TY - JOUR
T1 - Rear traction forces drive adherent tissue migration in vivo
AU - Yamaguchi, Naoya
AU - Zhang, Ziyi
AU - Schneider, Teseo
AU - Wang, Biran
AU - Panozzo, Daniele
AU - Knaut, Holger
N1 - Funding Information:
We thank R. Lehmann, L. Christiaen, D. Rifkin, M. Schober, J. Torres-Vázquez, W. Qian, P. Vagni, S. Lau and T. Colak-Champollion for critical comments; T. Gerson, T. Colak-Champollion and A. Feitzinger for reagents; T. Gerson, J. Proietti and S. Pirani for excellent fish care; N. Paknejad for advice on AFM; M. Cammer and Y. Deng for advice on microscopy; A. Liang, C. Petzold and K. Dancel-Manning for consultation and assistance with TEM work; and A. Ferrari and N. Chala for AFM consultation. The use of the NYULH DART Microscopy Laboratory (P30CA016087) and the Memorial Sloan Kettering Molecular Cytology Core Facility (P30 CA008748) is gratefully acknowledged. For providing the zebrafish knockout allele lamC1, we thank the Zebrafish International Resource Center. For providing the cdh1:cdh1-tdTomato line, we thank M. Cronan and D. Tobin. This work was supported by NIH grant NS102322 (H.K.), by an NYSTEM fellowship C322560GG (N.Y.), by an American Heart Association fellowship 20PRE35180164 (N.Y.), in part through the NYU IT High Performance Computing resources, services, and staff expertise, the NSF CAREER award 1652515 (D.N.), the NSF grants IIS-1320635 (D.N.), OAC-1835712 (D.N.), OIA-1937043 (D.N.), CHS-1908767 (D.N.), CHS-1901091 (D.N.), a gift from Adobe Research (D.N.), a gift from nTopology (D.N.), and a gift from Advanced Micro Devices (D.N.). sa9866
Publisher Copyright:
© 2022, The Author(s), under exclusive licence to Springer Nature Limited.
PY - 2022/2
Y1 - 2022/2
N2 - 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.
AB - 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.
KW - Actins/metabolism
KW - Animals
KW - Animals, Genetically Modified
KW - Basement Membrane/metabolism
KW - Chemokine CXCL12/genetics
KW - Chemotaxis
KW - Embryo, Nonmammalian/metabolism
KW - Gene Expression Regulation, Developmental
KW - Integrins/genetics
KW - Mechanotransduction, Cellular
KW - Morphogenesis
KW - Receptors, CXCR4/genetics
KW - Stress, Mechanical
KW - Talin/genetics
KW - Time Factors
KW - Zebrafish/embryology
KW - Zebrafish Proteins/genetics
UR - http://www.scopus.com/inward/record.url?scp=85124680337&partnerID=8YFLogxK
UR - http://www.scopus.com/inward/citedby.url?scp=85124680337&partnerID=8YFLogxK
U2 - 10.1038/s41556-022-00844-9
DO - 10.1038/s41556-022-00844-9
M3 - Article
C2 - 35165417
AN - SCOPUS:85124680337
VL - 24
SP - 194
EP - 204
JO - Nature Cell Biology
JF - Nature Cell Biology
SN - 1465-7392
IS - 2
ER -