Literature DB >> 24316147

The plasma membrane flattens out to fuel cell-surface growth during Drosophila cellularization.

Lauren Figard1, Heng Xu2, Hernan G Garcia3, Ido Golding4, Anna Marie Sokac5.   

Abstract

Cell-shape change demands cell-surface growth, but how growth is fueled and choreographed is still debated. Here we use cellularization, the first complete cytokinetic event in Drosophila embryos, to show that cleavage furrow ingression is kinetically coupled to the loss of surface microvilli. We modulate furrow kinetics with RNAi against the Rho1-GTPase regulator slam and show that furrow ingression controls the rate of microvillar depletion. Finally, we directly track the microvillar membrane and see it move along the cell surface and into ingressing furrows, independent of endocytosis. Together, our results demonstrate that the kinetics of the ingressing furrow regulate the utilization of a microvillar membrane reservoir. Because membranes of the furrow and microvilli are contiguous, we suggest that ingression drives unfolding of the microvilli and incorporation of microvillar membrane into the furrow. We conclude that plasma membrane folding/unfolding can contribute to the cell-shape changes that promote embryonic morphogenesis.
Copyright © 2013 Elsevier Inc. All rights reserved.

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Year:  2013        PMID: 24316147      PMCID: PMC3888437          DOI: 10.1016/j.devcel.2013.11.006

Source DB:  PubMed          Journal:  Dev Cell        ISSN: 1534-5807            Impact factor:   12.270


  56 in total

1.  Targeted new membrane addition in the cleavage furrow is a late, separate event in cytokinesis.

Authors:  C B Shuster; D R Burgess
Journal:  Proc Natl Acad Sci U S A       Date:  2002-03-12       Impact factor: 11.205

2.  Trafficking through Rab11 endosomes is required for cellularization during Drosophila embryogenesis.

Authors:  Anne Pelissier; Jean-Paul Chauvin; Thomas Lecuit
Journal:  Curr Biol       Date:  2003-10-28       Impact factor: 10.834

3.  MYO1A (brush border myosin I) dynamics in the brush border of LLC-PK1-CL4 cells.

Authors:  M J Tyska; M S Mooseker
Journal:  Biophys J       Date:  2002-04       Impact factor: 4.033

4.  slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo.

Authors:  Thomas Lecuit; Reba Samanta; Eric Wieschaus
Journal:  Dev Cell       Date:  2002-04       Impact factor: 12.270

Review 5.  F-actin bundles are derivatives of microvilli: What does this tell us about how bundles might form?

Authors:  D J DeRosier; L G Tilney
Journal:  J Cell Biol       Date:  2000-01-10       Impact factor: 10.539

6.  Lava lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization.

Authors:  J C Sisson; C Field; R Ventura; A Royou; W Sullivan
Journal:  J Cell Biol       Date:  2000-11-13       Impact factor: 10.539

7.  Polarized insertion of new membrane from a cytoplasmic reservoir during cleavage of the Drosophila embryo.

Authors:  T Lecuit; E Wieschaus
Journal:  J Cell Biol       Date:  2000-08-21       Impact factor: 10.539

8.  Slow as molasses is required for polarized membrane growth and germ cell migration in Drosophila.

Authors:  Jennifer A Stein; Heather Tarczy Broihier; Lisa A Moore; Ruth Lehmann
Journal:  Development       Date:  2002-08       Impact factor: 6.868

9.  Tubular endocytosis drives remodelling of the apical surface during epithelial morphogenesis in Drosophila.

Authors:  Piotr Fabrowski; Aleksandar S Necakov; Simone Mumbauer; Eva Loeser; Alessandra Reversi; Sebastian Streichan; John A G Briggs; Stefano De Renzis
Journal:  Nat Commun       Date:  2013       Impact factor: 14.919

10.  Actin cytoskeleton remodeling during early Drosophila furrow formation requires recycling endosomal components Nuclear-fallout and Rab11.

Authors:  Blake Riggs; Wendy Rothwell; Sarah Mische; Gilles R X Hickson; Johanne Matheson; Thomas S Hays; Gwyn W Gould; William Sullivan
Journal:  J Cell Biol       Date:  2003-10-06       Impact factor: 10.539

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  26 in total

1.  Membrane Supply and Demand Regulates F-Actin in a Cell Surface Reservoir.

Authors:  Lauren Figard; Mengyu Wang; Liuliu Zheng; Ido Golding; Anna Marie Sokac
Journal:  Dev Cell       Date:  2016-05-09       Impact factor: 12.270

2.  Going with the Flow (or Not).

Authors:  Ken Jacobson; Maryna Kapustina
Journal:  Biophys J       Date:  2019-08-05       Impact factor: 4.033

3.  Bleb Expansion in Migrating Cells Depends on Supply of Membrane from Cell Surface Invaginations.

Authors:  Mohammad Goudarzi; Katsiaryna Tarbashevich; Karina Mildner; Isabell Begemann; Jamie Garcia; Azadeh Paksa; Michal Reichman-Fried; Harsha Mahabaleshwar; Heiko Blaser; Johannes Hartwig; Dagmar Zeuschner; Milos Galic; Michel Bagnat; Timo Betz; Erez Raz
Journal:  Dev Cell       Date:  2017-11-22       Impact factor: 12.270

Review 4.  A membrane reservoir at the cell surface: unfolding the plasma membrane to fuel cell shape change.

Authors:  Lauren Figard; Anna Marie Sokac
Journal:  Bioarchitecture       Date:  2014-05-20

5.  Excess dNTPs Trigger Oscillatory Surface Flow in the Early Drosophila Embryo.

Authors:  Sayantan Dutta; Nareg J-V Djabrayan; Celia M Smits; Clarence W Rowley; Stanislav Y Shvartsman
Journal:  Biophys J       Date:  2020-03-29       Impact factor: 4.033

6.  Spatiotemporal Analysis of Cytokinetic Events in Fission Yeast.

Authors:  Bin Wei; Brian S Hercyk; Julius Habiyaremye; Maitreyi Das
Journal:  J Vis Exp       Date:  2017-02-20       Impact factor: 1.355

7.  A rapid, membrane-dependent pathway directs furrow formation through RalA in the early Drosophila embryo.

Authors:  Ryan M Holly; Lauren M Mavor; Zhongyuan Zuo; J Todd Blankenship
Journal:  Development       Date:  2015-06-19       Impact factor: 6.868

8.  Dynamics of Inductive ERK Signaling in the Drosophila Embryo.

Authors:  Bomyi Lim; Carmeline J Dsilva; Thomas J Levario; Hang Lu; Trudi Schüpbach; Ioannis G Kevrekidis; Stanislav Y Shvartsman
Journal:  Curr Biol       Date:  2015-06-18       Impact factor: 10.834

9.  Rab8 directs furrow ingression and membrane addition during epithelial formation in Drosophila melanogaster.

Authors:  Lauren M Mavor; Hui Miao; Zhongyuan Zuo; Ryan M Holly; Yi Xie; Dinah Loerke; J Todd Blankenship
Journal:  Development       Date:  2016-02-02       Impact factor: 6.868

Review 10.  Transcytosis in the development and morphogenesis of epithelial tissues.

Authors:  Nicholas D Serra; Meera V Sundaram
Journal:  EMBO J       Date:  2021-04-01       Impact factor: 11.598

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