Literature DB >> 25605934

Direct laser manipulation reveals the mechanics of cell contacts in vivo.

Kapil Bambardekar1, Raphaël Clément1, Olivier Blanc1, Claire Chardès1, Pierre-François Lenne2.   

Abstract

Cell-generated forces produce a variety of tissue movements and tissue shape changes. The cytoskeletal elements that underlie these dynamics act at cell-cell and cell-ECM contacts to apply local forces on adhesive structures. In epithelia, force imbalance at cell contacts induces cell shape changes, such as apical constriction or polarized junction remodeling, driving tissue morphogenesis. The dynamics of these processes are well-characterized; however, the mechanical basis of cell shape changes is largely unknown because of a lack of mechanical measurements in vivo. We have developed an approach combining optical tweezers with light-sheet microscopy to probe the mechanical properties of epithelial cell junctions in the early Drosophila embryo. We show that optical trapping can efficiently deform cell-cell interfaces and measure tension at cell junctions, which is on the order of 100 pN. We show that tension at cell junctions equilibrates over a few seconds, a short timescale compared with the contractile events that drive morphogenetic movements. We also show that tension increases along cell interfaces during early tissue morphogenesis and becomes anisotropic as cells intercalate during germ-band extension. By performing pull-and-release experiments, we identify time-dependent properties of junctional mechanics consistent with a simple viscoelastic model. Integrating this constitutive law into a tissue-scale model, we predict quantitatively how local deformations propagate throughout the tissue.

Entities:  

Keywords:  Myosin-II; cell mechanics; light-sheet microscopy; optical tweezers; tissue morphogenesis

Mesh:

Year:  2015        PMID: 25605934      PMCID: PMC4321260          DOI: 10.1073/pnas.1418732112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  31 in total

1.  Cinemechanometry (CMM): A method to determine the forces that drive morphogenetic movements from time-lapse images.

Authors:  P Graham Cranston; Jim H Veldhuis; Sriram Narasimhan; G Wayne Brodland
Journal:  Ann Biomed Eng       Date:  2010-07-08       Impact factor: 3.934

2.  Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2.

Authors:  Verena Kölsch; Thomas Seher; Gregorio J Fernandez-Ballester; Luis Serrano; Maria Leptin
Journal:  Science       Date:  2007-01-19       Impact factor: 47.728

3.  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

4.  Multicellular rosette formation links planar cell polarity to tissue morphogenesis.

Authors:  J Todd Blankenship; Stephanie T Backovic; Justina S P Sanny; Ori Weitz; Jennifer A Zallen
Journal:  Dev Cell       Date:  2006-10       Impact factor: 12.270

5.  The mechanical basis of morphogenesis. I. Epithelial folding and invagination.

Authors:  G M Odell; G Oster; P Alberch; B Burnside
Journal:  Dev Biol       Date:  1981-07-30       Impact factor: 3.582

6.  Anisotropies in cortical tension reveal the physical basis of polarizing cortical flows.

Authors:  Mirjam Mayer; Martin Depken; Justin S Bois; Frank Jülicher; Stephan W Grill
Journal:  Nature       Date:  2010-09-19       Impact factor: 49.962

7.  Confined lateral diffusion of membrane receptors as studied by single particle tracking (nanovid microscopy). Effects of calcium-induced differentiation in cultured epithelial cells.

Authors:  A Kusumi; Y Sako; M Yamamoto
Journal:  Biophys J       Date:  1993-11       Impact factor: 4.033

8.  Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics.

Authors:  M Shane Hutson; J Veldhuis; Xiaoyan Ma; Holley E Lynch; P Graham Cranston; G Wayne Brodland
Journal:  Biophys J       Date:  2009-12-16       Impact factor: 4.033

9.  Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis.

Authors:  Matteo Rauzi; Pascale Verant; Thomas Lecuit; Pierre-François Lenne
Journal:  Nat Cell Biol       Date:  2008-11-02       Impact factor: 28.824

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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  73 in total

1.  Local and tissue-scale forces drive oriented junction growth during tissue extension.

Authors:  Claudio Collinet; Matteo Rauzi; Pierre-François Lenne; Thomas Lecuit
Journal:  Nat Cell Biol       Date:  2015-09-21       Impact factor: 28.824

2.  Macro-optical trapping for sample confinement in light sheet microscopy.

Authors:  Zhengyi Yang; Peeter Piksarv; David E K Ferrier; Frank J Gunn-Moore; Kishan Dholakia
Journal:  Biomed Opt Express       Date:  2015-07-08       Impact factor: 3.732

3.  From discrete to continuum models of three-dimensional deformations in epithelial sheets.

Authors:  Nebojsa Murisic; Vincent Hakim; Ioannis G Kevrekidis; Stanislav Y Shvartsman; Basile Audoly
Journal:  Biophys J       Date:  2015-07-07       Impact factor: 4.033

Review 4.  Physical control of tissue morphogenesis across scales.

Authors:  Georgina A Stooke-Vaughan; Otger Campàs
Journal:  Curr Opin Genet Dev       Date:  2018-11-01       Impact factor: 5.578

Review 5.  Adaptive viscoelasticity of epithelial cell junctions: from models to methods.

Authors:  Kate E Cavanaugh; Michael F Staddon; Shiladitya Banerjee; Margaret L Gardel
Journal:  Curr Opin Genet Dev       Date:  2020-06-27       Impact factor: 5.578

Review 6.  E-cadherin junctions as active mechanical integrators in tissue dynamics.

Authors:  Thomas Lecuit; Alpha S Yap
Journal:  Nat Cell Biol       Date:  2015-05       Impact factor: 28.824

7.  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

8.  Functional Modulation of Receptor Proteins on Cellular Interface with Optogenetic System.

Authors:  Mizuki Endo; Takeaki Ozawa
Journal:  Adv Exp Med Biol       Date:  2021       Impact factor: 2.622

Review 9.  Programmed and self-organized flow of information during morphogenesis.

Authors:  Claudio Collinet; Thomas Lecuit
Journal:  Nat Rev Mol Cell Biol       Date:  2021-01-22       Impact factor: 94.444

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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