Abstract
Applications of natural viruses to nanotechnology have attracted much attention due to their fascinating nanostructures. However, chemical strategy to de novo design virus-like nanostructures is still in its infancy. In this review article, we describe novel C3-symmetric molecular design of peptides and their characteristic self-assembly into virus-like nanostructures. We have developed trigonal conjugates of β-sheet-forming peptides, trigonal conjugates of glutathione and a viral β-annulus peptide fragment.
Similar content being viewed by others
Log in or create a free account to read this content
Gain free access to this article, as well as selected content from this journal and more on nature.com
or
References
Niemeyer, C. M. Nanoparticles, Proteins, and Nucleic Acids: Biotechnology Meets Materials Science. Angew. Chem. Int. Ed. 40, 4128–4158 (2001).
Niemeyer, C. M. & Mirkin, C. A. (Eds.) Nanobiotechnology, (Wiley-VCH, Weinheim 2004).
Mirkin, C. A. & Niemeyer, C. M. (Eds.) Nanobiotechnology II, (Wiley-VCH, Weinheim 2007).
Seeman, N. C Nucleic acid nanostructures and topology. Angew. Chem. Int. Ed. 37, 3220–3238 (1998).
Seeman, N. C. DNA in a material world. Nature 421, 427–431 (2003).
Shih, W. M., Quispe, J. D. & Joyce, G. F. A 1.7-kilobase single-stranded DNA that folds into a nanoscale octahedron. Nature 427, 618–621 (2004).
Goodman, R. P., Schaap, I. A. T., Tardin, C. F., Erben, C. M., Berry, R. M., Schmidt, C. F. & Turberfield, A. J. Rapid chiral assembly of rigid DNA building blocks for molecular nanofabrication. Science 310, 1661–1665 (2005).
Matsuura, K., Yamashita, T., Igami, Y. & Kimizuka, N. ‘Nucleo-nanocages’: designed ternary oligodeoxyribonucleotides spontaneously form nanosized DNA cages. Chem. Commun. 376–377 (2003).
Matsuura, K., Masumoto, K., Igami, Y., Fujioka, T. & Kimizuka, N. In situ observation of spherical DNA assembly in water and the controlled release of bound dyes. Biomacromolecules 8, 2726–2732 (2007).
Rothemund, P. W. K. Folding DNA to create nanoscale shapes and patterns. Nature 440, 297–302 (2006).
Nangreave, J., Han, D., Liu, Y. & Yan, H. DNA origami: a history and current perspective. Curr. Opin. Chem. Biol. 14, 608–615 (2010).
Branden, C. & Tooze, J. Introduction to Protein Structure 2nd ed. (Garland Publishing, New York 1999).
Mao, C., Solis, D. J., Reiss, B. D., Kottmann, S. T., Sweeney, R. Y., Hayhurst, A., Georgiou, G., Iverson, B. & Belcher, A. M. Virus-based toolkit for the directed synthesis of magnetic and semiconducting nanowires. Science 303, 213–217 (2004).
Douglas, T. & Young, M. Viruses: making friends with old foes. Science 312, 873–875 (2006).
Steinmetz, N. F. & Evans, D. J. Utilisation of plant viruses in bionanotechnology. Org. Biomol. Chem. 5, 2891–2902 (2007).
Douglas, T. & Young, M. Host–guest encapsulation of materials by assembled virus protein cages. Nature 393, 152–155 (1998).
Douglas, T., Strable, E., Willits, D., Aitouchen, A., Libera, M. & Young, M. Protein engineering of a viral cage for constrained nanomaterials synthesis. Adv. Mater. 14, 415–418 (2002).
Comellas-Aragonès, M., Engelkamp, H., Claessen, V. I., Sommerdijik, N. A. J. M., Rowan, A. E., Christianen, P. C. M., Maan, J. C., Verduin, B. J. M., Cornelissen, J. J. L. M. & Nolte, R. J. M. A virus-based single-enzyme nanoreactor. Nat. Nanotech. 2, 635–639 (2007).
Minten, I. J., Hendriks, L. J. A., Nolte, R. J. M. & Cornelissen, J. J. L. M. Controlled encapsulation of multiple proteins in virus capsids. J. Am. Chem. Soc. 131, 17771–17773 (2009).
Strable, E., Johnson, J. E. & Finn, M. G. Natural nanochemical building blocks: icosahedral virus particles organized by attached oligonucleotides. Nano Lett. 4, 1385–1389 (2004).
