Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Letter
  • Published:

Translation of rod-like template sequences into homochiral assemblies of stacked helical oligomers

Nature Nanotechnology volume 12, pages 447–452 (2017)Cite this article

Subjects

Abstract

At the molecular level, translation refers to the production of a new entity according to a template that has a different chemical composition. In this way, chemical information may be translated from one molecule to another. The process is useful to synthesize structures and thus functions that might be difficult to create otherwise, and it reaches exquisite levels of efficiency in biological systems, as illustrated by protein expression from mRNA templates1,2 or by the assembly of the tobacco mosaic virus capsid protein according to the length of its RNA3. In synthetic systems, examples of template-directed syntheses are numerous4,5,6, but general and versatile schemes in which a non-natural sequence actually encodes the information necessary to produce a different sequence are few and far from being optimized7,8,9,10. Here we show a high-fidelity enzyme-free translation of long rod-like alkylcarbamate oligomers into well-defined sequences of stacked helical aromatic oligoamides. The features present in the rods, which include the number and distance between carbamate functions and stereogenic centres, template the self-assembly of complementary stacks of helices that each have a defined right (P) or left (M) handedness, length and single or double helicity. This process enables the production of very large (>20 kDa) abiotic artificial folded architectures (foldamers11) that may, for example, serve as scaffolds to organize appended functional features at positions in space defined with atomic precision across nanometric distances.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Figure 1: Principle of rod-to-foldaxane translation and molecules used.
Figure 2: Foldaxane assembly, diastereoselectivity and helix handedness induction.
Figure 3: Foldaxane structure elucidation.
Figure 4: Solution evidence of the uniqueness of self-assembled foldaxanes.
Figure 5: Formation of heteromeric stacks of oligomers on heteromeric rods.
Figure 6: Detection of heteromeric foldaxane sequences on heteromeric rods using IMMS.

Similar content being viewed by others

References

  1. Moore, P. B. & Steitz, T. A. The structural basis of large ribosomal subunit function. Annu. Rev. Biochem. 72, 813–850 (2003).

    Article  CAS  Google Scholar 

  2. Ogle, J. M. & Ramakrishnan, V. Structural insights into translational fidelity. Annu. Rev. Biochem. 74, 129–177 (2005).

    Article  CAS  Google Scholar 

  3. Namba, K. & Stubbs, G. Structure of tobacco mosaic virus at 3.6 Å resolution: implications for assembly. Science 231, 1401–1406 (1986).

    Article  CAS  Google Scholar 

  4. Petitjean, A., Nierengarten, H., van Dorsselaer, A. & Lehn, J.-M. Self-organization of oligomeric helical stacks controlled by substrate binding in a tobacco mosaic virus like self-assembly process. Angew. Chem. Int. Ed. 43, 3695–3699 (2004).

    Article  CAS  Google Scholar 

  5. Suzuki, K., Sato, S. & Fujita, M. Template synthesis of precisely monodisperse silica nanoparticles within self-assembled organometallic spheres. Nat. Chem. 2, 25–29 (2010).

    Article  CAS  Google Scholar 

  6. Kondratuk, D. V. et al. Supramolecular nesting of cyclic polymers. Nat. Chem. 7, 317–322 (2015).

    Article  CAS  Google Scholar 

  7. Lewandowski, B. et al. Sequence-specific peptide synthesis by an artificial small-molecule machine. Science 339, 189–193 (2013).

    Article  CAS  Google Scholar 

  8. He, Y. & Liu, D. R. Autonomous multistep organic synthesis in a single isothermal solution mediated by a DNA walker. Nat. Nanotech. 5, 778–782 (2010).

    Article  CAS  Google Scholar 

  9. McKee, M. L. et al. Multistep DNA-templated reactions for the synthesis of functional sequence controlled oligomers. Angew. Chem. Int. Ed. 49, 7948–7951 (2010).

    Article  CAS  Google Scholar 

  10. Meng, W. et al. An autonomous molecular assembler for programmable chemical synthesis. Nat. Chem. 8, 542–548 (2016).

    Article  CAS  Google Scholar 

  11. Guichard, G. & Huc, I. Synthetic foldamers. Chem. Commun. 47, 5933–5941 (2011).

    Article  CAS  Google Scholar 

  12. Tanatani, A., Mio, M. J. & Moore, J. S. The size-selective synthesis of folded oligomers by dynamic templation. J. Am. Chem. Soc. 124, 5934–5935 (2002).

