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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];  [1];  [1];  [1];  [1];  [1]
  1. Department of Mechanical, Aerospace, and Biomedical Engineering, and §Department of Physics and Astronomy, The University of Tennessee, Knoxville, Tennessee 37996, United States; Joint Institute for Biological Sciences, ⊥Biology and Soft Matter Division, #Shull Wollan Center—A Joint Center for Neutron Sciences, and ∇Center for Nanophase Materials Sciences, Oak Ridge National Laboratory, Oak Ridge, Tennessee 37831, United States
Publication Date:
Research Org.:
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22)
OSTI Identifier:
1427658
DOE Contract Number:  
AC05-00OR22725
Resource Type:
Journal Article
Resource Relation:
Journal Name: Langmuir; Journal Volume: 33; Journal Issue: 38
Country of Publication:
United States
Language:
English

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.
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. doi:10.1021/acs.langmuir.7b02022.
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. doi:10.1021/acs.langmuir.7b02022. https://www.osti.gov/servlets/purl/1427658.
@article{osti_1427658,
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 29 00:00:00 EDT 2017},
month = {Tue Aug 29 00:00:00 EDT 2017}
}