Open Access
Issue
Published:
12 July 2008
Elasticity, Strength and Resilience: A Comparative Study on Mechanical Signatures of α-Helix, β-Sheet and Tropocollagen Domains
Download citation
637
Views
26
Downloads
36
Crossref
N/A
WoS
0
Scopus
0
CSCD
In biology, structural design and materials engineering is unified through formation of hierarchical features with atomic resolution, from nano to macro. Three molecular building blocks are particularly prevalent in all structural protein materials: alpha helices (AHs), beta-sheets (BSs) and tropocollagen (TC). In this article we present a comparative study of these three key building blocks by focusing on their mechanical signatures, based on results from full-atomistic simulation studies. We find that each of the basic structures is associated with a characteristic material behavior: AH protein domains provide resilience at large deformation through energy dissipation at low force levels, BS protein domains provide great strength under shear loading, and tropocollagen molecules provide large elasticity for deformation recovery. This suggests that AHs, BSs, and TC molecules have mutually exclusive mechanical signatures. We correlate each of these basic properties with the molecule's structure and the associated fundamental rupture mechanisms. Our study may enable the use of abundant protein building blocks in nanoengineered materials, and may provide critical insight into basic biological mechanisms for bio-inspired nanotechnologies. The transfer towards the design of novel nanostructures could lead to new multifunctional and mechanically active, tunable, and changeable materials.
menu
Elasticity, Strength and Resilience: A Comparative Study on Mechanical Signatures of α-Helix, β-Sheet and Tropocollagen Domains
Abstract
In biology, structural design and materials engineering is unified through formation of hierarchical features with atomic resolution, from nano to macro. Three molecular building blocks are particularly prevalent in all structural protein materials: alpha helices (AHs), beta-sheets (BSs) and tropocollagen (TC). In this article we present a comparative study of these three key building blocks by focusing on their mechanical signatures, based on results from full-atomistic simulation studies. We find that each of the basic structures is associated with a characteristic material behavior: AH protein domains provide resilience at large deformation through energy dissipation at low force levels, BS protein domains provide great strength under shear loading, and tropocollagen molecules provide large elasticity for deformation recovery. This suggests that AHs, BSs, and TC molecules have mutually exclusive mechanical signatures. We correlate each of these basic properties with the molecule's structure and the associated fundamental rupture mechanisms. Our study may enable the use of abundant protein building blocks in nanoengineered materials, and may provide critical insight into basic biological mechanisms for bio-inspired nanotechnologies. The transfer towards the design of novel nanostructures could lead to new multifunctional and mechanically active, tunable, and changeable materials.
References(37)
Alberts, B.; Bray, D.; Lewis, J.; Raff, M.; Robert, K.; Watson, J. D. Molecular Biology of the Cell; Taylor & Francis: New York, NY, 2002.
Fratzl, P.; Weinkamer, R. Nature's hierarchical materials. Prog. Mater. Sci. 2007, 52: 1263–1334.
Smith, B. L.; Schäffer, T. E.; Viani, M.; Thompson, J. B.; Frederick, N. A.; Kindt, J.; Belcher, A.; Stucky, G. D.; Morse, D. E.; Hansma, P. K. Molecular mechanistic origin of the toughness of natural adhesives, fibres and composites. Nature 1999, 399(6738): 761–763.
Hirth, J. P.; Lothe, J. Theory of Dislocations; Wiley-Interscience: New York, NY, 1982.
Herrmann, H.; Aebi, U. Intermediate filaments: Molecular structure, assembly mechanism, and integration into functionally distinct intracellular scaffolds. Ann. Rev. Biochem. 2004, 73: 749–789.
Rowat, A. C. Lammerding, J.; Herrmann, H.; Aebi, U. Towards an integrated understanding of the structure and mechanics of the cell nucleus. Bioessays 2008, 30(3): 226–36.
Kreplak, L.; Fudge, D. Biomechanical properties of intermediate filaments: From tissues to single filaments and back. Bioessays 2007, 29(1): 26–35.
Du, N.; Liu, X. Y.; Narayanan, J.; Li, L.; Lim, M. L. M.; Li, D. Q. Design of superior spider silk: From nanostructure to mechanical properties. Biophys. J. 2006, 91(12): 4528–4535.
Vollrath, F.; Porter, D. Spider silk as archetypal protein elastomer. Soft Matter. 2006, 2(5): 377–385.
Termonia, Y. Molecular modeling of spider silk elasticity. Macromolecules 1994, 27(25): 7378–7381.
