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; Robert N. Kelsh

doi:10.1038/s41467-023-36876-4

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, Robert N. Kelsh

Research output: Contribution to journal › Article › peer-review

20 Citations (SciVal)

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.

Original language	English
Article number	1258
Journal	Nature Communications
Volume	14
Issue number	1
Early online date	6 Mar 2023
DOIs	https://doi.org/10.1038/s41467-023-36876-4
Publication status	Published - 6 Mar 2023

Funding

The authors gratefully acknowledge the Technical staff within the Department of Biology & Biochemistry at the University of Bath for technical support and assistance; Nathaniel S. Gray for providing us with ALK inhibitor, TAE684; Richard Jäger for p80 cDNA for template of NPM , reagents for BAC recombineering from Biological Resources Branch of Frederick National Library for Cancer Research, and Shin-ichi Higashijima for egfp -polyA cassette for recombineering. Rosalind John (University of Cardiff) kindly supplied the reagents for the RecA mediated PAC recombineering. We thank Marie Srotyr and Tia Dally for their technical assistance in experiments for Supplementary Fig. 11a. We thank Alfonso Martinez-Arias for helpful discussions in the early years of this project. We thank Adele Murrell and Andrew Ward for their critical comments on an earlier draft of this manuscript. This work was supported by Uehara Memorial Foundation (MN), Wellcome Trust VIP awards (M.N.), and BBSRC grants BB/ L00769X/1(R.N.K., H.S., T.S.) and BB/S015906/1 (R.N.K., J.H.P.D., K.C.S., G.B.) and BB/L007789/1 and BB/S01604X/1 (A.R.), National Natural Science Foundation of China, Grant Number: 31000542 (X.Y.), Royal Society International Exchange Cost Share 2017 Russia award (R.N.K.), Russian Foundation of Basic Researcher grant 17-54-10014 (V.J.M.), Ministry of Science and Higher Education of the Russian Federation Grant number 075-15-2021-601 (V.J.M.), and University of Bath PhD Studentship and ORS award (T.J.C.).

ASJC Scopus subject areas

General Chemistry
General Biochemistry,Genetics and Molecular Biology
General
General Physics and Astronomy

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10.1038/s41467-023-36876-4Licence: CC BY

Cite this

Subkhankulova, T., Camargo Sosa, K., Uroshlev, L. A., Nikaido, M., Shriever, N., Kasianov, A. S., Yang, X., Rodrigues, F. S. L. M., Carney, T. J., Bavister, G., Schwetlick, H., Dawes, J. H. P., Rocco, A., Makeev, V. J., & Kelsh, R. N. (2023). Zebrafish pigment cells develop directly from persistent highly multipotent progenitors. Nature Communications, 14(1), Article 1258. https://doi.org/10.1038/s41467-023-36876-4

Subkhankulova, T, Camargo Sosa, K, Uroshlev, LA, Nikaido, M, Shriever, N, Kasianov, AS, Yang, X, Rodrigues, FSLM, Carney, TJ, Bavister, G, Schwetlick, H , Dawes, JHP, Rocco, A, Makeev, VJ & Kelsh, RN 2023, 'Zebrafish pigment cells develop directly from persistent highly multipotent progenitors', Nature Communications, vol. 14, no. 1, 1258. https://doi.org/10.1038/s41467-023-36876-4

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title = "Zebrafish pigment cells develop directly from persistent highly multipotent progenitors",

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.",

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Zebrafish pigment cells develop directly from persistent highly multipotent progenitors

Abstract

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Rethinking the neural crest – a novel dynamic model of neural crest fate restriction

A Systems Biology Approach to Neural Crest Development

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Zebrafish pigment cells develop directly from persistent highly multipotent progenitors

Abstract

Funding

ASJC Scopus subject areas

Access to Document

Other files and links

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Rethinking the neural crest – a novel dynamic model of neural crest fate restriction

A Systems Biology Approach to Neural Crest Development

Cite this