Wang, Q., Lin, T., Tang, L., Johnson, J. E. & Finn, M. G Icosahedral virus particles as addressable nanoscale building blocks. Angew. Chem. Int. Ed. 41, 459–462 (2002).
Kaltgrad, E., O’Reilly, M. K., Liao, L., Han, S., Paulson, J. C. & Finn, M. G. On-virus construction of polyvalent glycan ligands for cell-surface receptors. J. Am. Chem. Soc. 130, 4578–4579 (2008).
Olson, J., Bricogne, G. & Harrison, S. C. Structure of tomato bushy stunt virus IV. The virus particle at 2.9 Å resolution. J. Mol. Biol. 171, 61–93 (1983).
Harrison, S. C. & Kirchhausen, T. Clathrin, cages, and coated vesicles. Cell 33, 650–652 (1983).
Fotin, A., Cheng, Y., Sliz, P., Grigorieff, N., Harrison, S. C., Kirchhausen, T. & Walz, T. Molecular model for a complete clathrin lattice from electron cyomicroscopy. Nature 432, 573–579 (2004).
Theil, E. C. Ferritin: Structure, gene regulation, and cellular function in animals, plants and microorganisms. Annu. Rev. Biochem. 56, 289–315 (1987).
Conn, M. M. & Rebek, J. Self-assembling capsules. Chem. Rev. 97, 1647–1668 (1997).
Tominaga, M., Suzuki, K., Kawano, M., Kusukawa, T., Ozeki, T., Sakamoto, S., Yamaguchi, K. & Fujita, M. Finite, spherical coordination networks that self-organize from 36 small components. Angew. Chem. Int. Ed. 43, 5621–5625 (2004).
Sun, Q.-F., Iwasa, J., Ogawa, D., Ishido, Y., Sato, S., Ozeki, T., Sei, Y., Yamaguchi, K. & Fujita, M. Self-assembled M24L48 polyhedra and their sharp structural switch upon subtle ligand variation. Science 328, 1144–1147 (2011).
Fujita, K., Kimura, S. & Imanishi, Y. Spherical self-assembly of a synthetic α-helical peptide in water. Langmuir 15, 4377–4379 (1999).
Kimura, S., Kim, D.-H., Sugiyama, J. & Imanishi, Y. Vesicular self-assembly of a helical peptide in water. Langmuir 15, 4461–4463 (1999).
Morikawa, M., Yoshihara, M., Endo, T. & Kimizuka, N. α-Helical polypeptide microcapsules formed by emulsion-templated self-assembly. Chem. Eur. J. 11, 1574–1578 (2005).
Ryadnov, M. G. & Woolfson, D. N. Engineering the morphology of a self-assembling protein fibre. Nat. Mater. 2, 329–332 (2003).
Ryadnov, M. G. & Woolfson, D. N. Introducing branches into a self-assembling peptide fiber. Angew. Chem. Int. Ed. 42, 3021–3023 (2003).
Zhou, M., Bentley, D. & Ghosh, I. Helical supramolecules and fibers utilizing leucine zipper-displaying dendrimers. J. Am. Chem. Soc. 126, 734–735 (2004).
Marini, D. M., Hwang, W., Lauffenburger, D. A., Zhang, S. & Kamm, R. D. Left-handed helical ribbon intermediates in the self-assembly of a β-sheet peptide. Nano Lett. 2, 295–299 (2002).
Yokoi, H., Kinoshita, T. & Zhang, S. Dynamic reassembly of peptide RADA16 nanofiber scaffold. Proc. Natl. Acad. Sci. USA 102, 8414–8419 (2005).
Padilla, J. E., Colovos, C. & Yeates, T. O. Nanohedra: using symmetry to design self-assembling protein cages, layers, crystals, and filaments. Proc. Natl. Acad. Sci. USA 98, 2217–2221 (2001).
Matsuura, K., Murasato, K. & Kimizuka, N. Artificial peptide-nanospheres self-assembled from three-way junctions of β-sheet-forming peptides. J. Am. Chem. Soc. 127, 10148–10149 (2005).
Murasato, K., Matsuura, K. & Kimizuka, N. Self-assembly of nanofiber with uniform width from wheel-type Trigonal-β-Sheet forming peptide. Biomacromolecules 9, 913–918 (2008).
Cochran, A. G., Skelton, N. J. & Starovasnik, M. A. Tryptophan zippers: stable, monomeric β-hairpins. Proc. Natl. Acad. Sci. USA 98, 5578–5583 (2001).
