Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.

<h4>Background</h4>Various physical parameters, including substrate rigidity, size of adhesive islands and micro-and nano-topographies, have been shown to differentially regulate cell fate in two-dimensional (2-D) cell cultures. Cells anchored in a three-dimensional (3-D) microenvironmen...

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Autores principales: Mirjam Ochsner, Marcus Textor, Viola Vogel, Michael L Smith
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Publicado: Public Library of Science (PLoS) 2010
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spelling oai:doaj.org-article:2cee3a338a074578bccd98b28edaeef62021-11-25T06:25:15ZDimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.1932-620310.1371/journal.pone.0009445https://doaj.org/article/2cee3a338a074578bccd98b28edaeef62010-03-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/20351781/pdf/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Various physical parameters, including substrate rigidity, size of adhesive islands and micro-and nano-topographies, have been shown to differentially regulate cell fate in two-dimensional (2-D) cell cultures. Cells anchored in a three-dimensional (3-D) microenvironment show significantly altered phenotypes, from altered cell adhesions, to cell migration and differentiation. Yet, no systematic analysis has been performed that studied how the integrated cellular responses to the physical characteristics of the environment are regulated by dimensionality (2-D versus 3-D).<h4>Methodology/principal findings</h4>Arrays of 5 or 10 microm deep microwells were fabricated in polydimethylsiloxane (PDMS). The actin cytoskeleton was compared for single primary fibroblasts adhering either to microfabricated adhesive islands (2-D) or trapped in microwells (3-D) of controlled size, shape, and wall rigidity. On rigid substrates (Young's Modulus = 1 MPa), cytoskeleton assembly within single fibroblast cells occurred in 3-D microwells of circular, rectangular, square, and triangular shapes with 2-D projected surface areas (microwell bottom surface area) and total surface areas of adhesion (microwell bottom plus wall surface area) that inhibited stress fiber assembly in 2-D. In contrast, cells did not assemble a detectable actin cytoskeleton in soft 3-D microwells (20 kPa), regardless of their shapes, but did so on flat, 2-D substrates. The dependency on environmental dimensionality was also reflected by cell viability and metabolism as probed by mitochondrial activities. Both were upregulated in 3-D cultured cells versus cells on 2-D patterns when surface area of adhesion and rigidity were held constant.<h4>Conclusion/significance</h4>These data indicate that cell shape and rigidity are not orthogonal parameters directing cell fate. The sensory toolbox of cells integrates mechanical (rigidity) and topographical (shape and dimensionality) information differently when cell adhesions are confined to 2-D or occur in a 3-D space.Mirjam OchsnerMarcus TextorViola VogelMichael L SmithPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 5, Iss 3, p e9445 (2010)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Mirjam Ochsner
Marcus Textor
Viola Vogel
Michael L Smith
Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
description <h4>Background</h4>Various physical parameters, including substrate rigidity, size of adhesive islands and micro-and nano-topographies, have been shown to differentially regulate cell fate in two-dimensional (2-D) cell cultures. Cells anchored in a three-dimensional (3-D) microenvironment show significantly altered phenotypes, from altered cell adhesions, to cell migration and differentiation. Yet, no systematic analysis has been performed that studied how the integrated cellular responses to the physical characteristics of the environment are regulated by dimensionality (2-D versus 3-D).<h4>Methodology/principal findings</h4>Arrays of 5 or 10 microm deep microwells were fabricated in polydimethylsiloxane (PDMS). The actin cytoskeleton was compared for single primary fibroblasts adhering either to microfabricated adhesive islands (2-D) or trapped in microwells (3-D) of controlled size, shape, and wall rigidity. On rigid substrates (Young's Modulus = 1 MPa), cytoskeleton assembly within single fibroblast cells occurred in 3-D microwells of circular, rectangular, square, and triangular shapes with 2-D projected surface areas (microwell bottom surface area) and total surface areas of adhesion (microwell bottom plus wall surface area) that inhibited stress fiber assembly in 2-D. In contrast, cells did not assemble a detectable actin cytoskeleton in soft 3-D microwells (20 kPa), regardless of their shapes, but did so on flat, 2-D substrates. The dependency on environmental dimensionality was also reflected by cell viability and metabolism as probed by mitochondrial activities. Both were upregulated in 3-D cultured cells versus cells on 2-D patterns when surface area of adhesion and rigidity were held constant.<h4>Conclusion/significance</h4>These data indicate that cell shape and rigidity are not orthogonal parameters directing cell fate. The sensory toolbox of cells integrates mechanical (rigidity) and topographical (shape and dimensionality) information differently when cell adhesions are confined to 2-D or occur in a 3-D space.
format article
author Mirjam Ochsner
Marcus Textor
Viola Vogel
Michael L Smith
author_facet Mirjam Ochsner
Marcus Textor
Viola Vogel
Michael L Smith
author_sort Mirjam Ochsner
title Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
title_short Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
title_full Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
title_fullStr Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
title_full_unstemmed Dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
title_sort dimensionality controls cytoskeleton assembly and metabolism of fibroblast cells in response to rigidity and shape.
publisher Public Library of Science (PLoS)
publishDate 2010
url https://doaj.org/article/2cee3a338a074578bccd98b28edaeef6
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AT marcustextor dimensionalitycontrolscytoskeletonassemblyandmetabolismoffibroblastcellsinresponsetorigidityandshape
AT violavogel dimensionalitycontrolscytoskeletonassemblyandmetabolismoffibroblastcellsinresponsetorigidityandshape
AT michaellsmith dimensionalitycontrolscytoskeletonassemblyandmetabolismoffibroblastcellsinresponsetorigidityandshape
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