ACS Publications. Most Trusted. Most Cited. Most Read
Highly Polyvalent DNA Motors Generate 100+ pN of Force via Autochemophoresis

OR SEARCH CITATIONS

My Activity
Publications

Figure 1Loading Img
Download Hi-Res ImageDownload to MS-PowerPointCite This:Nano Lett. 2019, 19, 10, 6977-6986
    Letter

    Highly Polyvalent DNA Motors Generate 100+ pN of Force via Autochemophoresis
    Click to copy article linkArticle link copied!

    • Aaron T. Blanchard
      Aaron T. Blanchard
      Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia 30322, United States
      More by Aaron T. Blanchard
    • Alisina S. Bazrafshan
      Alisina S. Bazrafshan
      Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
      More by Alisina S. Bazrafshan
    • Jacob Yi
      Jacob Yi
      Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
      More by Jacob Yi
    • Julia T. Eisman
      Julia T. Eisman
      Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
      More by Julia T. Eisman
    • Kevin M. Yehl
      Kevin M. Yehl
      Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
      More by Kevin M. Yehl
    • Teng Bian
      Teng Bian
      Department of Physics, Purdue University, West Lafayette, Indiana 47907, United States
      More by Teng Bian
    • Andrew Mugler
      Andrew Mugler
      Department of Physics, Purdue University, West Lafayette, Indiana 47907, United States
      More by Andrew Mugler
    • Khalid Salaita*
      Khalid Salaita
      Wallace H. Coulter Department of Biomedical Engineering, Georgia Institute of Technology and Emory University, Atlanta, Georgia 30322, United States
      Department of Chemistry, Emory University, Atlanta, Georgia 30322, United States
      *E-mail: [email protected]
      More by Khalid Salaita
      Orcidhttp://orcid.org/0000-0003-4138-3477
    Other Access OptionsSupporting Information (1)

    Nano Letters

    Cite this: Nano Lett. 2019, 19, 10, 6977–6986
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.nanolett.9b02311
    Published August 11, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Abstract

    Click to copy section linkSection link copied!
    Abstract Image

    Motor proteins such as myosin, kinesin, and dynein are essential to eukaryotic life and power countless processes including muscle contraction, wound closure, cargo transport, and cell division. The design of synthetic nanomachines that can reproduce the functions of these motors is a longstanding goal in the field of nanotechnology. DNA walkers, which are programmed to “walk” along defined tracks via the burnt bridge Brownian ratchet mechanism, are among the most promising synthetic mimics of these motor proteins. While these DNA-based motors can perform useful tasks such as cargo transport, they have not been shown to be capable of cooperating to generate large collective forces for tasks akin to muscle contraction. In this work, we demonstrate that highly polyvalent DNA motors (HPDMs), which can be viewed as cooperative teams of thousands of DNA walkers attached to a microsphere, can generate and sustain substantial forces in the 100+ pN regime. Specifically, we show that HPDMs can generate forces that can unzip and shear DNA duplexes (∼12 and ∼50 pN, respectively) and rupture biotin–streptavidin bonds (∼100–150 pN). To help explain these results, we present a variant of the burnt-bridge Brownian ratchet mechanism that we term autochemophoresis, wherein many individual force generating units generate a self-propagating chemomechanical gradient that produces large collective forces. In addition, we demonstrate the potential of this work to impact future engineering applications by harnessing HPDM autochemophoresis to deposit “molecular ink” via mechanical bond rupture. This work expands the capabilities of synthetic DNA motors to mimic the force-generating functions of biological motors. Our work also builds upon previous observations of autochemophoresis in bacterial transport processes, indicating that autochemophoresis may be a fundamental mechanism of pN-scale force generation in living systems.

    Copyright © 2019 American Chemical Society

    Subjects

    what are subjects

    Keywords

    what are keywords

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. Add or change your institution or let them know you’d like them to include access.

    Supporting Information

    Click to copy section linkSection link copied!

