TY - JOUR
T1 - Effects of mineralization on the hierarchical organization of collagen—a synchrotron X-ray scattering and polarized second harmonic generation study
AU - Zheng, Keke
AU - Zhong, Jingxiao
AU - Hu, Jingrui
AU - Nebbiolo, Eve
AU - Sanchez-Weatherby, Juan
AU - Tang, Tengteng
AU - Landis, William J.
AU - Chen, Junning
AU - Winlove, Peter
AU - Sherlock, Benjamin E.
AU - Bell, James
N1 - Publisher Copyright:
© 2024 The Authors.
PY - 2024/6/7
Y1 - 2024/6/7
N2 - The process of mineralization fundamentally alters collagenous tissue biomechanics. While the structure and organization of mineral particles have been widely studied, the impact of mineralization on collagen matrix structure, particularly at the molecular scale, requires further investigation. In this study, synchrotron X-ray scattering (XRD) and polarization-resolved second harmonic generation microscopy (pSHG) were used to study normally mineralizing turkey leg tendon in tissue zones representing different stages of mineralization. XRD data demonstrated statistically significant differences in collagen D-period, intermolecular spacing, fibril and molecular dispersion and relative supramolecular twists between non-mineralizing, early mineralizing and late mineralizing zones. pSHG analysis of the same tendon zones showed the degree of collagen fibril organization was significantly greater in early and late mineralizing zones compared to non-mineralizing zones. The combination of XRD and pSHG data provide new insights into hierarchical collagen–mineral interactions, notably concerning possible cleavage of intra- or interfibrillar bonds, occlusion and reorganization of collagen by mineral with time. The complementary application of XRD and fast, label-free and non-destructive pSHG optical measurements presents a pathway for future investigations into the dynamics of molecular scale changes in collagen in the presence of increasing mineral deposition.
AB - The process of mineralization fundamentally alters collagenous tissue biomechanics. While the structure and organization of mineral particles have been widely studied, the impact of mineralization on collagen matrix structure, particularly at the molecular scale, requires further investigation. In this study, synchrotron X-ray scattering (XRD) and polarization-resolved second harmonic generation microscopy (pSHG) were used to study normally mineralizing turkey leg tendon in tissue zones representing different stages of mineralization. XRD data demonstrated statistically significant differences in collagen D-period, intermolecular spacing, fibril and molecular dispersion and relative supramolecular twists between non-mineralizing, early mineralizing and late mineralizing zones. pSHG analysis of the same tendon zones showed the degree of collagen fibril organization was significantly greater in early and late mineralizing zones compared to non-mineralizing zones. The combination of XRD and pSHG data provide new insights into hierarchical collagen–mineral interactions, notably concerning possible cleavage of intra- or interfibrillar bonds, occlusion and reorganization of collagen by mineral with time. The complementary application of XRD and fast, label-free and non-destructive pSHG optical measurements presents a pathway for future investigations into the dynamics of molecular scale changes in collagen in the presence of increasing mineral deposition.
KW - mineralization
KW - collagen
KW - X-ray diffraction
KW - second harmonic generation
KW - nonlinear microscopy
KW - polarization resolved
UR - http://www.scopus.com/inward/record.url?scp=85195650522&partnerID=8YFLogxK
U2 - 10.1098/rsfs.2023.0046
DO - 10.1098/rsfs.2023.0046
M3 - Article
C2 - 39081623
SN - 2042-8898
VL - 14
JO - Interface Focus
JF - Interface Focus
IS - 3
M1 - 20230046
ER -