Literature DB >> 31229244

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

W Tyler McCleery1, Jim Veldhuis2, Monica E Bennett1, Holley E Lynch3, Xiaoyan Ma1, G Wayne Brodland2, M Shane Hutson4.   

Abstract

During Drosophila embryogenesis, the germband first extends to curl around the posterior end of the embryo and then retracts back; however, retraction is not simply the reversal of extension. At a tissue level, extension is coincident with ventral furrow formation, and at a cellular level, extension occurs via convergent cell neighbor exchanges in the germband, whereas retraction involves only changes in cell shape. To understand how cell shapes, tissue organization, and cellular forces drive germband retraction, we investigate this process using a whole-embryo, surface-wrapped cellular finite-element model. This model represents two key epithelial tissues-amnioserosa and germband-as adjacent sheets of two-dimensional cellular finite elements that are wrapped around an ellipsoidal three-dimensional approximation of an embryo. The model reproduces the detailed kinematics of in vivo retraction by fitting just one free model parameter, the tension along germband cell interfaces; all other cellular forces are constrained to follow ratios inferred from experimental observations. With no additional parameter adjustments, the model also reproduces quantitative assessments of mechanical stress using laser dissection and failures of retraction when amnioserosa cells are removed via mutations or microsurgery. Surprisingly, retraction in the model is robust to changes in cellular force values but is critically dependent on starting from a configuration with highly elongated amnioserosa cells. Their extreme cellular elongation is established during the prior process of germband extension and is then used to drive retraction. The amnioserosa is the one tissue whose cellular morphogenesis is reversed from germband extension to retraction, and this reversal coordinates the forces needed to retract the germband back to its pre-extension position and shape. In this case, cellular force strengths are less important than the carefully established cell shapes that direct them. VIDEO ABSTRACT.
Copyright © 2019 Biophysical Society. Published by Elsevier Inc. All rights reserved.

Entities:  

Year:  2019        PMID: 31229244      PMCID: PMC6626845          DOI: 10.1016/j.bpj.2019.05.023

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


  73 in total

1.  The mechanics of cell sorting and envelopment.

Authors:  G Wayne Brodland; H H Chen
Journal:  J Biomech       Date:  2000-07       Impact factor: 2.712

2.  The mechanics of heterotypic cell aggregates: insights from computer simulations.

Authors:  G W Brodland; H H Chen
Journal:  J Biomech Eng       Date:  2000-08       Impact factor: 2.097

3.  The Differential Interfacial Tension Hypothesis (DITH): a comprehensive theory for the self-rearrangement of embryonic cells and tissues.

Authors:  G Wayne Brodland
Journal:  J Biomech Eng       Date:  2002-04       Impact factor: 2.097

4.  Retraction of the Drosophila germ band requires cell-matrix interaction.

Authors:  Frieder Schöck; Norbert Perrimon
Journal:  Genes Dev       Date:  2003-03-01       Impact factor: 11.361

5.  Forces for morphogenesis investigated with laser microsurgery and quantitative modeling.

Authors:  M Shane Hutson; Yoichiro Tokutake; Ming-Shien Chang; James W Bloor; Stephanos Venakides; Daniel P Kiehart; Glenn S Edwards
Journal:  Science       Date:  2003-02-06       Impact factor: 47.728

6.  Cellular processes associated with germ band retraction in Drosophila.

Authors:  Frieder Schöck; Norbert Perrimon
Journal:  Dev Biol       Date:  2002-08-01       Impact factor: 3.582

7.  Dynamic analysis of actin cable function during Drosophila dorsal closure.

Authors:  Antonio Jacinto; William Wood; Sarah Woolner; Charlotte Hiley; Laura Turner; Clive Wilson; Alfonso Martinez-Arias; Paul Martin
Journal:  Curr Biol       Date:  2002-07-23       Impact factor: 10.834

8.  Role of the amnioserosa in germ band retraction of the Drosophila melanogaster embryo.

Authors:  M L Lamka; H D Lipshitz
Journal:  Dev Biol       Date:  1999-10-01       Impact factor: 3.582

9.  Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells.

Authors:  H Oda; S Tsukita
Journal:  J Cell Sci       Date:  2001-02       Impact factor: 5.285

10.  Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila.

Authors:  D P Kiehart; C G Galbraith; K A Edwards; W L Rickoll; R A Montague
Journal:  J Cell Biol       Date:  2000-04-17       Impact factor: 10.539

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