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Mechanics of trichocyte alpha-keratin fibers: Experiment, theory, and simulation

Published online by Cambridge University Press:  15 January 2015

Chia-Ching Chou ,
Emiliano Lepore ,
Paola Antonaci ,
Nicola Pugno  and
Markus J. Buehler
Chia-Ching Chou
Affiliation:
Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
Emiliano Lepore
Affiliation:
Laboratory of Bio-inspired & Graphene Nanomechanics, Department of Civil, Environmental and Mechanical Engineering, University of Trento, 38123 Trento, Italy
Paola Antonaci
Affiliation:
Laboratory of Bio-Inspired Nanomechanics “Giuseppe Maria Pugno”, Department of Structural, Geotechnical and Building Engineering, Politecnico di Torino, 10129 Torino, Italy
Nicola Pugno*
Affiliation:
Laboratory of Bio-inspired & Graphene Nanomechanics, Department of Civil, Environmental and Mechanical Engineering, University of Trento, 38123 Trento, Italy; Center for Materials & Microsystems, Fondazione Bruno Kessler, 38123 Povo (Trento), Italy; and School of Engineering & Materials Science, Queen Mary University of London, London E1 4NS, UK
Markus J. Buehler*
Affiliation:
Laboratory for Atomistic and Molecular Mechanics, Department of Civil and Environmental Engineering, Massachusetts Institute of Technology, Cambridge, MA 02139, USA
*
a) Address all correspondence to these authors. e-mail: nicola.pugno@unitn.it
b) e-mail: mbuehler@MIT.EDU
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Abstract

The mechanical behavior of human hair is determined by the interaction of trichocyte alpha keratin protein, matrix, and disulfide bonds crosslinking. Much effort has been spent to understand the link between the microscopic structure and the macroscopic fiber properties. Here we apply a mesoscopic coarse-grained model of the keratin macrofilament fibril combined with an analytical solution based on the concept of entropic hyperelasticity of the protein helix to investigate the link between the microscopic structure and the macroscopic properties of keratin fibers. The mesoscopic model provides good agreement with a wide range of experimental results. Based on the mesoscopic model, the predicted stress–strain curve of hair fibers agrees well with our own experimental measurements. The disulfide crosslink between the microfibril–matrix and matrix–matrix contributes to the initial modulus and provides stiffening at larger deformation of the trichocyte keratin fibers. The results show that the disulfide bonds reinforce the macrofilament and enhance the robustness of the macrofilament by facilitating the microfilaments to deform cooperatively. The availability of a mesoscopic model of this protein opens the possibility to further explore the relationship between microscopic chemical structure and macroscopic performance for a bottom-up description of soft materials.

Keywords

keratinhairmesoscale modeldisulfide bondalpha helix protein
Type
Articles
Information
Journal of Materials Research , Volume 30 , Issue 1: Focus Issue: Soft Nanomaterials , 14 January 2015 , pp. 26 - 35
Copyright
Copyright © Materials Research Society 2015 

