Literature DB >> 27834222

Polarized cortical tension drives zebrafish epiboly movements.

Amayra Hernández-Vega1, María Marsal1, Philippe-Alexandre Pouille1, Sébastien Tosi2, Julien Colombelli2, Tomás Luque3,4,5, Daniel Navajas3,4,5, Ignacio Pagonabarraga6, Enrique Martín-Blanco7.   

Abstract

The principles underlying the biomechanics of morphogenesis are largely unknown. Epiboly is an essential embryonic event in which three tissues coordinate to direct the expansion of the blastoderm. How and where forces are generated during epiboly, and how these are globally coupled remains elusive. Here we developed a method, hydrodynamic regression (HR), to infer 3D pressure fields, mechanical power, and cortical surface tension profiles. HR is based on velocity measurements retrieved from 2D+T microscopy and their hydrodynamic modeling. We applied HR to identify biomechanically active structures and changes in cortex local tension during epiboly in zebrafish. Based on our results, we propose a novel physical description for epiboly, where tissue movements are directed by a polarized gradient of cortical tension. We found that this gradient relies on local contractile forces at the cortex, differences in elastic properties between cortex components and the passive transmission of forces within the yolk cell. All in all, our work identifies a novel way to physically regulate concerted cellular movements that might be instrumental for the mechanical control of many morphogenetic processes.
© 2016 The Authors.

Entities:  

Keywords:  epiboly; hydrodynamics; mechanics; morphogenesis; zebrafish

Mesh:

Year:  2016        PMID: 27834222      PMCID: PMC5210093          DOI: 10.15252/embj.201694264

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


  56 in total

1.  Rheological analysis and measurement of neutrophil indentation.

Authors:  E B Lomakina; C M Spillmann; M R King; R E Waugh
Journal:  Biophys J       Date:  2004-09-10       Impact factor: 4.033

2.  Coordinated cell-shape changes control epithelial movement in zebrafish and Drosophila.

Authors:  Mathias Köppen; Beatriz García Fernández; Lara Carvalho; Antonio Jacinto; Carl-Philipp Heisenberg
Journal:  Development       Date:  2006-07       Impact factor: 6.868

3.  Actin-dependent cytoplasmic streaming in C. elegans oogenesis.

Authors:  Uta Wolke; Erin A Jezuit; James R Priess
Journal:  Development       Date:  2007-05-16       Impact factor: 6.868

Review 4.  Force generation, transmission, and integration during cell and tissue morphogenesis.

Authors:  Thomas Lecuit; Pierre-François Lenne; Edwin Munro
Journal:  Annu Rev Cell Dev Biol       Date:  2011-07-05       Impact factor: 13.827

5.  Forces driving epithelial spreading in zebrafish gastrulation.

Authors:  Martin Behrndt; Guillaume Salbreux; Pedro Campinho; Robert Hauschild; Felix Oswald; Julia Roensch; Stephan W Grill; Carl-Philipp Heisenberg
Journal:  Science       Date:  2012-10-12       Impact factor: 47.728

6.  Contact relations, surface activity, and cortical microfilaments of marginal cells of the enveloping layer and of the yolk syncytial and yolk cytoplasmic layers of fundulus before and during epiboly.

Authors:  T Betchaku; J P Trinkaus
Journal:  J Exp Zool       Date:  1978-12

Review 7.  Zebrafish epiboly: mechanics and mechanisms.

Authors:  Stephanie E Lepage; Ashley E E Bruce
Journal:  Int J Dev Biol       Date:  2010       Impact factor: 2.203

8.  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

9.  Cell movements during epiboly and gastrulation in zebrafish.

Authors:  R M Warga; C B Kimmel
Journal:  Development       Date:  1990-04       Impact factor: 6.868

10.  Microtubule arrays of the zebrafish yolk cell: organization and function during epiboly.

Authors:  L Solnica-Krezel; W Driever
Journal:  Development       Date:  1994-09       Impact factor: 6.868

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  6 in total

1.  Contractility, differential tension and membrane removal lead zebrafish epiboly biomechanics.

Authors:  Maria Marsal; Amayra Hernández-Vega; Enrique Martin-Blanco
Journal:  Cell Cycle       Date:  2017-06-07       Impact factor: 4.534

2.  Polarized cortical tension drives zebrafish epiboly movements.

Authors:  Amayra Hernández-Vega; María Marsal; Philippe-Alexandre Pouille; Sébastien Tosi; Julien Colombelli; Tomás Luque; Daniel Navajas; Ignacio Pagonabarraga; Enrique Martín-Blanco
Journal:  EMBO J       Date:  2016-11-09       Impact factor: 11.598

3.  Mechanical coordination is sufficient to promote tissue replacement during metamorphosis in Drosophila.

Authors:  Carla Prat-Rojo; Philippe-Alexandre Pouille; Javier Buceta; Enrique Martin-Blanco
Journal:  EMBO J       Date:  2019-12-20       Impact factor: 11.598

4.  AFM and Microrheology in the Zebrafish Embryo Yolk Cell.

Authors:  Maria Marsal; Ignasi Jorba; Elena Rebollo; Tomas Luque; Daniel Navajas; Enrique Martín-Blanco
Journal:  J Vis Exp       Date:  2017-11-29       Impact factor: 1.355

5.  Collective Cell Migration in Embryogenesis Follows the Laws of Wetting.

Authors:  Bernhard Wallmeyer; Sarah Trinschek; Sargon Yigit; Uwe Thiele; Timo Betz
Journal:  Biophys J       Date:  2018-01-09       Impact factor: 4.033

6.  Force-dependent remodeling of cytoplasmic ZO-1 condensates contributes to cell-cell adhesion through enhancing tight junctions.

Authors:  Noriyuki Kinoshita; Takamasa S Yamamoto; Naoko Yasue; Chiyo Takagi; Toshihiko Fujimori; Naoto Ueno
Journal:  iScience       Date:  2022-02-01
  6 in total

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