Structure-Function Relations and Rigidity Percolation in the Shear Properties of Articular Cartilage
Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to locali...
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Published in | Biophysical journal Vol. 107; no. 7; pp. 1721 - 1730 |
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Main Authors | , , , , , |
Format | Journal Article |
Language | English |
Published |
United States
Elsevier Inc
07.10.2014
Biophysical Society The Biophysical Society |
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Abstract | Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G∗| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G∗| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction vc lead to orders-of-magnitude changes in the modulus with |G∗| scaling as (vc – v0)ξ. Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue’s surface. |
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AbstractList | Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G(∗)| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G(∗)| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction vc lead to orders-of-magnitude changes in the modulus with |G(∗)| scaling as (vc - v0)(ξ). Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue's surface. Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G∗| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G∗| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction vc lead to orders-of-magnitude changes in the modulus with |G∗| scaling as (vc – v0)ξ. Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue’s surface. Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G*| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G*| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction ... lead to orders-of-magnitude changes in the modulus with |G*| scaling as ... Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue's surface. (ProQuest: ... denotes formulae/symbols omitted.) Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus | G ∗ | and both the collagen fiber orientation and polarization. We find a much stronger correlation between | G ∗ | and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction v c lead to orders-of-magnitude changes in the modulus with | G ∗ | scaling as ( v c – v 0 ) ξ . Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue’s surface. Among mammalian soft tissues, articular cartilage is particularly interesting because it can endure a lifetime of daily mechanical loading despite having minimal regenerative capacity. This remarkable resilience may be due to the depth-dependent mechanical properties, which have been shown to localize strain and energy dissipation. This paradigm proposes that these properties arise from the depth-dependent collagen fiber orientation. Nevertheless, this structure-function relationship has not yet been quantified. Here, we use confocal elastography, quantitative polarized light microscopy, and Fourier-transform infrared imaging to make same-sample measurements of the depth-dependent shear modulus, collagen fiber organization, and extracellular matrix concentration in neonatal bovine articular cartilage. We find weak correlations between the shear modulus |G super([lowast])| and both the collagen fiber orientation and polarization. We find a much stronger correlation between |G super([lowast])| and the concentration of collagen fibers. Interestingly, very small changes in collagen volume fraction v sub(c) lead to orders-of-magnitude changes in the modulus with |G super([lowast])| scaling as (v sub(c) - v sub(0)) super( xi ). Such dependencies are observed in the rheology of other biopolymer networks whose structure exhibits rigidity percolation phase transitions. Along these lines, we propose that the collagen network in articular cartilage is near a percolation threshold that gives rise to these large mechanical variations and localization of strain at the tissue's surface. |
Author | Silverberg, Jesse L. Das, Moumita Cohen, Itai Petersen, Poul B. Bonassar, Lawrence J. Barrett, Aliyah R. |
AuthorAffiliation | 1 Physics Department, Cornell University, Ithaca, New York 2 Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York 3 Biomedical Engineering, Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York 4 School of Physics & Astronomy, Rochester Institute of Technology, Rochester, New York |
AuthorAffiliation_xml | – name: 4 School of Physics & Astronomy, Rochester Institute of Technology, Rochester, New York – name: 2 Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York – name: 1 Physics Department, Cornell University, Ithaca, New York – name: 3 Biomedical Engineering, Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York |
Author_xml | – sequence: 1 givenname: Jesse L. surname: Silverberg fullname: Silverberg, Jesse L. email: jls533@cornell.edu organization: Physics Department, Cornell University, Ithaca, New York – sequence: 2 givenname: Aliyah R. surname: Barrett fullname: Barrett, Aliyah R. organization: Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York – sequence: 3 givenname: Moumita surname: Das fullname: Das, Moumita organization: School of Physics & Astronomy, Rochester Institute of Technology, Rochester, New York – sequence: 4 givenname: Poul B. surname: Petersen fullname: Petersen, Poul B. organization: Department of Chemistry and Chemical Biology, Cornell University, Ithaca, New York – sequence: 5 givenname: Lawrence J. surname: Bonassar fullname: Bonassar, Lawrence J. organization: Biomedical Engineering, Mechanical and Aerospace Engineering, Cornell University, Ithaca, New York – sequence: 6 givenname: Itai surname: Cohen fullname: Cohen, Itai organization: Physics Department, Cornell University, Ithaca, New York |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25296326$$D View this record in MEDLINE/PubMed |
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SubjectTerms | Animals Animals, Newborn Articular Biomechanical Phenomena Biopolymers Cartilage Cartilage, Articular - chemistry Cartilage, Articular - metabolism Cattle Cells Collagen Collagen - chemistry Collagen - metabolism Collagens Correlation Elasticity Imaging Techniques Fibers Mechanical properties Models, Biological Molecular structure Networks Percolation Rigidity Shear Strength Structure-Activity Relationship Systems Biophysics |
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Title | Structure-Function Relations and Rigidity Percolation in the Shear Properties of Articular Cartilage |
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