DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord
Abstract 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...
| Main Authors: | , , , |
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| Format: | Article |
| Language: | English |
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BMC
2023-03-01
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| Series: | Biological Research |
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| Online Access: | https://doi.org/10.1186/s40659-023-00422-9 |
| _version_ | 1827985091910959104 |
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| author | Xiuke Ouyang Bingtong Wu Haiyan Yu Bo Dong |
| author_facet | Xiuke Ouyang Bingtong Wu Haiyan Yu Bo Dong |
| author_sort | Xiuke Ouyang |
| collection | DOAJ |
| description | Abstract 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. |
| first_indexed | 2024-04-09T23:09:21Z |
| format | Article |
| id | doaj.art-0dad5031ce5e4ed38264c5edfe7e45df |
| institution | Directory Open Access Journal |
| issn | 0717-6287 |
| language | English |
| last_indexed | 2024-04-09T23:09:21Z |
| publishDate | 2023-03-01 |
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| series | Biological Research |
| spelling | doaj.art-0dad5031ce5e4ed38264c5edfe7e45df2023-03-22T10:28:14ZengBMCBiological Research0717-62872023-03-0156111610.1186/s40659-023-00422-9DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochordXiuke Ouyang0Bingtong Wu1Haiyan Yu2Bo Dong3Fang Zongxi Center, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaFang Zongxi Center, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaFang Zongxi Center, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaFang Zongxi Center, MoE Key Laboratory of Marine Genetics and Breeding, College of Marine Life Sciences, Ocean University of ChinaAbstract 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.https://doi.org/10.1186/s40659-023-00422-9EndocytosisDYRK1PhosphorylationLumen expansionBiological tube |
| spellingShingle | Xiuke Ouyang Bingtong Wu Haiyan Yu Bo Dong DYRK1-mediated phosphorylation of endocytic components is required for extracellular lumen expansion in ascidian notochord Biological Research Endocytosis DYRK1 Phosphorylation Lumen expansion Biological tube |
| 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 | Endocytosis DYRK1 Phosphorylation Lumen expansion Biological tube |
| url | https://doi.org/10.1186/s40659-023-00422-9 |
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