Literature DB >> 31409716

High stretchability, strength, and toughness of living cells enabled by hyperelastic vimentin intermediate filaments.

Jiliang Hu1, Yiwei Li1, Yukun Hao1, Tianqi Zheng1, Satish K Gupta1, German Alberto Parada2, Huayin Wu3, Shaoting Lin1, Shida Wang1, Xuanhe Zhao1,4, Robert D Goldman5, Shengqiang Cai6, Ming Guo7.   

Abstract

In many developmental and pathological processes, including cellular migration during normal development and invasion in cancer metastasis, cells are required to withstand severe deformations. The structural integrity of eukaryotic cells under small deformations has been known to depend on the cytoskeleton including actin filaments (F-actin), microtubules (MT), and intermediate filaments (IFs). However, it remains unclear how cells resist severe deformations since both F-actin and microtubules yield or disassemble under moderate strains. Using vimentin containing IFs (VIFs) as a model for studying the large family of IF proteins, we demonstrate that they dominate cytoplasmic mechanics and maintain cell viability at large deformations. Our results show that cytoskeletal VIFs form a stretchable, hyperelastic network in living cells. This network works synergistically with other cytoplasmic components, substantially enhancing the strength, stretchability, resilience, and toughness of cells. Moreover, we find the hyperelastic VIF network, together with other quickly recoverable cytoskeletal components, forms a mechanically robust structure which can mechanically recover after damage.

Entities:  

Keywords:  cell mechanics; cytoplasm; cytoskeleton; intermediate filament; vimentin

Mesh:

Substances:

Year:  2019        PMID: 31409716      PMCID: PMC6717279          DOI: 10.1073/pnas.1903890116

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


  38 in total

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Authors:  B Fabry; G N Maksym; J P Butler; M Glogauer; D Navajas; J J Fredberg
Journal:  Phys Rev Lett       Date:  2001-09-13       Impact factor: 9.161

Review 4.  Cytoarchitecture and physical properties of cytoplasm: volume, viscosity, diffusion, intracellular surface area.

Authors:  K Luby-Phelps
Journal:  Int Rev Cytol       Date:  2000

5.  Nonlinear elasticity in biological gels.

Authors:  Cornelis Storm; Jennifer J Pastore; F C MacKintosh; T C Lubensky; Paul A Janmey
Journal:  Nature       Date:  2005-05-12       Impact factor: 49.962

6.  Reversible stress softening of actin networks.

Authors:  Ovijit Chaudhuri; Sapun H Parekh; Daniel A Fletcher
Journal:  Nature       Date:  2007-01-18       Impact factor: 49.962

7.  Power laws in microrheology experiments on living cells: Comparative analysis and modeling.

Authors:  Martial Balland; Nicolas Desprat; Delphine Icard; Sophie Féréol; Atef Asnacios; Julien Browaeys; Sylvie Hénon; François Gallet
Journal:  Phys Rev E Stat Nonlin Soft Matter Phys       Date:  2006-08-09

Review 8.  Softness, strength and self-repair in intermediate filament networks.

Authors:  Oliver I Wagner; Sebastian Rammensee; Neha Korde; Qi Wen; Jean-Francois Leterrier; Paul A Janmey
Journal:  Exp Cell Res       Date:  2007-04-27       Impact factor: 3.905

9.  Micromechanical properties of keratin intermediate filament networks.

Authors:  Sivaraj Sivaramakrishnan; James V DeGiulio; Laszlo Lorand; Robert D Goldman; Karen M Ridge
Journal:  Proc Natl Acad Sci U S A       Date:  2008-01-16       Impact factor: 11.205

10.  EB1 regulates microtubule dynamics and tubulin sheet closure in vitro.

Authors:  Benjamin Vitre; Frédéric M Coquelle; Claire Heichette; Cyrille Garnier; Denis Chrétien; Isabelle Arnal
Journal:  Nat Cell Biol       Date:  2008-03-23       Impact factor: 28.824

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  30 in total

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3.  Vimentin filaments drive migratory persistence in polyploidal cancer cells.

Authors:  Botai Xuan; Deepraj Ghosh; Joy Jiang; Rachelle Shao; Michelle R Dawson
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Review 4.  Generation, Transmission, and Regulation of Mechanical Forces in Embryonic Morphogenesis.

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Journal:  Front Cell Dev Biol       Date:  2022-06-17

Review 7.  Intermediate filaments as effectors of differentiation.

Authors:  Catherine J Redmond; Pierre A Coulombe
Journal:  Curr Opin Cell Biol       Date:  2020-11-24       Impact factor: 8.382

8.  The vimentin cytoskeleton: when polymer physics meets cell biology.

Authors:  Alison E Patteson; Robert J Carroll; Daniel V Iwamoto; Paul A Janmey
Journal:  Phys Biol       Date:  2020-12-01       Impact factor: 2.583

9.  The force loading rate drives cell mechanosensing through both reinforcement and cytoskeletal softening.

Authors:  Ion Andreu; Bryan Falcones; Sebastian Hurst; Nimesh Chahare; Xarxa Quiroga; Anabel-Lise Le Roux; Zanetta Kechagia; Amy E M Beedle; Alberto Elosegui-Artola; Xavier Trepat; Ramon Farré; Timo Betz; Isaac Almendros; Pere Roca-Cusachs
Journal:  Nat Commun       Date:  2021-07-09       Impact factor: 14.919

Review 10.  Molecular cancer cell responses to solid compressive stress and interstitial fluid pressure.

Authors:  Purboja Purkayastha; Manish K Jaiswal; Tanmay P Lele
Journal:  Cytoskeleton (Hoboken)       Date:  2021-07-28
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