Rear traction forces drive adherent tissue migration in vivo

• Published in: Nature cell biology Vol. 24; no. 2; pp. 194 - 204
• Main Authors: Yamaguchi, Naoya, Zhang, Ziyi, Schneider, Teseo, Wang, Biran, Panozzo, Daniele, Knaut, Holger
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 01.02.2022; Nature Publishing Group
• Subjects: 14/28; 14/3; 14/35; 14/63; 38/35; 38/70; 631/136/1660; 631/80/79/2066; 631/80/84/2334; Actin; Actins - metabolism; Adhesion; Animal diseases; Animal tissues; Animals; Animals, Genetically Modified; Artificial chromosomes; Basement Membrane - metabolism; Basement Membrane - physiology; Biomedical and Life Sciences; Cancer Research; Cell Biology; Cell migration; Chemokine CXCL12 - genetics; Chemokine CXCL12 - metabolism; Chemokines; Chemotaxis; Danio rerio; Developmental Biology; Embryo, Nonmammalian - metabolism; Embryo, Nonmammalian - physiology; Embryogenesis; Embryonic growth stage; Gene Expression Regulation, Developmental; Homeostasis; Integrins; Integrins - genetics; Integrins - metabolism; Lateral line; Life Sciences; Mechanotransduction, Cellular; Morphogenesis; Physical stress; Receptors, CXCR4 - genetics; Receptors, CXCR4 - metabolism; Skin; Stem Cells; Stress, Mechanical; Substrates; Talin; Talin - genetics; Talin - metabolism; Time Factors; Traction force; Zebrafish; Zebrafish - embryology; Zebrafish - genetics; Zebrafish Proteins - genetics; Zebrafish Proteins - metabolism
• ISSN: 1465-7392; 1476-4679
• DOI: 10.1038/s41556-022-00844-9

During animal embryogenesis, homeostasis and disease, tissues push and pull on their surroundings to move forward. Although the force-generating machinery is known, it is unknown how tissues exert physical stresses on their substrate to generate motion in vivo. Here, we identify the force transmission machinery, the substrate and the stresses that a tissue, the zebrafish posterior lateral line primordium, generates during its migration. We find that the primordium couples actin flow through integrins to the basement membrane for forward movement. Talin- and integrin-mediated coupling is required for efficient migration, and its loss is partially compensated for by increased actin flow. Using Embryogram, an approach to measure stresses in vivo, we show that the rear of the primordium exerts higher stresses than the front, which suggests that this tissue pushes itself forward with its back. This unexpected strategy probably also underlies the motion of other tissues in animals. Yamaguchi et al. report an approach to measure stresses during cell migration in the zebrafish embryo in vivo, and suggest that collectively migrating cells may be pushed forward by their rear cells.