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

Yi E, Sato S, Takahashi A, Parameswaran H, Blute TA, Bartolák-Suki E, Suki B - Front Physiol (2016)

Bottom Line: 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.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.These results suggest that the decline in stiffness results from rupture of collagen followed by load transfer and subsequent rupture of alveolar walls.

View Article: PubMed Central - PubMed

Affiliation: Cell and Tissue Mechanics, Department of Biomedical Engineering, Boston University Boston, MA, USA.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus

Transmission electron microscopy (TEM) images of collagen structure for (A,B) undigested, no stretch, (C,D) undigested, 40% strain, (E,F) digested, no stretch, and (G,H) digested, 40% strain. All images were taken in the unstretched state. Arrows indicate regions of collagen degradation. Bar denote magnification.
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Figure 8: Transmission electron microscopy (TEM) images of collagen structure for (A,B) undigested, no stretch, (C,D) undigested, 40% strain, (E,F) digested, no stretch, and (G,H) digested, 40% strain. All images were taken in the unstretched state. Arrows indicate regions of collagen degradation. Bar denote magnification.

Mentions: To determine the structural changes at the level of collagen fibrils, electron microscopic images were also obtained in selected groups including C0%, C40%, D0%, and D40% (Figure 8). It can be seen that the fibers are wavy and closely packed when no enzyme and stretch was present, but they were straighter after stretch even though imaging was obtained in the unstretched condition. The fiber structure became irregular, loosely packed and damaged in the presence of enzymes. When enzymes were applied in the presence of stretch, the structure became heterogeneous with both intact and highly damaged collagen fibers. Large regions that contained little or no collagen were often seen in the digested and stretched tissues.


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

Yi E, Sato S, Takahashi A, Parameswaran H, Blute TA, Bartolák-Suki E, Suki B - Front Physiol (2016)

Transmission electron microscopy (TEM) images of collagen structure for (A,B) undigested, no stretch, (C,D) undigested, 40% strain, (E,F) digested, no stretch, and (G,H) digested, 40% strain. All images were taken in the unstretched state. Arrows indicate regions of collagen degradation. Bar denote magnification.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4940411&req=5

Figure 8: Transmission electron microscopy (TEM) images of collagen structure for (A,B) undigested, no stretch, (C,D) undigested, 40% strain, (E,F) digested, no stretch, and (G,H) digested, 40% strain. All images were taken in the unstretched state. Arrows indicate regions of collagen degradation. Bar denote magnification.
Mentions: To determine the structural changes at the level of collagen fibrils, electron microscopic images were also obtained in selected groups including C0%, C40%, D0%, and D40% (Figure 8). It can be seen that the fibers are wavy and closely packed when no enzyme and stretch was present, but they were straighter after stretch even though imaging was obtained in the unstretched condition. The fiber structure became irregular, loosely packed and damaged in the presence of enzymes. When enzymes were applied in the presence of stretch, the structure became heterogeneous with both intact and highly damaged collagen fibers. Large regions that contained little or no collagen were often seen in the digested and stretched tissues.

Bottom Line: 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.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.These results suggest that the decline in stiffness results from rupture of collagen followed by load transfer and subsequent rupture of alveolar walls.

View Article: PubMed Central - PubMed

Affiliation: Cell and Tissue Mechanics, Department of Biomedical Engineering, Boston University Boston, MA, USA.

ABSTRACT
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.

No MeSH data available.


Related in: MedlinePlus