Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos

To form tissues with unique functions and structures, it is important that the cells that comprise them maintain physical contact. On the other hand, with each mitosis, drastic changes in cell shapes, cell adhesion, and cytoskeletal architecture may cause such contacts to be temporarily weakened, ri...

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Main Authors: Hideko Utsumi, Taijiro Yabe, Sumito Koshida, Akira Yamashita, Shinji Takada
Format: Article
Language:English
Published: Frontiers Media S.A. 2024-03-01
Series:Frontiers in Cell and Developmental Biology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcell.2024.1375655/full
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author Hideko Utsumi
Hideko Utsumi
Taijiro Yabe
Taijiro Yabe
Taijiro Yabe
Sumito Koshida
Sumito Koshida
Sumito Koshida
Akira Yamashita
Akira Yamashita
Akira Yamashita
Shinji Takada
Shinji Takada
Shinji Takada
author_facet Hideko Utsumi
Hideko Utsumi
Taijiro Yabe
Taijiro Yabe
Taijiro Yabe
Sumito Koshida
Sumito Koshida
Sumito Koshida
Akira Yamashita
Akira Yamashita
Akira Yamashita
Shinji Takada
Shinji Takada
Shinji Takada
author_sort Hideko Utsumi
collection DOAJ
description To form tissues with unique functions and structures, it is important that the cells that comprise them maintain physical contact. On the other hand, with each mitosis, drastic changes in cell shapes, cell adhesion, and cytoskeletal architecture may cause such contacts to be temporarily weakened, risking improper development and maintenance of tissues. Despite such risks, tissues form properly during normal development. However, it is not well understood whether mitotic abnormalities affect tissue formation. Here, analysis of zebrafish embryos with aberrant mitosis shows that proper progression of mitosis is important to maintain cell contact in developing tissues. By screening mutants with abnormal trunk and tail development, we obtained a mutant with perturbed expression of some tissue-specific genes in embryonic caudal regions. The responsible gene is mastl/gwl, which is involved in progression of mitosis. Analysis focusing on the chordo-neural hinge (CNH), the primordium of axial tissues, shows that cell detachment from the CNH is increased in mastl mutant embryos. Time-lapse imaging reveals that this cell detachment occurs during mitosis. These results suggest that cells are unable to maintain contact due to abnormalities in progression of mitosis in mastl mutants.
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spelling doaj.art-6ca67af4c2a14a9f8c382e7816720fb02024-03-11T05:03:41ZengFrontiers Media S.A.Frontiers in Cell and Developmental Biology2296-634X2024-03-011210.3389/fcell.2024.13756551375655Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryosHideko Utsumi0Hideko Utsumi1Taijiro Yabe2Taijiro Yabe3Taijiro Yabe4Sumito Koshida5Sumito Koshida6Sumito Koshida7Akira Yamashita8Akira Yamashita9Akira Yamashita10Shinji Takada11Shinji Takada12Shinji Takada13National Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, JapanExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Aichi, JapanNational Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, JapanExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Aichi, JapanThe Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi, JapanNational Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, JapanThe Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi, JapanShumei University, Yachiyo, Chiba, JapanNational Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, JapanThe Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi, JapanGraduate School of Arts and Science, The university of Tokyo, Tokyo, JapanNational Institute for Basic Biology, National Institutes of Natural Sciences, Okazaki, Aichi, JapanExploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural Sciences, Okazaki, Aichi, JapanThe Graduate University for Advanced Studies (SOKENDAI), Okazaki, Aichi, JapanTo form tissues with unique functions and structures, it is important that the cells that comprise them maintain physical contact. On the other hand, with each mitosis, drastic changes in cell shapes, cell adhesion, and cytoskeletal architecture may cause such contacts to be temporarily weakened, risking improper development and maintenance of tissues. Despite such risks, tissues form properly during normal development. However, it is not well understood whether mitotic abnormalities affect tissue formation. Here, analysis of zebrafish embryos with aberrant mitosis shows that proper progression of mitosis is important to maintain cell contact in developing tissues. By screening mutants with abnormal trunk and tail development, we obtained a mutant with perturbed expression of some tissue-specific genes in embryonic caudal regions. The responsible gene is mastl/gwl, which is involved in progression of mitosis. Analysis focusing on the chordo-neural hinge (CNH), the primordium of axial tissues, shows that cell detachment from the CNH is increased in mastl mutant embryos. Time-lapse imaging reveals that this cell detachment occurs during mitosis. These results suggest that cells are unable to maintain contact due to abnormalities in progression of mitosis in mastl mutants.https://www.frontiersin.org/articles/10.3389/fcell.2024.1375655/fullMASTLmitosiszebrafishaxis elongationchordo-neural hingecell detachment
spellingShingle Hideko Utsumi
Hideko Utsumi
Taijiro Yabe
Taijiro Yabe
Taijiro Yabe
Sumito Koshida
Sumito Koshida
Sumito Koshida
Akira Yamashita
Akira Yamashita
Akira Yamashita
Shinji Takada
Shinji Takada
Shinji Takada
Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
Frontiers in Cell and Developmental Biology
MASTL
mitosis
zebrafish
axis elongation
chordo-neural hinge
cell detachment
title Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
title_full Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
title_fullStr Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
title_full_unstemmed Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
title_short Deficiency of mastl, a mitotic regulator, results in cell detachment from developing tissues of zebrafish embryos
title_sort deficiency of mastl a mitotic regulator results in cell detachment from developing tissues of zebrafish embryos
topic MASTL
mitosis
zebrafish
axis elongation
chordo-neural hinge
cell detachment
url https://www.frontiersin.org/articles/10.3389/fcell.2024.1375655/full
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