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.nanolett.9b02311.

    • Experimental and computational methods and supplemental figures, notes, and table (PDF)

    Terms & Conditions

    Most electronic Supporting Information files are available without a subscription to ACS Web Editions. Such files may be downloaded by article for research use (if there is a public use license linked to the relevant article, that license may permit other uses). Permission may be obtained from ACS for other uses through requests via the RightsLink permission system: http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    Click to copy section linkSection link copied!
    Citation Statements
    Explore this article's citation statements on scite.ai
    powered by  Scite

    This article is cited by 43 publications.

    1. Selma Piranej, Hiroaki Ogasawara, Luona Zhang, Krista Jackson, Alisina Bazrafshan, Khalid Salaita. On-Demand Photoactivation of DNA-Based Motor Motion. ACS Nano 2025, 19 (5) , 5363-5375. https://doi.org/10.1021/acsnano.4c13068
    2. Longjiang Ding, Na Liu. Rolling on the Chip: SARS-CoV-2 Detection by DNA Motors. ACS Central Science 2024, 10 (7) , 1311-1313. https://doi.org/10.1021/acscentsci.4c00940
    3. Selma Piranej, Luona Zhang, Alisina Bazrafshan, Mariana Marin, Gregory B. Melikian, Khalid Salaita. Rolosense: Mechanical Detection of SARS-CoV-2 Using a DNA-Based Motor. ACS Central Science 2024, 10 (7) , 1332-1347. https://doi.org/10.1021/acscentsci.4c00312
    4. Chan Li, Guohui Xue, Rong Wu, Jing Zhang, Yinghao Cheng, Guoqiao Huang, Huo Xu, Qiufeng Song, Ruize Cheng, Zhifa Shen, Chang Xue. Lighting up Lipidic Nanoflares with Self-Powered and Multivalent 3D DNA Rolling Motors for High-Efficiency MicroRNA Sensing in Serum and Living Cells. ACS Applied Materials & Interfaces 2024, 16 (1) , 281-291. https://doi.org/10.1021/acsami.3c14718
    5. Aaron T. Blanchard, Selma Piranej, Victor Pan, Khalid Salaita. Adhesive Dynamics Simulations of Highly Polyvalent DNA Motors. The Journal of Physical Chemistry B 2022, 126 (39) , 7495-7509. https://doi.org/10.1021/acs.jpcb.2c01897
    6. Ivan N. Unksov, Chapin S. Korosec, Pradheebha Surendiran, Damiano Verardo, Roman Lyttleton, Nancy R. Forde, Heiner Linke. Through the Eyes of Creators: Observing Artificial Molecular Motors. ACS Nanoscience Au 2022, 2 (3) , 140-159. https://doi.org/10.1021/acsnanoscienceau.1c00041
    7. Xianyi Cheng, Yaofei Bao, Shuo Liang, Bo Li, Yunlong Liu, Haiping Wu, Xueping Ma, Yanan Chu, Yang Shao, Qi Meng, Guohua Zhou, Qinxin Song, Bingjie Zou. Flap Endonuclease 1-Assisted DNA Walkers for Sensitively and Specifically Sensing ctDNAs. Analytical Chemistry 2021, 93 (27) , 9593-9601. https://doi.org/10.1021/acs.analchem.1c01765
    8. Alisina Bazrafshan, Maria-Eleni Kyriazi, Brandon Alexander Holt, Wenxiao Deng, Selma Piranej, Hanquan Su, Yuesong Hu, Afaf H. El-Sagheer, Tom Brown, Gabriel A. Kwong, Antonios G. Kanaras, Khalid Salaita. DNA Gold Nanoparticle Motors Demonstrate Processive Motion with Bursts of Speed Up to 50 nm Per Second. ACS Nano 2021, 15 (5) , 8427-8438. https://doi.org/10.1021/acsnano.0c10658