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References

REFERENCES

Oxenham, W.: The mechanics of wool structures R. Postle, G.A. Carnaby, and S. de Jong, Ellis Horwood, Chichester, 1988. pp. 462, price £59.50. ISBN 0-7458-0322-9. Br. Polym. J. 21(3), 279 (1989).CrossRefGoogle Scholar
Chou, S.F. and Overfelt, R.A.: Tensile deformation and failure of North American porcupine quills. Mater. Sci. Eng., C 31(8), 1729 (2011).CrossRefGoogle Scholar
Seshadri, I.P. and Bhushan, B.: In situ tensile deformation characterization of human hair with atomic force microscopy. Acta Mater. 56(4), 774 (2008).CrossRefGoogle Scholar
Fudge, D.S. and Gosline, J.M.: Molecular design of the α–keratin composite: Insights from a matrix–free model, hagfish slime threads. Proc. Biol. Sci. 271(1536), 291 (2004).CrossRefGoogle ScholarPubMed
Guthold, M., Liu, W., Sparks, E., Jawerth, L., Peng, L., Falvo, M., Superfine, R., Hantgan, R., and Lord, S.: A comparison of the mechanical and structural properties of fibrin fibers with other protein fibers. Cell Biochem. Biophys. 49(3), 165 (2007).CrossRefGoogle ScholarPubMed
Bertram, J.E. and Gosline, J.M.: Functional design of horse hoof keratin: The modulation of mechanical properties through hydration effects. J. Exp. Biol. 130(1), 121 (1987).CrossRefGoogle ScholarPubMed
Speakman, J.B.: 38—the intracellular structure of the wool fibre. J. Text. Inst., Trans. 18(10), T431 (1927).CrossRefGoogle Scholar
Astbury, W.T. and Woods, H.J.: X-ray studies of the structure of hair, wool, and related fabrics II. The molecular structure and elastic properties of hair keratin. Philos. Trans. R. Soc. London 232, 333 (1934).Google Scholar
Astbury, W.T. and Street, A.: X-ray studies of the structure of hair, wool, and related fibres I—general. Philos. Trans. R. Soc. London 230, 75 (1932).Google Scholar
Kreplak, L., Doucet, J., and Briki, F.: Unraveling double stranded alpha-helical coiled coils: An x-ray diffraction study on hard alpha-keratin fibers. Biopolymers 58(5), 526 (2001).3.0.CO;2-L>CrossRefGoogle Scholar
Kreplak, L., Doucet, J., Dumas, P., and Briki, F.: New aspects of the α-helix to β-sheet transition in stretched hard α-keratin fibers. Biophys. J. 87(1), 640 (2004).CrossRefGoogle ScholarPubMed
Hearle, J.W.S.: The structural mechanics of fibers. J. Polym. Sci., Part C: Polym. Symp. 20(1), 215 (1967).CrossRefGoogle Scholar
Hearle, J.W.S.: Chapman mechanical model for wool and other keratin fibers. Text. Res. J. 39(12), 1109 (1969).CrossRefGoogle Scholar
Hearle, J.W.S.: A critical review of the structural mechanics of wool and hair fibres. Int. J. Biol. Macromol. 27(2), 123 (2000).CrossRefGoogle ScholarPubMed
Feughelman, M. and Haly, A.R.: Structural features of keratin suggested by its mechanical properties. Biochim. Biophys. Acta 32(2), 596 (1959).CrossRefGoogle ScholarPubMed
Feughelman, M.: Role of the microfibrils in the mechanical-properties of alpha-keratins. J. Macromol. Sci. Phys. B16(1), 155 (1979).CrossRefGoogle Scholar
Feughelman, M.: A model for the mechanical-properties of the alpha-keratin cortex. Text. Res. J. 64(4), 236 (1994).CrossRefGoogle Scholar
Feughelman, M.: Mechanical Properties and Structure of Alpha-Keratin Fibres: Wool, Human Hair and Related Fibres (UNSW Press, Sydney, Australia, 1997).Google Scholar
Feughelman, M.: Natural protein fibers. J. Appl. Polym. Sci. 83(3), 489 (2002).CrossRefGoogle Scholar
Wortmann, F-J. and Zahn, H.: The stress/strain curve of α-keratin fibers and the structure of the intermediate filament. Text. Res. J. 64(12), 737 (1994).CrossRefGoogle Scholar
Chapman, B.M. and Feughelman, M.: Aspects of the structure of α-keratin derived from mechanical properties. J. Polym. Sci., Part C: Polym. Symp. 20(1), 189 (1967).CrossRefGoogle Scholar
Qin, Z., Kreplak, L., and Buehler, M.J.: Hierarchical structure controls nanomechanical properties of vimentin intermediate filaments. PLoS One 4(10), e7294 (2009).CrossRefGoogle ScholarPubMed
Qin, Z. and Buehler, M.: Structure and dynamics of human vimentin intermediate filament dimer and tetramer in explicit and implicit solvent models. J. Mol. Model. 17(1), 37 (2011).CrossRefGoogle ScholarPubMed
Qin, Z., Chou, C-C., Kreplak, L., and Buehler, M.: Structural, mechanical and functional properties of intermediate filaments from the atomistic to the cellular scales. In Advances in Cell Mechanics, Li, S. and Sun, B., ed.; Springer: Berlin, Heidelberg, 2012; p. 117.Google Scholar
