Nano-topography sensing by osteoclasts.

doi:10.1242/JCS.060954

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Nano-topography sensing by osteoclasts.

Journal Article•DOI•

Nano-topography sensing by osteoclasts.

Dafna Geblinger¹, Lia Addadi¹, Benjamin Geiger¹•Institutions (1)

Weizmann Institute of Science¹

01 May 2010-Journal of Cell Science (The Company of Biologists Ltd)-Vol. 123, Iss: 10, pp 1503-1510

TL;DR: It was observed that steps or sub-micrometer cracks on the smooth surface stimulate local ring formation, raising the possibility that similar imperfections on bone surfaces may stimulate local osteoclast resorptive activity.

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Abstract: Bone resorption by osteoclasts depends on the assembly of a specialized, actin-rich adhesive ‘sealing zone’ that delimits the area designed for degradation. In this study, we show that the level of roughness of the underlying adhesive surface has a profound effect on the formation and stability of the sealing zone and the associated F-actin. As our primary model substrate, we use ‘smooth’ and ‘rough’ calcite crystals with average topography values of 12 nm and 530 nm, respectively. We show that the smooth surfaces induce the formation of small and unstable actin rings with a typical lifespan of ~8 minutes, whereas the sealing zones formed on the rough calcite surfaces are considerably larger, and remain stable for more than 6 hours. It was further observed that steps or sub-micrometer cracks on the smooth surface stimulate local ring formation, raising the possibility that similar imperfections on bone surfaces may stimulate local osteoclast resorptive activity. The mechanisms whereby the physical properties of the substrate influence osteoclast behavior and their involvement in osteoclast function are discussed.

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Journal Article•DOI•

Balancing forces: architectural control of mechanotransduction

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Christopher C. DuFort¹, Matthew J. Paszek¹, Valerie M. Weaver¹•Institutions (1)

University of California, San Francisco¹

01 May 2011-Nature Reviews Molecular Cell Biology

TL;DR: Sustained disruptions in tensional homeostasis can be caused by alterations in the extracellular matrix, allowing it to serve as a mechanically based memory-storage device that can perpetuate a disease or restore normal tissue behaviour.

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Abstract: All cells exist within the context of a three-dimensional microenvironment in which they are exposed to mechanical and physical cues. These cues can be disrupted through perturbations to mechanotransduction, from the nanoscale-level to the tissue-level, which compromises tensional homeostasis to promote pathologies such as cardiovascular disease and cancer. The mechanisms of such perturbations suggest that a complex interplay exists between the extracellular microenvironment and cellular function. Furthermore, sustained disruptions in tensional homeostasis can be caused by alterations in the extracellular matrix, allowing it to serve as a mechanically based memory-storage device that can perpetuate a disease or restore normal tissue behaviour.

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875 citations

Cites background from "Nano-topography sensing by osteocla..."

...On a more specific level, the spatial presentation of ECM ligands, such as fibronectin, vitronectin, laminin and collagen, and the nanotopography of the ECM, control integrin organization, adhesion assembly, and signal transduction to direct cell behaviou...
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Journal Article•DOI•

Molecular Architecture and Function of Matrix Adhesions

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Benjamin Geiger¹, Kenneth M. Yamada²•Institutions (2)

Weizmann Institute of Science¹, National Institutes of Health²

01 May 2011-Cold Spring Harbor Perspectives in Biology

TL;DR: These cell adhesions play crucial roles in cell migration, proliferation, and determination of cell fate, and are mediated by membrane receptors such as the integrins, as well as many other components that comprise the adhesome.

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Abstract: Cell adhesions mediate important bidirectional interactions between cells and the extracellular matrix. They provide an interactive interface between the extracellular chemical and physical environment and the cellular scaffolding and signaling machinery. This dynamic, reciprocal regulation of intracellular processes and the matrix is mediated by membrane receptors such as the integrins, as well as many other components that comprise the adhesome. Adhesome constituents assemble themselves into different types of cell adhesion structures that vary in molecular complexity and change over time. These cell adhesions play crucial roles in cell migration, proliferation, and determination of cell fate.

