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Membrane Remodeling by DNA Origami Nanorods: Experiments Exploring the Parameter Space for Vesicle Remodeling

  • Sarah E. Zuraw-Weston
    Sarah E. Zuraw-Weston
    Department of Physics, University of Massachusetts Amherst, Hasbrouck Lab, 666 North Pleasant Street, Amherst, Massachusetts 01002, United States
  • Mahsa Siavashpouri
    Mahsa Siavashpouri
    Department of Physics, Brandeis University, Abelson-Bass-Yalem, 415 South Street, Waltham, Massachusetts 02454, United States
  • Maria E. Moustaka
    Maria E. Moustaka
    Department of Physics, Brandeis University, Abelson-Bass-Yalem, 415 South Street, Waltham, Massachusetts 02454, United States
  • Thomas Gerling
    Thomas Gerling
    Department of Physics, Technical University of Munich, James-Franck-Str., 1, Garching D-85748, Germany
  • Hendrik Dietz
    Hendrik Dietz
    Department of Physics, Technical University of Munich, James-Franck-Str., 1, Garching D-85748, Germany
  • Seth Fraden
    Seth Fraden
    Department of Physics, Brandeis University, Abelson-Bass-Yalem, 415 South Street, Waltham, Massachusetts 02454, United States
    More by Seth Fraden
  • Alexander E. Ribbe
    Alexander E. Ribbe
    Department of Polymer Science and Engineering, Silvio O. Conte National Center for Polymer Research, University of Massachusetts Amherst, 120 Governors Drive, Amherst, Massachusetts 01003, United States
  • , and 
  • Anthony D. Dinsmore*
    Anthony D. Dinsmore
    Department of Physics, University of Massachusetts Amherst, Hasbrouck Lab, 666 North Pleasant Street, Amherst, Massachusetts 01002, United States
    *Email: [email protected]
Cite this: Langmuir 2021, 37, 20, 6219–6231
Publication Date (Web):May 13, 2021
https://doi.org/10.1021/acs.langmuir.1c00416
Copyright © 2021 American Chemical Society

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    Abstract

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    Inspired by the ability of cell membranes to alter their shape in response to bound particles, we report an experimental study of long, slender nanorods binding to lipid bilayer vesicles and altering the membrane shape. Our work illuminates the role of particle concentration, adhesion strength, and membrane tension in determining the membrane morphology. We combined giant unilamellar vesicles with oppositely charged nanorods, carefully tuning the adhesion strength, membrane tension, and particle concentration. With increasing adhesion strength, the primary behaviors observed were membrane deformation, vesicle–vesicle adhesion, and vesicle rupture. These behaviors were observed in well-defined regions in the parameter space with sharp transitions between them. We observed the deformation of the membrane resulting in tubulation, textured surfaces, and small and large lipid–particle aggregates. These responses are robust and repeatable and provide a new physical understanding of the dependence on the shape, binding affinity, and particle concentration in membrane remodeling. The design principles derived from these experiments may lead to new bioinspired membrane-based materials.

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    Supporting Information

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    The Supporting Information is available free of charge at https://pubs.acs.org/doi/10.1021/acs.langmuir.1c00416.

    • Optical images of specific morphologies and time sequences; a more detailed state diagram; analysis of rod configurations seen in cryo-TEM images; illustration of the proposed aster structure; schematic of the sample cells used; and details of our continuum model for wrapping rods (PDF)

    • Confocal micrographs of three vesicles in the DXR regime shrinking down and being destroyed; x = 60%, crod = 10 nM (AVI)

    • Confocal images of two vesicles in the DXR regime that experience a sudden drop in their size before beginning to shrink and finally being destroyed; x =60%, crod = 10 nM (AVI)

    • Bright-field time lapse of a single vesicle in the DXR regime as it shrinks and is destroyed; x = 30%, crod = 1.5 nM (AVI)

    • Bright-field time lapse video of a vesicle in the DXX regime with textured surface; x = 0, crod = 1.5 nM (AVI)

    • Vesicle in the DXR regime with x = 10 mol % DOTAP combined with nanorods with crod = 10 nM concentration, showing large mobile spots (AVI)

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    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

    This article is cited by 5 publications.

    1. Stijn van der Ham, Jaime Agudo-Canalejo, Hanumantha Rao Vutukuri. Role of Shape in Particle-Lipid Membrane Interactions: From Surfing to Full Engulfment. ACS Nano 2024, 18 (15) , 10407-10416. https://doi.org/10.1021/acsnano.3c11106
    2. Kevin Jahnke, Kerstin Göpfrich. Engineering DNA-based cytoskeletons for synthetic cells. Interface Focus 2023, 13 (5) https://doi.org/10.1098/rsfs.2023.0028
    3. Satoshi Murata, Taro Toyota, Shin‐ichiro M. Nomura, Takashi Nakakuki, Akinori Kuzuya. Molecular Cybernetics: Challenges toward Cellular Chemical Artificial Intelligence. Advanced Functional Materials 2022, 32 (37) https://doi.org/10.1002/adfm.202201866
    4. Akinori Kuzuya. DNA Origami for Molecular Robotics. 2022, 297-304. https://doi.org/10.1002/9781119682561.ch14
    5. Alena Khmelinskaia, Henri G. Franquelim, Renukka Yaadav, Eugene P. Petrov, Petra Schwille. Membrane‐Mediated Self‐Organization of Rod‐Like DNA Origami on Supported Lipid Bilayers. Advanced Materials Interfaces 2021, 8 (24) https://doi.org/10.1002/admi.202101094

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