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DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord
BACKGROUND: The biological tube is a basal biology structure distributed in all multicellular animals, from worms to humans, and has diverse biological functions. Formation of tubular system is crucial for embryogenesis and adult metabolism. Ascidian Ciona notochord lumen is an excellent in vivo mod...
Autores principales: | , , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
BioMed Central
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10007804/ https://www.ncbi.nlm.nih.gov/pubmed/36899423 http://dx.doi.org/10.1186/s40659-023-00422-9 |
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author | Ouyang, Xiuke Wu, Bingtong Yu, Haiyan Dong, Bo |
author_facet | Ouyang, Xiuke Wu, Bingtong Yu, Haiyan Dong, Bo |
author_sort | Ouyang, Xiuke |
collection | PubMed |
description | BACKGROUND: The biological tube is a basal biology structure distributed in all multicellular animals, from worms to humans, and has diverse biological functions. Formation of tubular system is crucial for embryogenesis and adult metabolism. Ascidian Ciona notochord lumen is an excellent in vivo model for tubulogenesis. Exocytosis has been known to be essential for tubular lumen formation and expansion. The roles of endocytosis in tubular lumen expansion remain largely unclear. RESULTS: In this study, we first identified a dual specificity tyrosine-phosphorylation-regulated kinase 1 (DYRK1), the protein kinase, which was upregulated and required for ascidian notochord extracellular lumen expansion. We demonstrated that DYRK1 interacted with and phosphorylated one of the endocytic components endophilin at Ser263 that was essential for notochord lumen expansion. Moreover, through phosphoproteomic sequencing, we revealed that in addition to endophilin, the phosphorylation of other endocytic components was also regulated by DYRK1. The loss of function of DYRK1 disturbed endocytosis. Then, we demonstrated that clathrin-mediated endocytosis existed and was required for notochord lumen expansion. In the meantime, the results showed that the secretion of notochord cells is vigorous in the apical membrane. CONCLUSIONS: We found the co-existence of endocytosis and exocytosis activities in apical membrane during lumen formation and expansion in Ciona notochord. A novel signaling pathway is revealed that DYRK1 regulates the endocytosis by phosphorylation that is required for lumen expansion. Our finding thus indicates a dynamic balance between endocytosis and exocytosis is crucial to maintain apical membrane homeostasis that is essential for lumen growth and expansion in tubular organogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40659-023-00422-9. |
format | Online Article Text |
id | pubmed-10007804 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-100078042023-03-12 DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord Ouyang, Xiuke Wu, Bingtong Yu, Haiyan Dong, Bo Biol Res Research Article BACKGROUND: The biological tube is a basal biology structure distributed in all multicellular animals, from worms to humans, and has diverse biological functions. Formation of tubular system is crucial for embryogenesis and adult metabolism. Ascidian Ciona notochord lumen is an excellent in vivo model for tubulogenesis. Exocytosis has been known to be essential for tubular lumen formation and expansion. The roles of endocytosis in tubular lumen expansion remain largely unclear. RESULTS: In this study, we first identified a dual specificity tyrosine-phosphorylation-regulated kinase 1 (DYRK1), the protein kinase, which was upregulated and required for ascidian notochord extracellular lumen expansion. We demonstrated that DYRK1 interacted with and phosphorylated one of the endocytic components endophilin at Ser263 that was essential for notochord lumen expansion. Moreover, through phosphoproteomic sequencing, we revealed that in addition to endophilin, the phosphorylation of other endocytic components was also regulated by DYRK1. The loss of function of DYRK1 disturbed endocytosis. Then, we demonstrated that clathrin-mediated endocytosis existed and was required for notochord lumen expansion. In the meantime, the results showed that the secretion of notochord cells is vigorous in the apical membrane. CONCLUSIONS: We found the co-existence of endocytosis and exocytosis activities in apical membrane during lumen formation and expansion in Ciona notochord. A novel signaling pathway is revealed that DYRK1 regulates the endocytosis by phosphorylation that is required for lumen expansion. Our finding thus indicates a dynamic balance between endocytosis and exocytosis is crucial to maintain apical membrane homeostasis that is essential for lumen growth and expansion in tubular organogenesis. SUPPLEMENTARY INFORMATION: The online version contains supplementary material available at 10.1186/s40659-023-00422-9. BioMed Central 2023-03-11 /pmc/articles/PMC10007804/ /pubmed/36899423 http://dx.doi.org/10.1186/s40659-023-00422-9 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open AccessThis 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 licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence 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 licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
spellingShingle | Research Article Ouyang, Xiuke Wu, Bingtong Yu, Haiyan Dong, Bo DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title | DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title_full | DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title_fullStr | DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title_full_unstemmed | DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title_short | DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
title_sort | dyrk1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10007804/ https://www.ncbi.nlm.nih.gov/pubmed/36899423 http://dx.doi.org/10.1186/s40659-023-00422-9 |
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