TY - JOUR
T1 - Local increases in mechanical tension shape compartment boundaries by biasing cell intercalations
AU - Umetsu, Daiki
AU - Aigouy, Benoît
AU - Aliee, Maryam
AU - Sui, Liyuan
AU - Eaton, Suzanne
AU - Jülicher, Frank
AU - Dahmann, Christian
N1 - Funding Information:
This work was initiated while D.U. and C.D. were at the Max Planck Institute of Molecular Cell Biology and Genetics (MPI-CBG). We thank the MPI-CBG imaging facility for providing access to imaging equipment and S. Grill and M. Nishikawa for providing their laser ablation system. We thank K. Rudolf, F. Aurich, C. Gogdas, F.P. Herrmann, S. Jedlicka, R. Kindermann, S. Lübke, and A.-C. Stuhr for help with image processing, Y. Hong for fly stocks, and G. Salbreux and S. Grill for comments on the manuscript. This work was supported by the Japan Society for the Promotion of Science (D.U.) and the Deutsche Forschungsgemeinschaft (DA586/10, DA586/13-1, and DA586/14 to C.D.).
Copyright:
Copyright 2014 Elsevier B.V., All rights reserved.
PY - 2014/8/4
Y1 - 2014/8/4
N2 - Mechanical forces play important roles during tissue organization in developing animals. Many tissues are organized into adjacent, nonmixing groups of cells termed compartments [1-7]. Boundaries between compartments display a straight morphology and are associated with signaling centers that are important for tissue growth and patterning [8]. Local increases in mechanical tension at cell junctions along compartment boundaries have recently been shown to prevent cell mixing and to maintain straight boundaries [9-13]. The cellular mechanisms by which local increases in mechanical tension prevent cell mixing at compartment boundaries, however, remain poorly understood. Here, we have used live imaging and quantitative image analysis to determine cellular dynamics at and near the anteroposterior compartment boundaries of the Drosophila pupal abdominal epidermis. We show that cell mixing within compartments involves multiple cell intercalations. Frequency and orientation of cell intercalations are unchanged along the compartment boundaries; rather, an asymmetry in the shrinkage of junctions during intercalation is biased, resulting in cell rearrangements that suppress cell mixing. Simulations of tissue growth show that local increases in mechanical tension can account for this bias in junctional shrinkage. We conclude that local increases in mechanical tension maintain cell populations separate by influencing junctional rearrangements during cell intercalation.
AB - Mechanical forces play important roles during tissue organization in developing animals. Many tissues are organized into adjacent, nonmixing groups of cells termed compartments [1-7]. Boundaries between compartments display a straight morphology and are associated with signaling centers that are important for tissue growth and patterning [8]. Local increases in mechanical tension at cell junctions along compartment boundaries have recently been shown to prevent cell mixing and to maintain straight boundaries [9-13]. The cellular mechanisms by which local increases in mechanical tension prevent cell mixing at compartment boundaries, however, remain poorly understood. Here, we have used live imaging and quantitative image analysis to determine cellular dynamics at and near the anteroposterior compartment boundaries of the Drosophila pupal abdominal epidermis. We show that cell mixing within compartments involves multiple cell intercalations. Frequency and orientation of cell intercalations are unchanged along the compartment boundaries; rather, an asymmetry in the shrinkage of junctions during intercalation is biased, resulting in cell rearrangements that suppress cell mixing. Simulations of tissue growth show that local increases in mechanical tension can account for this bias in junctional shrinkage. We conclude that local increases in mechanical tension maintain cell populations separate by influencing junctional rearrangements during cell intercalation.
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U2 - 10.1016/j.cub.2014.06.052
DO - 10.1016/j.cub.2014.06.052
M3 - Article
C2 - 25065753
AN - SCOPUS:84905673640
VL - 24
SP - 1798
EP - 1805
JO - Current Biology
JF - Current Biology
SN - 0960-9822
IS - 15
ER -