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Encoding signal propagation on topology-programmed DNA origami

Nature Chemistry volume 16, pages 1408–1417 (2024)Cite this article

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Abstract

Biological systems often rely on topological transformation to reconfigure connectivity between nodes to guide the flux of molecular information. Here we develop a topology-programmed DNA origami system that encodes signal propagation at the nanoscale, analogous to topologically efficient information processing in cellular systems. We present a systematic molecular implementation of topological operations involving ‘glue–cut’ processes that can prompt global conformational change of DNA origami structures, with demonstrated major topological properties including genus, number of boundary components and orientability. By spatially arranging reactive DNA hairpins, we demonstrate signal propagation across transmission paths of varying lengths and orientations, and curvatures on the curved surfaces of three-dimensional origamis. These DNA origamis can also form dynamic scaffolds for regulating the spatial and temporal signal propagations whereby topological transformations spontaneously alter the location of nodes and boundary of signal propagation network. We anticipate that our strategy for topological operations will provide a general route to manufacture dynamic DNA origami nanostructures capable of performing global structural transformations under programmable control.

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Fig. 1: Topological transformation of DNA origami systems.
Fig. 2: Design and visualization of reconfigurable topological DNA origami.
Fig. 3: Three-dimensional origamis with spheroidal or hyperboloid configuration.
Fig. 4: Signal propagation via molecular wires on the curved surface.
Fig. 5: Multipurpose dual-rail gates on the reconfigurable DNA origami.

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Data availability

The data and experimental protocols for this work are available within Supplementary Information and from the corresponding author on request. Supplementary Information is available in the online version of the paper. The design files and oxDNA simulation results are available at https://nanobase.org/structure/184. Source data are provided with this paper.

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Acknowledgements

We express our gratitude to Y. Zou from the Department of Mathematics at East China Normal University for his valuable contributions to our discussions on the topology of DNA origamis. This work was supported by the National Science Foundation of China (grant nos. T2188102 and 21991134), the National Key R&D Program of China (2021YFF1200300), the Shanghai Science and Technology Committee (STCSM) (23ZR1479600) and the New Cornerstone Science Foundation.

Author information

Author notes

  1. These authors contributed equally: Wei Ji, Xiewei Xiong, Mengyao Cao, Yun Zhu.

Authors and Affiliations

  1. Shanghai Key Laboratory of Green Chemistry and Chemical Processes; Shanghai Center of Brain-inspired Intelligent Materials and Devices; Shanghai Frontiers Science Center of Molecule Intelligent Syntheses; School of Chemistry and Molecular Engineering, East China Normal University, Shanghai, China

    Wei Ji, Xiewei Xiong, Mengyao Cao, Yun Zhu, Li Li & Hao Pei

  2. School of Chemistry and Chemical Engineering, New Cornerstone Science Laboratory, Frontiers Science Center for Transformative Molecules, Zhangjiang Institute for Advanced Study and National Center for Translational Medicine, Shanghai Jiao Tong University, Shanghai, China

    Fei Wang & Chunhai Fan

  3. Institute of Molecular Medicine, Shanghai Key Laboratory for Nucleic Acids Chemistry and Nanomedicine, Renji Hospital, School of Medicine, Shanghai Jiao Tong University, Shanghai, China

    Chunhai Fan

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Contributions

H.P. and C.F. conceived and supervised the project. W.J. designed and performed the experiments. M.C. and Y.Z. conducted the origami synthesis as well as the AFM and PAGE analyses. X.X., M.C. and Y.Z. carried out the oxDNA simulations. H.P., W.J., X.X., C.F. and M.C. discussed the design. All authors contributed to data analysis and interpretation. X.X., L.L., M.C., Y.Z. C.F. and H.P. wrote the paper.

Corresponding authors

Correspondence to Chunhai Fan or Hao Pei.

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The authors declare no competing interests.

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Peer review information

Nature Chemistry thanks Ebbe Andersen and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–33, discussion and Table 1.

Supplementary Table 1

DNA sequences.

Supplementary Data 1

Source data for supplementary figures.

Supplementary Video 1

A video file showing the oxDNA simulated structures of 3D cross-link H.

Supplementary Video 2

A video file showing the oxDNA simulated structures of 3D cross-link S.

Supplementary Video 3

A video file showing the oxDNA simulated structures of 3D deformed figure-eight H.

Supplementary Video 4

A video file showing the oxDNA simulated structures of 3D deformed figure-eight S.

Supplementary Video 5

A video file showing the oxDNA simulated structures of 3D Möbius-shorts H.

Supplementary Video 6

A video file showing the oxDNA simulated structures of 3D Möbius-shorts S.

Source data

Source Data Fig. 4

Statistical source data.

Source Data Fig. 5

Statistical source data.

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Ji, W., Xiong, X., Cao, M. et al. Encoding signal propagation on topology-programmed DNA origami. Nat. Chem. 16, 1408–1417 (2024). https://doi.org/10.1038/s41557-024-01565-2

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