Literature DB >> 24022370

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

Yanlan Mao1, Alexander L Tournier, Andreas Hoppe, Lennart Kester, Barry J Thompson, Nicolas Tapon.   

Abstract

Orientation of cell divisions is a key mechanism of tissue morphogenesis. In the growing Drosophila wing imaginal disc epithelium, most of the cell divisions in the central wing pouch are oriented along the proximal-distal (P-D) axis by the Dachsous-Fat-Dachs planar polarity pathway. However, cells at the periphery of the wing pouch instead tend to orient their divisions perpendicular to the P-D axis despite strong Dachs polarization. Here, we show that these circumferential divisions are oriented by circumferential mechanical forces that influence cell shapes and thus orient the mitotic spindle. We propose that this circumferential pattern of force is not generated locally by polarized constriction of individual epithelial cells. Instead, these forces emerge as a global tension pattern that appears to originate from differential rates of cell proliferation within the wing pouch. Accordingly, we show that localized overgrowth is sufficient to induce neighbouring cell stretching and reorientation of cell division. Our results suggest that patterned rates of cell proliferation can influence tissue mechanics and thus determine the orientation of cell divisions and tissue shape.

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Year:  2013        PMID: 24022370      PMCID: PMC3817460          DOI: 10.1038/emboj.2013.197

Source DB:  PubMed          Journal:  EMBO J        ISSN: 0261-4189            Impact factor:   11.598


  57 in total

1.  The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing.

Authors:  Reza Farhadifar; Jens-Christian Röper; Benoit Aigouy; Suzanne Eaton; Frank Jülicher
Journal:  Curr Biol       Date:  2007-12-18       Impact factor: 10.834

2.  From the Cover: Directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering.

Authors:  Juan Huang; Wenke Zhou; Wei Dong; Annie M Watson; Yang Hong
Journal:  Proc Natl Acad Sci U S A       Date:  2009-05-08       Impact factor: 11.205

3.  Physical mechanisms shaping the Drosophila dorsoventral compartment boundary.

Authors:  Maryam Aliee; Jens-Christian Röper; Katharina P Landsberg; Constanze Pentzold; Thomas J Widmann; Frank Jülicher; Christian Dahmann
Journal:  Curr Biol       Date:  2012-05-03       Impact factor: 10.834

4.  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

5.  Cell competition, growth and size control in the Drosophila wing imaginal disc.

Authors:  Francisco A Martín; Salvador C Herrera; Ginés Morata
Journal:  Development       Date:  2009-11       Impact factor: 6.868

6.  Antagonistic growth regulation by Dpp and Fat drives uniform cell proliferation.

Authors:  Gerald Schwank; Gerardo Tauriello; Ryohei Yagi; Elizabeth Kranz; Petros Koumoutsakos; Konrad Basler
Journal:  Dev Cell       Date:  2011-01-18       Impact factor: 12.270

7.  Dachs: an unconventional myosin that functions downstream of Fat to regulate growth, affinity and gene expression in Drosophila.

Authors:  Yaopan Mao; Cordelia Rauskolb; Eunjoo Cho; Wei-Li Hu; Heather Hayter; Ginny Minihan; Flora N Katz; Kenneth D Irvine
Journal:  Development       Date:  2006-05-30       Impact factor: 6.868

8.  Integrating force-sensing and signaling pathways in a model for the regulation of wing imaginal disc size.

Authors:  Tinri Aegerter-Wilmsen; Maria B Heimlicher; Alister C Smith; Pierre Barbier de Reuille; Richard S Smith; Christof M Aegerter; Konrad Basler
Journal:  Development       Date:  2012-07-25       Impact factor: 6.868

9.  Model for the regulation of size in the wing imaginal disc of Drosophila.

Authors:  Tinri Aegerter-Wilmsen; Christof M Aegerter; Ernst Hafen; Konrad Basler
Journal:  Mech Dev       Date:  2006-12-29       Impact factor: 1.882

10.  Cell mechanics and feedback regulation of actomyosin networks.

Authors:  Rodrigo Fernandez-Gonzalez; Jennifer A Zallen
Journal:  Sci Signal       Date:  2009-12-15       Impact factor: 8.192

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  113 in total

Review 1.  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

2.  Cell mixing induced by myc is required for competitive tissue invasion and destruction.

Authors:  Romain Levayer; Barbara Hauert; Eduardo Moreno
Journal:  Nature       Date:  2015-08-19       Impact factor: 49.962

3.  The force and effect of cell proliferation.

Authors:  Pedro Campinho; Carl-Philipp Heisenberg
Journal:  EMBO J       Date:  2013-10-04       Impact factor: 11.598

Review 4.  Cell Extrusion: A Stress-Responsive Force for Good or Evil in Epithelial Homeostasis.

Authors:  Shizue Ohsawa; John Vaughen; Tatsushi Igaki
Journal:  Dev Cell       Date:  2018-02-05       Impact factor: 12.270

5.  Coupling intercellular molecular signalling with multicellular deformation for simulating three-dimensional tissue morphogenesis.

Authors:  Satoru Okuda; Yasuhiro Inoue; Tadashi Watanabe; Taiji Adachi
Journal:  Interface Focus       Date:  2015-04-06       Impact factor: 3.906

Review 6.  Physics of growing biological tissues: the complex cross-talk between cell activity, growth and resistance.

Authors:  Martine Ben Amar; Pierre Nassoy; Loic LeGoff
Journal:  Philos Trans A Math Phys Eng Sci       Date:  2019-05-06       Impact factor: 4.226

Review 7.  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

8.  Yorkie Functions at the Cell Cortex to Promote Myosin Activation in a Non-transcriptional Manner.

Authors:  Jiajie Xu; Pamela J Vanderzalm; Michael Ludwig; Ting Su; Sherzod A Tokamov; Richard G Fehon
Journal:  Dev Cell       Date:  2018-07-19       Impact factor: 12.270

9.  Endothelial Regeneration of Large Vessels Is a Biphasic Process Driven by Local Cells with Distinct Proliferative Capacities.

Authors:  Austin I McDonald; Aditya S Shirali; Raquel Aragón; Feiyang Ma; Gloria Hernandez; Don A Vaughn; Julia J Mack; Tiffany Y Lim; Hannah Sunshine; Peng Zhao; Vladimir Kalinichenko; Tsonwin Hai; Matteo Pelegrini; Reza Ardehali; M Luisa Iruela-Arispe
Journal:  Cell Stem Cell       Date:  2018-08-02       Impact factor: 24.633

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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