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Title: Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes

Abstract

In-plane lipid organization and phase separation in natural membranes play key roles in regulating many cellular processes. Highly cooperative, first-order phase transitions in model membranes consisting of few lipid components are well understood and readily detectable via calorimetry, densitometry, and fluorescence. However, far less is known about natural membranes containing numerous lipid species and high concentrations of cholesterol, for which thermotropic transitions are undetectable by the above-mentioned techniques. We demonstrate that membrane capacitance is highly sensitive to low-enthalpy thermotropic transitions taking place in complex lipid membranes. Specifically, we measured the electrical capacitance as a function of temperature for droplet interface bilayer model membranes of increasing compositional complexity, namely, (a) a single lipid species, (b) domain-forming ternary mixtures, and (c) natural brain total lipid extract (bTLE). We observed that, for single-species lipid bilayers and some ternary compositions, capacitance exhibited an abrupt, temperature-dependent change that coincided with the transition detected by other techniques. In addition, capacitance measurements revealed transitions in mixed-lipid membranes that were not detected by the other techniques. Most notably, capacitance measurements of bTLE bilayers indicated a transition at ~38 °C not seen with any other method. Likewise, capacitance measurements detected transitions in some well-studied ternary mixtures that, while knownmore » to yield coexisting lipid phases, are not detected with calorimetry or densitometry. These results indicate that capacitance is exquisitely sensitive to low-enthalpy membrane transitions because of its sensitivity to changes in bilayer thickness that occur when lipids and excess solvent undergo subtle rearrangements near a phase transition. Our findings also suggest that heterogeneity confers stability to natural membranes that function near transition temperatures by preventing unwanted defects and macroscopic demixing associated with high-enthalpy transitions commonly found in simpler mixtures.« less

Authors:
ORCiD logo [1];  [2];  [3]; ORCiD logo [4]; ORCiD logo [5];  [3]
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  1. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Mechanical, Aerospace, and Biomedical Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Division
  3. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Mechanical, Aerospace, and Biomedical Engineering
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biology and Soft Matter Division; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Neutron Science, Shull Wollan Center
  5. Univ. of Tennessee, Knoxville, TN (United States). Dept. of Mechanical, Aerospace, and Biomedical Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Nanophase Materials Science (CNMS)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
US Air Force Office of Scientific Research (AFOSR); USDOE Office of Science (SC), Basic Energy Sciences (BES)
OSTI Identifier:
1408576
Alternate Identifier(s):
OSTI ID: 1427658
Grant/Contract Number:  
AC05-00OR22725; FA9550-12-1-0464
Resource Type:
Accepted Manuscript
Journal Name:
Langmuir
Additional Journal Information:
Journal Volume: 33; Journal Issue: 38; Journal ID: ISSN 0743-7463
Publisher:
American Chemical Society
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Taylor, Graham J., Heberle, Frederick A., Seinfeld, Jason S., Katsaras, John, Collier, C. Patrick, and Sarles, Stephen A. Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes. United States: N. p., 2017. Web. doi:10.1021/acs.langmuir.7b02022.
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Taylor, Graham J., Heberle, Frederick A., Seinfeld, Jason S., Katsaras, John, Collier, C. Patrick, & Sarles, Stephen A. Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes. United States. https://doi.org/10.1021/acs.langmuir.7b02022
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Taylor, Graham J., Heberle, Frederick A., Seinfeld, Jason S., Katsaras, John, Collier, C. Patrick, and Sarles, Stephen A. Tue . "Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes". United States. https://doi.org/10.1021/acs.langmuir.7b02022. https://www.osti.gov/servlets/purl/1408576.
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@article{osti_1408576,
title = {Capacitive Detection of Low-Enthalpy, Higher-Order Phase Transitions in Synthetic and Natural Composition Lipid Membranes},
author = {Taylor, Graham J. and Heberle, Frederick A. and Seinfeld, Jason S. and Katsaras, John and Collier, C. Patrick and Sarles, Stephen A.},
abstractNote = {In-plane lipid organization and phase separation in natural membranes play key roles in regulating many cellular processes. Highly cooperative, first-order phase transitions in model membranes consisting of few lipid components are well understood and readily detectable via calorimetry, densitometry, and fluorescence. However, far less is known about natural membranes containing numerous lipid species and high concentrations of cholesterol, for which thermotropic transitions are undetectable by the above-mentioned techniques. We demonstrate that membrane capacitance is highly sensitive to low-enthalpy thermotropic transitions taking place in complex lipid membranes. Specifically, we measured the electrical capacitance as a function of temperature for droplet interface bilayer model membranes of increasing compositional complexity, namely, (a) a single lipid species, (b) domain-forming ternary mixtures, and (c) natural brain total lipid extract (bTLE). We observed that, for single-species lipid bilayers and some ternary compositions, capacitance exhibited an abrupt, temperature-dependent change that coincided with the transition detected by other techniques. In addition, capacitance measurements revealed transitions in mixed-lipid membranes that were not detected by the other techniques. Most notably, capacitance measurements of bTLE bilayers indicated a transition at ~38 °C not seen with any other method. Likewise, capacitance measurements detected transitions in some well-studied ternary mixtures that, while known to yield coexisting lipid phases, are not detected with calorimetry or densitometry. These results indicate that capacitance is exquisitely sensitive to low-enthalpy membrane transitions because of its sensitivity to changes in bilayer thickness that occur when lipids and excess solvent undergo subtle rearrangements near a phase transition. Our findings also suggest that heterogeneity confers stability to natural membranes that function near transition temperatures by preventing unwanted defects and macroscopic demixing associated with high-enthalpy transitions commonly found in simpler mixtures.},
doi = {10.1021/acs.langmuir.7b02022},
journal = {Langmuir},
number = 38,
volume = 33,
place = {United States},
year = {Tue Aug 15 00:00:00 EDT 2017},
month = {Tue Aug 15 00:00:00 EDT 2017}
}
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https://doi.org/10.1021/acs.langmuir.7b02022
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Works referenced in this record:

