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Structure and Composition of Native Membrane Derived Polymer-Supported Lipid Bilayers

  • Hudson P. Pace*
    Hudson P. Pace
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
    *E-mail: [email protected] (H.P.P.)
  • Jonas K. Hannestad
    Jonas K. Hannestad
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
    Biosciences and Materials, Research Institutes of Sweden, SE-501 15 Borås, Sweden
  • Antonious Armonious
    Antonious Armonious
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
  • Marco Adamo
    Marco Adamo
    Institute Laue-Langevin, 38000 Grenoble, France
    Department of Chemical Engineering, Imperial College London, London SW7 2AZ, United Kingdom
    More by Marco Adamo
  • Bjorn Agnarsson
    Bjorn Agnarsson
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
  • Anders Gunnarsson
    Anders Gunnarsson
    Discovery Sciences, IMED Biotech Unit, AstraZeneca, Gothenburg, Sweden
  • Samantha Micciulla
    Samantha Micciulla
    Institute Laue-Langevin, 38000 Grenoble, France
    Max Planck Institute of Colloids and Interfaces, 14476 Potsdam, Germany
  • Peter Sjövall
    Peter Sjövall
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
    Biosciences and Materials, Research Institutes of Sweden, SE-501 15 Borås, Sweden
  • Yuri Gerelli
    Yuri Gerelli
    Institute Laue-Langevin, 38000 Grenoble, France
    More by Yuri Gerelli
  • , and 
  • Fredrik Höök*
    Fredrik Höök
    Department of Physics, Chalmers University of Technology, SE-412 96 Göteborg, Sweden
    *E-mail: [email protected] (F.H.)
Cite this: Anal. Chem. 2018, 90, 21, 13065–13072
Publication Date (Web):October 15, 2018
https://doi.org/10.1021/acs.analchem.8b04110
Copyright © 2018 American Chemical Society

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    Abstract

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    Over the last two decades, supported lipid bilayers (SLBs) have been extensively used as model systems to study cell membrane structure and function. While SLBs have been traditionally produced from simple lipid mixtures, there has been a recent surge in compositional complexity to better mimic cellular membranes and thereby bridge the gap between classic biophysical approaches and cell experiments. To this end, native cellular membrane derived SLBs (nSLBs) have emerged as a new category of SLBs. As a new type of biomimetic material, an analytical workflow must be designed to characterize its molecular composition and structure. Herein, we demonstrate how a combination of fluorescence microscopy, neutron reflectometry, and secondary ion mass spectrometry offers new insights on structure, composition, and quality of nSLB systems formed using so-called hybrid vesicles, which are a mixture of native membrane material and synthetic lipids. With this approach, we demonstrate that the nSLB formed a continuous structure with complete mixing of the synthetic and native membrane components and a molecular stoichiometry that essentially mirrors that of the hybrid vesicles. Furthermore, structural investigation of the nSLB revealed that PEGylated lipids do not significantly thicken the hydration layer between the bilayer and substrate when on silicon substrates; however, nSLBs do have more topology than their simpler, purely synthetic counterparts. Beyond new insights regarding the structure and composition of nSLB systems, this work also serves to guide future researchers in producing and characterizing nSLBs from their cellular membrane of choice.

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    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.analchem.8b04110.

    • Additional information about how the SANS data was collected and used to calculate the percentage of NMV material in the nSLB in combination with the NR data is provided (PDF)

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    Cited By

    This article is cited by 18 publications.

