The Role of Vimentin Intermediate Filaments in Cortical and Cytoplasmic Mechanics

doi:10.1016/J.BPJ.2013.08.037

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The Role of Vimentin Intermediate Filaments in Cortical and Cytoplasmic Mechanics

Journal Article•DOI•

The Role of Vimentin Intermediate Filaments in Cortical and Cytoplasmic Mechanics

Ming Guo¹, Allen J. Ehrlicher¹, Allen J. Ehrlicher², Saleemulla Mahammad³, Hilary Fabich¹, Mikkel H. Jensen⁴, Mikkel H. Jensen¹, Jeffrey R. Moore⁴, Jeffrey J. Fredberg¹, Robert D. Goldman³, David A. Weitz¹ - Show less +7 more•Institutions (4)

Harvard University¹, Beth Israel Deaconess Medical Center², Northwestern University³, Boston University⁴

01 Oct 2013-Biophysical Journal (The Biophysical Society)-Vol. 105, Iss: 7, pp 1562-1568

TL;DR: Studying mouse embryonic fibroblasts derived from wild-type or vimentin(-/-) mice shows that VIFs both increase the mechanical integrity of cells and localize intracellular components.

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About: This article is published in Biophysical Journal.The article was published on 2013-10-01 and is currently open access. It has received 230 citations till now. The article focuses on the topics: Cytoskeleton & Intermediate filament.

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Journal Article•DOI•

Probing the Stochastic, Motor-Driven Properties of the Cytoplasm Using Force Spectrum Microscopy

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Ming Guo¹, Allen J. Ehrlicher¹, Allen J. Ehrlicher², Mikkel H. Jensen³, Mikkel H. Jensen¹, Malte Renz⁴, Jeffrey R. Moore³, Robert D. Goldman⁵, Jennifer Lippincott-Schwartz⁴, Fred C. MacKintosh⁶, David A. Weitz¹ - Show less +7 more•Institutions (6)

Harvard University¹, Beth Israel Deaconess Medical Center², Boston University³, National Institutes of Health⁴, Northwestern University⁵, VU University Amsterdam⁶

14 Aug 2014-Cell

TL;DR: This work introduces force-spectrum-microscopy (FSM) to directly quantify random forces within the cytoplasm of cells and thereby probe stochastic motor activity, and shows that force fluctuations substantially enhance intracellular movement of small and large components.

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439 citations

Cites methods from "The Role of Vimentin Intermediate F..."

...WT and Vim / mEFs (Guo et al., 2013) are cultured in DMEM with 10% fetal calf serum, 5 mM nonessential amino acids, 100 U/ml penicillin, and 100 mg/ml streptomycin....
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...15, in agreement with other measurements (Fabry et al., 2001; Guo et al., 2013)....
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...By measuring the resultant displacement of the bead, x(y), subjected to an applied sinusoidal trap oscillation with a force F at frequency y, we extracted the effective spring constant, K(y) = F(y)/x(y), for the intracellular environment (Guo et al., 2013; Mizuno et al., 2007)....
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Journal Article•DOI•

Impact of the physical microenvironment on tumor progression and metastasis.

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Fabian Spill¹, Daniel S. Reynolds², Roger D. Kamm¹, Muhammad H. Zaman³, Muhammad H. Zaman² - Show less +1 more•Institutions (3)

Massachusetts Institute of Technology¹, Boston University², Howard Hughes Medical Institute³

01 Aug 2016-Current Opinion in Biotechnology

TL;DR: A new appreciation for the role of mechanics in cancer is emerging because in vitro systems are becoming increasingly sophisticated in differentiating between distinct physical cues-ECM pore size, fiber alignment, and molecular composition-and elucidating the different roles these properties play in driving tumor progression and metastasis.

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378 citations

Journal Article•DOI•

Cell volume change through water efflux impacts cell stiffness and stem cell fate.

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Ming Guo¹, Adrian F. Pegoraro¹, Angelo S. Mao¹, Enhua H. Zhou¹, Praveen R. Arany², Yu Long Han¹, Yu Long Han³, Dylan T. Burnette⁴, Mikkel H. Jensen⁵, Mikkel H. Jensen¹, Karen E. Kasza¹, Karen E. Kasza⁶, Jeffrey R. Moore⁷, Fred C. MacKintosh⁸, Fred C. MacKintosh⁹, Jeffrey J. Fredberg¹, David J. Mooney¹, Jennifer Lippincott-Schwartz¹⁰, David A. Weitz¹ - Show less +15 more•Institutions (10)

Harvard University¹, University at Buffalo², Xi'an Jiaotong University³, Vanderbilt University⁴, California State University, Sacramento⁵, Columbia University⁶, University of Massachusetts Amherst⁷, Rice University⁸, VU University Amsterdam⁹, Howard Hughes Medical Institute¹⁰

10 Oct 2017-Proceedings of the National Academy of Sciences of the United States of America

TL;DR: A robust and unified relationship between cell stiffness and cell volume is identified and it is found that changes in cell volume, and hence stiffness, alter stem-cell differentiation, regardless of the method by which these are induced.

