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Journal of Biomechanical Engineering | Volume 139 | Issue 11 | research-article
Research Papers

Functionally Distinct Tendons From Elastin Haploinsufficient Mice Exhibit Mild Stiffening and Tendon-Specific Structural Alteration

[+] Author and Article Information
Jeremy D. Eekhoff

Department of Biomedical Engineering,
Washington University in St. Louis
One Brookings Drive,
St. Louis, MO 63130

Fei Fang

Department of Mechanical Engineering
and Materials Science,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130

Lindsey G. Kahan, Gabriela Espinosa, Austin J. Cocciolone

Department of Biomedical Engineering,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130

Jessica E. Wagenseil

Department of Mechanical Engineering and
Materials Science,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130

Robert P. Mecham

Department of Cell Biology and Physiology,
Washington University in St. Louis,
660 South Euclid Avenue,
St. Louis, MO 63110

Spencer P. Lake

Department of Mechanical Engineering and
Materials Science,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130;Department of Biomedical Engineering,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130;Department of Orthopaedic Surgery,
Washington University in St. Louis,
One Brookings Drive,
St. Louis, MO 63130
e-mail: lake.s@wustl.edu

1Corresponding author.

Manuscript received August 14, 2017; final manuscript received September 11, 2017; published online September 27, 2017. Assoc. Editor: Kyle Allen.

J Biomech Eng 139(11), 111003 (Sep 27, 2017) (9 pages) Paper No: BIO-17-1362; doi: 10.1115/1.4037932 History: Received August 14, 2017; Revised September 11, 2017
Article
References
Figures
Tables

Elastic fibers are present in low quantities in tendon, where they are located both within fascicles near tenocytes and more broadly in the interfascicular matrix (IFM). While elastic fibers have long been known to be significant in the mechanics of elastin-rich tissue (i.e., vasculature, skin, lungs), recent studies have suggested a mechanical role for elastic fibers in tendons that is dependent on specific tendon function. However, the exact contribution of elastin to properties of different types of tendons (e.g., positional, energy-storing) remains unknown. Therefore, this study purposed to evaluate the role of elastin in the mechanical properties and collagen alignment of functionally distinct supraspinatus tendons (SSTs) and Achilles tendons (ATs) from elastin haploinsufficient (HET) and wild type (WT) mice. Despite the significant decrease in elastin in HET tendons, a slight increase in linear stiffness of both tendons was the only significant mechanical effect of elastin haploinsufficiency. Additionally, there were significant changes in collagen nanostructure and subtle alteration to collagen alignment in the AT but not the SST. Hence, elastin may play only a minor role in tendon mechanical properties. Alternatively, larger changes to tendon mechanics may have been mitigated by developmental compensation of HET tendons and/or the role of elastic fibers may be less prominent in smaller mouse tendons compared to the larger bovine and human tendons evaluated in previous studies. Further research will be necessary to fully elucidate the influence of various elastic fiber components on structure–function relationships in functionally distinct tendons.
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Figures

Grahic Jump Location
Fig. 1

Images of a representative SST and AT prior to ramp to failure taken using the QPLI system. The bone is fixed on the left, and the free end of the tendon is clamped on the right. Stain lines, outlined with dotted lines, mark the boundaries of the ROI for analysis of DoLP and AoP. Data are analyzed as groups of pixels, where the AVG DoLP and STD AoP represent the strength of alignment and uniformity of orientation, respectively.

+Images of a representative SST and AT prior to ramp to failure taken using the QPLI system. The bone is fixed on the left, and the free end of the tendon is clamped on the right. Stain lines, outlined with dotted lines, mark the boundaries of the ROI for analysis of DoLP and AoP. Data are analyzed as groups of pixels, where the AVG DoLP and STD AoP represent the strength of alignment and uniformity of orientation, respectively.
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Images of a representative SST and AT prior to ramp to failure taken using the QPLI system. The bone is fixed on the left, and the free end of the tendon is clamped on the right. Stain lines, outlined with dotted lines, mark the boundaries of the ROI for analysis of DoLP and AoP. Data are analyzed as groups of pixels, where the AVG DoLP and STD AoP represent the strength of alignment and uniformity of orientation, respectively.
Grahic Jump Location
Fig. 2

CSA was greater in ATs than SSTs and was unaffected by genotype (a). Elastin content was decreased in HET tendons and was similar between tendon types (b). Collagen content was decreased in ATs and was unaffected by genotype (c). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.

+CSA was greater in ATs than SSTs and was unaffected by genotype (a). Elastin content was decreased in HET tendons and was similar between tendon types (b). Collagen content was decreased in ATs and was unaffected by genotype (c). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.
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CSA was greater in ATs than SSTs and was unaffected by genotype (a). Elastin content was decreased in HET tendons and was similar between tendon types (b). Collagen content was decreased in ATs and was unaffected by genotype (c). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.
Grahic Jump Location
Fig. 3

Distribution of SRB-stained elastic fibers (bright cyan; white arrows), tenocytes (blue), and collagen (cyan) in WT and HET SSTs and ATs. Few or no fibers were visible in SSTs (a,b). Stained fibers are visible in WT and HET ATs (c,d), where they conformed to collagen orientation and were often localized near tenocytes. No differences were evident between genotypes. Scale bar = 50 μm. Refer to online version for color figure.

