Convergent extension requires adhesion-dependent biomechanical integration of cell crawling and junction contraction

被引:12
|
作者
Weng, Shinuo [1 ]
Huebner, Robert J. [1 ]
Wallingford, John B. [1 ]
机构
[1] Univ Texas Austin, Dept Mol Biosci, Patterson Labs, 2401 Speedway, Austin, TX 78712 USA
来源
CELL REPORTS | 2022年 / 39卷 / 04期
关键词
XENOPUS; INTERCALATION; POLARITY; FORCE; SEGMENTATION; PRINCIPLES; ACTOMYOSIN; MOTILITY; MODEL; CATCH;
D O I
10.1016/j.celrep.2022.110666
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Convergent extension (CE) is an evolutionarily conserved collective cell movement that elongates several organ systems during development. Studies have revealed two distinct cellular mechanisms, one based on cell crawling and the other on junction contraction. Whether these two behaviors collaborate is unclear. Here, using live-cell imaging, we show that crawling and contraction act both independently and jointly but that CE is more effective when they are integrated via mechano-reciprocity. We thus developed a computational model considering both crawling and contraction. This model recapitulates the biomechanical efficacy of integrating the two modes and further clarifies how the two modes and their integration are influenced by cell adhesion. Finally, we use these insights to understand the function of an understudied catenin, Arvcf, during CE. These data are significant for providing interesting biomechanical and cell biological insights into a fundamental morphogenetic process that is implicated in human neural tube defects and skeletal dysplasias.
引用
收藏
页数:18
相关论文
共 50 条
  • [31] A LINK BETWEEN CYCLIN-A EXPRESSION AND ADHESION-DEPENDENT CELL-CYCLE PROGRESSION
    GUADAGNO, TM
    OHTSUBO, M
    ROBERTS, JM
    ASSOIAN, RK
    SCIENCE, 1993, 262 (5139) : 1572 - 1575
  • [32] Microtubule involvement in regulating cell contractility and adhesion-dependent signalling: a possible mechanism for polarization of cell motility
    Elbaum, M
    Chausovsky, A
    Levy, ET
    Shtutman, M
    Bershadsky, AD
    CELL BEHAVIOUR: CONTROL AND MECHANISM OF MOTILITY, 1999, 65 : 147 - 172
  • [33] Plakoglobin suppresses keratinocyte motility through both cell-cell adhesion-dependent and -independent mechanisms
    Yin, TF
    Getsios, S
    Caldelari, R
    Kowalczyk, AP
    Müller, EJ
    Jones, JCR
    Green, KJ
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (15) : 5420 - 5425
  • [34] Molecular mechanisms of cancer cell-cell interactions Cell-cell adhesion-dependent signaling of the tumor microenvironment
    Brady-Kalnay, Susann M.
    CELL ADHESION & MIGRATION, 2012, 6 (04) : 344 - 345
  • [35] Retention of a cell adhesion complex at the paranodal junction requires the cytoplasmic region of Caspr
    Gollan, L
    Sabanay, H
    Poliak, S
    Berglund, EO
    Ranscht, B
    Peles, E
    JOURNAL OF CELL BIOLOGY, 2002, 157 (07): : 1247 - 1256
  • [36] Modeling stochastic cell dynamics with adhesion anisotropy quantitatively reproduces convergent extension
    Firman, T. E.
    Ghosh, K.
    Blankenship, T.
    Loerke, D.
    MOLECULAR BIOLOGY OF THE CELL, 2013, 24
  • [37] Potentiation of cell migration by adhesion-dependent cooperative signals from the GTPase Rac and Raf kinase
    Leng, J
    Klemke, RL
    Reddy, AC
    Cheresh, DA
    JOURNAL OF BIOLOGICAL CHEMISTRY, 1999, 274 (53) : 37855 - 37861
  • [38] Force-dependent intercellular adhesion strengthening underlies asymmetric adherens junction contraction
    Cavanaugh, Kate E.
    Staddon, Michael F.
    Chmiel, Theresa A.
    Harmon, Robert
    Budnar, Srikanth
    Yap, Alpha S.
    Banerjee, Shiladitya
    Gardel, Margaret L.
    CURRENT BIOLOGY, 2022, 32 (09) : 1986 - +
  • [39] Tenascin-C inhibits oligodendrocyte precursor cell migration by both adhesion-dependent and adhesion-independent mechanisms
    Kiernan, BW
    Gotz, B
    Faissner, A
    ffrenchConstant, C
    MOLECULAR AND CELLULAR NEUROSCIENCE, 1996, 7 (04) : 322 - 335
  • [40] Cell adhesion-dependent membrane trafficking of a binding partner for the ebolavirus glycoprotein is a determinant of viral entry
    Dube, Derek
    Schornberg, Kathryn L.
    Shoemaker, Charles J.
    Delos, Sue E.
    Stantchev, Tzanko S.
    Clouse, Kathleen A.
    Broder, Christopher C.
    White, Judith M.
    PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (38) : 16637 - 16642