Cited by 53Lipid Membrane Structure and BehaviorAdvanced Fluorescence Microscopy TechniquesSpectroscopy and Quantum Chemical Studies

Label-free and charge-sensitive dynamic imaging of lipid membrane hydration on millisecond time scales

Open access
Tarun, Orly B., Hannesschläger, Christof, Pohl, Peter, Roke, Sylvie·2018·Proceedings of the National Academy of Sciences

Abstract

Significance: Lipid bilayer membranes are responsible for compartmentalization, signaling, transport, and flow of charge in living cells. Membranes self-assemble in aqueous solutions. Without a hydrating environment, membranes cannot exist. It is therefore surprising to note that the hydrating water is neglected in most membrane-related studies. We imaged membrane-bound oriented water by means of label-free second harmonic microscopy. We tracked, on millisecond time scales, membrane domain diffusion of condensed charged lipid domains, domain structure, and the spatial distribution of charge. Real-time electrostatic membrane potential maps were constructed using nonlinear optical theory. The spatiotemporal fluctuation in the membrane potential is surprisingly large and reveals the importance of charge fluctuations on membranes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1073/pnas.1719347115

Cites

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • GUV fusion occurs in the presence of transmembrane potentials but not in their absence.

    “We validate our mechanism by demonstrating experimentally, via video microscopy and second harmonic generation imaging 11 of interacting giant unilamellar vesicles (GUVs), that GUV fusion occurs in the presence of transmembrane potentials but not in their absence.”

    From Fusion of lipid membranes: an alternative pathway (2026) · cites this paper as [11]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

No references could be resolved yet.

