Engineering the cellular mechanical microenvironment – from bulk mechanics to the nanoscale

Matellan, Carlos; Hernández, Armando E. del Río

doi:10.1242/jcs.229013

Cited by 42 publications

(35 citation statements)

References 133 publications

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“…The ability to polarize in response to mechanical stimuli is fundamental for directed cell migration such as durotaxis or haptotaxis (King et al, 2016;Lachowski et al, 2017) and depends on differential, asymmetric activation of Rho GTPases such as RhoA and Rac1, which in turn orchestrate actin dynamics at the leading edge (Machacek et al, 2009;Cortes et al, 2019a). Accordingly, we found that actin polymerization and the RhoA/mDia system, which are regulated by GPER, are required for cell polarization and mechanosensing, in agreement with previous work that demonstrates that stiffness and haptotactic sensing by lamellipodia relies on RhoA-mediated actin protrusion, branching, and focal adhesion turnover (Puleo et al, 2019) independently from the ROCK/myosin-2 axis (King et al, 2016;Oakes et al, 2018;Matellan and Del Río Hernández, 2019).…”

Section: Discussionsupporting

confidence: 91%

G Protein-Coupled Estrogen Receptor Regulates Actin Cytoskeleton Dynamics to Impair Cell Polarization

Lachowski

Cortés

Matellan

et al. 2020

Front. Cell Dev. Biol.

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Mechanical forces regulate cell functions through multiple pathways. G protein-coupled estrogen receptor (GPER) is a seven-transmembrane receptor that is ubiquitously expressed across tissues and mediates the acute cellular response to estrogens. Here, we demonstrate an unidentified role of GPER as a cellular mechanoregulator. G protein-coupled estrogen receptor signaling controls the assembly of stress fibers, the dynamics of the associated focal adhesions, and cell polarization via RhoA GTPase (RhoA). G protein-coupled estrogen receptor activation inhibits F-actin polymerization and subsequently triggers a negative feedback that transcriptionally suppresses the expression of monomeric G-actin. Given the broad expression of GPER and the range of cytoskeletal changes modulated by this receptor, our findings position GPER as a key player in mechanotransduction.

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Section: Discussionsupporting

confidence: 91%

G Protein-Coupled Estrogen Receptor Regulates Actin Cytoskeleton Dynamics to Impair Cell Polarization

Lachowski

Cortés

Matellan

et al. 2020

Front. Cell Dev. Biol.

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“…The cellular morphology and the direction of cell migration depends on properties such as the density and stiffness of the surrounding ECM components ( Yeung et al, 2005 ; Wehner et al, 2013 ; Charrier et al, 2018 ; Matellan and del Rıó Hernández, 2019 ). In fins, mesenchymal cells are mostly shaped rounded at the base region and are elongated at the fin tip region.…”

Section: Discussionmentioning

confidence: 99%

The Physical Role of Mesenchymal Cells Driven by the Actin Cytoskeleton Is Essential for the Orientation of Collagen Fibrils in Zebrafish Fins

Kuroda

Itabashi

Iwane

et al. 2020

Front. Cell Dev. Biol.

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Fibrous collagen imparts physical strength and flexibility to tissues by forming huge complexes. The density and orientation of collagen fibers must be correctly specified for the optimal physical property of the collagen complex. However, little is known about its underlying cellular mechanisms. Actinotrichia are collagen fibers aligned at the fin-tip of bony fish and are easily visible under the microscope due to their thick, linear structure. We used the actinotrichia as a model system to investigate how cells manipulate collagen fibers. The 3D image obtained by focused ion beam scanning electron microscopy (FIB-SEM) showed that the pseudopodia of mesenchymal cells encircle the multiple actinotrichia. We then co-incubated the mesenchymal cells and actinotrichia in vitro , and time-lapse analysis revealed how cells use pseudopods to align collagen fiber orientation. This in vitro behavior is dependent on actin polymerization in mesenchymal cells. Inhibition of actin polymerization in mesenchymal cells results in mis-orientation of actinotrichia in the fin. These results reveal how mesenchymal cells are involved in fin formation and have important implications for the physical interaction between cells and collagen fibers.

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“…At this scale, mechanical properties, such as tissue stiffness, can vary widely depending on multiple factors including local cellular tension, ECM composition, and flow conditions, leading to inaccuracies in the description of the mechanical environment. [ 11,135,137,138 ] The challenges in implementing existing measurement techniques to characterize engineered, vascularized microstissues have hindered the mechanistic understanding of vascular development and vascular disease progression in complex 3D environments. However, novel approaches to measure cell‐generated forces and material properties have emerged that can begin to fill this gap.…”

Section: Measuring Cell and Tissue Mechanical Properties For Mechanotmentioning

confidence: 99%

Biofabrication Strategies and Engineered In Vitro Systems for Vascular Mechanobiology

Pradhan

Banda

Farino

et al. 2020

Adv Healthcare Materials

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The vascular system is integral for maintaining organ‐specific functions and homeostasis. Dysregulation in vascular architecture and function can lead to various chronic or acute disorders. Investigation of the role of the vascular system in health and disease has been accelerated through the development of tissue‐engineered constructs and microphysiological on‐chip platforms. These in vitro systems permit studies of biochemical regulation of vascular networks and parenchymal tissue and provide mechanistic insights into the biophysical and hemodynamic forces acting in organ‐specific niches. Detailed understanding of these forces and the mechanotransductory pathways involved is necessary to develop preventative and therapeutic strategies targeting the vascular system. This review describes vascular structure and function, the role of hemodynamic forces in maintaining vascular homeostasis, and measurement approaches for cell and tissue level mechanical properties influencing vascular phenomena. State‐of‐the‐art techniques for fabricating in vitro microvascular systems, with varying degrees of biological and engineering complexity, are summarized. Finally, the role of vascular mechanobiology in organ‐specific niches and pathophysiological states, and efforts to recapitulate these events using in vitro microphysiological systems, are explored. It is hoped that this review will help readers appreciate the important, but understudied, role of vascular‐parenchymal mechanotransduction in health and disease toward developing mechanotherapeutics for treatment strategies.

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Engineering the cellular mechanical microenvironment – from bulk mechanics to the nanoscale

Cited by 42 publications

References 133 publications

G Protein-Coupled Estrogen Receptor Regulates Actin Cytoskeleton Dynamics to Impair Cell Polarization

G Protein-Coupled Estrogen Receptor Regulates Actin Cytoskeleton Dynamics to Impair Cell Polarization

The Physical Role of Mesenchymal Cells Driven by the Actin Cytoskeleton Is Essential for the Orientation of Collagen Fibrils in Zebrafish Fins

Biofabrication Strategies and Engineered In Vitro Systems for Vascular Mechanobiology

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