Collective Cell Movement Promotes Synchronization of Coupled Genetic Oscillators

被引:39
作者
Uriu, Koichiro [1 ]
Morelli, Luis G. [2 ,3 ]
机构
[1] RIKEN, Theoret Biol Lab, Wako, Saitama, Japan
[2] Consejo Nacl Invest Cient & Tecn, FCEyN UBA, Dept Fis, RA-1033 Buenos Aires, DF, Argentina
[3] Consejo Nacl Invest Cient & Tecn, IFIBA, RA-1033 Buenos Aires, DF, Argentina
基金
日本学术振兴会;
关键词
SEGMENTATION CLOCK; VERTEBRATE SEGMENTATION; MIGRATION; DYNAMICS; MORPHOGENESIS; MECHANICS; ELONGATION; EXPRESSION; INITIATION; PATHWAY;
D O I
10.1016/j.bpj.2014.06.011
中图分类号
Q6 [生物物理学];
学科分类号
071011 ;
摘要
Collective cell movement is a crucial component of embryonic development. Intercellular interactions regulate collective cell movement by allowing cells to transfer information. A key question is how collective cell movement itself influences information flow produced in tissues by intercellular interactions. Here, we study the effect-of collective cell movement on the synchronization of locally coupled genetic oscillators. This study is motivated by the segmentation clock in zebrafish somitogenesis, where short-range correlated movement of cells has been observed. We describe the segmentation clock tissue by a Voronoi diagram, cell movement by the force balance of self-propelled and repulsive forces between cells, the dynamics of the direction of self-propelled motion, and the synchronization of genetic oscillators by locally coupled phase oscillators. We find that movement with a correlation length of about 2 similar to 3 cell diameters is optimal for the synchronization of coupled oscillators. Quantification of cell mixing reveals that this short-range correlation of cell movement allows cells to exchange neighbors most efficiently. Moreover, short-range correlated movement strongly destabilizes nonuniform spatial phase patterns, further promoting global synchronization. Our theoretical results suggest that collective cell Movement may enhance the synchronization of the segmentation clock in zebrafish somitogenesis. More generally, collective cell movement may promote information flow in tissues by enhancing cell mixing and destabilizing spurious patterns.
引用
收藏
页码:514 / 526
页数:13
相关论文
共 62 条
  • [1] Cell-cell signaling interactions coordinate multiple cell behaviors that drive morphogenesis of the lateral line
    Aman, Andy
    Piotrowski, Tatjana
    [J]. CELL ADHESION & MIGRATION, 2011, 5 (06) : 499 - 508
  • [2] A random cell motility gradient downstream of FGF controls elongation of an amniote embryo
    Benazeraf, Bertrand
    Francois, Paul
    Baker, Ruth E.
    Denans, Nicolas
    Little, Charles D.
    Pourquie, Olivier
    [J]. NATURE, 2010, 466 (7303) : 248 - 252
  • [3] Energy barriers and cell migration in densely packed tissues
    Bi, Dapeng
    Lopez, Jorge H.
    Schwarz, J. M.
    Manning, M. Lisa
    [J]. SOFT MATTER, 2014, 10 (12) : 1885 - 1890
  • [4] Contact inhibition of locomotion in vivo controls neural crest directional migration
    Carmona-Fontaine, Carlos
    Matthews, Helen K.
    Kuriyama, Sei
    Moreno, Mauricio
    Dunn, Graham A.
    Parsons, Maddy
    Stern, Claudio D.
    Mayor, Roberto
    [J]. NATURE, 2008, 456 (7224) : 957 - 961
  • [5] Tactile interactions lead to coherent motion and enhanced chemotaxis of migrating cells
    Coburn, Luke
    Cerone, Luca
    Torney, Colin
    Couzin, Iain D.
    Neufeld, Zoltan
    [J]. PHYSICAL BIOLOGY, 2013, 10 (04)
  • [6] Single-Cell-Resolution Imaging of the Impact of Notch Signaling and Mitosis on Segmentation Clock Dynamics
    Delaune, Emilie A.
    Francois, Paul
    Shih, Nathan P.
    Amacher, Sharon L.
    [J]. DEVELOPMENTAL CELL, 2012, 23 (05) : 995 - 1005
  • [7] Control of the segmentation process by graded MAPK/ERK activation in the chick embryo
    Delfini, MC
    Dubrulle, J
    Malapert, P
    Chal, J
    Pourquié, O
    [J]. PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2005, 102 (32) : 11343 - 11348
  • [8] Cell-Fibronectin Interactions Propel Vertebrate Trunk Elongation via Tissue Mechanics
    Dray, Nicolas
    Lawton, Andrew
    Nandi, Amitabha
    Juelich, Doerthe
    Emonet, Thierry
    Holley, Scott A.
    [J]. CURRENT BIOLOGY, 2013, 23 (14) : 1335 - 1341
  • [9] The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing
    Farhadifar, Reza
    Roeper, Jens-Christian
    Algouy, Benoit
    Eaton, Suzanne
    Juelicher, Frank
    [J]. CURRENT BIOLOGY, 2007, 17 (24) : 2095 - 2104
  • [10] Pattern Formation in Self-Propelled Particles with Density-Dependent Motility
    Farrell, F. D. C.
    Marchetti, M. C.
    Marenduzzo, D.
    Tailleur, J.
    [J]. PHYSICAL REVIEW LETTERS, 2012, 108 (24)