Literature DB >> 21295702

Control of the mitotic cleavage plane by local epithelial topology.

William T Gibson1, James H Veldhuis, Boris Rubinstein, Heather N Cartwright, Norbert Perrimon, G Wayne Brodland, Radhika Nagpal, Matthew C Gibson.   

Abstract

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.
Copyright © 2011 Elsevier Inc. All rights reserved.

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Year:  2011        PMID: 21295702      PMCID: PMC3491649          DOI: 10.1016/j.cell.2010.12.035

Source DB:  PubMed          Journal:  Cell        ISSN: 0092-8674            Impact factor:   41.582


  45 in total

1.  Mammalian spindle orientation and position respond to changes in cell shape in a dynein-dependent fashion.

Authors:  C B O'Connell; Y L Wang
Journal:  Mol Biol Cell       Date:  2000-05       Impact factor: 4.138

2.  Universality in two-dimensional cellular structures evolving by cell division and disappearance.

Authors:  MirFaez Miri; Nicolas Rivier
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2006-03-02

3.  The emergence of geometric order in proliferating metazoan epithelia.

Authors:  Matthew C Gibson; Ankit B Patel; Radhika Nagpal; Norbert Perrimon
Journal:  Nature       Date:  2006-08-09       Impact factor: 49.962

4.  Cytoplasmic Behavior during Division of Vacuolate Plant Cells.

Authors:  E W Sinnott; R Bloch
Journal:  Proc Natl Acad Sci U S A       Date:  1940-04-15       Impact factor: 11.205

5.  Integrin signaling regulates spindle orientation in Drosophila to preserve the follicular-epithelium monolayer.

Authors:  Ana Fernández-Miñán; María D Martín-Bermudo; Acaimo González-Reyes
Journal:  Curr Biol       Date:  2007-03-15       Impact factor: 10.834

6.  Get round and stiff for mitosis.

Authors:  Manuel Théry; Michel Bornens
Journal:  HFSP J       Date:  2008-03-24

7.  Exploring the effects of mechanical feedback on epithelial topology.

Authors:  Tinri Aegerter-Wilmsen; Alister C Smith; Alix J Christen; Christof M Aegerter; Ernst Hafen; Konrad Basler
Journal:  Development       Date:  2010-02       Impact factor: 6.868

8.  Defective planar cell polarity in polycystic kidney disease.

Authors:  Evelyne Fischer; Emilie Legue; Antonia Doyen; Faridabano Nato; Jean-François Nicolas; Vicente Torres; Moshe Yaniv; Marco Pontoglio
Journal:  Nat Genet       Date:  2005-12-11       Impact factor: 38.330

9.  The renewal of the epidermis: a topological mechanism.

Authors:  B Dubertret; N Rivier
Journal:  Biophys J       Date:  1997-07       Impact factor: 4.033

10.  Actin in the preprophase band of Allium cepa.

Authors:  B A Palevitz
Journal:  J Cell Biol       Date:  1987-06       Impact factor: 10.539

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  82 in total

Review 1.  Axonemal positioning and orientation in three-dimensional space for primary cilia: what is known, what is assumed, and what needs clarification.

Authors:  Cornelia E Farnum; Norman J Wilsman
Journal:  Dev Dyn       Date:  2011-11       Impact factor: 3.780

2.  A Mechanistic Collective Cell Model for Epithelial Colony Growth and Contact Inhibition.

Authors:  Sebastian Aland; Haralambos Hatzikirou; John Lowengrub; Axel Voigt
Journal:  Biophys J       Date:  2015-10-06       Impact factor: 4.033

Review 3.  Mechanical Forces and Growth in Animal Tissues.

Authors:  Loïc LeGoff; Thomas Lecuit
Journal:  Cold Spring Harb Perspect Biol       Date:  2015-08-10       Impact factor: 10.005

Review 4.  Molecular control of animal cell cytokinesis.

Authors:  Juan Pablo Fededa; Daniel W Gerlich
Journal:  Nat Cell Biol       Date:  2012-05-02       Impact factor: 28.824

5.  Differential proliferation rates generate patterns of mechanical tension that orient tissue growth.

Authors:  Yanlan Mao; Alexander L Tournier; Andreas Hoppe; Lennart Kester; Barry J Thompson; Nicolas Tapon
Journal:  EMBO J       Date:  2013-09-10       Impact factor: 11.598

6.  Might makes right: Using force to align the mitotic spindle.

Authors:  Oscar M Lancaster; Buzz Baum
Journal:  Nat Cell Biol       Date:  2011-07-01       Impact factor: 28.824

Review 7.  Universal rules for division plane selection in plants.

Authors:  Sabine Müller
Journal:  Protoplasma       Date:  2011-05-26       Impact factor: 3.356

Review 8.  Division orientation: disentangling shape and mechanical forces.

Authors:  Tara M Finegan; Dan T Bergstralh
Journal:  Cell Cycle       Date:  2019-05-21       Impact factor: 4.534

9.  A plant cell division algorithm based on cell biomechanics and ellipse-fitting.

Authors:  Metadel K Abera; Pieter Verboven; Thijs Defraeye; Solomon Workneh Fanta; Maarten L A T M Hertog; Jan Carmeliet; Bart M Nicolai
Journal:  Ann Bot       Date:  2014-09       Impact factor: 4.357

10.  Unified quantitative characterization of epithelial tissue development.

Authors:  Boris Guirao; Stéphane U Rigaud; Floris Bosveld; Anaïs Bailles; Jesús López-Gay; Shuji Ishihara; Kaoru Sugimura; François Graner; Yohanns Bellaïche
Journal:  Elife       Date:  2015-12-12       Impact factor: 8.140

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