Much attention has been given to the rupture of noncovalent chemical bonds in protein dynamics, and Bell's model has become widely used. In many cases, however, unbinding or unfolding requires that multiple energy barriers be overcome in parallel, in coordinated failure events. We examine one such system, slippage between s-sheet filaments of the self-assembling peptide RAD16-II ([RARADADA]2). RAD16-II forms amphiphilic s-sheet filaments, with alanine side chains forming the hydrophobic surface. In an aqueous environment, filaments are found in pairs, with their hydrophobic faces placed together. We examine slippage between two filaments using steered molecular dynamics simulations. We observe that alanine side chains on one s-sheet filament form a rectangular array, and the alanine side chains of the opposing sheet occupy the interstices. For slippage to occur, these methyl groups must jump from one interstice to the next. Since the alanines in one s-sheet are elastically linked, this failure occurs in a cooperative manner. Slippage of a single alanine side chain correlates with slippage of its immediate neighbors, and a dislocation propagates across the bound surface within a few picoseconds. We present a one-dimensional, coarse-grained model based on Langevin dynamics, that incorporates the basic elements of this system: multiple elastically linked particles each residing in an energy well and overcoming an energy barrier under applied force. The coarse-grained model shows good agreement with molecular dynamics results and provides a useful platform for studying coordinated failure events. [Supported by the NHLBI, EB003805.]