    Article  Google Scholar 

  13. Nishinaga, T., Tanatani, A., Oh, K. & Moore, J. S. Chain length-dependent affinity of helical foldamers for a rodlike guest. J. Am. Chem. Soc. 123, 1792–1793 (2001).

    Article  Google Scholar 

  14. Petitjean, A., Cuccia, L. A., Schmutz, M. & Lehn, J.-M. Naphthyridine-based helical foldamers and macrocycles: synthesis, cation binding, and supramolecular assemblies. J. Org. Chem. 73, 2481–2495 (2008).

    Article  CAS  Google Scholar 

  15. Gan, Q. et al. Helix–rod host–guest complexes with shuttling rates much faster than disassembly. Science 331, 1172–1175 (2011).

    Article  CAS  Google Scholar 

  16. Ferrand, Y., Gan, Q., Kauffmann, B., Jiang, H. & Huc, I. Template-induced screw motions within an aromatic amide foldamer double helix. Angew. Chem. Int. Ed. 50, 7572–7575 (2011).

    Article  CAS  Google Scholar 

  17. Zhang, D.-W., Zhao, X., Hou, J.-L. & Li, Z.-T. Aromatic amide foldamers: structures, properties, and functions. Chem. Rev. 112, 5271–5316 (2012).

    Article  CAS  Google Scholar 

  18. Clayden, J., Lund, A., Vallverdú, L. & Helliwell, M. Ultra-remote stereocontrol by conformational communication of information along a carbon chain. Nature 431, 966–971 (2004).

    Article  CAS  Google Scholar 

  19. Gan, Q. et al. Identification of a foldaxane kinetic byproduct during guest-induced single to double helix conversion. J. Am. Chem. Soc. 134, 15656–15659 (2012).

    Article  CAS  Google Scholar 

  20. Uetrecht, C., Rose, R. J., van Duijn, E., Lorenzen, K. & Heck, A. J. R. Ion mobility mass spectrometry of proteins and protein assemblies. Chem. Soc. Rev. 39, 1633–1655 (2010).

    Article  CAS  Google Scholar 

  21. Talotta, C., Gaeta, C., Qi, Z., Schalley, C. A. & Neri, P. Pseudorotaxanes with self-sorted sequence and stereochemical orientation. Angew. Chem. Int. Ed. 52, 7437–7441 (2013).

    Article  CAS  Google Scholar 

  22. Lee, S., Chen, C.-H. & Flood, A. H. A pentagonal cyanostar macrocycle with cyanostilbene CH donors binds anions and forms dialkylphosphate[3]rotaxanes. Nat. Chem. 5, 704–710 (2013).

    Article  CAS  Google Scholar 

  23. Belowich, M. E. et al. Positive cooperativity in the template-directed synthesis of monodisperse macromolecules. J. Am. Chem. Soc. 134, 5243–5261 (2012).

    Article  CAS  Google Scholar 

  24. Frampton, M. J. & Anderson, H. L. Insulated molecular wires. Angew. Chem. Int. Ed. 46, 1028–1064 (2007).

    Article  CAS  Google Scholar 

  25. Harada, A., Li, J. & Kamachi, M. The molecular necklace: a rotaxane containing many threaded α-cyclodextrins. Nature 356, 325–327 (1992).

    Article  CAS  Google Scholar 

  26. Sánchez-García, D. et al. Nanosized hybrid oligoamide foldamers: aromatic templates for the folding of multiple aliphatic units. J. Am. Chem. Soc. 131, 8642–8648 (2009).

    Article  Google Scholar 

  27. Zhao, H. et al. Chiral crystallization of aromatic helical foldamers via complementarities in shape and end functionalities. Chem. Sci. 3, 2042–2046 (2012).

    Article  CAS  Google Scholar 

  28. Nakano, K., Oyama, H., Nishimura, Y., Nakasako, S. & Nozaki, K. λ5-phospha[7]helicenes: synthesis, properties, and columnar aggregation with one-way chirality. Angew. Chem. Int. Ed. 51, 695–699 (2012).

    Article  CAS  Google Scholar 

  29. Haldar, D., Jiang, H., Léger, J.-M. & Huc, I. Double versus single helical structures of oligopyridine-dicarboxamide strands. Part 2: the role of side-chains. Tetrahedron 63, 6322–6330 (2007).

    Article  CAS  Google Scholar 

  30. Clark, T. D. & Ghadiri, M. R. Supramolecular design by covalent capture. Design of a peptide cylinder via hydrogen-bond-promoted intermolecular olefin metathesis. J. Am. Chem. Soc. 117, 12364–12365 (1995).

