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PMID: 15111647 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Regulation of sodium channel function by bilayer elasticity: the importance of hydrophobic coupling. Effects of Micelle-forming amphiphiles and cholesterol.

The Journal of general physiology ·Vol. 123 ·No. 5 ·2004-05-00 ·Pages 599-621

Lundbaek JA, Birn P, Hansen AJ, Søgaard R, Nielsen C, Girshman J, Bruno MJ, Tape SE, Egebjerg J, Greathouse DV, Mattice GL, Koeppe RE, Andersen OS

Abstract

Membrane proteins are regulated by the lipid bilayer composition. Specific lipid-protein interactions rarely are involved, which suggests that the regulation is due to changes in some general bilayer property (or properties). The hydrophobic coupling between a membrane-spanning protein and the surrounding bilayer means that protein conformational changes may be associated with a reversible, local bilayer deformation. Lipid bilayers are elastic bodies, and the energetic cost of the bilayer deformation contributes to the total energetic cost of the protein conformational change. The energetics and kinetics of the protein conformational changes therefore will be regulated by the bilayer elasticity, which is determined by the lipid composition. This hydrophobic coupling mechanism has been studied extensively in gramicidin channels, where the channel-bilayer hydrophobic interactions link a "conformational" change (the monomer<-->dimer transition) to an elastic bilayer deformation. Gramicidin channels thus are regulated by the lipid bilayer elastic properties (thickness, monolayer equilibrium curvature, and compression and bending moduli). To investigate whether this hydrophobic coupling mechanism could be a general mechanism regulating membrane protein function, we examined whether voltage-dependent skeletal-muscle sodium channels, expressed in HEK293 cells, are regulated by bilayer elasticity, as monitored using gramicidin A (gA) channels. Nonphysiological amphiphiles (beta-octyl-glucoside, Genapol X-100, Triton X-100, and reduced Triton X-100) that make lipid bilayers less "stiff", as measured using gA channels, shift the voltage dependence of sodium channel inactivation toward more hyperpolarized potentials. At low amphiphile concentration, the magnitude of the shift is linearly correlated to the change in gA channel lifetime. Cholesterol-depletion, which also reduces bilayer stiffness, causes a similar shift in sodium channel inactivation. These results provide strong support for the notion that bilayer-protein hydrophobic coupling allows the bilayer elastic properties to regulate membrane protein function.

MeSH Terms
Adaptation, Physiological/drug effects,physiology Cell Line Cell Membrane/drug effects,physiology Cholesterol/metabolism Elasticity Gramicidin/pharmacology Humans Hydrophobic and Hydrophilic Interactions Kidney/drug effects,physiology Lipid Bilayers/metabolism Mechanotransduction, Cellular/drug effects,physiology Membrane Fluidity/drug effects,physiology Membrane Potentials/drug effects,physiology Micelles Sodium Channels/drug effects,physiology Surface-Active Agents/metabolism
Chemicals
Lipid Bilayers Micelles Sodium Channels Surface-Active Agents Gramicidin Cholesterol
Authors & Affiliations
13 authors, click to expand affiliations / ORCID
Lundbaek Jens A
Novo Nordisk A/S, Måløv, Denmark. [email protected]
Birn Pia
Hansen Anker J
Søgaard Rikke
Nielsen Claus
Girshman Jeffrey
Bruno Michael J
Tape Sonya E
Egebjerg Jan
Greathouse Denise V
Mattice Gwendolyn L
Koeppe Roger E
Andersen Olaf S
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Article Info
Journal
The Journal of general physiology
Abbr.
J Gen Physiol
ISSN
0022-1295
DOI
10.1085/jgp.200308996
Email
[email protected]
Published
2004-05-00
Pages
599-621
Language
English
Region
United States
NLM ID
2985110R
PMCID
PMC2234500
Subset
IM
Grants
NCRR NIH HHS · P20 RR015569 · United States
NCRR NIH HHS · RR15569 · United States
NIGMS NIH HHS · GM34968 · United States
NIGMS NIH HHS · R01 GM021342 · United States
NIGMS NIH HHS · GM21342 · United States
External Links
PubMed source DOI: 10.1085/jgp.200308996 PMC Full Text View journal details
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