TY - JOUR
T1 - Micromechanical anisotropy and heterogeneity of the meniscus extracellular matrix
AU - Li, Qing
AU - Qu, Feini
AU - Han, Biao
AU - Wang, Chao
AU - Li, Hao
AU - Mauck, Robert L.
AU - Han, Lin
N1 - Funding Information:
This work was supported by the National Institutes of Health, Grants AR066824 to LH, EB002425 to RLM, and AR050950 to the Penn Center for Musculoskeletal Disorders (PCMD). It was also supported by the Drexel Areas of Research Excellence (DARE) initiative (to LH and CW).
Publisher Copyright:
© 2017 Acta Materialia Inc.
PY - 2017/5
Y1 - 2017/5
N2 - To understand how the complex biomechanical functions of the meniscus are endowed by the nanostructure of its extracellular matrix (ECM), we studied the anisotropy and heterogeneity in the micromechanical properties of the meniscus ECM. We used atomic force microscopy (AFM) to quantify the time-dependent mechanical properties of juvenile bovine meniscus at deformation length scales corresponding to the diameters of collagen fibrils. At this scale, anisotropy in the elastic modulus of the circumferential fibers, the major ECM structural unit, can be attributed to differences in fibril deformation modes: uncrimping when normal to the fiber axis, and laterally constrained compression when parallel to the fiber axis. Heterogeneity among different structural units is mainly associated with their variations in microscale fiber orientation, while heterogeneity across anatomical zones is due to alterations in collagen fibril diameter and alignment at the nanoscale. Unlike the elastic modulus, the time-dependent properties are more homogeneous and isotropic throughout the ECM. These results enable a detailed understanding of the meniscus structure-mechanics at the nanoscale, and can serve as a benchmark for understanding meniscus biomechanical functions, documenting disease progression and designing tissue repair strategies. Statement of Significance Meniscal damage is a common cause of joint injury, which can lead to the development of post-traumatic osteoarthritis among young adults. Restoration of meniscus function requires repairing its highly heterogeneous and complex extracellular matrix. Employing AFM, this study quantifies the anisotropic and heterogeneous features of the meniscus ECM structure and mechanics. The micromechanical properties are interpreted within the context of the collagen fibril nanostructure and its variation with tissue anatomical locations. These results provide a fundamental structure-mechanics knowledge benchmark, against which, repair and regeneration strategies can be developed and evaluated with respect to the specialized structural and functional complexity of the native tissue.
AB - To understand how the complex biomechanical functions of the meniscus are endowed by the nanostructure of its extracellular matrix (ECM), we studied the anisotropy and heterogeneity in the micromechanical properties of the meniscus ECM. We used atomic force microscopy (AFM) to quantify the time-dependent mechanical properties of juvenile bovine meniscus at deformation length scales corresponding to the diameters of collagen fibrils. At this scale, anisotropy in the elastic modulus of the circumferential fibers, the major ECM structural unit, can be attributed to differences in fibril deformation modes: uncrimping when normal to the fiber axis, and laterally constrained compression when parallel to the fiber axis. Heterogeneity among different structural units is mainly associated with their variations in microscale fiber orientation, while heterogeneity across anatomical zones is due to alterations in collagen fibril diameter and alignment at the nanoscale. Unlike the elastic modulus, the time-dependent properties are more homogeneous and isotropic throughout the ECM. These results enable a detailed understanding of the meniscus structure-mechanics at the nanoscale, and can serve as a benchmark for understanding meniscus biomechanical functions, documenting disease progression and designing tissue repair strategies. Statement of Significance Meniscal damage is a common cause of joint injury, which can lead to the development of post-traumatic osteoarthritis among young adults. Restoration of meniscus function requires repairing its highly heterogeneous and complex extracellular matrix. Employing AFM, this study quantifies the anisotropic and heterogeneous features of the meniscus ECM structure and mechanics. The micromechanical properties are interpreted within the context of the collagen fibril nanostructure and its variation with tissue anatomical locations. These results provide a fundamental structure-mechanics knowledge benchmark, against which, repair and regeneration strategies can be developed and evaluated with respect to the specialized structural and functional complexity of the native tissue.
KW - Anisotropy
KW - Extracellular matrix
KW - Heterogeneity
KW - Meniscus
KW - Nanoindentation
UR - http://www.scopus.com/inward/record.url?scp=85014547597&partnerID=8YFLogxK
U2 - 10.1016/j.actbio.2017.02.043
DO - 10.1016/j.actbio.2017.02.043
M3 - Article
C2 - 28242455
AN - SCOPUS:85014547597
SN - 1742-7061
VL - 54
SP - 356
EP - 366
JO - Acta Biomaterialia
JF - Acta Biomaterialia
ER -