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Abstract: Cells alter their mechanical properties in response to their local microenvironment; this plays a role in determining cell function and can even influence stem cell fate. Here, we identify a robust and unified relationship between cell stiffness and cell volume. As a cell spreads on a substrate, its volume decreases, while its stiffness concomitantly increases. We find that both cortical and cytoplasmic cell stiffness scale with volume for numerous perturbations, including varying substrate stiffness, cell spread area, and external osmotic pressure. The reduction of cell volume is a result of water efflux, which leads to a corresponding increase in intracellular molecular crowding. Furthermore, we find that changes in cell volume, and hence stiffness, alter stem-cell differentiation, regardless of the method by which these are induced. These observations reveal a surprising, previously unidentified relationship between cell stiffness and cell volume that strongly influences cell biology.

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331 citations

Cites background or result from "The Role of Vimentin Intermediate F..."

...However, the cell is a highly heterogeneous structure, and the interior is much softer; the cytoplasm of the cell is a weak elastic gel with a shear modulus that is three orders of magnitude lower than that of the cortex (17, 20)....
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...S3 (8, 16, 17); the results obtained with OMTC are in quantitative agreement with those obtained by using AFM (18, 19)....
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Journal Article•DOI•

The molecular architecture of lamins in somatic cells

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Yagmur Turgay¹, Matthias Eibauer¹, Anne E. Goldman², Takeshi Shimi², Maayan Khayat³, Kfir Ben-Harush, Anna Dubrovsky-Gaupp¹, K. Tanuj Sapra¹, Robert D. Goldman², Ohad Medalia³, Ohad Medalia¹ - Show less +7 more•Institutions (3)

University of Zurich¹, Northwestern University², Ben-Gurion University of the Negev³

09 Mar 2017-Nature

TL;DR: In this article, a detailed view of the organization of the lamin meshwork within the lamina was obtained using cryo-electron tomography, which showed that A-and B-type lamins assemble into tetrameric filaments of 3.5 nm thickness.

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Abstract: The nuclear lamina is a fundamental constituent of metazoan nuclei. It is composed mainly of lamins, which are intermediate filament proteins that assemble into a filamentous meshwork, bridging the nuclear envelope and chromatin. Besides providing structural stability to the nucleus, the lamina is involved in many nuclear activities, including chromatin organization, transcription and replication. However, the structural organization of the nuclear lamina is poorly understood. Here we use cryo-electron tomography to obtain a detailed view of the organization of the lamin meshwork within the lamina. Data analysis of individual lamin filaments resolves a globular-decorated fibre appearance and shows that A- and B-type lamins assemble into tetrameric filaments of 3.5 nm thickness. Thus, lamins exhibit a structure that is remarkably different from the other canonical cytoskeletal elements. Our findings define the architecture of the nuclear lamin meshworks at molecular resolution, providing insights into their role in scaffolding the nuclear lamina.

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319 citations

Journal Article•DOI•

The soft mechanical signature of glial scars in the central nervous system.

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Emad Moeendarbary¹, Emad Moeendarbary², Emad Moeendarbary³, Isabell P. Weber³, Graham K. Sheridan⁴, Graham K. Sheridan³, David E. Koser³, Sara Soleman³, Barbara Haenzi³, Elizabeth J. Bradbury⁵, James W. Fawcett³, Kristian Franze³ - Show less +8 more•Institutions (5)

University College London¹, Massachusetts Institute of Technology², University of Cambridge³, University of Brighton⁴, Wolfson Centre for Age-Related Diseases⁵

20 Mar 2017-Nature Communications

TL;DR: In this paper, the authors characterized spatiotemporal changes of the elastic stiffness of the injured rat neocortex and spinal cord at 1.5 and three weeks post-injury using atomic force microscopy.

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Abstract: Injury to the central nervous system (CNS) alters the molecular and cellular composition of neural tissue and leads to glial scarring, which inhibits the regrowth of damaged axons. Mammalian glial scars supposedly form a chemical and mechanical barrier to neuronal regeneration. While tremendous effort has been devoted to identifying molecular characteristics of the scar, very little is known about its mechanical properties. Here we characterize spatiotemporal changes of the elastic stiffness of the injured rat neocortex and spinal cord at 1.5 and three weeks post-injury using atomic force microscopy. In contrast to scars in other mammalian tissues, CNS tissue significantly softens after injury. Expression levels of glial intermediate filaments (GFAP, vimentin) and extracellular matrix components (laminin, collagen IV) correlate with tissue softening. As tissue stiffness is a regulator of neuronal growth, our results may help to understand why mammalian neurons do not regenerate after injury.

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254 citations

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References

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Journal Article•DOI•

Cell mechanics and the cytoskeleton

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Daniel A. Fletcher¹, Daniel A. Fletcher², R. Dyche Mullins³•Institutions (3)

University of California, Berkeley¹, Lawrence Berkeley National Laboratory², University of California, San Francisco³

28 Jan 2010-Nature

TL;DR: An important insight emerging from this work is that long-lived cytoskeletal structures may act as epigenetic determinants of cell shape, function and fate.

