Twisted cell flow facilitates three-dimensional somite morphogenesis in zebrafish

Tissue elongation is a fundamental morphogenetic process to construct complex embryonic structures. In zebrafish, somites rapidly elongate in both dorsal and ventral directions, transforming from a cuboidal to a V-shape within a few hours of development. Despite its significance, the cellular behaviors that directly lead to somite elongation have not been examined at single-cell resolution. Here, we describe the motion and shapes of all cells composing the dorsal half of the somite in three-dimensional space using lightsheet microscopy. We identified two types of cell movements-in horizontal and dorsal directions-that occur simultaneously within individual cells, creating a complex, twisted flow of cells during somite elongation. Chemical inhibition of Sdf1 signaling disrupted the collective movement in both directions and inhibited somite elongation, suggesting that Sdf1 signaling is crucial for this cell flow. Furthermore, three-dimensional computational modeling suggested that horizontal cell rotation accelerates the perpendicular elongation of the somite along the dorsoventral axis. Together, our study offers novel insights into the role of collective cell migration in tissue morphogenesis, which proceeds dynamically in the three-dimensional space of the embryo.

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Publication Details

Journal
Cells and Development
Published
2024-08-26
DOI
https://doi.org/10.1016/j.cdev.2024.203969
Citations
2
Primary Topic
Congenital heart defects research
Type
article
Field-Weighted Citation Impact
0.47

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article

Twisted cell flow facilitates three-dimensional somite morphogenesis in zebrafish

Toru Kawanishi, Harunobu Kametani, Takamichi Sushida, Yue Tong et al.
2 citations
Cells and Development
Congenital heart defects research
0.47
article

Twisted cell flow facilitates three-dimensional somite morphogenesis in zebrafish

Toru Kawanishi, Harunobu Kametani, Takamichi Sushida, Yue Tong, Hiroyuki Takeda, Masakazu Akiyama, Atsuko Shimada
article en
2 citations

Abstract

Tissue elongation is a fundamental morphogenetic process to construct complex embryonic structures. In zebrafish, somites rapidly elongate in both dorsal and ventral directions, transforming from a cuboidal to a V-shape within a few hours of development. Despite its significance, the cellular behaviors that directly lead to somite elongation have not been examined at single-cell resolution. Here, we describe the motion and shapes of all cells composing the dorsal half of the somite in three-dimensional space using lightsheet microscopy. We identified two types of cell movements-in horizontal and dorsal directions-that occur simultaneously within individual cells, creating a complex, twisted flow of cells during somite elongation. Chemical inhibition of Sdf1 signaling disrupted the collective movement in both directions and inhibited somite elongation, suggesting that Sdf1 signaling is crucial for this cell flow. Furthermore, three-dimensional computational modeling suggested that horizontal cell rotation accelerates the perpendicular elongation of the somite along the dorsoventral axis. Together, our study offers novel insights into the role of collective cell migration in tissue morphogenesis, which proceeds dynamically in the three-dimensional space of the embryo.

Cells and DevelopmentVol. 180
Tokyo University of Science (JP), Kyoto Sangyo University (JP), Kyoto University (JP), University of Fukuchiyama (JP), University of Toyama (JP), The University of Tokyo (JP)
Japan Society for the Promotion of Science
Life below water
Openalex Percentile: Top 36%
Congenital heart defects research
0.47
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Twisted cell flow facilitates three-dimensional somite morphogenesis in zebrafish — Toru Kawanishi, Harunobu Kametani, et al. · Cells and Development (2024) | TGRS Research Map | TGRS