Phase Separation in Biological Membranes: Integration of Theory and Experiment
journal, April 2010

Functions of Lipid Rafts in Biological Membranes
journal, November 1998

Lipid rafts: at a crossroad between cell biology and physics
journal, January 2007

  • Jacobson, Ken; Mouritsen, Ole G.; Anderson, Richard G. W.
  • Nature Cell Biology, Vol. 9, Issue 1
  • DOI: 10.1038/ncb0107-7

Lipid rafts and signal transduction
journal, October 2000

  • Simons, Kai; Toomre, Derek
  • Nature Reviews Molecular Cell Biology, Vol. 1, Issue 1
  • DOI: 10.1038/35036052

A lipid bound actin meshwork organizes liquid phase separation in model membranes
journal, March 2014

Lipid Bilayer Stability in Biological Membranes
book, January 1984

Calorimetric Evidence for the Liquid-Crystalline State of Lipids in a Biomembrane
journal, May 1969

  • Steim, J. M.; Tourtellotte, M. E.; Reinert, J. C.
  • Proceedings of the National Academy of Sciences, Vol. 63, Issue 1
  • DOI: 10.1073/pnas.63.1.104

Wild-type Escherichia coli Cells Regulate the Membrane Lipid Composition in a Window between Gel and Non-lamellar Structures
journal, March 1996

  • Morein, Sven; Andersson, Ann-Sofie; Rilfors, Leif
  • Journal of Biological Chemistry, Vol. 271, Issue 12
  • DOI: 10.1074/jbc.271.12.6801

X-ray diffraction studies of phase transitions in the membrane of Mycoplasma laidlawii
journal, January 1970

Lipid bilayer structure in the membrane of Mycoplasma laidlawii
journal, May 1971

Characterization of the plasma membrane of Mycoplasma laidlawii. VII. Phase transitions of membrane lipids
journal, October 1970

  • Melchior, Donald L.; Morowitz, Harold J.; Sturtevant, Julian M.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 219, Issue 1
  • DOI: 10.1016/0005-2736(70)90066-0

The effect of cholesterol and epicholesterol incorporation on the permeability and on the phase transition of intact Acholeplasma laidlawii cell membranes and derived liposomes
journal, January 1972

  • de Kruyff, B.; Demel, R. A.; dan Deenen, L. L. M.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 255, Issue 1
  • DOI: 10.1016/0005-2736(72)90032-6

