IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-38016-4.html
   My bibliography  Save this article

Acoel single-cell atlas reveals expression dynamics and heterogeneity of adult pluripotent stem cells

Author

Listed:
  • Ryan E. Hulett

    (Harvard University)

  • Julian O. Kimura

    (Harvard University)

  • D. Marcela Bolaños

    (Harvard University)

  • Yi-Jyun Luo

    (Harvard University
    Academia Sinica)

  • Carlos Rivera-López

    (Harvard University
    Harvard University)

  • Lorenzo Ricci

    (Harvard University)

  • Mansi Srivastava

    (Harvard University)

Abstract

Adult pluripotent stem cell (aPSC) populations underlie whole-body regeneration in many distantly-related animal lineages, but how the underlying cellular and molecular mechanisms compare across species is unknown. Here, we apply single-cell RNA sequencing to profile transcriptional cell states of the acoel worm Hofstenia miamia during postembryonic development and regeneration. We identify cell types shared across stages and their associated gene expression dynamics during regeneration. Functional studies confirm that the aPSCs, also known as neoblasts, are the source of differentiated cells and reveal transcription factors needed for differentiation. Subclustering of neoblasts recovers transcriptionally distinct subpopulations, the majority of which are likely specialized to differentiated lineages. One neoblast subset, showing enriched expression of the histone variant H3.3, appears to lack specialization. Altogether, the cell states identified in this study facilitate comparisons to other species and enable future studies of stem cell fate potentials.

Suggested Citation

  • Ryan E. Hulett & Julian O. Kimura & D. Marcela Bolaños & Yi-Jyun Luo & Carlos Rivera-López & Lorenzo Ricci & Mansi Srivastava, 2023. "Acoel single-cell atlas reveals expression dynamics and heterogeneity of adult pluripotent stem cells," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-38016-4
    DOI: 10.1038/s41467-023-38016-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-38016-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-38016-4?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. M. Lucila Scimone & Lauren E. Cote & Peter W. Reddien, 2017. "Orthogonal muscle fibres have different instructive roles in planarian regeneration," Nature, Nature, vol. 551(7682), pages 623-628, November.
    2. Simon J. Elsässer & Kyung-Min Noh & Nichole Diaz & C. David Allis & Laura A. Banaszynski, 2015. "Histone H3.3 is required for endogenous retroviral element silencing in embryonic stem cells," Nature, Nature, vol. 522(7555), pages 240-244, June.
    3. Andreas Hejnol & Mark Q. Martindale, 2008. "Acoel development indicates the independent evolution of the bilaterian mouth and anus," Nature, Nature, vol. 456(7220), pages 382-386, November.
    4. Amelie A. Raz & Mansi Srivastava & Ranja Salvamoser & Peter W. Reddien, 2017. "Acoel regeneration mechanisms indicate an ancient role for muscle in regenerative patterning," Nature Communications, Nature, vol. 8(1), pages 1-9, December.
    5. Johanna Taylor Cannon & Bruno Cossermelli Vellutini & Julian Smith & Fredrik Ronquist & Ulf Jondelius & Andreas Hejnol, 2016. "Xenacoelomorpha is the sister group to Nephrozoa," Nature, Nature, vol. 530(7588), pages 89-93, February.
    6. Lily L. Wong & Christina G. Bruxvoort & Nicholas I. Cejda & Matthew R. Delaney & Jannette Rodriguez Otero & David J. Forsthoefel, 2022. "Intestine-enriched apolipoprotein b orthologs are required for stem cell progeny differentiation and regeneration in planarians," Nature Communications, Nature, vol. 13(1), pages 1-19, 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. Paula Miramón-Puértolas & Eudald Pascual-Carreras & Patrick R. H. Steinmetz, 2024. "A population of Vasa2 and Piwi1 expressing cells generates germ cells and neurons in a sea anemone," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    2. Helen E. Robertson & Arnau Sebé-Pedrós & Baptiste Saudemont & Yann Loe-Mie & Anne-C. Zakrzewski & Xavier Grau-Bové & Marie-Pierre Mailhe & Philipp Schiffer & Maximilian J. Telford & Heather Marlow, 2024. "Single cell atlas of Xenoturbella bocki highlights limited cell-type complexity," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    3. Toshiyuki Fujita & Naoya Aoki & Chihiro Mori & Koichi J. Homma & Shinji Yamaguchi, 2024. "SoxC and MmpReg promote blastema formation in whole-body regeneration of fragmenting potworms Enchytraeus japonensis," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Patricia Álvarez-Campos & Helena García-Castro & Elena Emili & Alberto Pérez-Posada & Irene Olmo & Sophie Peron & David A. Salamanca-Díaz & Vincent Mason & Bria Metzger & Alexandra E. Bely & Nathan J., 2024. "Annelid adult cell type diversity and their pluripotent cellular origins," Nature Communications, Nature, vol. 15(1), pages 1-22, 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. Iqbal Mahmud & Guimei Tian & Jia Wang & Tarun E. Hutchinson & Brandon J. Kim & Nikee Awasthee & Seth Hale & Chengcheng Meng & Allison Moore & Liming Zhao & Jessica E. Lewis & Aaron Waddell & Shangtao , 2023. "DAXX drives de novo lipogenesis and contributes to tumorigenesis," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Guanshen Cui & Kangning Dong & Jia-Yi Zhou & Shang Li & Ying Wu & Qinghua Han & Bofei Yao & Qunlun Shen & Yong-Liang Zhao & Ying Yang & Jun Cai & Shihua Zhang & Yun-Gui Yang, 2023. "Spatiotemporal transcriptomic atlas reveals the dynamic characteristics and key regulators of planarian regeneration," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    3. Sophia Groh & Anna Viktoria Milton & Lisa Katherina Marinelli & Cara V. Sickinger & Angela Russo & Heike Bollig & Gustavo Pereira de Almeida & Andreas Schmidt & Ignasi Forné & Axel Imhof & Gunnar Scho, 2021. "Morc3 silences endogenous retroviruses by enabling Daxx-mediated histone H3.3 incorporation," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    4. Helen E. Robertson & Arnau Sebé-Pedrós & Baptiste Saudemont & Yann Loe-Mie & Anne-C. Zakrzewski & Xavier Grau-Bové & Marie-Pierre Mailhe & Philipp Schiffer & Maximilian J. Telford & Heather Marlow, 2024. "Single cell atlas of Xenoturbella bocki highlights limited cell-type complexity," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    5. Marko Dunjić & Felix Jonas & Gilad Yaakov & Roye More & Yoav Mayshar & Yoach Rais & Ayelet-Hashahar Orenbuch & Saifeng Cheng & Naama Barkai & Yonatan Stelzer, 2023. "Histone exchange sensors reveal variant specific dynamics in mouse embryonic stem cells," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    6. M. Lucila Scimone & Jennifer K. Cloutier & Chloe L. Maybrun & Peter W. Reddien, 2022. "The planarian wound epidermis gene equinox is required for blastema formation in regeneration," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    7. 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.
    8. Xiaowei Xu & Shoufu Duan & Xu Hua & Zhiming Li & Richard He & Zhiguo Zhang, 2022. "Stable inheritance of H3.3-containing nucleosomes during mitotic cell divisions," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    9. Eudald Pascual-Carreras & Marta Marín-Barba & Sergio Castillo-Lara & Pablo Coronel-Córdoba & Marta Silvia Magri & Grant N. Wheeler & Jose Luis Gómez-Skarmeta & Josep F. Abril & Emili Saló & Teresa Ade, 2023. "Wnt/β-catenin signalling is required for pole-specific chromatin remodeling during planarian regeneration," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    10. Junko Yaguchi & Kazumi Sakai & Atsushi Horiuchi & Takashi Yamamoto & Takahiro Yamashita & Shunsuke Yaguchi, 2024. "Light-modulated neural control of sphincter regulation in the evolution of through-gut," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    11. Sarah Tessier & Omar Ferhi & Marie-Claude Geoffroy & Román González-Prieto & Antoine Canat & Samuel Quentin & Marika Pla & Michiko Niwa-Kawakita & Pierre Bercier & Domitille Rérolle & Marilyn Tirard &, 2022. "Exploration of nuclear body-enhanced sumoylation reveals that PML represses 2-cell features of embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    12. Kentaro Mochizuki & Jafar Sharif & Kenjiro Shirane & Kousuke Uranishi & Aaron B. Bogutz & Sanne M. Janssen & Ayumu Suzuki & Akihiko Okuda & Haruhiko Koseki & Matthew C. Lorincz, 2021. "Repression of germline genes by PRC1.6 and SETDB1 in the early embryo precedes DNA methylation-mediated silencing," Nature Communications, Nature, vol. 12(1), pages 1-15, 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_s41467-023-38016-4. 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.