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507 citations

Cites background from "Nano-topography sensing by osteocla..."

...Cells can also respond to the micro- or even nano-topography of a surface to which they adhere (Curtis and Wilkinson 1997; Cukierman et al. 2001; Geiger et al. 2001; Baharloo et al. 2005; Grossner-Schreiber et al. 2006; Vogel et al. 2006; Geblinger et al. 2010)....
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...They can assemble into large, belt-like superstructures, and are implicated in matrix-modulating activities (e.g., bone resorption by osteoclasts (Geblinger et al. 2010) and matrix invasion by a variety of cancer cells (Gimona et al. 2008)....
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...2006), regulating their dynamic properties (Geblinger et al. 2010), and modulating their signaling activity....
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...Cells can also respond to the micro-topography or even nano-topography of a surface to which they adhere (Curtis and Wilkinson 1997; Cukierman et al. 2001; Geiger et al. 2001; Baharloo et al. 2005; Grossner-Schreiber et al. 2006; Vogel et al. 2006; Geblinger et al. 2010)....
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...…surface features that are known to play a role in guiding the formation of matrix adhesions (Cukierman et al. 2001; Geiger et al. 2001; Baharloo et al. 2005; Grossner-Schreiber et al. 2006), regulating their dynamic properties (Geblinger et al. 2010) and modulating their signaling activity....
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Journal Article•DOI•

Nanotopographical Control of Stem Cell Differentiation

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Laura E. McNamara¹, Rebecca J. McMurray¹, Manus J.P. Biggs², Fahsai Kantawong¹, Richard O.C. Oreffo³, Matthew J. Dalby¹ - Show less +2 more•Institutions (3)

University of Glasgow¹, Columbia University², University of Southampton³

01 Jan 2010-Journal of Tissue Engineering

TL;DR: Nanotopography is examined as a means to guide differentiation, and its application is described in the context of different subsets of stem cells, with a particular focus on skeletal (mesenchymal) stem cells.

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Abstract: Stem cells have the capacity to differentiate into various lineages, and the ability to reliably direct stem cell fate determination would have tremendous potential for basic research and clinical therapy. Nanotopography provides a useful tool for guiding differentiation, as the features are more durable than surface chemistry and can be modified in size and shape to suit the desired application. In this paper, nanotopography is examined as a means to guide differentiation, and its application is described in the context of different subsets of stem cells, with a particular focus on skeletal (mesenchymal) stem cells. To address the mechanistic basis underlying the topographical effects on stem cells, the likely contributions of indirect (biochemical signal-mediated) and direct (force-mediated) mechanotransduction are discussed. Data from proteomic research is also outlined in relation to topography-mediated fate determination, as this approach provides insight into the global molecular changes at the level of the functional effectors.

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349 citations

Cites background from "Nano-topography sensing by osteocla..."

...diverse cell types including fibroblasts [18, 22], osteoblasts [23], osteoclasts [24, 25], endothelial [15], smooth muscle [26], epithelial [27, 28], and epitenon cells [16]....
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Journal Article•DOI•

Degrading devices: invadosomes in proteolytic cell invasion.

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Stefan Linder, Christiane Wiesner, Mirko Himmel

10 Oct 2011-Annual Review of Cell and Developmental Biology

TL;DR: An overview of the field is provided, with special focus on current developments such as intracellular transport processes, ultrastructural analysis, the possible involvement of invadosomes in disease, and the tentative identification of invadoomes in 3D environments and in vivo.

