Skip to main page content
Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
, 92 (1), 70-5

Collagen Fibrils: Nanoscale Ropes

Affiliations

Collagen Fibrils: Nanoscale Ropes

Laurent Bozec et al. Biophys J.

Abstract

The formation of collagen fibrils from staggered repeats of individual molecules has become "accepted" wisdom. However, for over thirty years now, such a model has failed to resolve several structural and functional questions. In a novel approach, it was found, using atomic force microscopy, that tendon collagen fibrils are composed of subcomponents in a spiral disposition-that is, their structure is similar to that of macroscale ropes. Consequently, this arrangement was modeled and confirmed using elastic rod theory. This work provides new insight into collagen fibril structure and will have wide application-from the design of scaffolds for tissue engineering and a better understanding of pathogenesis of diseases of bone and tendon, to the conservation of irreplaceable parchment-based museum exhibits.

Figures

FIGURE 1
FIGURE 1
Atomic force microscopy of collagen fibrils. (a) Optical image showing the AFM tip above a sample of collagen fibrils on a glass slide (JPK Nanowizard). Scale bar, 10 μm. (b and c) Contact mode AFM images of digital tendon collagen fibrils. The AFM height (b; height range 0–242 nm) and error signal (deflection) (c) images show diversity in fibril morphology with several fibrils showing significant crimp (spiral morphology) along their length (arrowed in c), others retaining a straighter appearance; all display conserved axial D-banding. Scale bars = 5 μm (b) and 1 μm (c). (d) Contact mode AFM error signal image of rat tail collagen fibrils (scale bar, 1 μm). The fibrils are straighter (arrows) than those in (b and c) and display a similar D-banding size.
FIGURE 2
FIGURE 2
Local unwinding of collagen fibrils. Contact mode AFM error signal images of digital tendon collagen fibrils (scale bar, 500 nm). (a) A fibril is somewhat unwound (arrowed) but still displays axial D-banding. (b) The fibril is more unwound, has the appearance of a rope with linear substructures, and D-banding is less apparent. (c) The arrows indicate the presence of the “birdcaging” phenomenon along the length of the fibril, as seen in ropes or hawsers that are put under compressive forces or reverse twist. (d) Some of these regions (circled) display a multi-strand subfibrillar structure with at least three strands.
FIGURE 3
FIGURE 3
Local unwinding of collagen fibrils extracted from freshly dissected digitalis flexor tendon (rat). The arrows point to local structural disruptions occurring similarly during failure mode in industrial ropes.
FIGURE 4
FIGURE 4
Schematic of a two-ply model displaying L, the length of each strand; τ, the twist (angle per unit length) about the axis of each individual strand; and θ, the helical angle (the angle each strand makes with the axis of the cylinder).
FIGURE 5
FIGURE 5
Modeling the collagen fibril using elastic rod theory. (a) A single strand (top) and the corresponding full balanced two-ply (bottom) for φ0 = −30(2π) and no intrinsic twist. The unstressed rod has four straight lines drawn equidistantly on its surface. Only lines in front view are shown (red, single strand model; red and blue, two-ply model). No vertical pattern is obtained. (b) Front view of the pattern predicted in the six-ply model with intrinsic twist (top; six individual strands are color coded to aid distinction) and correspond to AFM observations: twisted fibril pattern with vertical banding and corrugated surface. The banding predicted by the model is aligned with an AFM image showing axial D-banding (bottom).
FIGURE 6
FIGURE 6
The inner structure of the collagen fibril. Contact mode AFM error signal image of digital tendon collagen fibrils (scale bar, 1 μm). The fibrils have “collapsed” onto the glass substrate and display their internal structure. This has a pleated or spiral conformation and closely resembles that of a rope, as shown in Fig. 4. The fibril presents a substructural pattern with an angle θ = (38.5 ± 8.0)°, n = 12 with respect to the long axis of the fibril (inset).
FIGURE 7
FIGURE 7
Examples of a rope solution with 9 and 12 strands displaying in both cases strong vertical banding.
FIGURE 8
FIGURE 8
Micron-scale entanglement of two collagen fibrils. Contact mode AFM error signal image of digital tendon collagen fibrils (scale bar, 2.5 μm) (higher magnification, inset). Two fibrils are entangled, presenting a two-ply rope structure as predicted from the model. This finding suggests that the rope model could be applied to the entire hierarchy of the collagen structure and not only to the evolution of the microfibril to fibril.

Similar articles

See all similar articles

Cited by 59 articles

See all "Cited by" articles

Publication types

LinkOut - more resources

Feedback