Twisted cell flow facilitates three-dimensional somite morphogenesis in zebrafish.

Collective cell migration Sdf1 signaling Somite elongation Whole-somite rotation Zebrafish

Journal

Cells & development
ISSN: 2667-2901
Titre abrégé: Cells Dev
Pays: Netherlands
ID NLM: 101775611

Informations de publication

Date de publication:
25 Aug 2024
Historique:
received: 09 03 2024
revised: 05 07 2024
accepted: 23 08 2024
medline: 28 8 2024
pubmed: 28 8 2024
entrez: 27 8 2024
Statut: aheadofprint

Résumé

Tissue elongation is a fundamental morphogenetic process to construct complex embryonic structures. In zebrafish, somites rapidly elongate in both dorsal and ventral directions and transform their cuboidal shape into 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 described 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 movement-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 the 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.

Identifiants

pubmed: 39191372
pii: S2667-2901(24)00079-2
doi: 10.1016/j.cdev.2024.203969
pii:
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

203969

Informations de copyright

Copyright © 2024. Published by Elsevier B.V.

Déclaration de conflit d'intérêts

Declaration of competing interest The authors declare no relevant financial or non-financial interests to disclose.

Auteurs

Harunobu Kametani (H)

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan.

Yue Tong (Y)

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan.

Atsuko Shimada (A)

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan.

Hiroyuki Takeda (H)

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan; Faculty of Life Sciences, Kyoto Sangyo University, Kyoto 603-8555, Japan. Electronic address: takeda_h@cc.kyoto-su.ac.jp.

Takamichi Sushida (T)

Faculty of Informatics, University of Fukuchiyama, Kyoto 620-0886, Japan. Electronic address: sushida-takamichi@fukuchiyama.ac.jp.

Masakazu Akiyama (M)

Department of Mathematics, Faculty of Science, Academic Assembly, University of Toyama, 3190 Gofuku, Toyama 930-8555, Japan. Electronic address: masakazu.akiyam@gmail.com.

Toru Kawanishi (T)

Department of Biological Sciences, Graduate School of Science, University of Tokyo, Bunkyo, Tokyo 113-0033, Japan; School of Life Science and Technology, Tokyo Institute of Technology, Yokohama 226-8501, Japan. Electronic address: toru.kawanishi@bio.titech.ac.jp.

Classifications MeSH