Phase transitions of phospholipid bilayers and membranes of Acholeplasma laidlawii B visualized by freeze fracturing electron microscopy
journal, November 1972

  • Verkleij, A. J.; Ververgaert, P. H. J.; Van Deenen, L. L. M.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 288, Issue 2
  • DOI: 10.1016/0005-2736(72)90253-2

Electrical capacitance of lipid bilayer membranes of hydrogenated egg lecithin at the temperature phase transition
journal, December 2002

  • Antonov, Valerij F.; Anosov, Andrej A.; Norik, Vladimir P.
  • European Biophysics Journal, Vol. 32, Issue 1
  • DOI: 10.1007/s00249-002-0266-7

Lipid phase transition in planar bilayer membrane and its effect on carrier- and pore-mediated ion transport.
journal, June 1980

  • Boheim, G.; Hanke, W.; Eibl, H.
  • Proceedings of the National Academy of Sciences, Vol. 77, Issue 6
  • DOI: 10.1073/pnas.77.6.3403

Phase transitions in planar bilayer membranes
journal, February 1975

Monolayer black membranes from bipolar lipids of archaebacteria and their temperature-induced structural changes
journal, February 1983

  • Gliozzi, Alessandra; Rolandi, Ranieri; De Rosa, Mario
  • The Journal of Membrane Biology, Vol. 75, Issue 1
  • DOI: 10.1007/BF01870798

Vesicle fusion to planar membranes is enhanced by cholesterol and low temperature
journal, January 2013

Changes in Single K+ Channel Behavior Induced by a Lipid Phase Transition
journal, December 2010

  • Seeger, Heiko M.; Aldrovandi, Laura; Alessandrini, Andrea
  • Biophysical Journal, Vol. 99, Issue 11
  • DOI: 10.1016/j.bpj.2010.10.042

Impedance Analysis of Lipid Domains in Phosphatidylcholine Bilayer Membranes Containing Ergosterol
journal, November 2005

Impedance Analysis of Phosphatidylcholine/α-Tocopherol System in Bilayer Lipid Membranes
journal, May 2005

Impedance analysis of phosphatidylcholine–cholesterol system in bilayer lipid membranes
journal, March 2005

Impedance analysis of a phosphatidylcholine–phosphatidylethanolamine system in bilayer lipid membranes
journal, July 2006

Physicochemical analysis of phosphatidylcholine-ceramide system in bilayer lipid membranes.
journal, December 2008

  • Naumowicz, Monika; Petelska, Aneta Dorota; Figaszewski, Zbigniew Artur
  • Acta Biochimica Polonica, Vol. 55, Issue 4
  • DOI: 10.18388/abp.2008_3033

Impedance Analysis of Complex Formation Equilibria in Phosphatidylcholine Bilayers Containing Decanoic Acid or Decylamine
journal, February 2011

  • Naumowicz, Monika; Petelska, Aneta Dorota; Figaszewski, Zbigniew Artur
  • Cell Biochemistry and Biophysics, Vol. 61, Issue 1
  • DOI: 10.1007/s12013-011-9171-y

Phase Separation in Lipid Membranes
journal, March 2011

Critical fluctuations in domain-forming lipid mixtures
journal, October 2007

  • Veatch, S. L.; Soubias, O.; Keller, S. L.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 45
  • DOI: 10.1073/pnas.0703513104

Closed-Loop Miscibility Gap and Quantitative Tie-Lines in Ternary Membranes Containing Diphytanoyl PC
journal, June 2006

The in vivo structure of biological membranes and evidence for lipid domains
journal, May 2017

Phase transition behaviors of the supported DPPC bilayer investigated by sum frequency generation (SFG) vibrational spectroscopy and atomic force microscopy (AFM)
journal, January 2016

  • Wu, Heng-Liang; Tong, Yujin; Peng, Qiling
  • Physical Chemistry Chemical Physics, Vol. 18, Issue 3
  • DOI: 10.1039/C5CP04960A

Diffusion in supported lipid bilayers: Influence of substrate and preparation technique on the internal dynamics
journal, December 2008

Comparison of Actin- and Glass-Supported Phospholipid Bilayer Diffusion Coefficients
journal, April 2015