    9. Yancheng Du, Jing Pan, Hengming Qiu, Chengde Mao, Jong Hyun Choi. Mechanistic Understanding of Surface Migration Dynamics with DNA Walkers. The Journal of Physical Chemistry B 2021, 125 (2) , 507-517. https://doi.org/10.1021/acs.jpcb.0c09048
    10. Brendan R. Deal, Rong Ma, Victor Pui-Yan Ma, Hanquan Su, James T. Kindt, Khalid Salaita. Engineering DNA-Functionalized Nanostructures to Bind Nucleic Acid Targets Heteromultivalently with Enhanced Avidity. Journal of the American Chemical Society 2020, 142 (21) , 9653-9660. https://doi.org/10.1021/jacs.0c01568
    11. Takanori Harashima, Akihiro Otomo, Ryota Iino. Rational engineering of DNA-nanoparticle motor with high speed and processivity comparable to motor proteins. Nature Communications 2025, 16 (1) https://doi.org/10.1038/s41467-025-56036-0
    12. Chapin S. Korosec, Ivan N. Unksov, Pradheebha Surendiran, Roman Lyttleton, Paul M. G. Curmi, Christopher N. Angstmann, Ralf Eichhorn, Heiner Linke, Nancy R. Forde. Motility of an autonomous protein-based artificial motor that operates via a burnt-bridge principle. Nature Communications 2024, 15 (1) https://doi.org/10.1038/s41467-024-45570-y
    13. Zheng Jiao, Lijuan Gao, Xueqing Jin, Jiaqi Li, Yuming Wang, Wenlong Chen, Li‐Tang Yan. Nonequilibrium Dynamics at Cellular Interfaces: Insights From Simulation and Theory. WIREs Computational Molecular Science 2024, 14 (6) https://doi.org/10.1002/wcms.1736
    14. Chun Xie, Kuiting Chen, Zhekun Chen, Yingxin Hu, Linqiang Pan. A Chemo‐Mechanically Coupled DNA Origami Clamp Capable of Generating Robust Compression Forces. Small 2024, 20 (42) https://doi.org/10.1002/smll.202401396
    15. Chunran Ma, Shiquan Li, Yuqi Zeng, Yifan Lyu. DNA-Based Molecular Machines: Controlling Mechanisms and Biosensing Applications. Biosensors 2024, 14 (5) , 236. https://doi.org/10.3390/bios14050236
    16. Kenta I. Ito, Yusuke Sato, Shoichi Toyabe. Design of artificial molecular motor inheriting directionality and scalability. Biophysical Journal 2024, 123 (7) , 858-866. https://doi.org/10.1016/j.bpj.2024.02.026
    17. Luona Zhang, Selma Piranej, Arshiya Namazi, Steven Narum, Khalid Salaita. “Turbo‐Charged” DNA Motors with Optimized Sequence Enable Single‐Molecule Nucleic Acid Sensing. Angewandte Chemie International Edition 2024, 63 (13) https://doi.org/10.1002/anie.202316851
    18. Luona Zhang, Selma Piranej, Arshiya Namazi, Steven Narum, Khalid Salaita. “Turbo‐Charged” DNA Motors with Optimized Sequence Enable Single‐Molecule Nucleic Acid Sensing. Angewandte Chemie 2024, 136 (13) https://doi.org/10.1002/ange.202316851
    19. Kevin Jahnke, Kerstin Göpfrich. Engineering DNA-based cytoskeletons for synthetic cells. Interface Focus 2023, 13 (5) https://doi.org/10.1098/rsfs.2023.0028
    20. Jorge Manrique Castro, Frank Sommerhage, Rishika Khanna, Andre Childs, David DeRoo, Swaminathan Rajaraman. High-throughput microbead assay system with a portable, cost-effective Wi-Fi imaging module, and disposable multi-layered microfluidic cartridges for virus and microparticle detection, and tracking. Biomedical Microdevices 2023, 25 (3) https://doi.org/10.1007/s10544-023-00661-3
    21. Ruixin Li, Anirudh S. Madhvacharyula, Yancheng Du, Harshith K. Adepu, Jong Hyun Choi. Mechanics of dynamic and deformable DNA nanostructures. Chemical Science 2023, 14 (30) , 8018-8046. https://doi.org/10.1039/D3SC01793A
