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WIREs Syst Biol Med
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How changes in fibril‐level organization correlate with the macrolevel behavior of articular cartilage

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Abstract The primary structural components of articular cartilage are the zonally differentiated interconnected network of collagen fibrils and proteoglycans, the latter having the potential to bind large amounts of water. Both components exist in a coupled relationship that gives rise to its remarkable mechanical properties. The response of cartilage to compression is governed both by the degree to which the hydrated proteoglycans are constrained within this fibrillar network and the ease with which the matrix fluid can be displaced. The functional properties of cartilage are therefore closely linked to the integrity of the fibrillar network. Our current understanding of this network has been derived via studies conducted at the macro, micro, and ultrastructural levels. Of particular interest to joint researchers and clinicians are issues relating to how the network structure varies both directionally and with zonal depth, how its integrity is maintained via mechanisms of fibril interconnectivity, and how it is modified by ageing, degeneration, and trauma. Physical models have been developed to explore modes of interconnectivity. Combined micromechanical and structural studies confirm the critical role that this interconnectivity must play but detailed descriptions at the molecular level remain elusive. Current computationally based models of cartilage have in some cases implemented the fibrillar component, albeit simplistically, as a separate structure. Considering how important a role fibril network interconnectivity plays in actual tissue structure and mechanical behavior, and especially how it changes with degeneration, a major challenge facing joint tissue modellers is how to incorporate such a feature in their models. WIREs Syst Biol Med 2013, 5:495–509. doi: 10.1002/wsbm.1220 This article is categorized under: Models of Systems Properties and Processes > Organ, Tissue, and Physiological Models

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Re‐drawn from Benninghoff who described this figure as “a schematic representation of the principal direction of the collagen fibrils in joint cartilage. The chondrons are represented as black elipses.”

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(a) Balloon‐and‐string model of AC‐on‐bone illustrating the functional coupling between the tension‐only collagen fibrils and the high‐swelling PGs. A three‐dimensional cage‐work, within which the PGs are constrained, is generated from the regular interconnections of the radially aligned string elements which are, in turn, repeatedly deflected obliquely. The string elements are anchored into a ‘subchondral’ base plate and at the upper level turn into the surface to form a strain‐limiting tangential layer. (b) Compression with localized load of 80 kg. (c) Shear load of 40 kg applied via strain‐limiting tangential layer. (Reprinted with permission from Ref . Copyright 1985 Informa plc)

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Micro‐to‐nano level images illustrating the normal cartilage‐on‐bone response to compression including the transition region of the deformed matrix near the edge of the indenter. (a) DIC image showing the overall pattern of deformation and associated shear boundary (or ‘chevron discontinuity’) rendered prominent by the lines of chondrocyte continuity. (Reprinted with permission from Ref . Copyright 2007 Elsevier Ltd). (b) Microlevel DIC image of matrix response typically observed at shear boundary as in the boxed region in (a). Note the intense creasing of the matrix above the boundary in contrast to the largely undisturbed matrix below. (c) SEM image of the boxed region in (b) showing the fibril continuity across the shear boundary. (d) SEM image of the boxed region in (c) showing repeating waves of fibrillar collapse that correlate with the DIC image in (b). (b–d: Reprinted with permission from Ref . Copyright 2010 Eslevier Ltd)

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TEM images of AC showing response of collagen network in general matrix to radial compression (a) prior to and (b) following PG removal. The fibrils in the compressed intact matrix have retained their spatial discreteness whereas the fibrils in the PG‐depleted matrix have responded via repeating waves of collapse to form a distinct band structure. Arrows indicate direction of compression. Scalebar 2 µm. (Reprinted with permission from Ref . Copyright 2005 John Wiley & Sons, Inc.)

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TEM image of the swollen softened or malacic cartilage matrix showing some fibril aggregation with crimp and a significant dispersion of the network elements. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 2002 John Wiley & Sons, Inc.)