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Abstract: The ability of a eukaryotic cell to resist deformation, to transport intracellular cargo and to change shape during movement depends on the cytoskeleton, an interconnected network of filamentous polymers and regulatory proteins. Recent work has demonstrated that both internal and external physical forces can act through the cytoskeleton to affect local mechanical properties and cellular behaviour. Attention is now focused on how cytoskeletal networks generate, transmit and respond to mechanical signals over both short and long timescales. An important insight emerging from this work is that long-lived cytoskeletal structures may act as epigenetic determinants of cell shape, function and fate.

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2,323 citations

"The Role of Vimentin Intermediate F..." refers background in this paper

...These two distinct cytoskeletal regions create a composite network that transmits mechanical signals from the extracellular matrix to the nucleus (36,37) while spatially organizing and mechanically protecting cellular components (38)....
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...In addition to contributing to cell mechanics, another major role of cytoplasmic VIFs is to spatially organize the contents of the cell (38)....
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Journal Article•DOI•

Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus

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Ning Wang¹, Jessica D. Tytell², Donald E. Ingber³•Institutions (3)

University of Illinois at Urbana–Champaign¹, Harvard University², Wyss Institute for Biologically Inspired Engineering³

01 Jan 2009-Nature Reviews Molecular Cell Biology

TL;DR: The molecular mechanisms by which forces might act at a distance to induce mechanochemical conversion in the nucleus and alter gene activities are explored.

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Abstract: Research in cellular mechanotransduction often focuses on how extracellular physical forces are converted into chemical signals at the cell surface. However, mechanical forces that are exerted on surface-adhesion receptors, such as integrins and cadherins, are also channelled along cytoskeletal filaments and concentrated at distant sites in the cytoplasm and nucleus. Here, we explore the molecular mechanisms by which forces might act at a distance to induce mechanochemical conversion in the nucleus and alter gene activities.

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1,582 citations

"The Role of Vimentin Intermediate F..." refers background in this paper

...These two distinct cytoskeletal regions create a composite network that transmits mechanical signals from the extracellular matrix to the nucleus (36,37) while spatially organizing and mechanically protecting cellular components (38)....
[...]

Journal Article•DOI•

Scaling the microrheology of living cells.

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Ben Fabry¹, Geoffrey N. Maksym², James P. Butler¹, Michael Glogauer¹, Daniel Navajas³, Jeffrey J. Fredberg¹ - Show less +2 more•Institutions (3)

Harvard University¹, Dalhousie University², University of Barcelona³

13 Sep 2001-Physical Review Letters

TL;DR: A scaling law is reported 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, and implies that cytoskeletal proteins may regulate cell mechanical properties mainly by modulating the effective noise temperature of the matrix.

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Abstract: 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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1,166 citations

"The Role of Vimentin Intermediate F..." refers result in this paper

...Both the power-law form and the value of b are in accord with the behavior of the cytoplasm, as well as with previous cortical measurements (15,27,28)....
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...This technique has been used extensively to measure material properties of cells (15,16) and the results agree quantitatively with measurements obtained with other methods, such as AFM....
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...This observation agrees with the power-law rheology observed previously for living cells and biopolymer networks (15,26)....
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Molecular Biology of the Cell (Fifth Edition)

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Bruce Alberts, Alexander Johnson, Julian Lewis, Martin Raff, Keith Roberts, Peter Walter - Show less +2 more

01 Jan 2008

1,139 citations

"The Role of Vimentin Intermediate F..." refers background in this paper

...However, it is the cytoplasm that surrounds all the key organelles, and its mechanical properties are critical for a large number of cellular processes ranging from large-scale events such as maintenance of cell shape and generation of cell motility to more localized events such as mechanotransduction, signaling, and gene regulation (1)....
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Journal Article•DOI•

Nonequilibrium mechanics of active cytoskeletal networks.

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Daisuke Mizuno¹, Catherine Tardin¹, Christoph F. Schmidt², Christoph F. Schmidt¹, Fred C. MacKintosh¹ - Show less +1 more•Institutions (2)

VU University Amsterdam¹, University of Göttingen²

19 Jan 2007-Science

TL;DR: A quantitative theoretical model is presented connecting the large-scale properties of this active gel to molecular force generation and qualitatively changing the viscoelastic response of the network in an adenosine triphosphate–dependent manner.

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Abstract: Cells both actively generate and sensitively react to forces through their mechanical framework, the cytoskeleton, which is a nonequilibrium composite material including polymers and motor proteins. We measured the dynamics and mechanical properties of a simple three-component model system consisting of myosin II, actin filaments, and cross-linkers. In this system, stresses arising from motor activity controlled the cytoskeletal network mechanics, increasing stiffness by a factor of nearly 100 and qualitatively changing the viscoelastic response of the network in an adenosine triphosphate–dependent manner. We present a quantitative theoretical model connecting the large-scale properties of this active gel to molecular force generation.

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857 citations

"The Role of Vimentin Intermediate F..." refers background in this paper

...For a homogeneous, incompressible viscoelastic material, this spring constant is related to a complex modulus, G 1⁄4 G0þiG00, through a generalization of the Stokes relation K 1⁄4 3pGd (22), where d is the bead diameter....
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