Streicher, W. W. & Makhatadze, G. I. Calorimetric evidence for a two-state unfolding of the β-hairpin peptide Trpzip4. J. Am. Chem. Soc. 128, 30–31 (2006).
Matsuura, K., Hayashi, H., Murasato, K. & Kimizuka, N. Trigonal tryptophane-zipper as a novel building block for pH-responding peptide nano-assemblies. Chem. Commun. 47, 265–267 (2011).
Matsuura, K., Murasato, K. & Kimizuka, N. Syntheses and self-assembling behaviors of pentagonal conjugates of tryptophane zipper-forming peptide. Int. J. Mol. Sci. 12, 5187–5199 (2011).
Reches, M. & Gazit, E. Casting metal nanowires within discrete self-assembled peptide nanotubes. Science 300, 625–627 (2003).
Gazit, E. Self-assembled peptide nanostructures: the design of molecular building blocks and their technological utilization. Chem. Soc. Rev. 36, 1263–1269 (2007).
Lyon, R. P. & Atkins, W. M. Self-assembly and gelation of oxidized glutathione in organic solvents. J. Am. Chem. Soc. 123, 4408–4413 (2001).
Mahajan, S. S., Paranji, R., Mehta, R., Lyon, R. P. & Atkins, W. M. A Glutathione-Based hydrogel and its site-selective interactions with water. Bioconj. Chem. 16, 1019–1026 (2005).
Matsuura, K., Matsuyama, H., Fukuda, T., Teramoto, T., Watanabe, K., Murasato, K. & Kimizuka, N. Spontaneous Self-assembly of nano-spheres from trigonal conjugate of glutathione in water. Soft Matter. 5, 2463–2470 (2009).
Ghosh, S., Reches, M., Gazit, E. & Verma, S. Bioinspired design of nanocages by self-assembling triskelion peptide elements. Angew. Chem. Int. Ed. 46, 2002–2004 (2007).
Matsuura, K., Tochio, K., Watanabe, K. & Kimizuka, N. Controlled release of guest molecules from spherical assembly of trigonal gultathione by disulfide recombination. Chem. Lett. 40, 711–713 (2011).
Matsuura, K., Fujino, K., Teramoto, T., Murasato, K. & Kimizuka, N. Glutathione nanospheres: self-assembly of conformation-regulated trigonal-glutathiones in water. Bull. Chem. Soc. Jpn. 83, 880–886 (2010).
Wiskur, S. L., Ait-Haddou, H., Lavigne, J. J. & Anslyn, E. V Teaching old indicators new tricks. Acc. Chem. Res. 34, 963–972 (2001).
Matsuura, K., Watanabe, K., Sakurai, K., Matsuzaki, T. & Kimizuka, N. Self-assembled synthetic viral capsids from a 24-mer viral peptide fragment. Angew. Chem. Int. Ed. 49, 9662–9665 (2010).
Acknowledgements
This research was partially supported by a Grant-in-Aid for Scientific Research on the Innovative Areas of ‘Fusion Materials’ (no. 2206) from the Ministry of Education, Science, Sports and Culture of Japan (MEXT), and by a Grant-in-Aid for Scientific Research (B) (no. 22350075) from Japan Society for the Promotion of Science. Synchrotron small angle X-ray scattering experiment was performed by Professor Salurai and Mr Matsuzaki (The University of Kitakyushu) on SPring-8 BL40B2 and BL45XU. I am deeply indebted to Professor Nobuo Kimizuka (Kyushu University) for his continuous encouragement and discussion throughout this work. Most of this study was conducted by our students. I am very much indebted to many of my co-workers and students. I thank to Dr Joseph Hui (Kyushu University) for reading this manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Matsuura, K. Construction of spherical virus-inspired peptide nanoassemblies. Polym J 44, 469–474 (2012). https://doi.org/10.1038/pj.2012.16
Received:
Revised:
Accepted:
Published:
Issue date:
DOI: https://doi.org/10.1038/pj.2012.16
Keywords
This article is cited by
-
Continual reproduction of self-assembling oligotriazole peptide nanomaterials
Nature Communications (2017)
-
Antimicrobial peptide capsids of de novo design
Nature Communications (2017)
-
Self-assembled artificial viral capsid decorated with gold nanoparticles
Polymer Journal (2015)
-
Guest-binding behavior of peptide nanocapsules self-assembled from viral peptide fragments
Polymer Journal (2013)
