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ABSTRACT The standard model for the structure of collagen in tendon is an ascending hierarchy of bundling. Collagen triple helices bundle into microfibrils, microfibrils bundle into subfibrils, and subfibrils bundle into fibrils, the basic structural unit of tendon. This model, developed primarily on the basis of x-ray diffraction results, is necessarily vague about the cross-sectional organization of fibrils and has led to the widespread assumption of laterally homogeneous closepacking. This assumption is inconsistent with data presented here. Using atomic force microscopy and micromanipulation, we observe how collagen fibrils from tendons behave mechanically as tubes. We conclude that the collagen fibril is an inhomogeneous structure composed of a relatively hard shell and a softer, less dense core.
INTRODUCTION
Collagens are a family of structural proteins reinforcing a variety of animal tissues including skin, bone, and tendon. Of all of the nonmineral constituents of the mammalian body there is more collagen than anything else. However, our understanding of the structure of collagen fibrils is rudimentary. Collagen diseases are typified by mechanical failure of associated tissues, and collagen products (leather, glue, gelatin) are valued for their unique mechanical properties. Knowledge of the molecular basis of the mechanical properties of collagen structures is thus important for both medical and technological applications.
In tissues, fibular collagens often form fibrils several hundred nanometers in diameter (Kadler, 1994). Native collagen fibrils exhibit a regular 67-nm banding observable in electron micrographs (Schmitt et al., 1942; Chapman and Hulmes, 1984). However, this D-spacing and banding pattern can also vary (Beniash et al., 2000). Banding also appears in topographical atomic force microscope images of hydrated, native fibrils (Fullwood et al., 1995; Bigi et al., 1997; Raspanti et al., 2001). X-ray diffraction data demonstrate that at least some collagen molecules within rat tail tendon fibrils have a well-defined crystal structure (Bear, 1942; North et al., 1954; Fraser et al., 1983; Fratzl et al., 1993; Hulmes et al., 1995; Prockop and Fertala, 1998). These data, however, also indicate that some, perhaps most, collagen molecules in rat tail tendons are in a state of liquidlike disorder (Fratzl et al., 1993; Hulmes et al., 1995; Prockop and Fertala, 1998). Moreover, nuclear magnetic resonance studies indicate that the collagen backbone is free to reorient within a collagen fibril (Trochia,...