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Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips

Most tissues in the body are under mechanical tension, and while enzymes mediate many cellular and extracellular processes, the effects of mechanical forces on enzyme reactions in the native extracellular matrix (ECM) are not fully understood. We hypothesized that physiological levels of mechanical...

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Autores principales: Yi, Eunice, Sato, Susumu, Takahashi, Ayuko, Parameswaran, Harikrishnan, Blute, Todd A., Bartolák-Suki, Erzsébet, Suki, Béla
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4940411/
https://www.ncbi.nlm.nih.gov/pubmed/27462275
http://dx.doi.org/10.3389/fphys.2016.00287
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author Yi, Eunice
Sato, Susumu
Takahashi, Ayuko
Parameswaran, Harikrishnan
Blute, Todd A.
Bartolák-Suki, Erzsébet
Suki, Béla
author_facet Yi, Eunice
Sato, Susumu
Takahashi, Ayuko
Parameswaran, Harikrishnan
Blute, Todd A.
Bartolák-Suki, Erzsébet
Suki, Béla
author_sort Yi, Eunice
collection PubMed
description Most tissues in the body are under mechanical tension, and while enzymes mediate many cellular and extracellular processes, the effects of mechanical forces on enzyme reactions in the native extracellular matrix (ECM) are not fully understood. We hypothesized that physiological levels of mechanical forces are capable of modifying the activity of collagenase, a key remodeling enzyme of the ECM. To test this, lung tissue Young's modulus and a nonlinearity index characterizing the shape of the stress-strain curve were measured in the presence of bacterial collagenase under static uniaxial strain of 0, 20, 40, and 80%, as well as during cyclic mechanical loading with strain amplitudes of ±10 or ±20% superimposed on 40% static strain, and frequencies of 0.1 or 1 Hz. Confocal and electron microscopy was used to determine and quantify changes in ECM structure. Generally, mechanical loading increased the effects of enzyme activity characterized by an irreversible decline in stiffness and tissue deterioration seen on both confocal and electron microscopic images. However, a static strain of 20% provided protection against digestion compared to both higher and lower strains. The decline in stiffness during digestion positively correlated with the increase in equivalent alveolar diameters and negatively correlated with the nonlinearity index. These results suggest that the decline in stiffness results from rupture of collagen followed by load transfer and subsequent rupture of alveolar walls. This study may provide new understanding of the role of collagen degradation in general tissue remodeling and disease progression.
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spelling pubmed-49404112016-07-26 Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips Yi, Eunice Sato, Susumu Takahashi, Ayuko Parameswaran, Harikrishnan Blute, Todd A. Bartolák-Suki, Erzsébet Suki, Béla Front Physiol Physiology Most tissues in the body are under mechanical tension, and while enzymes mediate many cellular and extracellular processes, the effects of mechanical forces on enzyme reactions in the native extracellular matrix (ECM) are not fully understood. We hypothesized that physiological levels of mechanical forces are capable of modifying the activity of collagenase, a key remodeling enzyme of the ECM. To test this, lung tissue Young's modulus and a nonlinearity index characterizing the shape of the stress-strain curve were measured in the presence of bacterial collagenase under static uniaxial strain of 0, 20, 40, and 80%, as well as during cyclic mechanical loading with strain amplitudes of ±10 or ±20% superimposed on 40% static strain, and frequencies of 0.1 or 1 Hz. Confocal and electron microscopy was used to determine and quantify changes in ECM structure. Generally, mechanical loading increased the effects of enzyme activity characterized by an irreversible decline in stiffness and tissue deterioration seen on both confocal and electron microscopic images. However, a static strain of 20% provided protection against digestion compared to both higher and lower strains. The decline in stiffness during digestion positively correlated with the increase in equivalent alveolar diameters and negatively correlated with the nonlinearity index. These results suggest that the decline in stiffness results from rupture of collagen followed by load transfer and subsequent rupture of alveolar walls. This study may provide new understanding of the role of collagen degradation in general tissue remodeling and disease progression. Frontiers Media S.A. 2016-07-12 /pmc/articles/PMC4940411/ /pubmed/27462275 http://dx.doi.org/10.3389/fphys.2016.00287 Text en Copyright © 2016 Yi, Sato, Takahashi, Parameswaran, Blute, Bartolák-Suki and Suki. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Physiology
Yi, Eunice
Sato, Susumu
Takahashi, Ayuko
Parameswaran, Harikrishnan
Blute, Todd A.
Bartolák-Suki, Erzsébet
Suki, Béla
Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title_full Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title_fullStr Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title_full_unstemmed Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title_short Mechanical Forces Accelerate Collagen Digestion by Bacterial Collagenase in Lung Tissue Strips
title_sort mechanical forces accelerate collagen digestion by bacterial collagenase in lung tissue strips
topic Physiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4940411/
https://www.ncbi.nlm.nih.gov/pubmed/27462275
http://dx.doi.org/10.3389/fphys.2016.00287
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