Decrease in Cell Volume Generates Contractile Forces Driving Dorsal Closure

被引:92
作者
Saias, Laure [1 ,2 ]
Swoger, Jim [2 ,3 ]
D'Angelo, Arturo [1 ,2 ]
Hayes, Peran [1 ,2 ]
Colombelli, Julien [4 ]
Sharpe, James [2 ,3 ,5 ]
Salbreux, Guillaume [6 ]
Solon, Jerome [1 ,2 ]
机构
[1] Ctr Genom Regulat, Cell & Dev Biol Programme, Barcelona 08003, Spain
[2] Univ Pompeu Fabra, Barcelona 08003, Spain
[3] Ctr Genom Regulat, EMBL CRG Syst Biol Unit, Barcelona 08003, Spain
[4] Inst Res Biomed, Adv Digital Microscopy, Barcelona 08028, Spain
[5] Inst Catalana Recerca & Estudis Avancats, Barcelona 08010, Spain
[6] Max Planck Inst Phys Komplexer Syst, D-01187 Dresden, Germany
关键词
NONMUSCLE MYOSIN-II; APICAL CONSTRICTION; DROSOPHILA EMBRYOS; MORPHOGENESIS; APOPTOSIS; DEATH; MECHANICS; INVAGINATION; MICROSCOPY; SHRINKAGE;
D O I
10.1016/j.devcel.2015.03.016
中图分类号
Q2 [细胞生物学];
学科分类号
071009 ; 090102 ;
摘要
Biological tissues must generate forces to shape organs and achieve proper development. Such forces often result from the contraction of an apical actomyosin meshwork. Here we describe an alternative mechanism for tissue contraction, based on individual cell volume change. We show that during Drosophila dorsal closure (DC), a wound healing-related process, the contraction of the amnioserosa (AS) is associated with a major reduction of the volume of its cells, triggered by caspase activation at the onset of the apoptotic program of AS cells. Cell volume decrease results in a contractile force that promotes tissue shrinkage. Estimating mechanical tensions with laser dissection and using 3D biophysical modeling, we show that the cell volume decrease acts together with the contraction of the actin cable surrounding the tissue to govern DC kinetics. Our study identifies a mechanism by which tissues generate forces and movements by modulating individual cell volume during development.
引用
收藏
页码:611 / 621
页数:11
相关论文
共 45 条
[11]   Mechanical control of global cell behaviour during dorsal closure in Drosophila [J].
Gorfinkiel, Nicole ;
Blanchard, Guy B. ;
Adams, Richard J. ;
Arias, Alfonso Martinez .
DEVELOPMENT, 2009, 136 (11) :1889-1898
[12]   Theory of epithelial sheet morphology in three dimensions [J].
Hannezo, Edouard ;
Prost, Jacques ;
Joanny, Jean-Francois .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2014, 111 (01) :27-32
[13]   ROLE FOR IONIC FLUXES ON CELL DEATH AND APOPTOTIC VOLUME DECREASE IN CULTURED CEREBELLAR GRANULE NEURONS [J].
Hernandez-Enriquez, B. ;
Arellano, R. O. ;
Moran, J. .
NEUROSCIENCE, 2010, 167 (02) :298-311
[14]   Optical sectioning deep inside live embryos by selective plane illumination microscopy [J].
Huisken, J ;
Swoger, J ;
Del Bene, F ;
Wittbrodt, J ;
Stelzer, EHK .
SCIENCE, 2004, 305 (5686) :1007-1009
[15]   Forces for morphogenesis investigated with laser microsurgery and quantitative modeling [J].
Hutson, MS ;
Tokutake, Y ;
Chang, MS ;
Bloor, JW ;
Venakides, S ;
Kiehart, DP ;
Edwards, GS .
SCIENCE, 2003, 300 (5616) :145-149
[16]   Plasma membrane aquaporin activity can affect the rate of apoptosis but is inhibited after apoptotic volume decrease [J].
Jablonski, EM ;
Webb, AN ;
McConnell, NA ;
Riley, MC ;
Hughes, FM .
AMERICAN JOURNAL OF PHYSIOLOGY-CELL PHYSIOLOGY, 2004, 286 (04) :C975-C985
[17]   Dynamic analysis of dorsal closure in Drosophila:: From genetics to cell biology [J].
Jacinto, A ;
Woolner, S ;
Martin, P .
DEVELOPMENTAL CELL, 2002, 3 (01) :9-19
[18]   Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila [J].
Kiehart, DP ;
Galbraith, CG ;
Edwards, KA ;
Rickoll, WL ;
Montague, RA .
JOURNAL OF CELL BIOLOGY, 2000, 149 (02) :471-490
[19]   Baculovirus caspase inhibitors P49 and P35 block virus-induced apoptosis downstream of effector caspase DrICE activation in Drosophila melanogaster cells [J].
Lannan, Erica ;
Vandergaast, Rianna ;
Friesen, Paul D. .
JOURNAL OF VIROLOGY, 2007, 81 (17) :9319-9330
[20]   Drosophila morphogenesis: tissue force laws and the modeling of dorsal closure [J].
Layton, Anita T. ;
Toyama, Yusuke ;
Yang, Guo-Qiang ;
Edwards, Glenn S. ;
Kiehart, Daniel P. ;
Venakides, Stephanos .
HFSP JOURNAL, 2009, 3 (06) :441-460