Literature DB >> 22404919

Cell ingression and apical shape oscillations during dorsal closure in Drosophila.

Adam Sokolow1, Yusuke Toyama, Daniel P Kiehart, Glenn S Edwards.   

Abstract

Programmed patterns of gene expression, cell-cell signaling, and cellular forces cause morphogenic movements during dorsal closure. We investigated the apical cell-shape changes that characterize amnioserosa cells during dorsal closure in Drosophila embryos with in vivo imaging of green-fluorescent-protein-labeled DE-cadherin. Time-lapsed, confocal images were assessed with a novel segmentation algorithm, Fourier analysis, and kinematic and dynamical modeling. We found two generic processes, reversible oscillations in apical cross-sectional area and cell ingression characterized by persistent loss of apical area. We quantified a time-dependent, spatially-averaged sum of intracellular and intercellular forces acting on each cell's apical belt of DE-cadherin. We observed that a substantial fraction of amnioserosa cells ingress near the leading edges of lateral epidermis, consistent with the view that ingression can be regulated by leading-edge cells. This is in addition to previously observed ingression processes associated with zipping and apoptosis. Although there is cell-to-cell variability in the maximum rate for decreasing apical area (0.3-9.5 μm(2)/min), the rate for completing ingression is remarkably constant (0.83 cells/min, r(2) > 0.99). We propose that this constant ingression rate contributes to the spatiotemporal regularity of mechanical stress exerted by the amnioserosa on each leading edge during closure.
Copyright © 2012 Biophysical Society. Published by Elsevier Inc. All rights reserved.

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Year:  2012        PMID: 22404919      PMCID: PMC3296024          DOI: 10.1016/j.bpj.2012.01.027

Source DB:  PubMed          Journal:  Biophys J        ISSN: 0006-3495            Impact factor:   4.033


  33 in total

1.  Drosophila Jun kinase regulates expression of decapentaplegic via the ETS-domain protein Aop and the AP-1 transcription factor DJun during dorsal closure.

Authors:  J R Riesgo-Escovar; E Hafen
Journal:  Genes Dev       Date:  1997-07-01       Impact factor: 11.361

2.  Drosophila Jun relays the Jun amino-terminal kinase signal transduction pathway to the Decapentaplegic signal transduction pathway in regulating epithelial cell sheet movement.

Authors:  X S Hou; E S Goldstein; N Perrimon
Journal:  Genes Dev       Date:  1997-07-01       Impact factor: 11.361

Review 3.  Dynamic analysis of dorsal closure in Drosophila: from genetics to cell biology.

Authors:  Antonio Jacinto; Sarah Woolner; Paul Martin
Journal:  Dev Cell       Date:  2002-07       Impact factor: 12.270

4.  Drosophila morphogenesis: tissue force laws and the modeling of dorsal closure.

Authors:  Anita T Layton; Yusuke Toyama; Guo-Qiang Yang; Glenn S Edwards; Daniel P Kiehart; Stephanos Venakides
Journal:  HFSP J       Date:  2009-12-15

5.  Shape oscillations of non-adhering fibroblast cells.

Authors:  G Salbreux; J F Joanny; J Prost; P Pullarkat
Journal:  Phys Biol       Date:  2007-11-21       Impact factor: 2.583

6.  Mechanical control of global cell behaviour during dorsal closure in Drosophila.

Authors:  Nicole Gorfinkiel; Guy B Blanchard; Richard J Adams; Alfonso Martinez Arias
Journal:  Development       Date:  2009-04-29       Impact factor: 6.868

7.  The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila.

Authors:  Daryl J V David; Alisa Tishkina; Tony J C Harris
Journal:  Development       Date:  2010-04-14       Impact factor: 6.868

Review 8.  High-resolution microscopic methods for the analysis of cellular movements in Drosophila embryos.

Authors:  D P Kiehart; R A Montague; W L Rickoll; D Foard; G H Thomas
Journal:  Methods Cell Biol       Date:  1994       Impact factor: 1.441

9.  Spontaneous oscillatory contraction without regulatory proteins in actin filament-reconstituted fibers.

Authors:  H Fujita; S Ishiwata
Journal:  Biophys J       Date:  1998-09       Impact factor: 4.033

10.  Pulsed contractions of an actin-myosin network drive apical constriction.

Authors:  Adam C Martin; Matthias Kaschube; Eric F Wieschaus
Journal:  Nature       Date:  2008-11-23       Impact factor: 49.962

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  35 in total

1.  Crumbs is an essential regulator of cytoskeletal dynamics and cell-cell adhesion during dorsal closure in Drosophila.

Authors:  David Flores-Benitez; Elisabeth Knust
Journal:  Elife       Date:  2015-11-06       Impact factor: 8.140

2.  Remodeling Tissue Interfaces and the Thermodynamics of Zipping during Dorsal Closure in Drosophila.

Authors:  Heng Lu; Adam Sokolow; Daniel P Kiehart; Glenn S Edwards
Journal:  Biophys J       Date:  2015-12-01       Impact factor: 4.033

Review 3.  Mathematical models of dorsal closure.

Authors:  A C Aristotelous; J M Crawford; G S Edwards; D P Kiehart; S Venakides
Journal:  Prog Biophys Mol Biol       Date:  2018-05-29       Impact factor: 3.667

4.  Elongated Cells Drive Morphogenesis in a Surface-Wrapped Finite-Element Model of Germband Retraction.

Authors:  W Tyler McCleery; Jim Veldhuis; Monica E Bennett; Holley E Lynch; Xiaoyan Ma; G Wayne Brodland; M Shane Hutson
Journal:  Biophys J       Date:  2019-06-05       Impact factor: 4.033

5.  Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer.

Authors:  Shao-Zhen Lin; Bo Li; Ganhui Lan; Xi-Qiao Feng
Journal:  Proc Natl Acad Sci U S A       Date:  2017-07-17       Impact factor: 11.205

6.  Amnioserosa cell constriction but not epidermal actin cable tension autonomously drives dorsal closure.

Authors:  Laurynas Pasakarnis; Erich Frei; Emmanuel Caussinus; Markus Affolter; Damian Brunner
Journal:  Nat Cell Biol       Date:  2016-10-17       Impact factor: 28.824

7.  Dynamics of PAR Proteins Explain the Oscillation and Ratcheting Mechanisms in Dorsal Closure.

Authors:  Clinton H Durney; Tony J C Harris; James J Feng
Journal:  Biophys J       Date:  2018-10-24       Impact factor: 4.033

8.  A cell-level biomechanical model of Drosophila dorsal closure.

Authors:  Qiming Wang; James J Feng; Len M Pismen
Journal:  Biophys J       Date:  2012-12-05       Impact factor: 4.033

Review 9.  The interplay between cell signalling and mechanics in developmental processes.

Authors:  Callie Johnson Miller; Lance A Davidson
Journal:  Nat Rev Genet       Date:  2013-10       Impact factor: 53.242

10.  Pathway to a phenocopy: Heat stress effects in early embryogenesis.

Authors:  Sarah M Crews; W Tyler McCleery; M Shane Hutson
Journal:  Dev Dyn       Date:  2015-11-16       Impact factor: 3.780

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