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Abstract: Podosomes and invadopodia, collectively known as invadosomes, are cell-matrix contacts in a variety of cell types, such as monocytic cells or cancer cells, that have to cross tissue barriers. Both structures share an actin-rich core, which distinguishes them from other matrix contacts, and are regulated by a multitude of signaling pathways including RhoGTPases, kinases, actin-associated proteins, and microtubule-dependent transport. Invadosomes recruit and secrete proteinases and are thus able to lyse extracellular matrix components. They are therefore considered to be potential key structures in proteolytic cell invasion in both physiological and pathological settings. This review provides an overview of the field, with special focus on current developments such as intracellular transport processes, ultrastructural analysis, the possible involvement of invadosomes in disease, and the tentative identification of invadosomes in 3D environments and in vivo.

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346 citations

Journal Article•DOI•

Extracellular matrix networks in bone remodeling.

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Andrea I. Alford¹, Kenneth M. Kozloff¹, Kurt D. Hankenson²•Institutions (2)

University of Michigan¹, Michigan State University²

01 Aug 2015-The International Journal of Biochemistry & Cell Biology

TL;DR: This comprehensive review will focus on how networks of ECM proteins function to regulate osteoclast- and osteoblast-mediated bone remodeling and the clinical significance of these networks on normal bone and as they relate to pathologies of bone mass and geometry will be considered.

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223 citations

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Journal Article•DOI•

THE MATERIAL BONE: Structure-Mechanical Function Relations

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S. Weiner¹, Hanoch Daniel Wagner¹•Institutions (1)

Weizmann Institute of Science¹

01 Aug 1998-Annual Review of Materials Science

TL;DR: The structure-mechanical relations at each of the hierarchical levels of organization are reviewed, highlighting wherever possible both underlying strategies and gaps in the authors' knowledge.

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Abstract: ▪ Abstract The term bone refers to a family of materials, all of which are built up of mineralized collagen fibrils. They have highly complex structures, described in terms of up to 7 hierarchical levels of organization. These materials have evolved to fulfill a variety of mechanical functions, for which the structures are presumably fine-tuned. Matching structure to function is a challenge. Here we review the structure-mechanical relations at each of the hierarchical levels of organization, highlighting wherever possible both underlying strategies and gaps in our knowledge. The insights gained from the study of these fascinating materials are not only important biologically, but may well provide novel ideas that can be applied to the design of synthetic materials.

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2,573 citations

"Nano-topography sensing by osteocla..." refers background in this paper

...Bone, composed of collagen fibers mineralized by carbonated apatite crystals (Weiner et al., 1999; Weiner and Wagner, 1998), is subject to continuous and tightly controlled remodeling, regulated primarily by two cell types, the bone-resorbing osteoclasts and the bone-depositing osteoblasts....
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Journal Article•DOI•

Environmental sensing through focal adhesions

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Benjamin Geiger¹, Joachim P. Spatz², Alexander D. Bershadsky¹•Institutions (2)

Weizmann Institute of Science¹, Max Planck Society²

01 Jan 2009-Nature Reviews Molecular Cell Biology

TL;DR: The mechanisms of such environmental sensing are discussed, based on the finely tuned crosstalk between the assembly of one type of integrin-based adhesion complex, namely focal adhesions, and the forces that are at work in the associated cytoskeletal network owing to actin polymerization and actomyosin contraction.

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Abstract: Recent progress in the design and application of artificial cellular microenvironments and nanoenvironments has revealed the extraordinary ability of cells to adjust their cytoskeletal organization, and hence their shape and motility, to minute changes in their immediate surroundings. Integrin-based adhesion complexes, which are tightly associated with the actin cytoskeleton, comprise the cellular machinery that recognizes not only the biochemical diversity of the extracellular neighbourhood, but also its physical and topographical characteristics, such as pliability, dimensionality and ligand spacing. Here, we discuss the mechanisms of such environmental sensing, based on the finely tuned crosstalk between the assembly of one type of integrin-based adhesion complex, namely focal adhesions, and the forces that are at work in the associated cytoskeletal network owing to actin polymerization and actomyosin contraction.

