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Internal dynamics of a supramolecular nanofibre

Nature Materials volume 13, pages 812–816 (2014)Cite this article

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Abstract

A large variety of functional self-assembled supramolecular nanostructures have been reported over recent decades1. The experimental approach to these systems initially focused on the design of molecules with specific interactions that lead to discrete geometric structures1,2,3,4, and more recently on the kinetics and mechanistic pathways of self-assembly5,6. However, there remains a major gap in our understanding of the internal conformational dynamics of these systems and of the links between their dynamics and function. Molecular dynamics simulations have yielded information on the molecular fluctuations of supramolecular assemblies5,6,7, yet experimentally it has been difficult to obtain analogous data with subnanometre spatial resolution. Using site-directed spin labelling and electron paramagnetic resonance spectroscopy, we measured the conformational dynamics of a self-assembled nanofibre in water through its 6.7 nm cross-section. Our measurements provide unique insight for the design of supramolecular functional materials.

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Figure 1: Peptide amphiphiles self-assemble into high-aspect-ratio nanofibres.
Figure 2: EPR spectra at specific sites through the cross-section of peptide amphiphile nanofibres.
Figure 3: The internal dynamics through the cross-section of peptide amphiphile nanofibres are obtained with subnanometre resolution and shown to depend on the presence of β-sheet-promoting amino acids.
Figure 4: Schematic molecular-graphics representation of peptide amphiphile nanofibres.

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References

  1. Palmer, L. C. & Stupp, S. I. Molecular self-assembly into one-dimensional nanostructures. Acc. Chem. Res. 41, 1674–1684 (2008).

    Article  CAS  Google Scholar 

  2. Hartgerink, J. D., Beniash, E. & Stupp, S. I. Self-assembly and mineralization of peptide-amphiphile nanofibers. Science 294, 1684 (2001).

    Article  CAS  Google Scholar 

  3. Whitesides, G. M. & Grzybowski, B. Self-assembly at all scales. Science 295, 2418–2421 (2002).

    Article  CAS  Google Scholar 

  4. Hill, J. P. et al. Self-assembled hexa-peri-hexabenzocoronene graphitic nanotube. Science 304, 1481–1483 (2004).

    Article  CAS  Google Scholar 

  5. Klein, M. L. & Shinoda, W. Large-scale molecular dynamics simulations of self-assembling systems. Science 321, 798–800 (2008).

    Article  CAS  Google Scholar 

  6. Lee, O. S., Stupp, S. I. & Schatz, G. C. Atomistic molecular dynamics simulations of peptide amphiphile self-assembly into cylindrical nanofibers. J. Am. Chem. Soc. 133, 3677–3683 (2011).

    Article  CAS  Google Scholar 

  7. Venable, R. M., Zhang, Y., Hardy, B. J. & Pastor, R. W. Molecular dynamics simulations of a lipid bilayer and of hexadecane: An investigation of membrane fluidity. Science 262, 223–226 (1993).

    Article  CAS  Google Scholar 

  8. Shaw, D. E. et al. Atomic-level characterization of the structural dynamics of proteins. Science 330, 341–346 (2010).

    Article  CAS  Google Scholar 

  9. Buchete, N-V., Tycko, R. & Hummer, G. Molecular dynamics simulations of Alzheimer’s β-amyloid protofilaments. J. Mol. Biol. 353, 804–821 (2005).

    Article  CAS  Google Scholar 

  10. McHaourab, H. S., Lietzow, M. A., Hideg, K. & Hubbell, W. L. Motion of spin-labeled side chains in T4 lysozyme. Correlation with protein structure and dynamics. Biochemistry 35, 7692–7704 (1996).

    Article  CAS  Google Scholar 

  11. Török, M. et al. Structural and dynamic features of Alzheimer’s Aβ peptide in amyloid fibrils studied by site-directed spin labeling. J. Biol. Chem. 277, 40810–40815 (2002).

    Article  Google Scholar 

  12. Newcomb, C. J. et al. Cell death versus cell survival instructed by supramolecular cohesion of nanostructures. Nature Commun. 5, 3321 (2014).

    Article  Google Scholar 

  13. Gilbert, P. M. et al. Substrate elasticity regulates skeletal muscle stem cell self-renewal in culture. Sci. Signaling 329, 1078 (2010).

    CAS  Google Scholar 

  14. Sur, S. et al. A hybrid nanofiber matrix to control the survival and maturation of brain neurons. Biomaterials 33, 545–555 (2012).

    Article  CAS  Google Scholar 

  15. Goldberger, J. E., Berns, E. J., Bitton, R., Newcomb, C. J. & Stupp, S. I. Electrostatic control of bioactivity. Angew. Chem. Int. Ed. 50, 6292–6295 (2011).

    Article  CAS  Google Scholar 

  16. Velichko, Y. S., Stupp, S. I. & de la Cruz, M. O. Molecular simulation study of peptide amphiphile self-assembly. J. Phys. Chem. B 112, 2326–2334 (2008).