Chou, C.C. and Buehler, M.J.: Structure and mechanical properties of human trichocyte keratin intermediate filament protein. Biomacromolecules 13(11), 3522 (2012).CrossRefGoogle ScholarPubMed
Azoia, N.G., Fernandes, M.M., Micaêlo, N.M., Soares, C.M., and Cavaco-Paulo, A.: Molecular modeling of hair keratin/peptide complex: Using MM-PBSA calculations to describe experimental binding results. Proteins 80(5), 1409 (2012).CrossRefGoogle ScholarPubMed
Akkermans, R.L.C. and Warren, P.B.: Multiscale modelling of human hair. Philos. Trans. A Math. Phys. Eng. Sci. 362(1821), 1783 (2004).CrossRefGoogle ScholarPubMed
Ackbarow, T., Sen, D., Thaulow, C., and Buehler, M.J.: Alpha-helical protein networks are self-protective and flaw-tolerant. PLoS One 4(6), e6015 (2009).CrossRefGoogle ScholarPubMed
Qin, Z. and Buehler, M.J.: Mechanical properties of crosslinks controls failure mechanism of hierarchical intermediate filament networks. Theor. Appl. Mech. Lett. 2(1), 13-014005 (2012).CrossRefGoogle Scholar
Buehler, M.J.: Nature designs tough collagen: Explaining the nanostructure of collagen fibrils. Proc. Natl. Acad. Sci. 103(33), 12285 (2006).CrossRefGoogle ScholarPubMed
Buehler, M.J.: Molecular nanomechanics of nascent bone: Fibrillar toughening by mineralization. Nanotechnology 18(29), 295102 (2007).CrossRefGoogle Scholar
Buehler, M.J.: Nanomechanics of collagen fibrils under varying cross-link densities: Atomistic and continuum studies. J. Mech. Behav. Biomed. Mater. 1(1), 59 (2008).CrossRefGoogle ScholarPubMed
Ackbarow, T. and Buehler, M.: Superelasticity, energy dissipation and strain hardening of vimentin coiled-coil intermediate filaments: Atomistic and continuum studies. J. Mater. Sci. 42(21), 8771 (2007).CrossRefGoogle Scholar
Buehler, M.J.: Hierarchical chemo-nanomechanics of proteins: Entropic elasticity, protein unfolding and molecular fracture. J. Mech. Mater. Struct. 2(6), 1019 (2007).CrossRefGoogle Scholar
Plimpton, S.: Fast parallel algorithms for short-range molecular dynamics. J. Comput. Phys. 117(1), 1 (1995).CrossRefGoogle Scholar
Keten, S., Chou, C.C., van Duin, A.C.T., and Buehler, M.J.: Tunable nanomechanics of protein disulfide bonds in redox microenvironments. J. Mech. Behav. Biomed. Mater. 5(1), 32 (2012).CrossRefGoogle ScholarPubMed
Kreplak, L., Franbourg, A., Briki, F., Leroy, F., Dallé, D., and Doucet, J.: A new deformation model of hard α-keratin fibers at the nanometer scale: Implications for hard α-keratin intermediate filament mechanical properties. Biophys. J. 82(4), 2265 (2002).CrossRefGoogle ScholarPubMed
Kajiura, Y., Watanabe, S., Itou, T., Nakamura, K., Iida, A., Inoue, K., Yagi, N., Shinohara, Y., and Amemiya, Y.: Structural analysis of human hair single fibres by scanning microbeam SAXS. J. Struct. Biol. 155(3), 438 (2006).CrossRefGoogle ScholarPubMed
Zahn, H.: Progress report on hair keratin research. Int. J. Cosmet. Sci. 24(3), 163 (2002).CrossRefGoogle ScholarPubMed
Ackbarow, T. and Buehler, M.J.: Hierarchical coexistence of universality and diversity controls robustness and multi-functionality in protein materials. J. Comput. Theor. Nanosci. 5(7), 1193 (2008).CrossRefGoogle Scholar
Ackbarow, T., Keten, S., and Buehler, M.J.: A multi-timescale strength model of alpha-helical protein domains. J. Phys: Condens. Matter 21(3), 035111 (2009).Google ScholarPubMed
Sokolova, A.V., Kreplak, L., Wedig, T., Mücke, N., Svergun, D.I., Herrmann, H., Aebi, U., and Strelkov, S.V.: Monitoring intermediate filament assembly by small-angle x-ray scattering reveals the molecular architecture of assembly intermediates. Proc. Natl. Acad. Sci. 103(44), 16206 (2006).CrossRefGoogle ScholarPubMed
Qin, Z., Fabre, A., and Buehler, M.: Structure and mechanism of maximum stability of isolated alpha-helical protein domains at a critical length scale. Eur. Phys. J. E: Soft Matter 36(5), 1 (2013).CrossRefGoogle Scholar
Greenberg, D.A. and Fudge, D.S.: Regulation of hard α-keratin mechanics via control of intermediate filament hydration: Matrix squeeze revisited. Proc. Biol. Sci. 280(1750), 20122158 (2013).Google ScholarPubMed
Paquin, R. and Colomban, P.: Nanomechanics of single keratin fibres: A Raman study of the alpha-helix ->beta-sheet transition and the effect of water. J. Raman Spectrosc. 38(5), 504 (2007).CrossRefGoogle Scholar