  • Sterling, Sarah M.; Dawes, Ryan; Allgeyer, Edward S.
  • Biophysical Journal, Vol. 108, Issue 8
  • DOI: 10.1016/j.bpj.2015.02.033

Ternary Lipid Bilayers Containing Cholesterol in a High Curvature Silica Xerogel Environment
journal, June 2010

  • Goksu, Emel I.; Longo, Marjorie L.
  • Langmuir, Vol. 26, Issue 11
  • DOI: 10.1021/la9046885

Supported Lipid Bilayers on Mica and Silicon Oxide: Comparison of the Main Phase Transition Behavior
journal, July 2010

  • Seeger, Heiko M.; Cerbo, Alessandro Di; Alessandrini, Andrea
  • The Journal of Physical Chemistry B, Vol. 114, Issue 27
  • DOI: 10.1021/jp1026477

Droplet interface bilayers
journal, January 2008

  • Bayley, Hagan; Cronin, Brid; Heron, Andrew
  • Molecular BioSystems, Vol. 4, Issue 12
  • DOI: 10.1039/b808893d

Determining Membrane Capacitance by Dynamic Control of Droplet Interface Bilayer Area
journal, December 2011

  • Gross, Linda C. M.; Heron, Andrew J.; Baca, Sylvan C.
  • Langmuir, Vol. 27, Issue 23
  • DOI: 10.1021/la203081v

Direct in situ measurement of specific capacitance, monolayer tension, and bilayer tension in a droplet interface bilayer
journal, January 2015

  • Taylor, Graham J.; Venkatesan, Guru A.; Collier, C. Patrick
  • Soft Matter, Vol. 11, Issue 38
  • DOI: 10.1039/C5SM01005E

Physicochemical characterization of 1,2-diphytanoyl-sn-glycero-3-phosphocholine in model membrane systems
journal, July 1979

  • Lindsey, H.; Petersen, N. O.; Chan, Sunney I.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 555, Issue 1
  • DOI: 10.1016/0005-2736(79)90079-8

Phase diagram of a 4-component lipid mixture: DSPC/DOPC/POPC/chol
journal, September 2013

  • Konyakhina, Tatyana M.; Wu, Jing; Mastroianni, James D.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 9
  • DOI: 10.1016/j.bbamem.2013.05.020

Control of a Nanoscopic-to-Macroscopic Transition: Modulated Phases in Four-Component DSPC/DOPC/POPC/Chol Giant Unilamellar Vesicles
journal, July 2011

  • Konyakhina, Tatyana M.; Goh, Shih Lin; Amazon, Jonathan
  • Biophysical Journal, Vol. 101, Issue 2
  • DOI: 10.1016/j.bpj.2011.06.019

Bilayer Thickness Mismatch Controls Domain Size in Model Membranes
journal, February 2013

  • Heberle, Frederick A.; Petruzielo, Robin S.; Pan, Jianjun
  • Journal of the American Chemical Society, Vol. 135, Issue 18
  • DOI: 10.1021/ja3113615

Heating-Enabled Formation of Droplet Interface Bilayers Using Escherichia coli Total Lipid Extract
journal, December 2014

  • Taylor, Graham J.; Sarles, Stephen A.
  • Langmuir, Vol. 31, Issue 1
  • DOI: 10.1021/la503471m

Adhesive force between paired microdroplets coated with lipid monolayers
journal, January 2013

  • Yanagisawa, Miho; Yoshida, Taka-aki; Furuta, Miyuki
  • Soft Matter, Vol. 9, Issue 25
  • DOI: 10.1039/c3sm50938a

Tuning lipid mixtures to induce or suppress domain formation across leaflets of unsupported asymmetric bilayers
journal, January 2008

  • Collins, M. D.; Keller, S. L.
  • Proceedings of the National Academy of Sciences, Vol. 105, Issue 1
  • DOI: 10.1073/pnas.0702970105

On demand modulation of lipid composition in an individual bilayer
journal, January 2017

  • Danial, John S. H.; Cronin, Bríd; Mallik, Chandini
  • Soft Matter, Vol. 13, Issue 9
  • DOI: 10.1039/C6SM01774F

Phase Separations in Binary and Ternary Cholesterol-Phospholipid Mixtures
journal, May 2010

