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Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation

BACKGROUND: In vitro experiments on the functional roles of extracellular matrix (ECM) components usually involve the culture of cells on surfaces coated with purified ECM components. These experiments can seldom recuperate the spatial arrangement of ECM found in vivo. In this study, we have overcom...

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Autores principales: Tang, Sze Wing, Tong, Wing Yin, Shen, Wei, Yeung, Kelvin W K, Lam, Yun Wah
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2014
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3987840/
https://www.ncbi.nlm.nih.gov/pubmed/24661496
http://dx.doi.org/10.1186/1471-2121-15-10
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author Tang, Sze Wing
Tong, Wing Yin
Shen, Wei
Yeung, Kelvin W K
Lam, Yun Wah
author_facet Tang, Sze Wing
Tong, Wing Yin
Shen, Wei
Yeung, Kelvin W K
Lam, Yun Wah
author_sort Tang, Sze Wing
collection PubMed
description BACKGROUND: In vitro experiments on the functional roles of extracellular matrix (ECM) components usually involve the culture of cells on surfaces coated with purified ECM components. These experiments can seldom recuperate the spatial arrangement of ECM found in vivo. In this study, we have overcome this obstacle by using histological sections of bovine Achilles tendon as cell culture substrates. RESULTS: We found that tendon sections can be viewed as a pre-formed block of ECM in which the collagen fibrils exhibited a spatial regularity unraveled in any artificially constructed scaffold. By carving the tendon at different angles relative to its main axis, we created different surfaces with distinct spatial arrangements of collagen fibrils. To assess the cellular responses to these surfaces, human mesenchymal stem cells (MSCs) were directly cultured on these sections, hence exposed to the collagen with different spatial orientations. Cells seeded on longitudinal tendon sections adopted a highly elongated and aligned morphology, and expressed an increased level of tenomodulin, suggesting that the collagen fibrils present in this section provide a microenvironment that facilitates cell morphogenesis and differentiation. However, MSC elongation, alignment and induction of tenomodulin diminished dramatically even as the sectioned angle changed slightly. CONCLUSION: Our results suggest that cell functions are influenced not only by the type or concentration of ECM components, but also by the precise spatial arrangements of these molecules. The method developed in this study offers a simple and robust way for the studying of cell-ECM interactions, and opens many research avenues in the field of matrix biology.
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spelling pubmed-39878402014-04-16 Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation Tang, Sze Wing Tong, Wing Yin Shen, Wei Yeung, Kelvin W K Lam, Yun Wah BMC Cell Biol Research Article BACKGROUND: In vitro experiments on the functional roles of extracellular matrix (ECM) components usually involve the culture of cells on surfaces coated with purified ECM components. These experiments can seldom recuperate the spatial arrangement of ECM found in vivo. In this study, we have overcome this obstacle by using histological sections of bovine Achilles tendon as cell culture substrates. RESULTS: We found that tendon sections can be viewed as a pre-formed block of ECM in which the collagen fibrils exhibited a spatial regularity unraveled in any artificially constructed scaffold. By carving the tendon at different angles relative to its main axis, we created different surfaces with distinct spatial arrangements of collagen fibrils. To assess the cellular responses to these surfaces, human mesenchymal stem cells (MSCs) were directly cultured on these sections, hence exposed to the collagen with different spatial orientations. Cells seeded on longitudinal tendon sections adopted a highly elongated and aligned morphology, and expressed an increased level of tenomodulin, suggesting that the collagen fibrils present in this section provide a microenvironment that facilitates cell morphogenesis and differentiation. However, MSC elongation, alignment and induction of tenomodulin diminished dramatically even as the sectioned angle changed slightly. CONCLUSION: Our results suggest that cell functions are influenced not only by the type or concentration of ECM components, but also by the precise spatial arrangements of these molecules. The method developed in this study offers a simple and robust way for the studying of cell-ECM interactions, and opens many research avenues in the field of matrix biology. BioMed Central 2014-03-25 /pmc/articles/PMC3987840/ /pubmed/24661496 http://dx.doi.org/10.1186/1471-2121-15-10 Text en Copyright © 2014 Tang et al.; licensee BioMed Central Ltd. http://creativecommons.org/licenses/by/2.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Tang, Sze Wing
Tong, Wing Yin
Shen, Wei
Yeung, Kelvin W K
Lam, Yun Wah
Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title_full Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title_fullStr Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title_full_unstemmed Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title_short Stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
title_sort stringent requirement for spatial arrangement of extracellular matrix in supporting cell morphogenesis and differentiation
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3987840/
https://www.ncbi.nlm.nih.gov/pubmed/24661496
http://dx.doi.org/10.1186/1471-2121-15-10
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