IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-36875-5.html
   My bibliography  Save this article

Creating complex protocells and prototissues using simple DNA building blocks

Author

Listed:
  • Nishkantha Arulkumaran

    (University College London)

  • Mervyn Singer

    (University College London)

  • Stefan Howorka

    (University Collegfige London)

  • Jonathan R. Burns

    (University Collegfige London)

Abstract

Building synthetic protocells and prototissues hinges on the formation of biomimetic skeletal frameworks. Recreating the complexity of cytoskeletal and exoskeletal fibers, with their widely varying dimensions, cellular locations and functions, represents a major material hurdle and intellectual challenge which is compounded by the additional demand of using simple building blocks to ease fabrication and control. Here we harness simplicity to create complexity by assembling structural frameworks from subunits that can support membrane-based protocells and prototissues. We show that five oligonucleotides can anneal into nanotubes or fibers whose tunable thicknesses and lengths spans four orders of magnitude. We demonstrate that the assemblies’ location inside protocells is controllable to enhance their mechanical, functional and osmolar stability. Furthermore, the macrostructures can coat the outside of protocells to mimic exoskeletons and support the formation of millimeter-scale prototissues. Our strategy could be exploited in the bottom-up design of synthetic cells and tissues, to the generation of smart material devices in medicine.

Suggested Citation

  • Nishkantha Arulkumaran & Mervyn Singer & Stefan Howorka & Jonathan R. Burns, 2023. "Creating complex protocells and prototissues using simple DNA building blocks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36875-5
    DOI: 10.1038/s41467-023-36875-5
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-36875-5
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-36875-5?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. Thomas Litschel & Charlotte F. Kelley & Danielle Holz & Maral Adeli Koudehi & Sven K. Vogel & Laura Burbaum & Naoko Mizuno & Dimitrios Vavylonis & Petra Schwille, 2021. "Reconstitution of contractile actomyosin rings in vesicles," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Stephanie Lauback & Kara R. Mattioli & Alexander E. Marras & Maxim Armstrong & Thomas P. Rudibaugh & Ratnasingham Sooryakumar & Carlos E. Castro, 2018. "Real-time magnetic actuation of DNA nanodevices via modular integration with stiff micro-levers," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    3. Siddharth Agarwal & Melissa A. Klocke & Passa E. Pungchai & Elisa Franco, 2021. "Dynamic self-assembly of compartmentalized DNA nanotubes," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    4. Daniel A. Fletcher & R. Dyche Mullins, 2010. "Cell mechanics and the cytoskeleton," Nature, Nature, vol. 463(7280), pages 485-492, January.
    5. Qingchuan Li & Shubin Li & Xiangxiang Zhang & Weili Xu & Xiaojun Han, 2020. "Programmed magnetic manipulation of vesicles into spatially coded prototissue architectures arrays," Nature Communications, Nature, vol. 11(1), pages 1-9, December.
    6. Guido Bolognesi & Mark S. Friddin & Ali Salehi-Reyhani & Nathan E. Barlow & Nicholas J. Brooks & Oscar Ces & Yuval Elani, 2018. "Sculpting and fusing biomimetic vesicle networks using optical tweezers," Nature Communications, Nature, vol. 9(1), pages 1-11, December.
    7. Tim Sanchez & Daniel T. N. Chen & Stephen J. DeCamp & Michael Heymann & Zvonimir Dogic, 2012. "Spontaneous motion in hierarchically assembled active matter," Nature, Nature, vol. 491(7424), pages 431-434, 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. Jorik Waeterschoot & Willemien Gosselé & Špela Lemež & Xavier Casadevall i Solvas, 2024. "Artificial cells for in vivo biomedical applications through red blood cell biomimicry," Nature Communications, Nature, vol. 15(1), pages 1-17, 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. Xiangxiang Zhang & Chao Li & Fukai Liu & Wei Mu & Yongshuo Ren & Boyu Yang & Xiaojun Han, 2022. "High-throughput production of functional prototissues capable of producing NO for vasodilation," Nature Communications, Nature, vol. 13(1), pages 1-11, December.
    2. Jorik Waeterschoot & Willemien Gosselé & Špela Lemež & Xavier Casadevall i Solvas, 2024. "Artificial cells for in vivo biomedical applications through red blood cell biomimicry," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    3. Gábor Pete & Ádám Timár & Sigurdur Örn Stefánsson & Ivan Bonamassa & Márton Pósfai, 2024. "Physical networks as network-of-networks," Nature Communications, Nature, vol. 15(1), pages 1-8, December.
