Control of the Mitotic Cleavage Plane by Local Epithelial Topology

被引:149
作者
Gibson, William T. [1 ,2 ,3 ,5 ]
Veldhuis, James H. [4 ]
Rubinstein, Boris [1 ]
Cartwright, Heather N. [1 ]
Perrimon, Norbert [5 ]
Brodland, G. Wayne [4 ]
Nagpal, Radhika [2 ]
Gibson, Matthew C. [1 ,6 ]
机构
[1] Stowers Inst Med Res, Kansas City, MO 64110 USA
[2] Harvard Univ, Sch Engn & Appl Sci, Cambridge, MA 02138 USA
[3] Harvard Univ, Program Biophys, Cambridge, MA 02138 USA
[4] Univ Waterloo, Dept Civil & Environm Engn, Waterloo, ON N2L 3G1, Canada
[5] Harvard Univ, Sch Med, Howard Hughes Med Inst, Dept Genet, Boston, MA 02115 USA
[6] Kansas Univ Med Ctr, Dept Anat & Cell Biol, Kansas City, MO 64110 USA
基金
加拿大自然科学与工程研究理事会; 美国国家科学基金会;
关键词
REGULATES SPINDLE ORIENTATION; ORIENTED CELL-DIVISION; MECHANICAL SIGNALS; 1ST CLEAVAGE; DROSOPHILA; SHAPE; POLARITY; NUCLEUS; MITOSIS; MICROTUBULES;
D O I
10.1016/j.cell.2010.12.035
中图分类号
Q5 [生物化学]; Q7 [分子生物学];
学科分类号
071010 ; 081704 ;
摘要
For nearly 150 years, it has been recognized that cell shape strongly influences the orientation of the mitotic cleavage plane (e. g., Hofmeister, 1863). However, we still understand little about the complex interplay between cell shape and cleavage-plane orientation in epithelia, where polygonal cell geometries emerge from multiple factors, including cell packing, cell growth, and cell division itself. Here, using mechanical simulations, we show that the polygonal shapes of individual cells can systematically bias the long-axis orientations of their adjacent mitotic neighbors. Strikingly, analyses of both animal epithelia and plant epidermis confirm a robust and nearly identical correlation between local cell topology and cleavage-plane orientation in vivo. Using simple mathematics, we show that this effect derives from fundamental packing constraints. Our results suggest that local epithelial topology is a key determinant of cleavage-plane orientation, and that cleavage-plane bias may be a widespread property of polygonal cell sheets in plants and animals.
引用
收藏
页码:427 / 438
页数:12
相关论文
共 56 条
[1]   Exploring the effects of mechanical feedback on epithelial topology [J].
Aegerter-Wilmsen, Tinri ;
Smith, Alister C. ;
Christen, Alix J. ;
Aegerter, Christof M. ;
Hafen, Ernst ;
Basler, Konrad .
DEVELOPMENT, 2010, 137 (03) :499-506
[2]   Live imaging of Drosophila imaginal disc development [J].
Aldaz, Silvia ;
Escudero, Luis M. ;
Freeman, Matthew .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2010, 107 (32) :14217-14222
[3]   The orientation of cell divisions determines the shape of Drosophila organs [J].
Baena-López, LA ;
Baonza, A ;
García-Bellido, A .
CURRENT BIOLOGY, 2005, 15 (18) :1640-1644
[4]   THE 1ST CLEAVAGE PLANE AND THE EMBRYONIC AXIS ARE DETERMINED BY SEPARATE MECHANISMS IN XENOPUS-LAEVIS .2. EXPERIMENTAL DISSOCIATION BY LATERAL COMPRESSION OF THE EGG [J].
BLACK, SD ;
VINCENT, JP .
DEVELOPMENTAL BIOLOGY, 1988, 128 (01) :65-71
[5]   Computer simulations of mitosis and interdependencies between mitosis orientation, cell shape and epithelia reshaping [J].
Brodland, GW ;
Veldhuis, JH .
JOURNAL OF BIOMECHANICS, 2002, 35 (05) :673-681
[6]   Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion [J].
Buschmann, Henrik ;
Chan, Jordi ;
Sanchez-Pulido, Luis ;
Andrade-Navarro, Miguel A. ;
Doonan, John H. ;
Lloyd, Clive W. .
CURRENT BIOLOGY, 2006, 16 (19) :1938-1943
[7]   Cell-level finite element studies of viscous cells in planar aggregates [J].
Chen, HH ;
Brodland, GW .
JOURNAL OF BIOMECHANICAL ENGINEERING-TRANSACTIONS OF THE ASME, 2000, 122 (04) :394-401
[8]   DIVISION RULES FOR POLYGONAL CELLS [J].
COWAN, R ;
MORRIS, VB .
JOURNAL OF THEORETICAL BIOLOGY, 1988, 131 (01) :33-42
[9]   Two-dimensional froths and the dynamics of biological tissues [J].
Dubertret, B ;
Aste, T ;
Ohlenbusch, HM ;
Rivier, N .
PHYSICAL REVIEW E, 1998, 58 (05) :6368-6378
[10]   The renewal of the epidermis: A topological mechanism [J].
Dubertret, B ;
Rivier, N .
BIOPHYSICAL JOURNAL, 1997, 73 (01) :38-44