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A reversibly gated protein-transporting membrane channel made of DNA

Author

Listed:
  • Swarup Dey

    (Biodesign Center for Molecular Design and Biomimetics (at the Biodesign Institute) at Arizona State University
    Arizona State University)

  • Adam Dorey

    (University College London)

  • Leeza Abraham

    (Biodesign Center for Molecular Design and Biomimetics (at the Biodesign Institute) at Arizona State University
    Arizona State University)

  • Yongzheng Xing

    (University College London)

  • Irene Zhang

    (Biodesign Center for Molecular Design and Biomimetics (at the Biodesign Institute) at Arizona State University)

  • Fei Zhang

    (Rutgers University)

  • Stefan Howorka

    (University College London)

  • Hao Yan

    (Biodesign Center for Molecular Design and Biomimetics (at the Biodesign Institute) at Arizona State University
    Arizona State University)

Abstract

Controlled transport of biomolecules across lipid bilayer membranes is of profound significance in biological processes. In cells, cargo exchange is mediated by dedicated channels that respond to triggers, undergo a nanomechanical change to reversibly open, and thus regulate cargo flux. Replicating these processes with simple yet programmable chemical means is of fundamental scientific interest. Artificial systems that go beyond nature’s remit in transport control and cargo are also of considerable interest for biotechnological applications but challenging to build. Here, we describe a synthetic channel that allows precisely timed, stimulus-controlled transport of folded and functional proteins across bilayer membranes. The channel is made via DNA nanotechnology design principles and features a 416 nm2 opening cross-section and a nanomechanical lid which can be controllably closed and re-opened via a lock-and-key mechanism. We envision that the functional DNA device may be used in highly sensitive biosensing, drug delivery of proteins, and the creation of artificial cell networks.

Suggested Citation

  • Swarup Dey & Adam Dorey & Leeza Abraham & Yongzheng Xing & Irene Zhang & Fei Zhang & Stefan Howorka & Hao Yan, 2022. "A reversibly gated protein-transporting membrane channel made of DNA," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
  • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28522-2
    DOI: 10.1038/s41467-022-28522-2
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    References listed on IDEAS

    as
    1. Shiksha Mantri & K. Tanuj Sapra & Stephen Cheley & Thomas H. Sharp & Hagan Bayley, 2013. "An engineered dimeric protein pore that spans adjacent lipid bilayers," Nature Communications, Nature, vol. 4(1), pages 1-10, June.
    2. Katherine E. Dunn & Frits Dannenberg & Thomas E. Ouldridge & Marta Kwiatkowska & Andrew J. Turberfield & Jonathan Bath, 2015. "Guiding the folding pathway of DNA origami," Nature, Nature, vol. 525(7567), pages 82-86, September.
    3. Chunfu Xu & Peilong Lu & Tamer M. Gamal El-Din & Xue Y. Pei & Matthew C. Johnson & Atsuko Uyeda & Matthew J. Bick & Qi Xu & Daohua Jiang & Hua Bai & Gabriella Reggiano & Yang Hsia & T J Brunette & Jia, 2020. "Computational design of transmembrane pores," Nature, Nature, vol. 585(7823), pages 129-134, September.
    4. Tim Diederichs & Genevieve Pugh & Adam Dorey & Yongzheng Xing & Jonathan R. Burns & Quoc Hung Nguyen & Marc Tornow & Robert Tampé & Stefan Howorka, 2019. "Synthetic protein-conductive membrane nanopores built with DNA," Nature Communications, Nature, vol. 10(1), pages 1-11, December.
    5. Rowena A. Bull & Thiruni N. Adikari & James M. Ferguson & Jillian M. Hammond & Igor Stevanovski & Alicia G. Beukers & Zin Naing & Malinna Yeang & Andrey Verich & Hasindu Gamaarachchi & Ki Wook Kim & F, 2020. "Analytical validity of nanopore sequencing for rapid SARS-CoV-2 genome analysis," Nature Communications, Nature, vol. 11(1), pages 1-8, December.
    6. Bernard Yurke & Andrew J. Turberfield & Allen P. Mills & Friedrich C. Simmel & Jennifer L. Neumann, 2000. "A DNA-fuelled molecular machine made of DNA," Nature, Nature, vol. 406(6796), pages 605-608, August.
    7. Ebbe S. Andersen & Mingdong Dong & Morten M. Nielsen & Kasper Jahn & Ramesh Subramani & Wael Mamdouh & Monika M. Golas & Bjoern Sander & Holger Stark & Cristiano L. P. Oliveira & Jan Skov Pedersen & V, 2009. "Self-assembly of a nanoscale DNA box with a controllable lid," Nature, Nature, vol. 459(7243), pages 73-76, May.
    8. Rasmus P. Thomsen & Mette Galsgaard Malle & Anders Hauge Okholm & Swati Krishnan & Søren S.-R. Bohr & Rasmus Schøler Sørensen & Oliver Ries & Stefan Vogel & Friedrich C. Simmel & Nikos S. Hatzakis & J, 2019. "A large size-selective DNA nanopore with sensing applications," Nature Communications, Nature, vol. 10(1), pages 1-10, December.
    9. Takahiro Muraoka & Daiki Noguchi & Rinshi S. Kasai & Kohei Sato & Ryo Sasaki & Kazuhito V. Tabata & Toru Ekimoto & Mitsunori Ikeguchi & Kiyoto Kamagata & Norihisa Hoshino & Hiroyuki Noji & Tomoyuki Ak, 2020. "A synthetic ion channel with anisotropic ligand response," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    10. Minghui Liu & Jinglin Fu & Christian Hejesen & Yuhe Yang & Neal W. Woodbury & Kurt Gothelf & Yan Liu & Hao Yan, 2013. "A DNA tweezer-actuated enzyme nanoreactor," Nature Communications, Nature, vol. 4(1), pages 1-5, October.
    11. Shawn M. Douglas & Hendrik Dietz & Tim Liedl & Björn Högberg & Franziska Graf & William M. Shih, 2009. "Self-assembly of DNA into nanoscale three-dimensional shapes," Nature, Nature, vol. 459(7245), pages 414-418, May.
    12. Vivek V. Thacker & Lars O. Herrmann & Daniel O. Sigle & Tao Zhang & Tim Liedl & Jeremy J. Baumberg & Ulrich F. Keyser, 2014. "DNA origami based assembly of gold nanoparticle dimers for surface-enhanced Raman scattering," Nature Communications, Nature, vol. 5(1), pages 1-7, May.
    13. Swati Krishnan & Daniela Ziegler & Vera Arnaut & Thomas G. Martin & Korbinian Kapsner & Katharina Henneberg & Andreas R. Bausch & Hendrik Dietz & Friedrich C. Simmel, 2016. "Molecular transport through large-diameter DNA nanopores," Nature Communications, Nature, vol. 7(1), pages 1-7, November.
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    2. Qi Yang & Xu Chang & Jung Yeon Lee & Minu Saji & Fei Zhang, 2023. "DNA T-shaped crossover tiles for 2D tessellation and nanoring reconfiguration," Nature Communications, Nature, vol. 14(1), pages 1-11, December.

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