Zebrafish pigment cells develop directly from persistent highly multipotent progenitors
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 tran...
| Main Authors: | , , , , , , , , , , , , , , |
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| Other Authors: | |
| Format: | Journal Article |
| Language: | English |
| Published: |
2023
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| Subjects: | |
| Online Access: | https://hdl.handle.net/10356/169754 |
| _version_ | 1811688732256894976 |
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| author | Subkhankulova, Tatiana Sosa, Karen Camargo Uroshlev, Leonid A. Nikaido, Masataka Shriever, Noah Kasianov, Artem S. Yang, Xueyan Rodrigues, Frederico S. L. M. Carney, Tom J. Bavister, Gemma Schwetlick, Hartmut Dawes, Jonathan H. P. Rocco, Andrea Makeev, Vsevolod J. Kelsh, Robert N. |
| author2 | Lee Kong Chian School of Medicine (LKCMedicine) |
| author_facet | Lee Kong Chian School of Medicine (LKCMedicine) Subkhankulova, Tatiana Sosa, Karen Camargo Uroshlev, Leonid A. Nikaido, Masataka Shriever, Noah Kasianov, Artem S. Yang, Xueyan Rodrigues, Frederico S. L. M. Carney, Tom J. Bavister, Gemma Schwetlick, Hartmut Dawes, Jonathan H. P. Rocco, Andrea Makeev, Vsevolod J. Kelsh, Robert N. |
| author_sort | Subkhankulova, Tatiana |
| collection | NTU |
| description | 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. |
| first_indexed | 2024-10-01T05:36:53Z |
| format | Journal Article |
| id | ntu-10356/169754 |
| institution | Nanyang Technological University |
| language | English |
| last_indexed | 2024-10-01T05:36:53Z |
| publishDate | 2023 |
| record_format | dspace |
| spelling | ntu-10356/1697542023-08-06T15:38:17Z Zebrafish pigment cells develop directly from persistent highly multipotent progenitors Subkhankulova, Tatiana Sosa, Karen Camargo Uroshlev, Leonid A. Nikaido, Masataka Shriever, Noah Kasianov, Artem S. Yang, Xueyan Rodrigues, Frederico S. L. M. Carney, Tom J. Bavister, Gemma Schwetlick, Hartmut Dawes, Jonathan H. P. Rocco, Andrea Makeev, Vsevolod J. Kelsh, Robert N. Lee Kong Chian School of Medicine (LKCMedicine) Science::Medicine Leukocyte Tyrosine Kinase Multipotent Stem Cell 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. Published version 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.). 2023-08-02T01:30:32Z 2023-08-02T01:30:32Z 2023 Journal Article Subkhankulova, T., Sosa, K. C., 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), 1258-. https://dx.doi.org/10.1038/s41467-023-36876-4 2041-1723 https://hdl.handle.net/10356/169754 10.1038/s41467-023-36876-4 36878908 2-s2.0-85149958709 1 14 1258 en Nature Communications © The Author(s) 2023. Open Access. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/ licenses/by/4.0/. application/pdf |
| spellingShingle | Science::Medicine Leukocyte Tyrosine Kinase Multipotent Stem Cell Subkhankulova, Tatiana Sosa, Karen Camargo Uroshlev, Leonid A. Nikaido, Masataka Shriever, Noah Kasianov, Artem S. Yang, Xueyan Rodrigues, Frederico S. L. M. Carney, Tom J. Bavister, Gemma Schwetlick, Hartmut Dawes, Jonathan H. P. Rocco, Andrea Makeev, Vsevolod J. Kelsh, Robert N. Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title | Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title_full | Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title_fullStr | Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title_full_unstemmed | Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title_short | Zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| title_sort | zebrafish pigment cells develop directly from persistent highly multipotent progenitors |
| topic | Science::Medicine Leukocyte Tyrosine Kinase Multipotent Stem Cell |
| url | https://hdl.handle.net/10356/169754 |
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