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2,322 citations

"Nano-topography sensing by osteocla..." refers background in this paper

...…cell proliferation, gene expression and cell viability (Bershadsky et al., 2006a; Chen et al., 1997; Diener et al., 2005; Discher et al., 2005; Engler et al., 2006; Geiger et al., 2009; Kunzler et al., 2007; Lo et al., 2000; Roach et al., 2007; Saltel et al., 2004; Vogel and Sheetz, 2006)....
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...…a widespread cellular phenomenon, whereby cells collect information on the substrate on which they grow, integrate it, and develop a response (Bershadsky et al., 2006a; Chen et al., 1997; Diener et al., 2005; Discher et al., 2005; Engler et al., 2006; Geiger et al., 2009; Vogel and Sheetz, 2006)....
[...]
...Although the mechanisms underlying these sensory functions are poorly understood, growing evidence suggests that protein unfolding, and reorganization of multiprotein complexes, play a key role in this process (Geiger et al., 2009; Wolfenson et al., 2009)....
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...…respond to chemical and physical properties of the underlying matrix, such as rigidity, mechanical activity, ligand density and dimensionality (Bershadsky et al., 2006a; Chen et al., 1997; Diener et al., 2005; Discher et al., 2005; Engler et al., 2006; Geiger et al., 2009; Vogel and Sheetz, 2006)....
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Journal Article•DOI•

Force and focal adhesion assembly: a close relationship studied using elastic micropatterned substrates

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Nathalie Q. Balaban¹, Ulrich S. Schwarz¹, Daniel Riveline², Polina Goichberg¹, Gila Tzur¹, Ilana Sabanay¹, Diana Mahalu¹, Samuel A. Safran¹, Alexander D. Bershadsky¹, Lia Addadi¹, Benjamin Geiger¹ - Show less +7 more•Institutions (2)

Weizmann Institute of Science¹, Joseph Fourier University²

01 May 2001-Nature Cell Biology

TL;DR: The results put clear constraints on the possible molecular mechanisms for the mechanosensory response of focal adhesions to applied force.

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Abstract: Mechanical forces play a major role in the regulation of cell adhesion and cytoskeletal organization. In order to explore the molecular mechanism underlying this regulation, we have investigated the relationship between local force applied by the cell to the substrate and the assembly of focal adhesions. A novel approach was developed for real-time, high-resolution measurements of forces applied by cells at single adhesion sites. This method combines micropatterning of elastomer substrates and fluorescence imaging of focal adhesions in live cells expressing GFPtagged vinculin. Local forces are correlated with the orientation, total fluorescence intensity and area of the focal adhesions, indicating a constant stress of 5.5 ± 2 nNμm-2. The dynamics of the force-dependent modulation of focal adhesions were characterized by blocking actomyosin contractility and were found to be on a time scale of seconds. The results put clear constraints on the possible molecular mechanisms for the mechanosensory response of focal adhesions to applied force.

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2,161 citations

"Nano-topography sensing by osteocla..." refers background in this paper

...Mechanical force applied to integrin adhesions was shown to strongly influence adhesion formation and dynamics (Balaban et al., 2001; Riveline et al., 2001)....
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...Several mechanisms underlying the cellular response to topographical features have been suggested for a variety of cell types (Balaban et al., 2001; Gov and Gopinathan, 2006; Patel et al., 2001; Riveline et al., 2001; Tarricone et al., 2001; Ulmer et al., 2008; Van Aelst et al., 1996; Vogel and…...
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Journal Article•DOI•

Local force and geometry sensing regulate cell functions.

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Viola Vogel¹, Michael P. Sheetz²•Institutions (2)

École Polytechnique Fédérale de Lausanne¹, Columbia University²

01 Apr 2006-Nature Reviews Molecular Cell Biology

TL;DR: Tissue scaffolds that have been engineered at the micro- and nanoscale level now enable better dissection of the mechanosensing, transduction and response mechanisms of eukaryotic cells.