    22. Laurie Stevens, Sophie de Buyl, Bortolo Matteo Mognetti. The sliding motility of the bacilliform virions of Influenza A viruses. Soft Matter 2023, 19 (24) , 4491-4501. https://doi.org/10.1039/D3SM00371J
    23. 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. A modular spring-loaded actuator for mechanical activation of membrane proteins. Nature Communications 2022, 13 (1) https://doi.org/10.1038/s41467-022-30745-2
    24. Takeshi Sugawara, Kunihiko Kaneko, . Chemophoresis engine: A general mechanism of ATPase-driven cargo transport. PLOS Computational Biology 2022, 18 (7) , e1010324. https://doi.org/10.1371/journal.pcbi.1010324
    25. Mark Rempel, Eldon Emberly. Optimizing Efficiency and Motility of a Polyvalent Molecular Motor. Micromachines 2022, 13 (6) , 914. https://doi.org/10.3390/mi13060914
    26. Selma Piranej, Alisina Bazrafshan, Khalid Salaita. Chemical-to-mechanical molecular computation using DNA-based motors with onboard logic. Nature Nanotechnology 2022, 17 (5) , 514-523. https://doi.org/10.1038/s41565-022-01080-w
    27. Pedro A. Soria Ruiz, Falko Ziebert, Igor M. Kulić. Physics of self-rolling viruses. Physical Review E 2022, 105 (5) https://doi.org/10.1103/PhysRevE.105.054411
    28. Aaron Blanchard, J. Dale Combs, Joshua M. Brockman, Anna V. Kellner, Roxanne Glazier, Hanquan Su, Rachel L. Bender, Alisina S. Bazrafshan, Wenchun Chen, M. Edward Quach, Renhao Li, Alexa L. Mattheyses, Khalid Salaita. Turn-key mapping of cell receptor force orientation and magnitude using a commercial structured illumination microscope. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-021-24602-x
    29. Qunye He, Yanfei Liu, Ke Li, Yuwei Wu, Ting Wang, Yifu Tan, Ting Jiang, Xiaoqin Liu, Zhenbao Liu. Deoxyribonucleic acid anchored on cell membranes for biomedical application. Biomaterials Science 2021, 9 (20) , 6691-6717. https://doi.org/10.1039/D1BM01057C
    30. Aaron T. Blanchard. Burnt bridge ratchet motor force scales linearly with polyvalency: a computational study. Soft Matter 2021, 17 (25) , 6056-6062. https://doi.org/10.1039/D1SM00676B
    31. Aaron T Blanchard, Khalid Salaita. Multivalent molecular tension probes as anisotropic mechanosensors: concept and simulation. Physical Biology 2021, 18 (3) , 034001. https://doi.org/10.1088/1478-3975/abd333
    32. Falko Ziebert, Igor M. Kulić. How Influenza’s Spike Motor Works. Physical Review Letters 2021, 126 (21) https://doi.org/10.1103/PhysRevLett.126.218101
    33. David Arredondo, Matthew R. Lakin, Darko Stefanovic, Milan N. Stojanovic. Development and Application of Catalytic DNA in Nanoscale Robotics. 2021, 293-306. https://doi.org/10.1002/9783527825424.ch15
    34. Chapin S. Korosec, Lavisha Jindal, Mathew Schneider, Ignacio Calderon de la Barca, Martin J. Zuckermann, Nancy R. Forde, Eldon Emberly. Substrate stiffness tunes the dynamics of polyvalent rolling motors. Soft Matter 2021, 17 (6) , 1468-1479. https://doi.org/10.1039/D0SM01811B
    35. Heeyuen Koh, Jae Gyung Lee, Jae Young Lee, Ryan Kim, Osamu Tabata, Jin-Woo Kim, DO-Nyun Kim. Design Approaches and Computational Tools for DNA Nanostructures. IEEE Open Journal of Nanotechnology 2021, 2 , 86-100. https://doi.org/10.1109/OJNANO.2021.3119913