Fluorescence probe partitioning between Lo/Ld phases in lipid membranes
journal, September 2007

  • Baumgart, Tobias; Hunt, Geoff; Farkas, Elaine R.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1768, Issue 9
  • DOI: 10.1016/j.bbamem.2007.05.012

Phase behavior and domain size in sphingomyelin-containing lipid bilayers
journal, April 2013

  • Petruzielo, Robin S.; Heberle, Frederick A.; Drazba, Paul
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1828, Issue 4
  • DOI: 10.1016/j.bbamem.2013.01.007

Comparison of Three Ternary Lipid Bilayer Mixtures: FRET and ESR Reveal Nanodomains
journal, November 2010

The Effect of Membrane Lipid Composition on the Formation of Lipid Ultrananodomains
journal, October 2015

Temperature-dependent structural changes in planar bilayer membranes: Solvent “freeze-out”
journal, July 1974

Fluid phase lipid areas and bilayer thicknesses of commonly used phosphatidylcholines as a function of temperature
journal, November 2011

  • Kučerka, Norbert; Nieh, Mu-Ping; Katsaras, John
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 1808, Issue 11
  • DOI: 10.1016/j.bbamem.2011.07.022

The organization of n-alkanes in lipid bilayers
journal, April 1980

  • McIntosh, T. J.; Simon, S. A.; MacDonald, R. C.
  • Biochimica et Biophysica Acta (BBA) - Biomembranes, Vol. 597, Issue 3
  • DOI: 10.1016/0005-2736(80)90219-9

Tensions and free energies of formation of "solventless" lipid bilayers. Measurement of high contact angles
journal, March 1983

Voltage dependence of the capacitance and area of black lipid membranes
journal, November 1981

Critical Phenomena in a Surfactant/Water/Oil System. Basic Study on the Correlation between Solubilization, Microemulsion, and Ultralow Interfacial Tensions
journal, April 1981

  • Kunieda, Hironobu; Friberg, Stig E.
  • Bulletin of the Chemical Society of Japan, Vol. 54, Issue 4
  • DOI: 10.1246/bcsj.54.1010

The lipid bilayer as a ‘solvent’ for small hydrophobic molecules
journal, July 1976

Adhesion of Water Droplets in Organic Solvent
journal, October 1998

How principles of domain formation in model membranes may explain ambiguities concerning lipid raft formation in cells
journal, December 2005

Lipid ion channels
journal, August 2010

The Temperature Dependence of Lipid Membrane Permeability, its Quantized Nature, and the Influence of Anesthetics
journal, June 2009

  • Blicher, Andreas; Wodzinska, Katarzyna; Fidorra, Matthias
  • Biophysical Journal, Vol. 96, Issue 11
  • DOI: 10.1016/j.bpj.2009.01.062

The appearance of single-ion channels in unmodified lipid bilayer membranes at the phase transition temperature
journal, February 1980

  • Antonov, V. F.; Petrov, V. V.; Molnar, A. A.
  • Nature, Vol. 283, Issue 5747
  • DOI: 10.1038/283585a0

1 H NMR Shows Slow Phospholipid Flip-Flop in Gel and Fluid Bilayers
journal, February 2017

Lipid droplets, lipophagy, and beyond
journal, August 2016

  • Wang, Chao-Wen
  • Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids, Vol. 1861, Issue 8
  • DOI: 10.1016/j.bbalip.2015.12.010

Biogenesis of the multifunctional lipid droplet: Lipids, proteins, and sites
journal, March 2014

  • Pol, Albert; Gross, Steven P.; Parton, Robert G.
  • The Journal of Cell Biology, Vol. 204, Issue 5
  • DOI: 10.1083/jcb.201311051

Preparation of fatty acid methyl esters for gas-liquid chromatography
journal, September 2009

  • Ichihara, Ken'ichi; Fukubayashi, Yumeto
  • Journal of Lipid Research, Vol. 51, Issue 3
  • DOI: 10.1194/jlr.D001065

Preparation of giant vesicles by external AC electric fields. Kinetics and applications
book, January 2007

  • Angelova, M. I.; Soleau, S.; Meleard, Ph.
  • Progress in Colloid & Polymer Science
  • DOI: 10.1007/BFb0116295
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