Influence of decorin on the mechanical, compositional, and structural properties of the mouse patellar tendon.
ABSTRACT The interactions of small leucine-rich proteoglycans (SLRPs) with collagen fibrils, their association with water, and their role in fibrillogenesis suggests that SLRPs may play an important role in tendon mechanics. Some studies have assessed the role of SLRPs in the mechanical response of the tendon, but the relationships between sophisticated mechanics, assembly of collagen, and SLRPs have not been well characterized. Decorin content was varied in a dose dependent manner using decorin null, decorin heterozygote, and wild type mice. Quantitative measures of mechanical (tension and compression), compositional, and structural changes of the mouse patellar tendon were evaluated. Viscoelastic, tensile dynamic modulus was increased in the decorin heterozygous tendons compared to wild type. These tendons also had a significant decrease in total collagen and no structural changes compared to wild type. Decorin null tendons did not have any mechanical changes; however, a significant decrease in the average fibril diameter was found. No differences were seen between genotypes in elastic or compressive properties, and all tendons demonstrated viscoelastic mechanical dependence on strain rate and frequency. These results suggest that decorin, a member of the SLRP family, plays a role in tendon viscoelasticity that cannot be completely explained by its role in collagen fibrillogenesis. In addition, reductions in decorin do not cause large changes in indentation compressive properties, suggesting that other factors contribute to these properties. Understanding these relationships may ultimately help guide development of tissue engineered constructs or treatment modalities.
- SourceAvailable from: David E Birk[show abstract] [hide abstract]
ABSTRACT: The formation of collagen fibrils, fibril bundles, and tissue-specific collagen macroaggregates by chick embryo tendon fibroblasts was studied using conventional and high voltage electron microscopy. During chick tendon morphogenesis, there are at least three extracellular compartments responsible for three levels of matrix organization: collagen fibrils, bundles, and collagen macroaggregates. Our observations indicate that the initial extracellular events in collagen fibrillogenesis occur within narrow cytoplasmic recesses, presumably under close cellular regulation. Collagen fibrils are formed within these deep, narrow recesses, which are continuous with the extracellular space. Where these narrow recesses fuse with the cell surface, it becomes highly convoluted with folds and processes that envelope forming fibril bundles. The bundles laterally associate and coalesce, forming aggregates within a third cell-defined extracellular compartment. Our interpretation is that this third compartment forms as cell processes retract and cytoplasm is withdrawn between bundles. These studies define a hierarchical organization within the tendon, extending from fibril assembly to fascicle formation. Correlation of different levels of extracellular compartmentalization with tissue architecture provides insight into the cellular controls involved in collagen fibril and higher order assembly and a better understanding of how collagen fibrils are collected into structural groups, positioned, and woven into functional tissue-specific collagen macroaggregates.The Journal of Cell Biology 08/1986; 103(1):231-40. · 10.82 Impact Factor
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ABSTRACT: The objective of this study was to develop a nonlinear and anisotropic three-dimensional mathematical model of tendon behavior in which the structural components of fibers, matrix, and fiber-matrix interactions are explicitly incorporated and to use this model to infer the contributions of these structures to tendon mechanical behavior. We hypothesized that this model would show that: (i) tendon mechanical behavior is not solely governed by the isotropic matrix and fiber stretch, but is also influenced by fiber-matrix interactions; and (ii) shear fiber-matrix interaction terms will better describe tendon mechanical behavior than bulk fiber-matrix interaction terms. Model versions that did and did not include fiber-matrix interaction terms were applied to experimental tendon stress-strain data in longitudinal and transverse orientations, and the R2 goodness-of-fit was evaluated. This study showed that models that included fiber-matrix interaction terms improved the fit to longitudinal data (R2(toe) = 0.88, R2(Lin) = 0.94) over models that only included isotropic matrix and fiber stretch terms (R2(Toe) = 0.36, R2(Lin) = 0.84). Shear fiber-matrix interaction terms proved to be responsible for the best fit to data and to contribute to stress-strain nonlinearity. The mathematical model of tendon behavior developed in this study showed that fiber-matrix interactions are an important contributor to tendon behavior The more complete characterization of mechanical behavior afforded by this mathematical model can lead to an improved understanding of structure-function relationships in soft tissues and, ultimately, to the development of tissue-engineered therapies for injury or degeneration.Journal of Biomechanical Engineering 05/2005; 127(2):345-50. · 1.52 Impact Factor
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ABSTRACT: Tendons have complex mechanical behaviors that are viscoelastic, nonlinear, and anisotropic. It is widely held that these behaviors are provided for by the tissue's composition and structure. However, little data are available to quantify such structure-function relationships. This study quantified tendon mechanical behaviors, including viscoelasticity and nonlinearity, for groups of mice that were genetically engineered for altered extracellular matrix proteins. Uniaxial tensile stress-relaxation experiments were performed on tail tendon fascicles from the following groups: eight week old decorin knockout, eight week old reduced type I collagen, three week old control, and eight week old control. Data were fit using Fung's quasilinear viscoelastic model, where the model parameters represent the linear viscoelastic and nonlinear elastic response. The viscoelastic properties demonstrated a larger and faster stress relaxation for the decorin knockout and a smaller and slower stress relaxation for the three week control. The elastic parameter, A, in the eight week control group was significantly greater than in the collagen reduction and three week control groups. This study provides quantitative evidence for structure-function relationships in tendon, including the role of proteoglycan in viscoelasticity. Future studies should directly correlate composition and structure with tendon mechanics for the design and evaluation of tissue-engineered constructs or tendon repairs.Annals of Biomedical Engineering 06/2003; 31(5):599-605. · 2.58 Impact Factor