IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-28522-2.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-28522-2
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-022-28522-2?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    Cited by:

    1. Xiaoming Liu & Fengyu Liu & Hemani Chhabra & Christopher Maffeo & Zhuo Chen & Qiang Huang & Aleksei Aksimentiev & Tatsuo Arai, 2024. "A lumen-tunable triangular DNA nanopore for molecular sensing and cross-membrane transport," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Xiaoming Liu & Fengyu Liu & Hemani Chhabra & Christopher Maffeo & Zhuo Chen & Qiang Huang & Aleksei Aksimentiev & Tatsuo Arai, 2024. "A lumen-tunable triangular DNA nanopore for molecular sensing and cross-membrane transport," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    2. Smrithi Krishnan R & Kalyanashis Jana & Amina H. Shaji & Karthika S. Nair & Anjali Devi Das & Devika Vikraman & Harsha Bajaj & Ulrich Kleinekathöfer & Kozhinjampara R. Mahendran, 2022. "Assembly of transmembrane pores from mirror-image peptides," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    3. Katya Ahmad & Abid Javed & Conor Lanphere & Peter V. Coveney & Elena V. Orlova & Stefan Howorka, 2023. "Structure and dynamics of an archetypal DNA nanoarchitecture revealed via cryo-EM and molecular dynamics simulations," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    4. Zhao Zhang & Zhaomeng Feng & Xiaowei Zhao & Dominique Jean & Zhiheng Yu & Edwin R. Chapman, 2023. "Functionalization and higher-order organization of liposomes with DNA nanostructures," Nature Communications, Nature, vol. 14(1), pages 1-9, December.
    5. Molly F. Parsons & Matthew F. Allan & Shanshan Li & Tyson R. Shepherd & Sakul Ratanalert & Kaiming Zhang & Krista M. Pullen & Wah Chiu & Silvi Rouskin & Mark Bathe, 2023. "3D RNA-scaffolded wireframe origami," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    6. Francis Schuknecht & Karol Kołątaj & Michael Steinberger & Tim Liedl & Theobald Lohmueller, 2023. "Accessible hotspots for single-protein SERS in DNA-origami assembled gold nanorod dimers with tip-to-tip alignment," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    7. Vishal Maingi & Zhao Zhang & Chris Thachuk & Namita Sarraf & Edwin R. Chapman & Paul W. K. Rothemund, 2023. "Digital nanoreactors to control absolute stoichiometry and spatiotemporal behavior of DNA receptors within lipid bilayers," Nature Communications, Nature, vol. 14(1), pages 1-12, December.
    8. Ioanna Smyrlaki & Ferenc Fördős & Iris Rocamonde-Lago & Yang Wang & Boxuan Shen & Antonio Lentini & Vincent C. Luca & Björn Reinius & Ana I. Teixeira & Björn Högberg, 2024. "Soluble and multivalent Jag1 DNA origami nanopatterns activate Notch without pulling force," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    9. Jianxin Yang & Tianle Pan & Zhenming Xie & Wu Yuan & Ho-Pui Ho, 2024. "In-tube micro-pyramidal silicon nanopore for inertial-kinetic sensing of single molecules," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    10. Hong Kang & Yuexuan Yang & Bryan Wei, 2024. "Synthetic molecular switches driven by DNA-modifying enzymes," Nature Communications, Nature, vol. 15(1), pages 1-9, December.
    11. Yusuke Takezawa & Keita Mori & Wei-En Huang & Kotaro Nishiyama & Tong Xing & Takahiro Nakama & Mitsuhiko Shionoya, 2023. "Metal-mediated DNA strand displacement and molecular device operations based on base-pair switching of 5-hydroxyuracil nucleobases," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    12. Sungwook Woo & Sinem K. Saka & Feng Xuan & Peng Yin, 2024. "Molecular robotic agents that survey molecular landscapes for information retrieval," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    13. Justin A. Peruzzi & Taylor F. Gunnels & Hailey I. Edelstein & Peilong Lu & David Baker & Joshua N. Leonard & Neha P. Kamat, 2024. "Enhancing extracellular vesicle cargo loading and functional delivery by engineering protein-lipid interactions," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    14. Andreas Walbrun & Tianhe Wang & Michael Matthies & Petr Šulc & Friedrich C. Simmel & Matthias Rief, 2024. "Single-molecule force spectroscopy of toehold-mediated strand displacement," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    15. Fabian Schnitter & Benedikt Rieß & Christian Jandl & Job Boekhoven, 2022. "Memory, switches, and an OR-port through bistability in chemically fueled crystals," Nature Communications, Nature, vol. 13(1), pages 1-8, December.
    16. Jolien Van Cleemput & Willem van Snippenberg & Laurens Lambrechts & Amélie Dendooven & Valentino D’Onofrio & Liesbeth Couck & Wim Trypsteen & Jan Vanrusselt & Sebastiaan Theuns & Nick Vereecke & Thier, 2021. "Organ-specific genome diversity of replication-competent SARS-CoV-2," Nature Communications, Nature, vol. 12(1), pages 1-11, December.
    17. Martina F. Ober & Anna Baptist & Lea Wassermann & Amelie Heuer-Jungemann & Bert Nickel, 2022. "In situ small-angle X-ray scattering reveals strong condensation of DNA origami during silicification," Nature Communications, Nature, vol. 13(1), pages 1-7, December.
    18. Jae-Hyun Park & Kouki Kawakami & Naito Ishimoto & Tatsuya Ikuta & Mio Ohki & Toru Ekimoto & Mitsunori Ikeguchi & Dong-Sun Lee & Young-Ho Lee & Jeremy R. H. Tame & Asuka Inoue & Sam-Yong Park, 2023. "Structural basis for ligand recognition and signaling of hydroxy-carboxylic acid receptor 2," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    19. Marcello DeLuca & Daniel Duke & Tao Ye & Michael Poirier & Yonggang Ke & Carlos Castro & Gaurav Arya, 2024. "Mechanism of DNA origami folding elucidated by mesoscopic simulations," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    20. A. Mills & N. Aissaoui & D. Maurel & J. Elezgaray & F. Morvan & J. J. Vasseur & E. Margeat & R. B. Quast & J. Lai Kee-Him & N. Saint & C. Benistant & A. Nord & F. Pedaci & G. Bellot, 2022. "A modular spring-loaded actuator for mechanical activation of membrane proteins," Nature Communications, Nature, vol. 13(1), pages 1-10, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-28522-2. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.