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Although the axial D-periodic spacing is a well-recognized nanomorphological feature of type I collagen fibrils, the existence of a distribution of values has been largely overlooked since its discovery seven decades ago. Studies based on single fibril measurements occasionally noted variation in D-spacing values, but accredited it with no biological significance. Recent quantitative characterizations supported that a 10-nm collagen D-spacing distribution is intrinsic to collagen fibrils in various tissues as well as in vitro self-assembly of reconstituted collagen. In addition, the distribution is altered in Osteogenesis Imperfecta and long-term estrogen deprivation. Bone collagen is organized into lamellar sheets of bundles at the micro-scale, and D-spacings within a bundle of a lamella are mostly identical, whereas variations among different bundles contribute to the full-scale distribution. This seems to be a very general phenomenon for the protein as the same type of D-spacing/bundle organization is observed for dermal and tendon collagen. More research investigation of collagen nanomorphology in connection to bone biology is required to fully understand these new observations. Here we review the data demonstrating the existence of a D-spacing distribution, the impact of disease on the distribution and possible explanations for the origin of D-spacing variations based on various collagen fibrillogenesis models.

Variation in type I collagen fibril nanomorphology: the significance and origin