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Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis

Cell morphology and tissue integrity are essential for embryogenesis. Caveolins are membrane proteins that induce the formation of surface pits called caveolae that serve as membrane reservoirs for cell and tissue protection during development. In vertebrates, caveolin 1 (Cav1) and caveolin 3 (Cav3)...

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Autores principales: Bhattachan, Punit, Rae, James, Yu, Haiyan, Jung, WooRam, Wei, Jiankai, Parton, Robert G., Dong, Bo
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7383883/
https://www.ncbi.nlm.nih.gov/pubmed/31914618
http://dx.doi.org/10.1096/fj.201901281R
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author Bhattachan, Punit
Rae, James
Yu, Haiyan
Jung, WooRam
Wei, Jiankai
Parton, Robert G.
Dong, Bo
author_facet Bhattachan, Punit
Rae, James
Yu, Haiyan
Jung, WooRam
Wei, Jiankai
Parton, Robert G.
Dong, Bo
author_sort Bhattachan, Punit
collection PubMed
description Cell morphology and tissue integrity are essential for embryogenesis. Caveolins are membrane proteins that induce the formation of surface pits called caveolae that serve as membrane reservoirs for cell and tissue protection during development. In vertebrates, caveolin 1 (Cav1) and caveolin 3 (Cav3) are required for caveola formation. However, the formation of caveola and the function of caveolins in invertebrates are largely unknown. In this study, three caveolins, Cav‐a, Cav‐b, and CavY, are identified in the genome of the invertebrate chordate Ciona spp. Based on phylogenetic analysis, Cav‐a is found to be closely related to the vertebrate Cav1 and Cav3. In situ hybridization shows that Cav‐a is expressed in Ciona embryonic notochord and muscle. Cell‐free experiments, model cell culture systems, and in vivo experiments demonstrate that Ciona Cav‐a has the ability to induce membrane curvature at the plasma membrane. Knockdown of Cav‐a in Ciona embryos causes loss of invaginations in the plasma membrane and results in the failure of notochord elongation and lumenogenesis. Expression of a dominant‐negative Cav‐a point mutation causes cells to change shape and become displaced from the muscle and notochord to disrupt tissue integrity. Furthermore, we demonstrate that Cav‐a vesicles show polarized trafficking and localize at the luminal membrane during notochord lumenogenesis. Taken together, these results show that the invertebrate chordate caveolin from Ciona plays crucial roles in tissue integrity and morphology by inducing membrane curvature and intracellular vesicle trafficking during embryogenesis.
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spelling pubmed-73838832020-07-27 Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis Bhattachan, Punit Rae, James Yu, Haiyan Jung, WooRam Wei, Jiankai Parton, Robert G. Dong, Bo FASEB J Research Articles Cell morphology and tissue integrity are essential for embryogenesis. Caveolins are membrane proteins that induce the formation of surface pits called caveolae that serve as membrane reservoirs for cell and tissue protection during development. In vertebrates, caveolin 1 (Cav1) and caveolin 3 (Cav3) are required for caveola formation. However, the formation of caveola and the function of caveolins in invertebrates are largely unknown. In this study, three caveolins, Cav‐a, Cav‐b, and CavY, are identified in the genome of the invertebrate chordate Ciona spp. Based on phylogenetic analysis, Cav‐a is found to be closely related to the vertebrate Cav1 and Cav3. In situ hybridization shows that Cav‐a is expressed in Ciona embryonic notochord and muscle. Cell‐free experiments, model cell culture systems, and in vivo experiments demonstrate that Ciona Cav‐a has the ability to induce membrane curvature at the plasma membrane. Knockdown of Cav‐a in Ciona embryos causes loss of invaginations in the plasma membrane and results in the failure of notochord elongation and lumenogenesis. Expression of a dominant‐negative Cav‐a point mutation causes cells to change shape and become displaced from the muscle and notochord to disrupt tissue integrity. Furthermore, we demonstrate that Cav‐a vesicles show polarized trafficking and localize at the luminal membrane during notochord lumenogenesis. Taken together, these results show that the invertebrate chordate caveolin from Ciona plays crucial roles in tissue integrity and morphology by inducing membrane curvature and intracellular vesicle trafficking during embryogenesis. John Wiley and Sons Inc. 2019-11-30 2020-01 /pmc/articles/PMC7383883/ /pubmed/31914618 http://dx.doi.org/10.1096/fj.201901281R Text en © 2019 The Authors. The FASEB Journal published by Wiley Periodicals, Inc. on behalf of Federation of American Societies for Experimental Biology This is an open access article under the terms of the http://creativecommons.org/licenses/by-nc/4.0/ License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes.
spellingShingle Research Articles
Bhattachan, Punit
Rae, James
Yu, Haiyan
Jung, WooRam
Wei, Jiankai
Parton, Robert G.
Dong, Bo
Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title_full Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title_fullStr Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title_full_unstemmed Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title_short Ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
title_sort ascidian caveolin induces membrane curvature and protects tissue integrity and morphology during embryogenesis
topic Research Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7383883/
https://www.ncbi.nlm.nih.gov/pubmed/31914618
http://dx.doi.org/10.1096/fj.201901281R
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