    1. Manorama Dey, Anurag Sharma, Garvita Dhanawat, Divya Gupta, Krishnan H. Harshan, Nagma Parveen. Synergistic Binding of SARS-CoV-2 to ACE2 and Gangliosides in Native Lipid Membranes. ACS Infectious Diseases 2024, 10 (3) , 907-916. https://doi.org/10.1021/acsinfecdis.3c00519
    2. David J. H. Cant, Yiwen Pei, Andrey Shchukarev, Madeleine Ramstedt, Sara S. Marques, Marcela A. Segundo, Jeremie Parot, Alicja Molska, Sven E. Borgos, Alexander G. Shard, Caterina Minelli. Cryo-XPS for Surface Characterization of Nanomedicines. The Journal of Physical Chemistry A 2023, 127 (39) , 8220-8227. https://doi.org/10.1021/acs.jpca.3c03879
    3. Geetanjali Negi, Anurag Sharma, Monika Chaudhary, Divya Gupta, Krishnan H. Harshan, Nagma Parveen. SARS-CoV-2 Binding to Terminal Sialic Acid of Gangliosides Embedded in Lipid Membranes. ACS Infectious Diseases 2023, 9 (7) , 1346-1361. https://doi.org/10.1021/acsinfecdis.3c00106
    4. Antonius Armanious, Yuri Gerelli, Samantha Micciulla, Hudson P. Pace, Rebecca J. L. Welbourn, Mattias Sjöberg, Björn Agnarsson, Fredrik Höök. Probing the Separation Distance between Biological Nanoparticles and Cell Membrane Mimics Using Neutron Reflectometry with Sub-Nanometer Accuracy. Journal of the American Chemical Society 2022, 144 (45) , 20726-20738. https://doi.org/10.1021/jacs.2c08456
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    6. Alessandra Luchini, Frederik Grønbæk Tidemand, Nicolai Tidemand Johansen, Mario Campana, Javier Sotres, Michael Ploug, Marité Cárdenas, Lise Arleth. Peptide Disc Mediated Control of Membrane Protein Orientation in Supported Lipid Bilayers for Surface-Sensitive Investigations. Analytical Chemistry 2020, 92 (1) , 1081-1088. https://doi.org/10.1021/acs.analchem.9b04125
    7. Wai Cheng Wong, Jz-Yuan Juo, Chih-Hsiang Lin, Yi-Hung Liao, Ching-Ya Cheng, Chia-Lung Hsieh. Characterization of Single-Protein Dynamics in Polymer-Cushioned Lipid Bilayers Derived from Cell Plasma Membranes. The Journal of Physical Chemistry B 2019, 123 (30) , 6492-6504. https://doi.org/10.1021/acs.jpcb.9b03789
    8. Jinhua Zhang, Francis Schuknecht, Ludwig Habermann, Alexander Pattis, Jonathan Heine, Stefanie D. Pritzl, Dirk Trauner, Theobald Lohmüller. Label‐Free Time‐Resolved Monitoring of Photolipid Bilayer Isomerization by Plasmonic Sensing. Advanced Optical Materials 2024, 12 https://doi.org/10.1002/adom.202302266
    9. Minkwon Cha, Sang Hyeok Jeong, Jaehun Jung, Yoonjin Baeg, Sung‐Soo Park, Seoyoon Bae, Chan Seok Lim, Jun Hyuk Park, Jie‐Oh Lee, Yong Song Gho, Seung Wook Oh, Min Ju Shon. Quantitative imaging of vesicle–protein interactions reveals close cooperation among proteins. Journal of Extracellular Vesicles 2023, 12 (5) https://doi.org/10.1002/jev2.12322
    10. Jiaqian Zhao, Chengcheng Wang, Xinran Zhang, Junmin Li, Yuqiao Liu, Xinyu Pan, Ling Zhu, Dajing Chen, Tian Xie. Cell membrane coated electrochemical sensor for kinetic measurements of GLUT transport. Analytica Chimica Acta 2022, 1226 , 340263. https://doi.org/10.1016/j.aca.2022.340263
    11. Marta Bally, Stephan Block, Fredrik Höök, Göran Larson, Nagma Parveen, Gustaf E. Rydell. Physicochemical tools for studying virus interactions with targeted cell membranes in a molecular and spatiotemporally resolved context. Analytical and Bioanalytical Chemistry 2021, 413 (29) , 7157-7178. https://doi.org/10.1007/s00216-021-03510-5
    12. Paul Joyce, Silver Jõemetsa, Simon Isaksson, Shakhawath Hossain, Per Larsson, Christel Bergström, Fredrik Höök. TIRF Microscopy‐Based Monitoring of Drug Permeation Across a Lipid Membrane Supported on Mesoporous Silica. Angewandte Chemie 2021, 133 (4) , 2097-2101. https://doi.org/10.1002/ange.202011931
    13. Paul Joyce, Silver Jõemetsa, Simon Isaksson, Shakhawath Hossain, Per Larsson, Christel Bergström, Fredrik Höök. TIRF Microscopy‐Based Monitoring of Drug Permeation Across a Lipid Membrane Supported on Mesoporous Silica. Angewandte Chemie International Edition 2021, 60 (4) , 2069-2073. https://doi.org/10.1002/anie.202011931
    14. Paul Joyce, Hanna Ulmefors, Sajedeh Maghrebi, Santhni Subramaniam, Anthony Wignall, Silver Jõemetsa, Fredrik Höök, Clive A. Prestidge. Enhancing the Cellular Uptake and Antibacterial Activity of Rifampicin through Encapsulation in Mesoporous Silica Nanoparticles. Nanomaterials 2020, 10 (4) , 815. https://doi.org/10.3390/nano10040815
    15. Xingyu Chen, Jianshu Li. Bioinspired by cell membranes: functional polymeric materials for biomedical applications. Materials Chemistry Frontiers 2020, 4 (3) , 750-774. https://doi.org/10.1039/C9QM00717B
    16. Jeremy H. Lakey. Recent advances in neutron reflectivity studies of biological membranes. Current Opinion in Colloid & Interface Science 2019, 42 , 33-40. https://doi.org/10.1016/j.cocis.2019.02.012
    17. Abdul Rahim Ferhan, Bo Kyeong Yoon, Soohyun Park, Tun Naw Sut, Hokyun Chin, Jae Hyeon Park, Joshua A. Jackman, Nam-Joon Cho. Solvent-assisted preparation of supported lipid bilayers. Nature Protocols 2019, 14 (7) , 2091-2118. https://doi.org/10.1038/s41596-019-0174-2
    18. Burkhard Bechinger. Supported Lipid Bilayers. 2019, 1-8. https://doi.org/10.1007/978-3-642-35943-9_566-1

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