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      Nuclear envelope: a new frontier in plant mechanosensing?

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          Abstract

          In animals, it is now well established that forces applied at the cell surface are propagated through the cytoskeleton to the nucleus, leading to deformations of the nuclear structure and, potentially, to modification of gene expression. Consistently, altered nuclear mechanics has been related to many genetic disorders, such as muscular dystrophy, cardiomyopathy and progeria. In plants, the integration of mechanical signals in cell and developmental biology has also made great progress. Yet, while the link between cell wall stresses and cytoskeleton is consolidated, such cortical mechanical cues have not been integrated with the nucleoskeleton. Here, we propose to take inspiration from studies on animal nuclei to identify relevant methods amenable to probing nucleus mechanics and deformation in plant cells, with a focus on microrheology. To identify potential molecular targets, we also compare the players at the nuclear envelope, namely lamina and LINC complex, in both plant and animal nuclei. Understanding how mechanical signals are transduced to the nucleus across kingdoms will likely have essential implications in development (e.g. how mechanical cues add robustness to gene expression patterns), in the nucleoskeleton–cytoskeleton nexus (e.g. how stress is propagated in turgid/walled cells), as well as in transcriptional control, chromatin biology and epigenetics.

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          Most cited references102

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          Local force and geometry sensing regulate cell functions.

          The shapes of eukaryotic cells and ultimately the organisms that they form are defined by cycles of mechanosensing, mechanotransduction and mechanoresponse. Local sensing of force or geometry is transduced into biochemical signals that result in cell responses even for complex mechanical parameters such as substrate rigidity and cell-level form. These responses regulate cell growth, differentiation, shape changes and cell death. Recent tissue scaffolds that have been engineered at the micro- and nanoscale level now enable better dissection of the mechanosensing, transduction and response mechanisms.
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            Scaling the microrheology of living cells.

            We report a scaling law that governs both the elastic and frictional properties of a wide variety of living cell types, over a wide range of time scales and under a variety of biological interventions. This scaling identifies these cells as soft glassy materials existing close to a glass transition, and implies that cytoskeletal proteins may regulate cell mechanical properties mainly by modulating the effective noise temperature of the matrix. The practical implications are that the effective noise temperature is an easily quantified measure of the ability of the cytoskeleton to deform, flow, and reorganize.
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              Flexural rigidity of microtubules and actin filaments measured from thermal fluctuations in shape

              Microtubules are long, proteinaceous filaments that perform structural functions in eukaryotic cells by defining cellular shape and serving as tracks for intracellular motor proteins. We report the first accurate measurements of the flexural rigidity of microtubules. By analyzing the thermally driven fluctuations in their shape, we estimated the mean flexural rigidity of taxol-stabilized microtubules to be 2.2 x 10(-23) Nm2 (with 6.4% uncertainty) for seven unlabeled microtubules and 2.1 x 10(-23) Nm2 (with 4.7% uncertainty) for eight rhodamine-labeled microtubules. These values are similar to earlier, less precise estimates of microtubule bending stiffness obtained by modeling flagellar motion. A similar analysis on seven rhodamine-phalloidin- labeled actin filaments gave a flexural rigidity of 7.3 x 10(-26) Nm2 (with 6% uncertainty), consistent with previously reported results. The flexural rigidity of these microtubules corresponds to a persistence length of 5,200 microns showing that a microtubule is rigid over cellular dimensions. By contrast, the persistence length of an actin filament is only approximately 17.7 microns, perhaps explaining why actin filaments within cells are usually cross-linked into bundles. The greater flexural rigidity of a microtubule compared to an actin filament mainly derives from the former's larger cross-section. If tubulin were homogeneous and isotropic, then the microtubule's Young's modulus would be approximately 1.2 GPa, similar to Plexiglas and rigid plastics. Microtubules are expected to be almost inextensible: the compliance of cells is due primarily to filament bending or sliding between filaments rather than the stretching of the filaments themselves.
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                Author and article information

                Contributors
                +33 4 72 72 88 75 , olivier.hamant@ens-lyon.fr
                Journal
                Biophys Rev
                Biophys Rev
                Biophysical Reviews
                Springer Berlin Heidelberg (Berlin/Heidelberg )
                1867-2450
                1867-2469
                12 August 2017
                12 August 2017
                August 2017
                : 9
                : 4
                : 389-403
                Affiliations
                [1 ]ISNI 0000 0001 2175 9188, GRID grid.15140.31, Laboratoire Reproduction et Développement des Plantes, , Université de Lyon, ENS de Lyon, UCB Lyon 1, CNRS, INRA, ; 69342 Lyon, France
                [2 ]ISNI 0000 0004 1788 6194, GRID grid.469994.f, Laboratoire Matières et Systèmes Complexes, , Université Paris-Diderot and CNRS, UMR 7057, Sorbonne Paris Cité, ; Paris, France
                [3 ]ISNI 0000 0001 2157 9291, GRID grid.11843.3f, Institut de Biologie Moléculaire des Plantes, , CNRS, Université de Strasbourg, ; 67000 Strasbourg, France
                Author information
                http://orcid.org/0000-0001-6906-6620
                Article
                302
                10.1007/s12551-017-0302-6
                5578935
                28801801
                3d548c32-76fc-42ab-b982-930d6cd3f228
                © The Author(s) 2017

                Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

                History
                : 19 April 2017
                : 28 July 2017
                Funding
                Funded by: FundRef http://dx.doi.org/10.13039/501100000781, European Research Council;
                Award ID: ERC-2013-CoG-615739
                Award Recipient :
                Funded by: CNRS
                Award ID: NEstress
                Award Recipient :
                Funded by: Schlumberger Foundation for Education and Research
                Funded by: FundRef http://dx.doi.org/10.13039/501100001665, Agence Nationale de la Recherche;
                Award ID: ANR-11-IDEX-0005-02
                Award ID: ANR-11-LABX-0071
                Award Recipient :
                Categories
                Review
                Custom metadata
                © International Union for Pure and Applied Biophysics (IUPAB) and Springer-Verlag GmbH Germany 2017

                Biophysics
                nuclear envelope,lamina,linc complex,cytoskeleton,chromatin,mechanical force,microrheology,plants
                Biophysics
                nuclear envelope, lamina, linc complex, cytoskeleton, chromatin, mechanical force, microrheology, plants

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