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Photolipid Bilayer Permeability is Controlled by Transient Pore Formation

  • Stefanie D. Pritzl
    Stefanie D. Pritzl
    Chair for Photonics and Optoelectronics, Nano-Institute Munich, Department of Physics, Ludwig-Maximilians-Universität (LMU), Königinstraße 10, 80539 Munich, Germany
  • Patrick Urban
    Patrick Urban
    Chair for Photonics and Optoelectronics, Nano-Institute Munich, Department of Physics, Ludwig-Maximilians-Universität (LMU), Königinstraße 10, 80539 Munich, Germany
  • Alexander Prasselsperger
    Alexander Prasselsperger
    Chair for Photonics and Optoelectronics, Nano-Institute Munich, Department of Physics, Ludwig-Maximilians-Universität (LMU), Königinstraße 10, 80539 Munich, Germany
  • David B. Konrad
    David B. Konrad
    Department of Chemistry, Ludwig-Maximilians-Universität München, Butenandtstraße 5-13, 81377 Munich, Germany
    Department of Pharmacy, Ludwig-Maximilians-Universität München, Butenandtstraße 5-13, 81377 Munich, Germany
  • James A. Frank
    James A. Frank
    Vollum Institute, Oregon Health & Science University, 3181 SW Sam Jackson Park Road, Portland, Oregon 97239, United States
  • Dirk Trauner*
    Dirk Trauner
    Department of Chemistry, Ludwig-Maximilians-Universität München, Butenandtstraße 5-13, 81377 Munich, Germany
    Department of Chemistry, New York University, Silver Center, 100 Washington Square East, Room 712, New York 10003, United States
    *(D.T.) Email: [email protected]
    More by Dirk Trauner
  • , and 
  • Theobald Lohmüller*
    Theobald Lohmüller
    Chair for Photonics and Optoelectronics, Nano-Institute Munich, Department of Physics, Ludwig-Maximilians-Universität (LMU), Königinstraße 10, 80539 Munich, Germany
    *(T.L.) Email: [email protected]
Cite this: Langmuir 2020, 36, 45, 13509–13515
Publication Date (Web):November 3, 2020
https://doi.org/10.1021/acs.langmuir.0c02229
Copyright © 2020 American Chemical Society

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    Abstract

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    Controlling the release or uptake of (bio-) molecules and drugs from liposomes is critically important for a range of applications in bioengineering, synthetic biology, and drug delivery. In this paper, we report how the reversible photoswitching of synthetic lipid bilayer membranes made from azobenzene-containing phosphatidylcholine (azo-PC) molecules (photolipids) leads to increased membrane permeability. We show that cell-sized, giant unilamellar vesicles (GUVs) prepared from photolipids display leakage of fluorescent dyes after irradiation with UV-A and visible light. Langmuir–Blodgett and patch-clamp measurements show that the permeability is the result of transient pore formation. By comparing the trans-to-cis and cis-to-trans isomerization process, we find that this pore formation is the result of area fluctuations and a change of the area cross-section between both photolipid isomers.

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    Cited By

    This article is cited by 23 publications.