+Distribution of SRB-stained elastic fibers (bright cyan; white arrows), tenocytes (blue), and collagen (cyan) in WT and HET SSTs and ATs. Few or no fibers were visible in SSTs (a,b). Stained fibers are visible in WT and HET ATs (c,d), where they conformed to collagen orientation and were often localized near tenocytes. No differences were evident between genotypes. Scale bar = 50 μm. Refer to online version for color figure.
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Distribution of SRB-stained elastic fibers (bright cyan; white arrows), tenocytes (blue), and collagen (cyan) in WT and HET SSTs and ATs. Few or no fibers were visible in SSTs (a,b). Stained fibers are visible in WT and HET ATs (c,d), where they conformed to collagen orientation and were often localized near tenocytes. No differences were evident between genotypes. Scale bar = 50 μm. Refer to online version for color figure.
Grahic Jump Location
Fig. 4

Representative TEM micrographs from WT and HET SSTs and ATs (a,b,e,f). Scale bar = 500 nm. Elastin haploinsufficiency caused no change in SST collagen nanostructure (c,d), while HET ATs had decreased area fraction (g) and altered fibril diameter distribution (h). *Genotype effect p < 0.05.

+ Representative TEM micrographs from WT and HET SSTs and ATs (a,b,e,f). Scale bar = 500 nm. Elastin haploinsufficiency caused no change in SST collagen nanostructure (c,d), while HET ATs had decreased area fraction (g) and altered fibril diameter distribution (h). *Genotype effect p < 0.05.
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Representative TEM micrographs from WT and HET SSTs and ATs (a,b,e,f). Scale bar = 500 nm. Elastin haploinsufficiency caused no change in SST collagen nanostructure (c,d), while HET ATs had decreased area fraction (g) and altered fibril diameter distribution (h). *Genotype effect p < 0.05.
Grahic Jump Location
Fig. 5

Representative TEM micrograph from a HET SST showing groups of fibrillin microfibrils with varying amounts of elastin, circled in white. Scale bar = 500 nm.

+Representative TEM micrograph from a HET SST showing groups of fibrillin microfibrils with varying amounts of elastin, circled in white. Scale bar = 500 nm.
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Representative TEM micrograph from a HET SST showing groups of fibrillin microfibrils with varying amounts of elastin, circled in white. Scale bar = 500 nm.
Grahic Jump Location
Fig. 6

Changes in collagen alignment during stress relaxation are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP decreased (a,c) and STD AoP increased (b,d) as time progressed. There was a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: The initial time of the test was set to 1 s to allow graphical representation on a logarithmic scale. AVG DoLP y-axes do not start at 0.

+Changes in collagen alignment during stress relaxation are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP decreased (a,c) and STD AoP increased (b,d) as time progressed. There was a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: The initial time of the test was set to 1 s to allow graphical representation on a logarithmic scale. AVG DoLP y-axes do not start at 0.
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Changes in collagen alignment during stress relaxation are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP decreased (a,c) and STD AoP increased (b,d) as time progressed. There was a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: The initial time of the test was set to 1 s to allow graphical representation on a logarithmic scale. AVG DoLP y-axes do not start at 0.
Grahic Jump Location
Fig. 7

Toe stiffness was similar across both genotypes and tendon types (a). Linear stiffness was greater in ATs and was increased in HET tendons (b). Transition displacement and transition force were greater in ATs and not affected by genotype (c,d). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.

+Toe stiffness was similar across both genotypes and tendon types (a). Linear stiffness was greater in ATs and was increased in HET tendons (b). Transition displacement and transition force were greater in ATs and not affected by genotype (c,d). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.
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Toe stiffness was similar across both genotypes and tendon types (a). Linear stiffness was greater in ATs and was increased in HET tendons (b). Transition displacement and transition force were greater in ATs and not affected by genotype (c,d). Two-way ANOVA *genotype effect p < 0.05; #tendon type effect p < 0.05.
Grahic Jump Location
Fig. 8

Changes in collagen alignment during ramp to failure are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP increased (a,c) and STD AoP decreased (b,d) with increasing strain. There was a greater increase in AVG DoLP from initial to transition regions and a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: AVG DoLP y-axes do not start at 0.

+Changes in collagen alignment during ramp to failure are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP increased (a,c) and STD AoP decreased (b,d) with increasing strain. There was a greater increase in AVG DoLP from initial to transition regions and a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: AVG DoLP y-axes do not start at 0.
View Large  |  Save Figure  |  Download Slide (.ppt)
Changes in collagen alignment during ramp to failure are represented by AVG DoLP and STD AoP. In both tendons, AVG DoLP increased (a,c) and STD AoP decreased (b,d) with increasing strain. There was a greater increase in AVG DoLP from initial to transition regions and a trend toward decreased STD AoP in HET ATs compared to WT ATs. Note: AVG DoLP y-axes do not start at 0.

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