    4. Matt D. G. Hughes & Sophie Cussons & Benjamin S. Hanson & Kalila R. Cook & Tímea Feller & Najet Mahmoudi & Daniel L. Baker & Robert Ariëns & David A. Head & David J. Brockwell & Lorna Dougan, 2023. "Building block aspect ratio controls assembly, architecture, and mechanics of synthetic and natural protein networks," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    5. Chao Jiang & Hong-Yu Luo & Xinpeng Xu & Shuo-Xing Dou & Wei Li & Dongshi Guan & Fangfu Ye & Xiaosong Chen & Ming Guo & Peng-Ye Wang & Hui Li, 2023. "Switch of cell migration modes orchestrated by changes of three-dimensional lamellipodium structure and intracellular diffusion," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    6. Aravind Chandrasekaran & Kristin Graham & Jeanne C. Stachowiak & Padmini Rangamani, 2024. "Kinetic trapping organizes actin filaments within liquid-like protein droplets," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    7. Shubin Li & Yingming Zhao & Shuqi Wu & Xiangxiang Zhang & Boyu Yang & Liangfei Tian & Xiaojun Han, 2023. "Regulation of species metabolism in synthetic community systems by environmental pH oscillations," Nature Communications, Nature, vol. 14(1), pages 1-10, December.
    8. Daniela Sorrentino & Simona Ranallo & Francesco Ricci & Elisa Franco, 2024. "Developmental assembly of multi-component polymer systems through interconnected synthetic gene networks in vitro," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    9. Siddharth Agarwal & Dino Osmanovic & Mahdi Dizani & Melissa A. Klocke & Elisa Franco, 2024. "Dynamic control of DNA condensation," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    10. Jingjing Zhao & Xiaojun Han, 2024. "Investigation of artificial cells containing the Par system for bacterial plasmid segregation and inheritance mimicry," Nature Communications, Nature, vol. 15(1), pages 1-11, December.
    11. Songyang Liu & Yanwen Zhang & Xiaoxiao He & Mei Li & Jin Huang & Xiaohai Yang & Kemin Wang & Stephen Mann & Jianbo Liu, 2022. "Signal processing and generation of bioactive nitric oxide in a model prototissue," Nature Communications, Nature, vol. 13(1), pages 1-12, December.
    12. Muqing Cao & Xiaoxiao Zou & Chaoyi Li & Zaisheng Lin & Ni Wang & Zhongju Zou & Youqiong Ye & Joachim Seemann & Beth Levine & Zaiming Tang & Qing Zhong, 2023. "An actin filament branching surveillance system regulates cell cycle progression, cytokinesis and primary ciliogenesis," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    13. Bibi Najma & Minu Varghese & Lev Tsidilkovski & Linnea Lemma & Aparna Baskaran & Guillaume Duclos, 2022. "Competing instabilities reveal how to rationally design and control active crosslinked gels," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    14. Salgado-García, R., 2022. "Active particles in reactive disordered media: How does adsorption affect diffusion?," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 603(C).
    15. Jiu-Tao Hang & Yu Kang & Guang-Kui Xu & Huajian Gao, 2021. "A hierarchical cellular structural model to unravel the universal power-law rheological behavior of living cells," Nature Communications, Nature, vol. 12(1), pages 1-7, December.
    16. Tom Brandstätter & David B. Brückner & Yu Long Han & Ricard Alert & Ming Guo & Chase P. Broedersz, 2023. "Curvature induces active velocity waves in rotating spherical tissues," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    17. Mallikarjun, Rahul & Pal, Arnab, 2023. "Chiral run-and-tumble walker: Transport and optimizing search," Physica A: Statistical Mechanics and its Applications, Elsevier, vol. 622(C).
    18. Antonio Lamura & Adriano Tiribocchi, 2021. "Shearing Effects on the Phase Coarsening of Binary Mixtures Using the Active Model B," Mathematics, MDPI, vol. 9(23), pages 1-13, November.
    19. Gaurav Luthria & Ran Li & Stephanie Wang & Mark Prytyskach & Rainer H. Kohler & Douglas A. Lauffenburger & Timothy J. Mitchison & Ralph Weissleder & Miles A. Miller, 2020. "In vivo microscopy reveals macrophage polarization locally promotes coherent microtubule dynamics in migrating cancer cells," Nature Communications, Nature, vol. 11(1), pages 1-17, December.
    20. Yuhang Zhang & Jingyi Du & Xian Liu & Fei Shang & Yunxin Deng & Jiaqing Ye & Yukai Wang & Jie Yan & Hu Chen & Miao Yu & Shimin Le, 2024. "Multi-domain interaction mediated strength-building in human α-actinin dimers unveiled by direct single-molecule quantification," Nature Communications, Nature, vol. 15(1), pages 1-17, 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:14:y:2023:i:1:d:10.1038_s41467-023-36875-5. 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.