Mostaert, A. S.; Higgins, M. J. Nanoscale mechanical characterisation of amyloid fibrils discovered in a natural adhesive. J. Biol. Phys. 2006, 32(5): 393–401.
Smith, J. F.; Knowles, T. P. J.; Dobson, C. M.; MacPhee, C. E.; Welland, M. E. Characterization of the nanoscale properties of individual amyloid fibrils. P. Natl. Acad. Sci. U. S. A. 2006, 103(43): 15806–15811.
Slotta, U.; Hess, S.; Spiess, k.; Stromer, T.; Serpell, L.; Scheibel, T. Spider silk and amyloid fibrils: A structural comparison. Macromol. Biosci. 2007, 7(2): 183–188.
Ricard-Blum, S.; Ruggiero, F.; van der Rest, M. The collagen superfarmily. Collagen. . 2005, 35–84.
Gelse, K.; Poschl, E.; Aigner; T. Collagens–structure, function, and biosynthesis. Adv. Drug Delivery Rev. 2003, 55(12): 1531–1546.
Vincent, J. F. V. Structural Biomaterials; Princeton University Press: Princeton, NJ, 1990.
Ingber, D. E. Cellular mechanotransduction: Putting all the pieces together again. FASEB J. 2006, 20(7): 811–827.
Papapostolou, D.; Smith, A. M.; Atkins, D. T.; Oliver, S. J.; Ryadnov, M. G.; Serpell, L. C.; Woolfson, D. N. Engineering nanoscale order into a designed protein fiber. P. Natl. Acad. Sci. USA 2007, 104(26): 10853–10858.
Langer, R.; Tirrell, D. A. Designing materials for biology and medicine. Nature 2004, 428(6982): 487–492.
Smeenk, J. M.; Otten, M. B.; Thies, J.; Tirrell, D. A.; Stunnenberg H. G.; van Hest J. C. Controlled assembly of macromolecular beta-sheet fibrils. Angew. Chem. Int. Ed. Engl. 2005, 44(13): 1968–1971.
Zhao, X. J.; Zhang, S. G. Molecular designer self-assembling peptides. Chem. Soc. Rev. 2006, 35(11): 1105–1110.
Mershin, A.; Cook, B.; Kaiser, L.; Zhang, S. G. A classic assembly of nanobiomaterials. Nat. Biotechnol. 2005, 23(11): 1379–1380.
Sotomayor, M.; Schulten, K. Single-molecule expzeriments in vitro and in silico. Science 2007, 316(5828): 1144–1148.
Ackbarow, T.; Chen, X. F.; Keten, S.; Buehler, M. J. Hierarchies, multiple energy barriers and robustness govern the fracture mechanics of alpha helical and beta-sheet protein domains. P. Natl. Acad. Sci. USA 2007, 104: 16410–16415
Buehler, M. J. Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. P. Natl. Acad. Sci. USA 2006, 103(33): 12285–12290.
Schwaiger, I.; Sattler, C.; Hostetter, D. R.; Rief, M. The myosin coiled-coil is a truly elastic protein structure. Nat. Mater. 2002, 1(4): 232–235.
Root, D. D.; Yadavalli, V. K.; Forbes, J. G.; Wang, K. Coiled-coil nanomechanics and uncoiling and unfolding of the superhelix and alpha helices of myosin. Biophys. J. 2006, 90(8): 2852–2866.
Buehler, M. J. Hierarchical chemo-nanomechanics of stretching protein molecules: Entropic elasticity, protein unfolding and molecular fracture. J. Mech. Mater. Struct. 2007, 2(6): 1019–1057.
Ackbarow, T.; Buehler, M. J. Superelasticity, energy dissipation and strain hardening of vimentin coiled-coil intermediate filaments: Atomistic and continuum studies. J. Mater. Sci. 2007, 42(21): 8771–8787.
Buehler, M. J.; Wong, S. Y. Entropic elasticity controls nanomechanics of single tropocollagen molecules. Biophys. J. 2007, 93(1): 37–43.
Buehler, M. J. Atomistic and continuum modeling of mechanical properties of collagen: Elasticity, fracture and self-assembly. J. Mater. Res. 2006, 21(8): 1947–1961.
Cui, X. Q.; Li, C. M.; Zang, J. F.; Zhou, Q.; Gan, Y.; Bao, H. F.; Guo, J.; Biocatalytic generation of ppy-enzyme-CNT nanocomposite: From network assembly to film growth. J. Phys. Chem. C 2007, 111(5): 2025–2031.
FEEDBACK 
TOP