    Article  CAS  Google Scholar 

  31. Li, J., Carnall, J. M. A., Stuart, M. C. A. & Otto, S. Hydrogel formation upon photoinduced covalent capture of macrocycle stacks from dynamic combinatorial libraries. Angew. Chem. Int. Ed. 50, 8384–8386 (2011).

    Article  CAS  Google Scholar 

  32. Shvartsburg, A. A., Mashkevich, S. V., Baker, E. S. & Smith, R. D. Optimization of algorithms for ion mobility calculations. J. Phys. Chem. A 111, 2002–2010 (2007).

    Article  CAS  Google Scholar 

  33. Siu, C.-K., Guo, Y., Saminathan, I. S., Hopkinson, A. C. & Siu, K. W. Optimization of parameters used in algorithms of ion-mobility calculation for conformational analyses. J. Phys. Chem. B 114, 1204–1212 (2010).

    Article  CAS  Google Scholar 

  34. Kabsch, W. XDS. Acta Cryst. D66, 125–132 (2010).

    Google Scholar 

  35. Palatinus, L. & Chapuis, G. SUPERFLIP—a computer program for the solution of crystal structures by charge flipping in arbitrary dimensions. J. Appl. Cryst. 40, 786–790 (2007).

    Article  CAS  Google Scholar 

  36. Sheldrick, G. M. SHELXT—integrated space-group and crystal-structure determination. Acta Crystallogr. A 71, 3–8 (2015).

    Article  Google Scholar 

  37. Sheldrick, G. M. Crystal structure refinement with SHELXL. Acta Crystallogr. C 71, 3–8 (2015).

    Google Scholar 

  38. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of COOT. Acta Crystallogr. D 66, 486–501 (2010).

    Article  CAS  Google Scholar 

  39. Hübschle, C. B., Sheldrick, G. M. & Dittrich, B. Shelxle: a Qt graphical user interface for SHELXL. J. Appl. Cryst. 44, 1281–1284 (2011).

    Article  Google Scholar 

  40. Spek, A. L. Single-crystal structure validation with the program PLATON. J. Appl. Cryst. 36, 7–13 (2003).

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This work was supported by the Conseil Régional d'Aquitaine, the China Scholarship Council and the European Research Council under the European Union's Seventh Framework Programme (Grant Agreement No. ERC-2012-AdG-320892). The authors thank Christoph Mueller-Dieckmann (ESRF beamline ID29) for providing beamtime and help during the data collection.

Author information

Author notes

  1. Quan Gan

    Present address: Present address: School of Chemistry and Chemical Engineering, Huazhong University of Science and Technology, Wuhan 430074, China,

Authors and Affiliations

  1. Université de Bordeaux, CNRS, IPB, CBMN – UMR 5248, Institut Européen de Chimie et Biologie, 2 rue Robert Escarpit, Pessac, 33600, France

    Quan Gan, Xiang Wang, Yann Ferrand & Ivan Huc

  2. Université de Bordeaux, CNRS, INSERM, IECB – UMS3033 – US001, Institut Européen de Chimie et Biologie, 2 rue Robert Escarpit, Pessac, 33600, France

    Brice Kauffmann & Frédéric Rosu

Authors
  1. Quan Gan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiang Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Brice Kauffmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Frédéric Rosu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yann Ferrand
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivan Huc
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Q.G. and X.W synthesised all the new compounds and contributed equally to this work. Q.G. and X.W. carried out solution studies. B.K. collected X-ray data and solved the crystal structures. F.R. carried out ion mobility mass spectrometry measurements. I.H. and Y.F. designed the study. I.H. and Y.F. wrote the manuscript. All the authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Ivan Huc.

Ethics declarations

Competing interests

The authors declare no competing financial interests.

Supplementary information

Supplementary information

Supplementary information (PDF 3142 kb)

Supplementary information

Supplementary Movie 1 (MP4 9059 kb)

Supplementary information

Supplementary Movie 2 (MP4 10485 kb)

Supplementary information

Supplementary Movie 3 (MP4 5146 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gan, Q., Wang, X., Kauffmann, B. et al. Translation of rod-like template sequences into homochiral assemblies of stacked helical oligomers. Nature Nanotech 12, 447–452 (2017). https://doi.org/10.1038/nnano.2017.15

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/nnano.2017.15

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing