ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES
RETURN TO ISSUEPREVResearch ArticleNEXT

Measuring Lipid Asymmetry in Planar Supported Bilayers by Fluorescence Interference Contrast Microscopy

View Author Information
Department of Molecular Physiology and Biological Physics, University of Virginia, Charlottesville, Virginia 22908-0736
Cite this: Langmuir 2005, 21, 4, 1377–1388
Publication Date (Web):January 15, 2005
https://doi.org/10.1021/la047654w
Copyright © 2005 American Chemical Society

    Article Views

    1447

    Altmetric

    -

    Citations

    121
    LEARN ABOUT THESE METRICS
    Other access options

    Abstract

    Abstract Image

    There is substantial scientific and practical interest in engineering supported lipid bilayers with asymmetric lipid distributions as models for biological cell membranes. In principle, it should be possible to make asymmetric supported lipid bilayers by either the Langmuir−Blodgett/Schäfer (LB/LS) or Langmuir−Blodgett/vesicle fusion (LB/VF) techniques (Kalb et al. Biochim. Biophys. Acta1992, 1103, 307−316). However, the retention of asymmetry in biologically relevant lipid bilayers has never been experimentally examined in any of these systems. In the present work, we developed a technique that is based on fluorescence interference contrast (FLIC) microscopy to measure lipid asymmetry in supported bilayers. We compared the final degree of lipid asymmetry in LB/LS and LB/VF bilayers with and without cholesterol in liquid-ordered (lo) and liquid-disordered (ld) phases. Of five different fluorescent lipid probes that were examined, 1,2-dipalmitoyl-phosphatidylethanolamine-N-[lissamine rhodamine B] was the best for studying supported bilayers of complex composition and phase by FLIC microscopy. An asymmetrically labeled bilayer made by the LB/LS method was found to be at best 70−80% asymmetric once completed. In LB/LS bilayers of either lo or ld phase, cholesterol increased the degree of lipid mixing between the opposing monolayers. The use of a tethered polymer support for the initial monolayer did not improve lipid asymmetry in the resulting bilayer. However, asymmetric LB/VF bilayers retained nearly 100% asymmetric label, with or without the use of a tethered polymer support. Finally, lipid mixing across the center of LB/LS bilayers was found to have drastic effects on the appearance of ldlo phase coexistence as shown by epifluorescence microscopy.

    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. You can change your affiliated institution below.

    *

     To whom correspondence should be addressed. E-mail:  [email protected]. Tel:  (434) 982-3578. Fax:  (434) 982-1616.

    Cited By

    This article is cited by 121 publications.

    1. Min-Kang Hsieh, Yalun Yu, Jeffery B. Klauda. All-Atom Modeling of Complex Cellular Membranes. Langmuir 2022, 38 (1) , 3-17. https://doi.org/10.1021/acs.langmuir.1c02084
    2. Mariia Savenko, Timothée Rivel, Semen Yesylevskyy, Christophe Ramseyer. Influence of Substrate Hydrophilicity on Structural Properties of Supported Lipid Systems on Graphene, Graphene Oxides, and Silica. The Journal of Physical Chemistry B 2021, 125 (29) , 8060-8074. https://doi.org/10.1021/acs.jpcb.1c04615
    3. Simou Sun, Chang Liu, Danixa Rodriguez Melendez, Tinglu Yang, Paul S. Cremer. Immobilization of Phosphatidylinositides Revealed by Bilayer Leaflet Decoupling. Journal of the American Chemical Society 2020, 142 (30) , 13003-13010. https://doi.org/10.1021/jacs.0c03800
    4. Guilherme B. Berselli, Nirod Kumar Sarangi, Sivaramakrishnan Ramadurai, Paul V. Murphy, Tia E. Keyes. Microcavity-Supported Lipid Membranes: Versatile Platforms for Building Asymmetric Lipid Bilayers and for Protein Recognition. ACS Applied Bio Materials 2019, 2 (8) , 3404-3417. https://doi.org/10.1021/acsabm.9b00378
    5. James Kurniawan, João Francisco Ventrici de Souza, Amanda T. Dang, Gang-yu Liu, Tonya L. Kuhl. Preparation and Characterization of Solid-Supported Lipid Bilayers Formed by Langmuir–Blodgett Deposition: A Tutorial. Langmuir 2018, 34 (51) , 15622-15639. https://doi.org/10.1021/acs.langmuir.8b03504
    6. Takuhiro Otosu, Shoichi Yamaguchi. Quantifying the Diffusion of Lipids in the Proximal/Distal Leaflets of a Supported Lipid Bilayer by Two-Dimensional Fluorescence Lifetime Correlation Spectroscopy. The Journal of Physical Chemistry B 2018, 122 (45) , 10315-10319. https://doi.org/10.1021/acs.jpcb.8b08614
    7. Marie Markones, Carina Drechsler, Michael Kaiser, Louma Kalie, Heiko Heerklotz, and Sebastian Fiedler . Engineering Asymmetric Lipid Vesicles: Accurate and Convenient Control of the Outer Leaflet Lipid Composition. Langmuir 2018, 34 (5) , 1999-2005. https://doi.org/10.1021/acs.langmuir.7b03189
    8. Yixing Chen, Halil I. Okur, Cornelis Lütgebaucks, and Sylvie Roke . Zwitterionic and Charged Lipids Form Remarkably Different Structures on Nanoscale Oil Droplets in Aqueous Solution. Langmuir 2018, 34 (3) , 1042-1050. https://doi.org/10.1021/acs.langmuir.7b02896
    9. Toshinori Motegi, Kenji Yamazaki, Toshio Ogino, and Ryugo Tero . Substrate-Induced Structure and Molecular Dynamics in a Lipid Bilayer Membrane. Langmuir 2017, 33 (51) , 14748-14755. https://doi.org/10.1021/acs.langmuir.7b03212
    10. J. P. Michel, Y. X. Wang, I. Kiesel, Y. Gerelli, and V. Rosilio . Disruption of Asymmetric Lipid Bilayer Models Mimicking the Outer Membrane of Gram-Negative Bacteria by an Active Plasticin. Langmuir 2017, 33 (41) , 11028-11039. https://doi.org/10.1021/acs.langmuir.7b02864
    11. Drew Marquardt, Frederick A. Heberle, Tatiana Miti, Barbara Eicher, Erwin London, John Katsaras, and Georg Pabst . 1H NMR Shows Slow Phospholipid Flip-Flop in Gel and Fluid Bilayers. Langmuir 2017, 33 (15) , 3731-3741. https://doi.org/10.1021/acs.langmuir.6b04485
    12. Frederick A. Heberle, Drew Marquardt, Milka Doktorova, Barbara Geier, Robert F. Standaert, Peter Heftberger, Benjamin Kollmitzer, Jonathan D. Nickels, Robert A. Dick, Gerald W. Feigenson, John Katsaras, Erwin London, and Georg Pabst . Subnanometer Structure of an Asymmetric Model Membrane: Interleaflet Coupling Influences Domain Properties. Langmuir 2016, 32 (20) , 5195-5200. https://doi.org/10.1021/acs.langmuir.5b04562
    13. Xiaojun Shi, Maryam Kohram, Xiaodong Zhuang, and Adam W. Smith . Interactions and Translational Dynamics of Phosphatidylinositol Bisphosphate (PIP2) Lipids in Asymmetric Lipid Bilayers. Langmuir 2016, 32 (7) , 1732-1741. https://doi.org/10.1021/acs.langmuir.5b02814
    14. Agustín Mangiarotti and Natalia Wilke . Energetics of the Phase Transition in Free-Standing versus Supported Lipid Membranes. The Journal of Physical Chemistry B 2015, 119 (28) , 8718-8724. https://doi.org/10.1021/acs.jpcb.5b04397
    15. Yong-Sang Ryu, Daehan Yoo, Nathan J. Wittenberg, Luke R. Jordan, Sin-Doo Lee, Atul N. Parikh, and Sang-Hyun Oh . Lipid Membrane Deformation Accompanied by Disk-to-Ring Shape Transition of Cholesterol-Rich Domains. Journal of the American Chemical Society 2015, 137 (27) , 8692-8695. https://doi.org/10.1021/jacs.5b04559
    16. Jelena Drazenovic, Selver Ahmed, Nicole-Marie Tuzinkiewicz, and Stephanie L. Wunder . Lipid Exchange and Transfer on Nanoparticle Supported Lipid Bilayers: Effect of Defects, Ionic Strength, and Size. Langmuir 2015, 31 (2) , 721-731. https://doi.org/10.1021/la503967m
    17. Ilaria Visco, Salvatore Chiantia, and Petra Schwille . Asymmetric Supported Lipid Bilayer Formation via Methyl-β-Cyclodextrin Mediated Lipid Exchange: Influence of Asymmetry on Lipid Dynamics and Phase Behavior. Langmuir 2014, 30 (25) , 7475-7484. https://doi.org/10.1021/la500468r
    18. Paul Kühler, Max Weber, and Theobald Lohmüller . Plasmonic Nanoantenna Arrays for Surface-Enhanced Raman Spectroscopy of Lipid Molecules Embedded in a Bilayer Membrane. ACS Applied Materials & Interfaces 2014, 6 (12) , 8947-8952. https://doi.org/10.1021/am5023418
    19. Hanna P. Wacklin . Composition and Asymmetry in Supported Membranes Formed by Vesicle Fusion. Langmuir 2011, 27 (12) , 7698-7707. https://doi.org/10.1021/la200683e
    20. Jason D. Perlmutter and Jonathan N. Sachs . Interleaflet Interaction and Asymmetry in Phase Separated Lipid Bilayers: Molecular Dynamics Simulations. Journal of the American Chemical Society 2011, 133 (17) , 6563-6577. https://doi.org/10.1021/ja106626r
    21. Chen Wan, Volker Kiessling, David S. Cafiso, and Lukas K. Tamm . Partitioning of Synaptotagmin I C2 Domains between Liquid-Ordered and Liquid-Disordered Inner Leaflet Lipid Phases. Biochemistry 2011, 50 (13) , 2478-2485. https://doi.org/10.1021/bi101864k
    22. Ahmad Arouri, Volker Kiessling, Lukas Tamm, Margitta Dathe, and Alfred Blume . Morphological Changes Induced by the Action of Antimicrobial Peptides on Supported Lipid Bilayers. The Journal of Physical Chemistry B 2011, 115 (1) , 158-167. https://doi.org/10.1021/jp107577k
    23. Roxane M. Fabre and Daniel R. Talham. Stable Supported Lipid Bilayers on Zirconium Phosphonate Surfaces. Langmuir 2009, 25 (21) , 12644-12652. https://doi.org/10.1021/la901920y
    24. Ryugo Tero, Toru Ujihara and Tsuneo Urisu. Lipid Bilayer Membrane with Atomic Step Structure: Supported Bilayer on a Step-and-Terrace TiO2(100) Surface. Langmuir 2008, 24 (20) , 11567-11576. https://doi.org/10.1021/la801080f
    25. Chiho Kataoka-Hamai, Hiromi Inoue and Yuji Miyahara. Detection of Supported Lipid Bilayers Using Their Electric Charge. Langmuir 2008, 24 (17) , 9916-9920. https://doi.org/10.1021/la801623m
    26. Chen Wan,, Volker Kiessling, and, Lukas K. Tamm. Coupling of Cholesterol-Rich Lipid Phases in Asymmetric Bilayers. Biochemistry 2008, 47 (7) , 2190-2198. https://doi.org/10.1021/bi7021552
    27. Benjamin L. Stottrup,, Alison M. Heussler, and, Tracy A. Bibelnieks. Determination of Line Tension in Lipid Monolayers by Fourier Analysis of Capillary Waves. The Journal of Physical Chemistry B 2007, 111 (38) , 11091-11094. https://doi.org/10.1021/jp074898r
    28. Morgan D. Mager and, Nicholas A. Melosh. Lipid Bilayer Deposition and Patterning via Air Bubble Collapse. Langmuir 2007, 23 (18) , 9369-9377. https://doi.org/10.1021/la701372b
    29. Jin Liu and, John C. Conboy. Asymmetric Distribution of Lipids in a Phase Segregated Phospholipid Bilayer Observed by Sum-Frequency Vibrational Spectroscopy. The Journal of Physical Chemistry C 2007, 111 (25) , 8988-8999. https://doi.org/10.1021/jp0690547
    30. Linda J. Johnston. Nanoscale Imaging of Domains in Supported Lipid Membranes. Langmuir 2007, 23 (11) , 5886-5895. https://doi.org/10.1021/la070108t
    31. Fernanda F. Rossetti,, Marcus Textor, and, Ilya Reviakine. Asymmetric Distribution of Phosphatidyl Serine in Supported Phospholipid Bilayers on Titanium Dioxide. Langmuir 2006, 22 (8) , 3467-3473. https://doi.org/10.1021/la053000r
    32. Mikhail Merzlyakov,, Edwin Li, and, Kalina Hristova. Directed Assembly of Surface-Supported Bilayers with Transmembrane Helices. Langmuir 2006, 22 (3) , 1247-1253. https://doi.org/10.1021/la051933h
    33. Caroline M. Ajo-Franklin,, Chiaki Yoshina-Ishii, and, Steven G. Boxer. Probing the Structure of Supported Membranes and Tethered Oligonucleotides by Fluorescence Interference Contrast Microscopy. Langmuir 2005, 21 (11) , 4976-4983. https://doi.org/10.1021/la0468388
    34. Dominik Dziura, Maksymilian Dziura, Drew Marquardt. Studying lipid flip-flop in asymmetric liposomes using 1H NMR and TR-SANS. 2024https://doi.org/10.1016/bs.mie.2024.02.012
    35. Milka Doktorova, Ilya Levental, Frederick A. Heberle. Seeing the Membrane from Both Sides Now: Lipid Asymmetry and Its Strange Consequences. Cold Spring Harbor Perspectives in Biology 2023, 15 (12) , a041393. https://doi.org/10.1101/cshperspect.a041393
    36. Nancy Nisticò, Maria Greco, Maria Chiara Bruno, Elena Giuliano, Paolo Sinopoli, Donato Cosco. Biomimetic lipid membranes: An overview on their properties and applications. Applied Materials Today 2023, 35 , 101998. https://doi.org/10.1016/j.apmt.2023.101998
    37. Mokhtar Mapar, Mattias Sjöberg, Vladimir P. Zhdanov, Björn Agnarsson, Fredrik Höök. Label-free quantification of protein binding to lipid vesicles using transparent waveguide evanescent-field scattering microscopy with liquid control. Biomedical Optics Express 2023, 14 (8) , 4003. https://doi.org/10.1364/BOE.490051
    38. Robert E. Coffman, Katelyn N. Kraichely, Alex J. B. Kreutzberger, Volker Kiessling, Lukas K. Tamm, Dixon J. Woodbury. Drunken lipid membranes, not drunken SNARE proteins, promote fusion in a model of neurotransmitter release. Frontiers in Molecular Neuroscience 2022, 15 https://doi.org/10.3389/fnmol.2022.1022756
    39. Ryugo Tero, Natsumi Kobayashi. Substrate-induced electrostatic potential varies composition of supported lipid bilayer containing anionic lipid. Japanese Journal of Applied Physics 2022, 61 (SC) , SC1026. https://doi.org/10.35848/1347-4065/ac3fcc
    40. Sarah B. Nyenhuis, Nakul Karandikar, Volker Kiessling, Alex J. B. Kreutzberger, Anusa Thapa, Binyong Liang, Lukas K. Tamm, David S. Cafiso. Conserved arginine residues in synaptotagmin 1 regulate fusion pore expansion through membrane contact. Nature Communications 2021, 12 (1) https://doi.org/10.1038/s41467-021-21090-x
    41. Bineet Sharma, Hossein Moghimianavval, Sung-Won Hwang, Allen P. Liu. Synthetic Cell as a Platform for Understanding Membrane-Membrane Interactions. Membranes 2021, 11 (12) , 912. https://doi.org/10.3390/membranes11120912
    42. Joerg Nikolaus, Kasey Hancock, Maria Tsemperouli, David Baddeley, Erdem Karatekin. Optimal Detection of Fusion Pore Dynamics Using Polarized Total Internal Reflection Fluorescence Microscopy. Frontiers in Molecular Biosciences 2021, 8 https://doi.org/10.3389/fmolb.2021.740408
    43. Haden L. Scott, Kristen B. Kennison, Thais A. Enoki, Milka Doktorova, Jacob J. Kinnun, Frederick A. Heberle, John Katsaras. Model Membrane Systems Used to Study Plasma Membrane Lipid Asymmetry. Symmetry 2021, 13 (8) , 1356. https://doi.org/10.3390/sym13081356
    44. A.V. Shokurov, D.N. Novak, P.V. Ostroverkhov, M.A. Grin, A.V. Zaytseva, O.A. Raitman, F. Moroté, T. Cohen-Bouhacina, C. Grauby-Heywang, S.L. Selektor. Lipid monolayer as a simple model membrane for comparative assessment of the photodynamic therapy photosensitizer efficiency via macroscopic measurements. Journal of Photochemistry and Photobiology B: Biology 2020, 210 , 111958. https://doi.org/10.1016/j.jphotobiol.2020.111958
    45. Maria J. Sarmento, Martin Hof, Radek Šachl. Interleaflet Coupling of Lipid Nanodomains – Insights From in vitro Systems. Frontiers in Cell and Developmental Biology 2020, 8 https://doi.org/10.3389/fcell.2020.00284
    46. Kenta Imai, Tomoko Horio, Toshiaki Hattori, Kazuaki Sawada, Ryugo Tero. Lipid bilayer formation on an ion image sensor and measurement of time response of potential dependency on ion concentration. Japanese Journal of Applied Physics 2019, 58 (SD) , SDDK06. https://doi.org/10.7567/1347-4065/ab088a
    47. Graham Taylor, Mary-Anne Nguyen, Subhadeep Koner, Eric Freeman, C. Patrick Collier, Stephen A. Sarles. Electrophysiological interrogation of asymmetric droplet interface bilayers reveals surface-bound alamethicin induces lipid flip-flop. Biochimica et Biophysica Acta (BBA) - Biomembranes 2019, 1861 (1) , 335-343. https://doi.org/10.1016/j.bbamem.2018.07.001
    48. S. Dobroiu, F.C.M.J.M. van Delft, J. Aveyard-Hanson, Prasad Shetty, D.V. Nicolau. Fluorescence Interference Contrast-enabled structures improve the microarrays performance. Biosensors and Bioelectronics 2019, 123 , 251-259. https://doi.org/10.1016/j.bios.2018.09.009
    49. Zhiqi Tian, Jihong Gong, Michael Crowe, Ming Lei, Dechang Li, Baohua Ji, Jiajie Diao. Biochemical studies of membrane fusion at the single-particle level. Progress in Lipid Research 2019, 73 , 92-100. https://doi.org/10.1016/j.plipres.2019.01.001
    50. Nathaly Marín-Medina, Andrea Mescola, Andrea Alessandrini. Effects of the peptide Magainin H2 on Supported Lipid Bilayers studied by different biophysical techniques. Biochimica et Biophysica Acta (BBA) - Biomembranes 2018, 1860 (12) , 2635-2643. https://doi.org/10.1016/j.bbamem.2018.10.003
    51. Ross S. Gunderson, Aurelia R. Honerkamp-Smith. Liquid-liquid phase transition temperatures increase when lipid bilayers are supported on glass. Biochimica et Biophysica Acta (BBA) - Biomembranes 2018, 1860 (10) , 1965-1971. https://doi.org/10.1016/j.bbamem.2018.05.001
    52. Volker Kiessling, Alex J. B. Kreutzberger, Binyong Liang, Sarah B. Nyenhuis, Patrick Seelheim, J. David Castle, David S. Cafiso, Lukas K. Tamm. A molecular mechanism for calcium-mediated synaptotagmin-triggered exocytosis. Nature Structural & Molecular Biology 2018, 25 (10) , 911-917. https://doi.org/10.1038/s41594-018-0130-9
    53. Rafael L. Schoch, Itay Barel, Frank L. H. Brown, Gilad Haran. Lipid diffusion in the distal and proximal leaflets of supported lipid bilayer membranes studied by single particle tracking. The Journal of Chemical Physics 2018, 148 (12) https://doi.org/10.1063/1.5010341
    54. Štěpánka Skalová, Vlastimil Vyskočil, Jiří Barek, Tomáš Navrátil. Model Biological Membranes and Possibilities of Application of Electrochemical Impedance Spectroscopy for their Characterization. Electroanalysis 2018, 30 (2) , 207-219. https://doi.org/10.1002/elan.201700649
    55. Barbara Eicher, Drew Marquardt, Frederick A. Heberle, Ilse Letofsky-Papst, Gerald N. Rechberger, Marie-Sousai Appavou, John Katsaras, Georg Pabst. Intrinsic Curvature-Mediated Transbilayer Coupling in Asymmetric Lipid Vesicles. Biophysical Journal 2018, 114 (1) , 146-157. https://doi.org/10.1016/j.bpj.2017.11.009
    56. Carmen González-Henríquez, Vanessa Villegas-Opazo, Dallits Sagredo-Oyarce, Mauricio Sarabia-Vallejos, Claudio Terraza. Thermal Response Analysis of Phospholipid Bilayers Using Ellipsometric Techniques. Biosensors 2017, 7 (4) , 34. https://doi.org/10.3390/bios7030034
    57. Alex J.B. Kreutzberger, Volker Kiessling, Binyong Liang, Sung-Tae Yang, J. David Castle, Lukas K. Tamm. Asymmetric Phosphatidylethanolamine Distribution Controls Fusion Pore Lifetime and Probability. Biophysical Journal 2017, 113 (9) , 1912-1915. https://doi.org/10.1016/j.bpj.2017.09.014
    58. Frederick A. Heberle, Georg Pabst. Complex biomembrane mimetics on the sub-nanometer scale. Biophysical Reviews 2017, 9 (4) , 353-373. https://doi.org/10.1007/s12551-017-0275-5
    59. Jonathan Brewer, Henrik Seir Thoke, Roberto P. Stock, Luis A. Bagatolli. Enzymatic studies on planar supported membranes using a widefield fluorescence LAURDAN Generalized Polarization imaging approach. Biochimica et Biophysica Acta (BBA) - Biomembranes 2017, 1859 (5) , 888-895. https://doi.org/10.1016/j.bbamem.2017.01.024
    60. Carla M. Rosetti, Agustín Mangiarotti, Natalia Wilke. Sizes of lipid domains: What do we know from artificial lipid membranes? What are the possible shared features with membrane rafts in cells?. Biochimica et Biophysica Acta (BBA) - Biomembranes 2017, 1859 (5) , 789-802. https://doi.org/10.1016/j.bbamem.2017.01.030
    61. Asma Poursoroush, Maria Maddalena Sperotto, Mohamed Laradji. Phase behavior of supported lipid bilayers: A systematic study by coarse-grained molecular dynamics simulations. The Journal of Chemical Physics 2017, 146 (15) https://doi.org/10.1063/1.4981008
    62. Volker Kiessling, Binyong Liang, Alex J. B. Kreutzberger, Lukas K. Tamm. Planar Supported Membranes with Mobile SNARE Proteins and Quantitative Fluorescence Microscopy Assays to Study Synaptic Vesicle Fusion. Frontiers in Molecular Neuroscience 2017, 10 https://doi.org/10.3389/fnmol.2017.00072
    63. Johnna R. St. Clair, Qing Wang, Guangtao Li, Erwin London. Preparation and Physical Properties of Asymmetric Model Membrane Vesicles. 2017, 1-27. https://doi.org/10.1007/978-981-10-6244-5_1
    64. Maria Maddalena Sperotto, Alberta Ferrarini. Spontaneous Lipid Flip-Flop in Membranes: A Still Unsettled Picture from Experiments and Simulations. 2017, 29-60. https://doi.org/10.1007/978-981-10-6244-5_2
    65. Roland Faller. Molecular modeling of lipid probes and their influence on the membrane. Biochimica et Biophysica Acta (BBA) - Biomembranes 2016, 1858 (10) , 2353-2361. https://doi.org/10.1016/j.bbamem.2016.02.014
    66. Sung-Tae Yang, Alex J.B. Kreutzberger, Jinwoo Lee, Volker Kiessling, Lukas K. Tamm. The role of cholesterol in membrane fusion. Chemistry and Physics of Lipids 2016, 199 , 136-143. https://doi.org/10.1016/j.chemphyslip.2016.05.003
    67. C Monzel, K Sengupta. Measuring shape fluctuations in biological membranes. Journal of Physics D: Applied Physics 2016, 49 (24) , 243002. https://doi.org/10.1088/0022-3727/49/24/243002
    68. Jonathan D. Nickels, Jeremy C. Smith, Xiaolin Cheng. Lateral organization, bilayer asymmetry, and inter-leaflet coupling of biological membranes. Chemistry and Physics of Lipids 2015, 192 , 87-99. https://doi.org/10.1016/j.chemphyslip.2015.07.012
    69. Drew Marquardt, Barbara Geier, Georg Pabst. Asymmetric Lipid Membranes: Towards More Realistic Model Systems. Membranes 2015, 5 (2) , 180-196. https://doi.org/10.3390/membranes5020180
    70. Volker Kiessling, Sung-Tae Yang, Lukas K. Tamm. Supported Lipid Bilayers as Models for Studying Membrane Domains. 2015, 1-23. https://doi.org/10.1016/bs.ctm.2015.03.001
    71. Volker Kiessling, Binyong Liang, Lukas K. Tamm. Reconstituting SNARE-mediated membrane fusion at the single liposome level. 2015, 339-363. https://doi.org/10.1016/bs.mcb.2015.02.005
    72. Celesta Fong, Aurelia W. Dong, Anita J. Hill, Ben J. Boyd, Calum J. Drummond. Positron annihilation lifetime spectroscopy (PALS): a probe for molecular organisation in self-assembled biomimetic systems. Physical Chemistry Chemical Physics 2015, 17 (27) , 17527-17540. https://doi.org/10.1039/C5CP01921D
    73. Andrea Alessandrini, Paolo Facci. Model Bio‐Membranes Investigated by AFM and AFS: A Suitable Tool to Unravel Lipid Organization and their Interaction with Proteins. 2014, 185-226. https://doi.org/10.1002/9781119028642.ch7
    74. Andrea Alessandrini, Paolo Facci. Phase transitions in supported lipid bilayers studied by AFM. Soft Matter 2014, 10 (37) , 7145-7164. https://doi.org/10.1039/C4SM01104J
    75. Xirui Zhang, Philipp Spuhler, David Freedman, M Ünlü. Spectral Self-Interference Fluorescence Microscopy to Study Conformation of Biomolecules with Nanometer Accuracy. 2013, 345-386. https://doi.org/10.1201/b15615-10
    76. Noor F. Hussain, Amanda P. Siegel, Yifan Ge, Rainer Jordan, Christoph A. Naumann. Bilayer Asymmetry Influences Integrin Sequestering in Raft-Mimicking Lipid Mixtures. Biophysical Journal 2013, 104 (10) , 2212-2221. https://doi.org/10.1016/j.bpj.2013.04.020
    77. Samaneh Mashaghi, Tayebeh Jadidi, Gijsje Koenderink, Alireza Mashaghi. Lipid Nanotechnology. International Journal of Molecular Sciences 2013, 14 (2) , 4242-4282. https://doi.org/10.3390/ijms14024242
    78. Jin Liu, Krystal L. Brown, John C. Conboy. The effect of cholesterol on the intrinsic rate of lipid flip–flop as measured by sum-frequency vibrational spectroscopy. Faraday Discuss. 2013, 161 , 45-61. https://doi.org/10.1039/C2FD20083J
    79. Laura Picas, Pierre-Emmanuel Milhiet, Jordi Hernández-Borrell. Atomic force microscopy: A versatile tool to probe the physical and chemical properties of supported membranes at the nanoscale. Chemistry and Physics of Lipids 2012, 165 (8) , 845-860. https://doi.org/10.1016/j.chemphyslip.2012.10.005
    80. Andrea Alessandrini, Paolo Facci. Nanoscale mechanical properties of lipid bilayers and their relevance in biomembrane organization and function. Micron 2012, 43 (12) , 1212-1223. https://doi.org/10.1016/j.micron.2012.03.013
    81. Ryugo Tero. Substrate Effects on the Formation Process, Structure and Physicochemical Properties of Supported Lipid Bilayers. Materials 2012, 5 (12) , 2658-2680. https://doi.org/10.3390/ma5122658
    82. John M. Sanderson. Resolving the kinetics of lipid, protein and peptide diffusion in membranes. Molecular Membrane Biology 2012, 29 (5) , 118-143. https://doi.org/10.3109/09687688.2012.678018
    83. Peter J. Quinn. Lipid–lipid interactions in bilayer membranes: Married couples and casual liaisons. Progress in Lipid Research 2012, 51 (3) , 179-198. https://doi.org/10.1016/j.plipres.2012.01.001
    84. M.L. Longo. 5.4 Atomic Force Microscopy and Fluorescence Microscopy of Lipid Bilayers. 2012, 37-62. https://doi.org/10.1016/B978-0-12-374920-8.00505-1
    85. Wei Deng, Sankaranarayanan Srinivasan, Xiaofeng Zheng, John A. Putkey, Renhao Li. Interaction of Calmodulin with l-Selectin at the Membrane Interface: Implication on the Regulation of l-Selectin Shedding. Journal of Molecular Biology 2011, 411 (1) , 220-233. https://doi.org/10.1016/j.jmb.2011.05.041
    86. Volker Kiessling, Marta K. Domanska, Lukas K. Tamm. Single SNARE-Mediated Vesicle Fusion Observed In Vitro by Polarized TIRFM. Biophysical Journal 2010, 99 (12) , 4047-4055. https://doi.org/10.1016/j.bpj.2010.10.022
    87. Claudia Steinem, Andreas Janshoff. Multicomponent membranes on solid substrates: Interfaces for protein binding. Current Opinion in Colloid & Interface Science 2010, 15 (6) , 479-488. https://doi.org/10.1016/j.cocis.2010.06.004
    88. Marie-Cécile Giocondi, Daisuke Yamamoto, Eric Lesniewska, Pierre-Emmanuel Milhiet, Toshio Ando, Christian Le Grimellec. Surface topography of membrane domains. Biochimica et Biophysica Acta (BBA) - Biomembranes 2010, 1798 (4) , 703-718. https://doi.org/10.1016/j.bbamem.2009.09.015
    89. Ann E. Oliver, Atul N. Parikh. Templating membrane assembly, structure, and dynamics using engineered interfaces. Biochimica et Biophysica Acta (BBA) - Biomembranes 2010, 1798 (4) , 839-850. https://doi.org/10.1016/j.bbamem.2009.12.029
    90. Anna Kułakowska, Piotr Jurkiewicz, Jan Sýkora, Aleš Benda, Yves Mely, Martin Hof. Fluorescence Lifetime Tuning—A Novel Approach to Study Flip-Flop Kinetics in Supported Phospholipid Bilayers. Journal of Fluorescence 2010, 20 (2) , 563-569. https://doi.org/10.1007/s10895-009-0581-9
    91. Richard M. Epand, Annick Thomas, Robert Brasseur, Raquel F. Epand. Cholesterol Interaction with Proteins That Partition into Membrane Domains: An Overview. 2010, 253-278. https://doi.org/10.1007/978-90-481-8622-8_9
    92. Erik Reimhult, Martina K. Baumann, Stefan Kaufmann, Karthik Kumar, Philipp R. Spycher. Advances in nanopatterned and nanostructured supported lipid membranes and their applications. Biotechnology and Genetic Engineering Reviews 2010, 27 (1) , 185-216. https://doi.org/10.1080/02648725.2010.10648150
    93. Marta K. Domanska, Volker Kiessling, Alexander Stein, Dirk Fasshauer, Lukas K. Tamm. Single Vesicle Millisecond Fusion Kinetics Reveals Number of SNARE Complexes Optimal for Fast SNARE-mediated Membrane Fusion. Journal of Biological Chemistry 2009, 284 (46) , 32158-32166. https://doi.org/10.1074/jbc.M109.047381
    94. David H. Murray, Lukas K. Tamm, Volker Kiessling. Supported double membranes. Journal of Structural Biology 2009, 168 (1) , 183-189. https://doi.org/10.1016/j.jsb.2009.02.008
    95. John Oreopoulos, Christopher M. Yip. Combinatorial microscopy for the study of protein–membrane interactions in supported lipid bilayers: Order parameter measurements by combined polarized TIRFM/AFM. Journal of Structural Biology 2009, 168 (1) , 21-36. https://doi.org/10.1016/j.jsb.2009.02.011
    96. Edwin Li, Mikhail Merzlyakov, Janice Lin, Peter Searson, Kalina Hristova. Utility of surface-supported bilayers in studies of transmembrane helix dimerization. Journal of Structural Biology 2009, 168 (1) , 53-60. https://doi.org/10.1016/j.jsb.2009.03.005
    97. Carl E. Creutz, J. Michael Edwardson. Organization and synergistic binding of copine I and annexin A1 on supported lipid bilayers observed by atomic force microscopy. Biochimica et Biophysica Acta (BBA) - Biomembranes 2009, 1788 (9) , 1950-1961. https://doi.org/10.1016/j.bbamem.2009.06.009
    98. Kazutoshi Iijima, Norihiro Soga, Teruhiko Matsubara, Toshinori Sato. Observations of the distribution of GM3 in membrane microdomains by atomic force microscopy. Journal of Colloid and Interface Science 2009, 337 (2) , 369-374. https://doi.org/10.1016/j.jcis.2009.05.032
    99. H.M. Seeger, G. Marino, A. Alessandrini, P. Facci. Effect of Physical Parameters on the Main Phase Transition of Supported Lipid Bilayers. Biophysical Journal 2009, 97 (4) , 1067-1076. https://doi.org/10.1016/j.bpj.2009.03.068
    100. Mehmet Dogan, M. Irsadi Aksun, Anna K. Swan, Bennett B. Goldberg, M. Selim Ünlü. Closed-form representations of field components of fluorescent emitters in layered media. Journal of the Optical Society of America A 2009, 26 (6) , 1458. https://doi.org/10.1364/JOSAA.26.001458
    Load all citations

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect