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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Main Authors: Eunice Yi, Susumu Sato, Ayuko Takahashi, Harikrishnan Parameswaran, Todd A Blute, Erzsébet Bartolák-Suki, Bela Suki
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-07-01
Series:Frontiers in Physiology
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00287/full
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author Eunice Yi
Susumu Sato
Ayuko Takahashi
Harikrishnan Parameswaran
Todd A Blute
Erzsébet Bartolák-Suki
Bela Suki
author_facet Eunice Yi
Susumu Sato
Ayuko Takahashi
Harikrishnan Parameswaran
Todd A Blute
Erzsébet Bartolák-Suki
Bela Suki
author_sort Eunice Yi
collection DOAJ
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 1Hz. 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 doaj.art-ec4eee9eadb14e9c8df28386136be4dd2022-12-21T22:08:02ZengFrontiers Media S.A.Frontiers in Physiology1664-042X2016-07-01710.3389/fphys.2016.00287204830MECHANICAL FORCES ACCELERATE COLLAGEN DIGESTION BY BACTERIAL COLLAGENASE IN LUNG TISSUE STRIPSEunice Yi0Susumu Sato1Ayuko Takahashi2Harikrishnan Parameswaran3Todd A Blute4Erzsébet Bartolák-Suki5Bela Suki6Boston UniversityBoston UniversityBoston UniversityBoston UniversityBoston UniversityBoston UniversityBoston UniversityMost 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 1Hz. 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.http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00287/fullMicroscopy, Electroncomputational modelstretchstiffnessCleavage
spellingShingle Eunice Yi
Susumu Sato
Ayuko Takahashi
Harikrishnan Parameswaran
Todd A Blute
Erzsébet Bartolák-Suki
Bela Suki
MECHANICAL FORCES ACCELERATE COLLAGEN DIGESTION BY BACTERIAL COLLAGENASE IN LUNG TISSUE STRIPS
Frontiers in Physiology
Microscopy, Electron
computational model
stretch
stiffness
Cleavage
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 Microscopy, Electron
computational model
stretch
stiffness
Cleavage
url http://journal.frontiersin.org/Journal/10.3389/fphys.2016.00287/full
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