Research works printed but not linked: 40

  1. [1]Simons K Vaz WLC 2004 Model systems, lipid rafts, and cell membranes Annu Rev Biophys Biomol Struct 33 269 295 15139814
  2. [2]van Meer G de Kroon AIPM 2011 Lipid map of the mammalian cell J Cell Sci 124 5 8 21172818
  3. [3]Marsh D 2013 Handbook of Lipid Bilayers CRC Press Boca Raton, FL 2nd Ed
  4. [4]Jackson JD 1998 Classical Electrodynamics Wiley New York 3rd Ed
  5. [5]Veatch SL Keller SL 2005 Seeing spots: Complex phase behavior in simple membranes Biochim Biophys Acta 1746 172 185 16043244
  6. [6]Kress A 2013 Mapping the local organization of cell membranes using excitation-polarization-resolved confocal fluorescence microscopy Biophys J 105 127 136 23823231 PMC3699755
  7. [7]Eggeling C 2009 Direct observation of the nanoscale dynamics of membrane lipids in a living cell Nature 457 1159 1162 19098897
  8. [8]Korlach J Schwille P Webb WW Feigenson GW 1999 Characterization of lipid bilayer phases by confocal microscopy and fluorescence correlation spectroscopy Proc Natl Acad Sci USA 96 8461 8466 10411897 PMC17538
  9. [9]Potma E de Boeij WP van Haastert PJM Wiersma DA 2001 Real-time visualization of intracellular hydrodynamics in single living cells Proc Natl Acad Sci USA 98 1577 1582 11171993 PMC29299
  10. [10]Rinia HA Burger KNJ Bonn M Mu M 2008 Quantitative label-free imaging of lipid composition and packing of individual cellular lipid droplets using multiplex CARS microscopy Biophys J 95 4908 4914 18689461 PMC2576358
  11. [11]Li L Cheng J-X 2008 Label-free coherent anti-Stokes Raman scattering imaging of coexisting lipid domains in single bilayers J Phys Chem B 112 1576 1579 18215035
  12. [12]Nguyen TT Conboy JC 2011 High-throughput screening of drug-lipid membrane interactions via counter-propagating second harmonic generation imaging Anal Chem 83 5979 5988 21696170 PMC3328353
  13. [13]de Wit G Danial JSH Kukura P Wallace MI 2015 Dynamic label-free imaging of lipid nanodomains Proc Natl Acad Sci USA 112 12299 12303 26401022 PMC4603517
  14. [14]Howland MC Szmodis AW Sanii B Parikh AN 2007 Characterization of physical properties of supported phospholipid membranes using imaging ellipsometry at optical wavelengths Biophys J 92 1306 1317 17142265 PMC1783900
  15. [15]Shim S-H 2012 Super-resolution fluorescence imaging of organelles in live cells with photoswitchable membrane probes Proc Natl Acad Sci USA 109 13978 13983 22891300 PMC3435176
  16. [16]Mashaghi A 2014 Label-free characterization of biomembranes: From structure to dynamics Chem Soc Rev 43 887 900 24253187
  17. [17]Liu J Conboy JC 2004 Direct measurement of the transbilayer movement of phospholipids by sum-frequency vibrational spectroscopy J Am Chem Soc 126 8376 8377 15237984
  18. [18]Roke S Schins J Müller M Bonn M 2003 Vibrational spectroscopic investigation of the phase diagram of a biomimetic lipid monolayer Phys Rev Lett 90 128101 12688904
  19. [20]Horner A Akimov SA Pohl P 2013 Long and short lipid molecules experience the same interleaflet drag in lipid bilayers Phys Rev Lett 110 268101 23848924 PMC4486369
  20. [22]Kriech MA Conboy JC 2005 Imaging chirality with surface second harmonic generation microscopy J Am Chem Soc 127 2834 2835 15740102
  21. [23]Dissalvo AE 2015 Membrane Hydration the Role of Water in the Structure and Function of Biological Membranes Springer Heidelberg
  22. [24]Macias-Romero C 2014 High throughput second harmonic imaging for label-free biological applications Opt Express 22 31102 31112 25607059
  23. [25]Macias-Romero C Nahalka I Okur HI Roke S 2017 Optical imaging of surface chemistry and dynamics in confinement Science 357 784 788 28729352
  24. [26]Montal M Mueller P 1972 Formation of bimolecular membranes from lipid monolayers and a study of their electrical properties Proc Natl Acad Sci USA 69 3561 3566 4509315 PMC389821
  25. [27]Gutsmann T Heimburg T Keyser U Mahendran KR Winterhalter M 2015 Protein reconstitution into freestanding planar lipid membranes for electrophysiological characterization Nat Protoc 10 188 198 25551663
  26. [28]Alvarez O Latorre R 1978 Voltage-dependent capacitance in lipid bilayers made from monolayers Biophys J 21 1 17 620076 PMC1473368
  27. [29]Peterson U 2002 Origin of membrane dipole potential: Contribution of the phospholipid fatty acid chains Chem Phys Lipids 117 19 27 12191841
  28. [30]van Meer G Voelker DR Feigenson GW 2008 Membrane lipids: Where they are and how they behave Nat Rev Mol Cell Biol 9 112 124 18216768 PMC2642958
  29. [31]Roke S Gonella G 2012 Nonlinear light scattering and spectroscopy of particles and droplets in liquids Annu Rev Phys Chem 63 353 378 22263911
  30. [32]Smolentsev N Lütgebaucks C Okur HI de Beer AGF Roke S 2016 Intermolecular headgroup interaction and hydration as driving forces for lipid transmembrane asymmetry J Am Chem Soc 138 4053 4060 26938772
  31. [35]Lütgebaucks C Macias-Romero C Roke S 2017 Characterization of the interface of binary mixed DOPC:DOPS liposomes in water: The impact of charge condensation J Chem Phys 146 044701 28147550
  32. [36]Hunter RJ 2001 Foundations of Colloid Science Oxford Univ Press Oxford
  33. [38]Okur HI Kherb J Cremer PS 2013 Cations bind only weakly to amides in aqueous solutions J Am Chem Soc 135 5062 5067 23517474
  34. [39]Tsui FC Ojcius DM Hubbell WL 1986 The intrinsic pKa values for phosphatidylserine and phosphatidylethanolamine in phosphatidylcholine host bilayers Biophys J 49 459 468 3955180 PMC1329485
  35. [40]Bakht O Pathak P London E 2007 Effect of the structure of lipids favoring disordered domain formation on the stability of cholesterol-containing ordered domains (lipid rafts): Identification of multiple raft-stabilization mechanisms Biophys J 93 4307 4318 17766350 PMC2098711
  36. [41]Cicuta P Keller SL Veatch SL 2007 Diffusion of liquid domains in lipid bilayer membranes J Phys Chem B 111 3328 3331 17388499
  37. [42]Collins MD Keller SL 2008 Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers Proc Natl Acad Sci USA 105 124 128 18172219 PMC2224171
  38. [44]Sezgin E 2012 Partitioning, diffusion, and ligand binding of raft lipid analogs in model and cellular plasma membranes Biochim Biophys Acta 1818 1777 1784 22450237
  39. [45]Klymchenko AS Kreder R 2014 Fluorescent probes for lipid rafts: From model membranes to living cells Chem Biol 21 97 113 24361047
  40. [48]Manning GS 2007 Counterion condensation on charged spheres, cylinders, and planes J Phys Chem B 111 8554 8559 17388468

Cited by

Sorted by citations

Authors
Tarun, O. B., Hannesschläger, C., Pohl, P., & Roke, S.
Affiliations
  • École Polytechnique Fédérale de Lausanne (CH)
  • Institute of Biophysics, Johannes Kepler University Linz, A-4020 Linz, Austria
  • Johannes Kepler University of Linz (AT)
Corresponding author
Roke, Sylvie
Venue
Proceedings of the National Academy of Sciences
Published
2018-04-02
Volume
115
Issue
16
Pages
4081-4086
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2796090647
Cited by
53
References
0
Citations by year
2026: 4 · 2025: 6 · 2024: 5 · 2023: 5 · 2022: 6 · 2021: 12 · 2020: 5 · 2019: 7 · 2018: 3
FWCI
2.36
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Infoscience (Ecole Polytechnique Fédérale de Lausanne) (submittedVersion, cc-by-nc-nd)
Funders
  • Swiss National Science Foundation (200021-140472)
  • Austrian Science Fund (P23679)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
  • Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Spectroscopy and Quantum Chemical Studies
Keywords
second harmonic generation microscopy, label-free imaging, charge-dipole interactions, water orientation, membrane potential, electrostatic potential mapping, ionic strength effects, pH effect, membrane dynamics, nonlinear optics, lipid bilayers
MeSH terms
Diffusion, Lipid Bilayers, Membrane Lipids, Membrane Potentials, Time Factors, Water, Microscopy, Confocal, Hydrophobic and Hydrophilic Interactions

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review