    1. Arash Manafirad, Cintia A. Menendez, Gustavo R. Perez-Lemus, S. Thayumanavan, Juan J. de Pablo, Anthony D. Dinsmore. Structural and Mechanical Response of Two-Component Photoswitchable Lipid Bilayer Vesicles. Langmuir 2023, 39 (45) , 15932-15941. https://doi.org/10.1021/acs.langmuir.3c01764
    2. Jie Hu, Di Wu, Qingqing Pan, Hanmei Li, Jing Zhang, Fang Geng. Recent Development of Photoresponsive Liposomes Based on Organic Photosensitizers, Au Nanoparticles, and Azobenzene Derivatives for Nanomedicine. ACS Applied Nano Materials 2022, 5 (10) , 14171-14190. https://doi.org/10.1021/acsanm.2c03167
    3. Stefanie D. Pritzl, Johannes Morstein, Sophia Kahler, David B. Konrad, Dirk Trauner, Theobald Lohmüller. Postsynthetic Photocontrol of Giant Liposomes via Fusion-Based Photolipid Doping. Langmuir 2022, 38 (39) , 11941-11949. https://doi.org/10.1021/acs.langmuir.2c01685
    4. Stefanie D. Pritzl, David B. Konrad, Martina F. Ober, Alexander F. Richter, James A. Frank, Bert Nickel, Dirk Trauner, Theobald Lohmüller. Optical Membrane Control with Red Light Enabled by Red-Shifted Photolipids. Langmuir 2022, 38 (1) , 385-393. https://doi.org/10.1021/acs.langmuir.1c02745
    5. 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
    6. Yusuf Qutbuddin, Ainoa Guinart, Svetozar Gavrilović, Kareem Al Nahas, Ben L. Feringa, Petra Schwille. Light‐Activated Synthetic Rotary Motors in Lipid Membranes Induce Shape Changes Through Membrane Expansion. Advanced Materials 2024, 6 https://doi.org/10.1002/adma.202311176
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    9. Larissa Socrier, Claudia Steinem. Photo‐Lipids: Light‐Sensitive Nano‐Switches to Control Membrane Properties. ChemPlusChem 2023, 88 (11) https://doi.org/10.1002/cplu.202300203
    10. Tiefan Huang, Zhixin Su, Kun Hou, Jianxian Zeng, Hu Zhou, Lin Zhang, Suzana P. Nunes. Advanced stimuli-responsive membranes for smart separation. Chemical Society Reviews 2023, 52 (13) , 4173-4207. https://doi.org/10.1039/D2CS00911K
    11. Nina Hartrampf, Samuel M. Leitao, Nils Winter, Henry Toombs-Ruane, James A. Frank, Petra Schwille, Dirk Trauner, Henri G. Franquelim. Structural diversity of photoswitchable sphingolipids for optodynamic control of lipid microdomains. Biophysical Journal 2023, 122 (11) , 2325-2341. https://doi.org/10.1016/j.bpj.2023.02.029
    12. Larissa Socrier, Somayeh Ahadi, Mathias Bosse, Cindy Montag, Daniel B. Werz, Claudia Steinem. Optical Manipulation of Gb 3 Enriched Lipid Domains: Impact of Isomerization on Gb 3 ‐Shiga Toxin B Interaction. Chemistry – A European Journal 2023, 29 (4) https://doi.org/10.1002/chem.202202766
    13. Hejian Xiong, Kevin A. Alberto, Jonghae Youn, Jaume Taura, Johannes Morstein, Xiuying Li, Yang Wang, Dirk Trauner, Paul A. Slesinger, Steven O. Nielsen, Zhenpeng Qin. Optical control of neuronal activities with photoswitchable nanovesicles. Nano Research 2023, 16 (1) , 1033-1041. https://doi.org/10.1007/s12274-022-4853-x
    14. Tristan Wegner, Ranjini Laskar, Frank Glorius. Lipid mimetics: A versatile toolbox for lipid biology and beyond. Current Opinion in Chemical Biology 2022, 71 , 102209. https://doi.org/10.1016/j.cbpa.2022.102209
    15. Paola Albanese, Simone Cataldini, Chloe Z.-J. Ren, Nadia Valletti, Jlenia Brunetti, Jack L.-Y. Chen, Federico Rossi. Light-Switchable Membrane Permeability in Giant Unilamellar Vesicles. Pharmaceutics 2022, 14 (12) , 2777. https://doi.org/10.3390/pharmaceutics14122777
    16. Miriam Di Martino, Lucia Sessa, Martina Di Matteo, Barbara Panunzi, Stefano Piotto, Simona Concilio. Azobenzene as Antimicrobial Molecules. Molecules 2022, 27 (17) , 5643. https://doi.org/10.3390/molecules27175643
    17. Shoupeng Cao, Lucas Caire da Silva, Katharina Landfester. Light‐Activated Membrane Transport in Polymeric Cell‐Mimics. Angewandte Chemie 2022, 134 (34) https://doi.org/10.1002/ange.202205266
    18. Shoupeng Cao, Lucas Caire da Silva, Katharina Landfester. Light‐Activated Membrane Transport in Polymeric Cell‐Mimics. Angewandte Chemie International Edition 2022, 61 (34) https://doi.org/10.1002/anie.202205266
    19. Fucsia Crea, Antreas Vorkas, Aoife Redlich, Rubén Cruz, Chaowei Shi, Dirk Trauner, Adam Lange, Ramona Schlesinger, Joachim Heberle. Photoactivation of a Mechanosensitive Channel. Frontiers in Molecular Biosciences 2022, 9 https://doi.org/10.3389/fmolb.2022.905306
    20. Federico Baserga, Antreas Vorkas, Fucsia Crea, Luiz Schubert, Jheng-Liang Chen, Aoife Redlich, Mariafrancesca La Greca, Julian Storm, Sabine Oldemeyer, Kirsten Hoffmann, Ramona Schlesinger, Joachim Heberle. Membrane Protein Activity Induces Specific Molecular Changes in Nanodiscs Monitored by FTIR Difference Spectroscopy. Frontiers in Molecular Biosciences 2022, 9 https://doi.org/10.3389/fmolb.2022.915328
    21. Martina F. Ober, Adrian Müller-Deku, Anna Baptist, Benjamin Ajanović, Heinz Amenitsch, Oliver Thorn-Seshold, Bert Nickel. SAXS measurements of azobenzene lipid vesicles reveal buffer-dependent photoswitching and quantitative Z→E isomerisation by X-rays. Nanophotonics 2022, 11 (10) , 2361-2368. https://doi.org/10.1515/nanoph-2022-0053
    22. Alexander Sailer, Joyce C. M. Meiring, Constanze Heise, Linda N. Pettersson, Anna Akhmanova, Julia Thorn‐Seshold, Oliver Thorn‐Seshold. Pyrrole Hemithioindigo Antimitotics with Near‐Quantitative Bidirectional Photoswitching that Photocontrol Cellular Microtubule Dynamics with Single‐Cell Precision**. Angewandte Chemie 2021, 133 (44) , 23888-23897. https://doi.org/10.1002/ange.202104794
    23. Alexander Sailer, Joyce C. M. Meiring, Constanze Heise, Linda N. Pettersson, Anna Akhmanova, Julia Thorn‐Seshold, Oliver Thorn‐Seshold. Pyrrole Hemithioindigo Antimitotics with Near‐Quantitative Bidirectional Photoswitching that Photocontrol Cellular Microtubule Dynamics with Single‐Cell Precision**. Angewandte Chemie International Edition 2021, 60 (44) , 23695-23704. https://doi.org/10.1002/anie.202104794

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