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Zebrafish pigment cells develop directly from persistent highly multipotent progenitors

Author

Listed:
  • Tatiana Subkhankulova

    (University of Bath, Claverton Down)

  • Karen Camargo Sosa

    (University of Bath, Claverton Down)

  • Leonid A. Uroshlev

    (Russian Academy of Sciences)

  • Masataka Nikaido

    (University of Bath, Claverton Down
    University of Hyogo)

  • Noah Shriever

    (University of Bath, Claverton Down)

  • Artem S. Kasianov

    (Russian Academy of Sciences
    Moscow Institute of Physics and Technology
    A.A. Kharkevich Institute for Information Transmission Problems (IITP))

  • Xueyan Yang

    (University of Bath, Claverton Down
    School of Life Sciences, Fudan University)

  • Frederico S. L. M. Rodrigues

    (University of Bath, Claverton Down)

  • Thomas J. Carney

    (University of Bath, Claverton Down
    Nanyang Technological University)

  • Gemma Bavister

    (University of Bath, Claverton Down)

  • Hartmut Schwetlick

    (University of Bath, Claverton Down)

  • Jonathan H. P. Dawes

    (University of Bath, Claverton Down)

  • Andrea Rocco

    (FHMS, University of Surrey
    FEPS, University of Surrey)

  • Vsevolod J. Makeev

    (Russian Academy of Sciences
    Moscow Institute of Physics and Technology
    Kazan Federal University)

  • Robert N. Kelsh

    (University of Bath, Claverton Down)

Abstract

Neural crest cells are highly multipotent stem cells, but it remains unclear how their fate restriction to specific fates occurs. The direct fate restriction model hypothesises that migrating cells maintain full multipotency, whilst progressive fate restriction envisages fully multipotent cells transitioning to partially-restricted intermediates before committing to individual fates. Using zebrafish pigment cell development as a model, we show applying NanoString hybridization single cell transcriptional profiling and RNAscope in situ hybridization that neural crest cells retain broad multipotency throughout migration and even in post-migratory cells in vivo, with no evidence for partially-restricted intermediates. We find that leukocyte tyrosine kinase early expression marks a multipotent stage, with signalling driving iridophore differentiation through repression of fate-specific transcription factors for other fates. We reconcile the direct and progressive fate restriction models by proposing that pigment cell development occurs directly, but dynamically, from a highly multipotent state, consistent with our recently-proposed Cyclical Fate Restriction model.

Suggested Citation

  • Tatiana Subkhankulova & Karen Camargo Sosa & Leonid A. Uroshlev & Masataka Nikaido & Noah Shriever & Artem S. Kasianov & Xueyan Yang & Frederico S. L. M. Rodrigues & Thomas J. Carney & Gemma Bavister , 2023. "Zebrafish pigment cells develop directly from persistent highly multipotent progenitors," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36876-4
    DOI: 10.1038/s41467-023-36876-4
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    References listed on IDEAS

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    1. Waltman, Ludo & van Eck, Nees Jan & Noyons, Ed C.M., 2010. "A unified approach to mapping and clustering of bibliometric networks," Journal of Informetrics, Elsevier, vol. 4(4), pages 629-635.
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