Symmetrically banded collagen fibrils: Observations on a new cross striation pattern in vivo

Abstract

Collagen fibrils with a symmetric banding pattern, an as yet overlooked component of the extracellular matrix, were found in the reticular layer of the basement membrane of human sebaceous glands. In longitudinal sections this newly described banding pattern is D-periodic (D = 67 nm) resembling the period length of native type collagen fibrils. In cross sections the symmetrically banded fibrils are irregularly outlined. The period length and the symmetric banding pattern led to the assumption that collagen molecules are staggered by the distance D, similar to native type collagen fibrils, but are arranged antiparallel. This hypothesis was tested by antiparallel superposing transparent photocopies of native type fibrils. In addition, schematic drawings of the cross striation pattern of native type fibrils were superposed in reverse directions by means of computerized image-manipulation. A model of molecular alignment was evolved from these experiments, which is characterized by two features: 1) pairs of antiparallel collagen molecules are D-staggered and 2) the two molecules of a pair are slightly shifted from precise register. The proposed model is the only one correlating with the data obtained from direct measurements on symmetrically cross striated fibrils. The fibrils described in the present study represent a supramolecular aggregate of collagen previously not observed in vivo.

Structural polymorphism of collagen type I–heparin cofibrils

“…63,64 In that respect the current study offers an interesting model for the formation of some structurally heterogeneous polymorphic forms that can be found in nature. 10,11…”

“…7 The property of the collagen systems to exhibit varying structural and hierarchical characteristics, else known as collagen polymorphism, has been observed both in vitro 8,9 and in vivo. 10,11 It was shown that the collagen polymorphism is significantly influenced by factors like presence of GAGs, 12,13 other forms of collagen, 14,15 presence/absence of telopeptide regions, 16,17 methods of purification, 18 temperature, 19 pH and salinity of the solutions. 7,20 The numerous reports account for the identification of novel banding patterns, growth mechanisms, and morphological properties of these systems deviating to different extents from the classical collagen type I.…”

“…The most studied classical forms, apart from the native asymmetric collagen type I D-banding of 67 nm, include various types of fibrous longspacing (FLS) collagen (utilizing symmetric arrangement of tropocollagen) 21,22 and segment longspacing (SLS) fibrils 23,24 with periodic asymmetric pattern, both sharing non-D periodic bandings. Other examples include D-periodic fibrils generally being D-periodic symmetric (DPS) 8,10 and oblique-striated asymmetric tactoids. 8,25 The vast majority of in vitro studies that were used to draw conclusions about collagen type I systems include work with acid-soluble tropocollagen, which typically produces long cylindrical fibrils.…”

The need for advanced three-dimensional neural models and developing enabling technologies

“…It is worth noting that on the scale with which cells interact with their substrate, micropatterning techniques often generate physical structures that may themselves serve to guide focal adhesion (FA) formation. Investigations into the molecular process by which cells adhere to surface motifs demonstrate that cells are sensitive to topographical cues on the nanometer scale; collagen I, II, III, and V fibrils in vivo all present a banding pattern known as the D-period with a regular interval of 67nm [57] . Removal of this D-period in collagen I has been shown to completely erase the ability of aligned fibrils on a 2D substrate to produce cultures of aligned fibroblasts in vitro suggesting a key role played by this pattern in guiding cell alignment [58] .…”

Structure and function of ECM-inspired composite collagen type I scaffolds

“…26 Although the correct 67 nm D-pattern as seen in microscopy studies appears to be the least discussed feature of collagen I fibrils, the literature still abounds with reports about their property to exhibit varying structural and hierarchical characteristics which are different from the classical collagen I, also known as collagen polymorphism, as observed both in vitro 27,28 and in vivo. 29,30 Amongst the major factors shown to affect it are the presence of GAGs/PGs [31][32][33] and other forms of collagen, 34,35 intactness of telopeptides, 36,37 purification protocols, 38 concentration, 39,40 temperature, 41 pH, and salinity of the solutions. 42,43 The numerous reports also account for the identification of novel banding patterns, growth mechanisms, and morphological properties of these systems deviating to a different extent from the classical collagen type I.…”