Zebrafish pigment cells develop directly from persistent highly multipotent progenitors

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, Hartmut Schwetlick, Jonathan H. P. Dawes, Andrea Rocco, Vsevolod J. Makeev and Robert N. Kelsh ()
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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
Noah Shriever: University of Bath, Claverton Down
Artem S. Kasianov: Russian Academy of Sciences
Xueyan Yang: University of Bath, Claverton Down
Frederico S. L. M. Rodrigues: University of Bath, Claverton Down
Thomas J. Carney: University of Bath, Claverton Down
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
Vsevolod J. Makeev: Russian Academy of Sciences
Robert N. Kelsh: University of Bath, Claverton Down

Nature Communications, 2023, vol. 14, issue 1, 1-19

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41467-023-36876-4

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