
    18. Xavier Contreras & David Depierre & Charbel Akkawi & Marina Srbic & Marion Helsmoortel & Maguelone Nogaret & Matthieu LeHars & Kader Salifou & Alexandre Heurteau & Olivier Cuvier & Rosemary Kiernan, 2023. "PAPγ associates with PAXT nuclear exosome to control the abundance of PROMPT ncRNAs," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    19. Sheng-You Liao & Dmytro Rudoy & Sander B. Frank & Luan T. Phan & Olga Klezovitch & Julian Kwan & Ilsa Coleman & Michael C. Haffner & Dapei Li & Peter S. Nelson & Andrew Emili & Valeri Vasioukhin, 2023. "SND1 binds to ERG and promotes tumor growth in genetic mouse models of prostate cancer," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    20. Thadeous J Kacmarczyk & Caitlin Bourque & Xihui Zhang & Yanwen Jiang & Yariv Houvras & Alicia Alonso & Doron Betel, 2015. "Multiplexing of ChIP-Seq Samples in an Optimized Experimental Condition Has Minimal Impact on Peak Detection," PLOS ONE, Public Library of Science, vol. 10(6), pages 1-15, June.

    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:12:y:2021:i:1:d:10.1038_s41467-021-24624-5. 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.