    Article  CAS  Google Scholar 

  17. Paramonov, S. E., Jun, H-W. & Hartgerink, J. D. Self-assembly of peptide-amphiphile nanofibers: The roles of hydrogen bonding and amphiphilic packing. J. Am. Chem. Soc. 128, 7291–7298 (2006).

    Article  CAS  Google Scholar 

  18. Paramonov, S. E., Jun, H-W. & Hartgerink, J. D. Self-assembly of peptide-amphiphile nanofibers: The roles of hydrogen bonding and amphiphilic packing. J. Am. Chem. Soc. 128, 7291–7298 (2006).

    Article  CAS  Google Scholar 

  19. Toniolo, C., Crisma, M. & Formaggio, F. TOAC, a nitroxide spin-labeled, achiral Cα-tetrasubstituted α-amino acid, is an excellent tool in material science and biochemistry. J. Peptide Sci. 47, 153–158 (1998).

    Article  CAS  Google Scholar 

  20. Karim, C. B., Kirby, T. L., Zhang, Z., Nesmelov, Y. & Thomas, D. D. Phospholamban structural dynamics in lipid bilayers probed by a spin label rigidly coupled to the peptide backbone. Proc. Natl Acad. Sci. USA 101, 14437–14442 (2004).

    Article  CAS  Google Scholar 

  21. Budil, D. E., Lee, S., Saxena, S. & Freed, J. H. Nonlinear-least-squares analysis of slow-motion EPR spectra in one and two dimensions using a modified Levenberg-Marquardt algorithm. J. Magn. Reson. Ser. A 120, 155–189 (1996).

    Article  CAS  Google Scholar 

  22. Levine, H. Thioflavine T interaction with synthetic Alzheimer’s disease β-amyloid peptides: Detection of amyloid aggregation in solution. Protein Sci. 2, 404–410 (1993).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Director, Office of Science, Office of Basic Energy Sciences, Materials Sciences and Engineering Division of the US Department of Energy under Award # DE-FG02-00ER45810. J.B.M. acknowledges a postdoctoral fellowship through the National Institutes of Health National Research Service Award # 1F32AR06195501. J.H.O. acknowledges an IBNAM-Baxter early career award. EPR experiments were carried out at The Medical College of Wisconsin, National Biomedical EPR Center, supported by National Institutes of Health Grant P41 EB001980, and also at Northwestern University under support of the National Heart, Lung and Blood Institute of the National Institutes of Health (NIH-HL-13531). X-ray diffraction experiments were carried out at beamline 5ID-D of the Advanced Photon Source at Argonne National Laboratory. Use of the Advanced Photon Source at Argonne National Laboratory was supported by the US Department of Energy, Office of Science, Office of Basic Energy Sciences, under Contract No. DE-AC02-06CH11357. This work also made use of Northwestern University’s Biological Imaging Facility (BIF) for electron microscopy and the Integrated Molecular Structure Education and Research Center (IMSERC) for mass spectrometry and FTIR spectroscopy. The authors acknowledge S. Han for helpful discussions and M. Seniw for illustrations.

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  1. John B. Matson

    Present address: Present Address: Department of Chemistry, Virginia Tech, Blacksburg, Virginia 24060, USA.,

Authors and Affiliations

  1. Institute for BioNanotechnology in Medicine, Northwestern University, 303 East Superior Street, Suite 11-131, Chicago, Illinois 60611, USA

    Julia H. Ortony, Christina J. Newcomb, John B. Matson & Samuel I. Stupp

  2. Department of Materials Science and Engineering, Northwestern University, 2220 Campus Drive, Evanston, Illinois 60208, USA

    Christina J. Newcomb & Samuel I. Stupp

  3. Department of Chemistry, Northwestern University, 2220 Campus Drive, Evanston, Illinois 60208, USA

    Liam C. Palmer, Peter E. Doan, Brian M. Hoffman & Samuel I. Stupp

  4. Department of Medicine, Northwestern University, 251 East Huron Street, Chicago, Illinois 60611, USA

    Samuel I. Stupp

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Contributions

J.H.O. designed and performed experiments, and analysed data. C.J.N. synthesized chemicals, performed experiments and analysed data. J.B.M. synthesized chemicals. L.C.P. assisted in data analysis and writing. P.E.D. assisted in performing experiments. L.C.P., B.M.H., S.I.S. and C.J.N. provided intellectual input. J.H.O. and S.I.S. wrote the manuscript.

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Correspondence to Julia H. Ortony or Samuel I. Stupp.

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The authors declare no competing financial interests.

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Ortony, J., Newcomb, C., Matson, J. et al. Internal dynamics of a supramolecular nanofibre. Nature Mater 13, 812–816 (2014). https://doi.org/10.1038/nmat3979

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