Dynamics in Natural and Designed Elastins and Their Relation to Elastic Fiber Structure and Recoil
Ma. Faye Charmagne A. Carvajal,
Jonathan M. Preston,
Nour M. Jamhawi,
T. Michael Sabo,
James M. Aramini,
Richard J. Wittebort,
Posted 15 Jul 2020
bioRxiv DOI: 10.1101/2020.07.14.202523
Posted 15 Jul 2020
Elastin fibers assemble in the extracellular matrix from the precursor protein tropoelastin and provide the flexibility and spontaneous recoil required for arterial function. Unlike many proteins, a structure-function mechanism for elastin has been elusive. We have performed detailed NMR relaxation studies of the dynamics of the minielastins 24x' and 20x' using solution NMR, and of purified bovine elastin fibers in the presence and absence of mechanical stress using solid state NMR. The low sequence complexity of the minielastins enables us to determine dynamical timescales and degrees of local ordering with residue-specific resolution in the cross-link and hydrophobic modules using NMR relaxation. We find an extremely high degree of disorder, with order parameters for the entirety of the hydrophobic domains near zero, resembling that of simple chemical polymers and less than the order parameters that have been observed in other intrinsically disordered proteins. We find that backbone order parameters in natural, purified elastin fibers are comparable to those found in 24x'and 20x' in solution. The difference in dynamics, compared to the minielastins, is that backbone correlation times are significantly slowed in purified elastin. Moreover, when elastin is mechanically stretched, the high chain disorder in purified elastin is retained - showing that any change in local ordering is below that detectable in our experiment. Combined with our previous finding of a 10-fold increase in the ordering of water when fully hydrated elastin fibers are stretched by 50%, these results support the hypothesis that stretch induced solvent ordering, i.e., the hydrophobic effect, is a key player in the elastic recoil of elastin as opposed to configurational entropy loss.
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