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Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics

Collagen and proteoglycans work in unison in the ECM to bear loads, store elastic energy and then dissipate excess energy to avoid tissue fatigue and premature mechanical failure. While collagen fibers store elastic energy by stretching the flexible regions in the triple helix, they do so by lowerin...

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Autores principales: Silver, Frederick H., Kelkar, Nikita, Deshmukh, Tanmay
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8301845/
https://www.ncbi.nlm.nih.gov/pubmed/34356642
http://dx.doi.org/10.3390/biom11071018
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author Silver, Frederick H.
Kelkar, Nikita
Deshmukh, Tanmay
author_facet Silver, Frederick H.
Kelkar, Nikita
Deshmukh, Tanmay
author_sort Silver, Frederick H.
collection PubMed
description Collagen and proteoglycans work in unison in the ECM to bear loads, store elastic energy and then dissipate excess energy to avoid tissue fatigue and premature mechanical failure. While collagen fibers store elastic energy by stretching the flexible regions in the triple helix, they do so by lowering their free energy through a reduction in the entropy and a decrease in charge–charge repulsion. Entropic increases occur when the load is released that drive the reversibility of the process and transmission of excess energy. Energy is dissipated by sliding of collagen fibrils by each other with the aid of decorin molecules that reside on the d and e bands of the native D repeat pattern. Fluid flow from the hydration layer associated with the decorin and collagen fibrils hydraulically dissipates energy during sliding. The deformation is reversed by osmotic forces that cause fluid to reform a hydration shell around the collagen fibrils when the loads are removed. In this paper a model is presented describing the organization of collagen fibers in the skin and cell–collagen mechanical relationships that exist based on non-invasive measurements made using vibrational optical coherence tomography. It is proposed that under external stress, collagen fibers form a tensional network in the plane of the skin. Collagen fiber tension along with forces generated by fibroblasts exerted on collagen fibers lead to an elastic modulus that is almost uniform throughout the plane of the skin. Tensile forces acting on cells and tissues may provide a baseline for stimulation of normal mechanotransduction. We hypothesize that during aging, changes in cellular metabolism, cell–collagen interactions and light and UV light exposure cause down regulation of mechanotransduction and tissue metabolism leading to tissue atrophy.
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spelling pubmed-83018452021-07-24 Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics Silver, Frederick H. Kelkar, Nikita Deshmukh, Tanmay Biomolecules Article Collagen and proteoglycans work in unison in the ECM to bear loads, store elastic energy and then dissipate excess energy to avoid tissue fatigue and premature mechanical failure. While collagen fibers store elastic energy by stretching the flexible regions in the triple helix, they do so by lowering their free energy through a reduction in the entropy and a decrease in charge–charge repulsion. Entropic increases occur when the load is released that drive the reversibility of the process and transmission of excess energy. Energy is dissipated by sliding of collagen fibrils by each other with the aid of decorin molecules that reside on the d and e bands of the native D repeat pattern. Fluid flow from the hydration layer associated with the decorin and collagen fibrils hydraulically dissipates energy during sliding. The deformation is reversed by osmotic forces that cause fluid to reform a hydration shell around the collagen fibrils when the loads are removed. In this paper a model is presented describing the organization of collagen fibers in the skin and cell–collagen mechanical relationships that exist based on non-invasive measurements made using vibrational optical coherence tomography. It is proposed that under external stress, collagen fibers form a tensional network in the plane of the skin. Collagen fiber tension along with forces generated by fibroblasts exerted on collagen fibers lead to an elastic modulus that is almost uniform throughout the plane of the skin. Tensile forces acting on cells and tissues may provide a baseline for stimulation of normal mechanotransduction. We hypothesize that during aging, changes in cellular metabolism, cell–collagen interactions and light and UV light exposure cause down regulation of mechanotransduction and tissue metabolism leading to tissue atrophy. MDPI 2021-07-12 /pmc/articles/PMC8301845/ /pubmed/34356642 http://dx.doi.org/10.3390/biom11071018 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Silver, Frederick H.
Kelkar, Nikita
Deshmukh, Tanmay
Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title_full Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title_fullStr Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title_full_unstemmed Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title_short Molecular Basis for Mechanical Properties of ECMs: Proposed Role of Fibrillar Collagen and Proteoglycans in Tissue Biomechanics
title_sort molecular basis for mechanical properties of ecms: proposed role of fibrillar collagen and proteoglycans in tissue biomechanics
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8301845/
https://www.ncbi.nlm.nih.gov/pubmed/34356642
http://dx.doi.org/10.3390/biom11071018
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