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Molecular mechanics of coiled coils loaded in the shear geometry

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Goktas,  Melis
Kerstin Blank, Mechano(bio)chemie, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Luo,  Chuanfu
Ana Vila Verde, Theorie & Bio-Systeme, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Sullan,  Ruby May A.
Kerstin Blank, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Bergues-Pupo,  Ana E.
Ana Vila Verde, Theorie & Bio-Systeme, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Lipowsky,  Reinhard
Theorie & Bio-Systeme, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Vila Verde,  Ana
Ana Vila Verde, Theorie & Bio-Systeme, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Blank,  Kerstin G.
Kerstin Blank, Mechano(bio)chemie, Max Planck Institute of Colloids and Interfaces, Max Planck Society;

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Citation

Goktas, M., Luo, C., Sullan, R. M. A., Bergues-Pupo, A. E., Lipowsky, R., Vila Verde, A., et al. (2018). Molecular mechanics of coiled coils loaded in the shear geometry. Chemical Science, 9(20), 4610-4621. doi:10.1039/C8SC01037D.


Cite as: https://hdl.handle.net/21.11116/0000-0001-4025-D
Abstract
Coiled coils are important nanomechanical building blocks in biological and biomimetic materials. A mechanistic molecular understanding of their structural response to mechanical load is essential for elucidating their role in tissues and for utilizing and tuning these building blocks in materials applications. Using a combination of single-molecule force spectroscopy (SMFS) and steered molecular dynamics (SMD) simulations, we have investigated the mechanics of synthetic heterodimeric coiled coils of different length (3-4 heptads) when loaded in shear geometry. Upon shearing, we observe an initial rise in the force, which is followed by a constant force plateau and ultimately strand separation. The force required for strand separation depends on the coiled coil length and the applied loading rate, suggesting that coiled coil shearing occurs out of equilibrium. This out-of-equilibrium behaviour is determined by a complex structural response which involves helix uncoiling, uncoiling-assisted sliding of the helices relative to each other in the direction of the applied force as well as uncoiling-assisted dissociation perpendicular to the force axis. These processes follow a hierarchy of timescales with helix uncoiling being faster than sliding and sliding being faster than dissociation. In SMFS experiments, strand separation is dominated by uncoiling-assisted dissociation and occurs at forces between 25-45 pN for the shortest 3-heptad coiled coil and between 35-50 pN for the longest 4-heptad coiled coil. These values are highly similar to the forces required for shearing apart short double-stranded DNA oligonucleotides, reinforcing the potential role of coiled coils as nanomechanical building blocks in applications where protein-based structures are desired.