    36. Ying Tu, Xuefeng Wang. Recent Advances in Cell Adhesive Force Microscopy. Sensors 2020, 20 (24) , 7128. https://doi.org/10.3390/s20247128
    37. Julián Valero, Marko Škugor. Mechanisms, Methods of Tracking and Applications of DNA Walkers: A Review. ChemPhysChem 2020, 21 (17) , 1971-1988. https://doi.org/10.1002/cphc.202000235
    38. Chapin S. Korosec, David A. Sivak, Nancy R. Forde. Apparent superballistic dynamics in one-dimensional random walks with biased detachment. Physical Review Research 2020, 2 (3) https://doi.org/10.1103/PhysRevResearch.2.033520
    39. Alisina Bazrafshan, Travis A. Meyer, Hanquan Su, Joshua M. Brockman, Aaron T. Blanchard, Selma Piranej, Yuxin Duan, Yonggang Ke, Khalid Salaita. Tunable DNA Origami Motors Translocate Ballistically Over μm Distances at nm/s Speeds. Angewandte Chemie 2020, 132 (24) , 9601-9608. https://doi.org/10.1002/ange.201916281
    40. Alisina Bazrafshan, Travis A. Meyer, Hanquan Su, Joshua M. Brockman, Aaron T. Blanchard, Selma Piranej, Yuxin Duan, Yonggang Ke, Khalid Salaita. Tunable DNA Origami Motors Translocate Ballistically Over μm Distances at nm/s Speeds. Angewandte Chemie International Edition 2020, 59 (24) , 9514-9521. https://doi.org/10.1002/anie.201916281
    41. David Arredondo, Darko Stefanovic. Effect of polyvalency on tethered molecular walkers on independent one-dimensional tracks. Physical Review E 2020, 101 (6) https://doi.org/10.1103/PhysRevE.101.062101
    42. Aaron T. Blanchard, Joshua M. Brockman, Khalid Salaita, Alexa L. Mattheyses. Variable incidence angle linear dichroism (VALiD): a technique for unique 3D orientation measurement of fluorescent ensembles. Optics Express 2020, 28 (7) , 10039. https://doi.org/10.1364/OE.381676
    43. P. H. (Erik) Hamming, Nico J. Overeem, Jurriaan Huskens. Correction: Influenza as a molecular walker. Chemical Science 2020, 11 (9) , 2567-2567. https://doi.org/10.1039/D0SC90015J
    Download PDF
    Go to Nano Letters
    Get e-Alerts
    Get e-Alerts

    Nano Letters

    Cite this: Nano Lett. 2019, 19, 10, 6977–6986
    Click to copy citationCitation copied!
    https://doi.org/10.1021/acs.nanolett.9b02311
    Published August 11, 2019
    Copyright © 2019 American Chemical Society
    Request reuse permissions

    Article Views

    2094

    Altmetric

    -

    Citations

    43
    Learn about these metrics

    Article Views are the COUNTER-compliant sum of full text article downloads since November 2008 (both PDF and HTML) across all institutions and individuals. These metrics are regularly updated to reflect usage leading up to the last few days.

    Citations are the number of other articles citing this article, calculated by Crossref and updated daily. Find more information about Crossref citation counts.

    The Altmetric Attention Score is a quantitative measure of the attention that a research article has received online. Clicking on the donut icon will load a page at altmetric.com with additional details about the score and the social media presence for the given article. Find more information on the Altmetric Attention Score and how the score is calculated.