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(a) TEM image showing destructuring of the collagen network in healthy AC because of repeated impact loading. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 1986 BMJ Publishing Group). (b) TEM image showing destructuring of the collagen network in healthy AC resulting from sequential PG and collagen degradation. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 2005 John Wiley & Sons, Inc.)

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TEM image of fibrillar architecture in general matrix of malacic bovine AC. Note pronounced aggregation of radially aligned fibrils and secondary transverse tangling. Scalebar 2 µm. (Reprinted with permission from Ref . Copyright 2002 John Wiley & Sons, Inc.)

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Series of images of an analog of the fibrillar network in cartilage and illustrating its potential to undergo destructuring and aggregation, and created from an initial radial array of parallel strings incorporating repeating sites of interconnectivity along their lengths. In all images the radial direction representing the ‘native’ orientation of the array elements is vertical. The fibrillar model represented in images (a–c) contain radial elements that have 100% entwinement‐based interconnections: (a) is the intact array, (b) and (c) showing partial and advanced destructuring, respectively. Note the increasing amount of near‐transverse tangling that is always associated with any localized destructuring of the fibrillar network into near parallel, radial aggregates. The fibrillar model in images (d–f) incorporate only 30% entwinement‐based interconnections (identified by solid circles), the remaining 70% being nonentwinement based and thus able to be removed without residual tangling; (d) is the intact array, (e) and (f) illustrate partial and advanced destructuring, respectively. Note that this advanced degree of ‘degradation’ leads to large scale rearrangement of array into aggregated parallel bundles aligned in the radial direction. (Reprinted with permission from Ref . Copyright 2002 John Wiley & Sons, Inc.)

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(a) TEM image of a mildly degenerate matrix exhibiting more extended fibril aggregation and mild crimp morphology. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 2002 John Wiley & Sons, Inc.). (b) SEM view of strong radial arrays in general matrix of OA femoral head cartilage. Scalebar 2 µm. (Reprinted with permission from Ref . Copyright 2002 John Wiley & Sons, Inc.)

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(a) DIC image of the general matrix of healthy cartilage exhibiting a near‐amorphous texture of the extracellular regions. Scalebar 25 µm. (Reprinted with permission from Ref . Copyright 2005 John Wiley & Sons, Inc.). (b) DIC image of the general matrix of mildly malacic cartilage exhibiting a strong radial fibrosity or texture and an associated crimp in the extracellular regions. Scalebar 25 µm. (Reprinted with permission from Ref Copyright 2003 John Wiley & Sons, Inc.)

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TEM image showing nodal clustering of many individual fibrils in the general matrix of healthy bovine AC. Overall alignment of fibrils is radial. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 1986 John Wiley & Sons, Inc.)

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SEM image showing examples of fibrillar entwinement in general matrix. Overall direction of fibrils is radial. Scalebar 2 µm. (Reprinted with permission from Ref . Copright 2002 John Wiley & Sons, Inc.)

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TEM image showing clear example of fibrillar entwinement in general matrix of cartilage produced by a single repeatedly kinked radial fibril. Several fibril elements are shown in the schematic reconstruction obtained from stereo image pair, the kinked fibril emphasized in black. Scalebar 1 µm. (Reprinted with permission from Ref . Copyright 1989 Informa plc)

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Images illustrating the microrupture propagation technique used by Broom to investigate the directional structure–strength relationships in the AC matrix. DIC images showing (a) radial and (b) transverse rupture propagation behavior respectively. The schematic reconstructions (c–e) show the inferred fibrillar rearrangements occurring during radial and transverse rupture. The circled regions in (e) locate sites where a skewed form of radial tearing occurs in the transverse experiment. Solid arrows indicate tensile loading directions.

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A schematic representation of the morphological model of AC as proposed by Broom. Note that in this model the arcade concept proposed by Benninghoff is extended to incorporate a repeating short‐range obliquity of the radial fibrils in order to create a pseudorandom configuration in the general matrix. (Reprinted with permission from Ref . Copyright 2005 John Wiley & Sons, Inc.)

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