Unraveling and Sliding of Polypeptide Strands Underlies the Exceptional Toughness of the Triple-Helix Collagen Molecule.

Abstract

Fibril-forming tropocollagens (TCs) play an essential role in tissue biomechanics. They are ubiquitous in mammals and other animal tissues, where they provide passive mechanical functions. While molecular dynamics simulations have targeted the mechanics of individual TCs, experimental data on their tensile mechanical properties remain scarce. As a consequence, the link between the unique triple-helix structure of the collagen molecule and macro-mechanical properties of collagenous tissues is not well understood. To close this gap, we have investigated isolated TCs grafted on the tip of atomic force microscopy (AFM) probes as well as adsorbed TC films using a surface force apparatus (SFA). AFM force spectroscopy showed that an individual TC can be stretched without failing to a contour length of up to 900 nm─nearly three times its native length─over thousands of stretching cycles. The molecule was retracted from a strongly adhering mica surface by pulling on one of the α-chains, forcing the triple-helix to unravel. During this process, the α-chains slipped progressively, irreversibly, and almost entirely past each other before being caught by strong physical interactions between overlapping chain ends. SFA measurements showed that strong electrostatic interactions bind TC to mica and prevent TC aggregation, supporting the AFM results. These findings indicate that a controlled slippage mechanism underpins the exceptional toughness of TCs, collagen fibrils, and collagen-rich tissues such as tendons and skin.