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Abstract: 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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2,147 citations

"Nano-topography sensing by osteocla..." refers background in this paper

...Such channels could affect signaling activity at the adhesion sites (Patel et al., 2001; Vogel and Sheetz, 2006)....
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...…cell proliferation, gene expression and cell viability (Bershadsky et al., 2006a; Chen et al., 1997; Diener et al., 2005; Discher et al., 2005; Engler et al., 2006; Geiger et al., 2009; Kunzler et al., 2007; Lo et al., 2000; Roach et al., 2007; Saltel et al., 2004; Vogel and Sheetz, 2006)....
[...]
...…underlying the cellular response to topographical features have been suggested for a variety of cell types (Balaban et al., 2001; Gov and Gopinathan, 2006; Patel et al., 2001; Riveline et al., 2001; Tarricone et al., 2001; Ulmer et al., 2008; Van Aelst et al., 1996; Vogel and Sheetz, 2006)....
[...]
...…a widespread cellular phenomenon, whereby cells collect information on the substrate on which they grow, integrate it, and develop a response (Bershadsky et al., 2006a; Chen et al., 1997; Diener et al., 2005; Discher et al., 2005; Engler et al., 2006; Geiger et al., 2009; Vogel and Sheetz, 2006)....
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...…may induce the ventral cell membrane to adapt to a rough topography, leading to an uneven distribution of proteins (e.g. bar-domain proteins) that tend to partition into areas of high curvature (Gov and Gopinathan, 2006; Tarricone et al., 2001; Van Aelst et al., 1996; Vogel and Sheetz, 2006)....
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Journal Article•DOI•

Focal Contacts as Mechanosensors Externally Applied Local Mechanical Force Induces Growth of Focal Contacts by an Mdia1-Dependent and Rock-Independent Mechanism

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Daniel Riveline¹, Daniel Riveline², Eli Zamir³, Nathalie Q. Balaban², Ulrich S. Schwarz², Toshimasa Ishizaki⁴, Shuh Narumiya⁴, Zvi Kam², Benjamin Geiger², Alexander D. Bershadsky² - Show less +6 more•Institutions (4)

Joseph Fourier University¹, Weizmann Institute of Science², Max Planck Society³, Kyoto University⁴

11 Jun 2001-Journal of Cell Biology

TL;DR: Experiments show that integrin-containing focal complexes behave as individual mechanosensors exhibiting directional assembly in response to local force, and that external tension force bypasses the requirement for ROCK-mediated myosin II contractility in the induction of focal contacts.

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Abstract: The transition of cell–matrix adhesions from the initial punctate focal complexes into the mature elongated form, known as focal contacts, requires GTPase Rho activity. In particular, activation of myosin II–driven contractility by a Rho target known as Rho-associated kinase (ROCK) was shown to be essential for focal contact formation. To dissect the mechanism of Rho-dependent induction of focal contacts and to elucidate the role of cell contractility, we applied mechanical force to vinculin-containing dot-like adhesions at the cell edge using a micropipette. Local centripetal pulling led to local assembly and elongation of these structures and to their development into streak-like focal contacts, as revealed by the dynamics of green fluorescent protein–tagged vinculin or paxillin and interference reflection microscopy. Inhibition of Rho activity by C3 transferase suppressed this force-induced focal contact formation. However, constitutively active mutants of another Rho target, the formin homology protein mDia1 (Watanabe, N., T. Kato, A. Fujita, T. Ishizaki, and S. Narumiya. 1999. Nat. Cell Biol. 1:136–143), were sufficient to restore force-induced focal contact formation in C3 transferase-treated cells. Force-induced formation of the focal contacts still occurred in cells subjected to myosin II and ROCK inhibition. Thus, as long as mDia1 is active, external tension force bypasses the requirement for ROCK-mediated myosin II contractility in the induction of focal contacts. Our experiments show that integrin-containing focal complexes behave as individual mechanosensors exhibiting directional assembly in response to local force.

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1,450 citations