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

Abstract

We investigate the permeability of lipid membranes for fluorescence dyes and ions. We find that permeability reaches a maximum close to the chain melting transition of the membranes. Close to transitions, fluctuations in area and compressibility are high, leading to an increased likelihood of spontaneous lipid pore formation. Fluorescence correlation spectroscopy reveals the permeability for rhodamine dyes across 100-nm vesicles. Using fluorescence correlation spectroscopy, we find that the permeability of vesicle membranes for fluorescence dyes is within error proportional to the excess heat capacity. To estimate defect size we measure the conductance of solvent-free planar lipid bilayer. Microscopically, we show that permeation events appear as quantized current events very similar to those reported for channel proteins. Further, we demonstrate that anesthetics lead to a change in membrane permeability that can be predicted from their effect on heat capacity profiles. Depending on temperature, the permeability can be enhanced or reduced. We demonstrate that anesthetics decrease channel conductance and ultimately lead to blocking of the lipid pores in experiments performed at or above the chain melting transition. Our data suggest that the macroscopic increase in permeability close to transitions and microscopic lipid ion channel formation are the same physical process.

Drunken Membranes: Short-Chain Alcohols Alter Fusion of Liposomes to Planar Lipid Bilayers

“…In support of the indirect pathway, it has been proposed (21), and supported by statistical thermodynamics (3,22) and coarse-grain modeling (23), that alcohol changes the lateral pressure within the membrane and that this increase can bias ion channels toward the closed state. In support of the direct pathway it has be shown that both ethanol (24) and other anesthetics (25) can change the permeability of lipid membranes.…”

Analysis of laser-induced heating in optical neuronal guidance

“…There are no reports on neuronal growth in temperature microgradients in the literature, but it is known that bulk neuronal development is temperature-dependent (Ishida and Cheng, 1991;Fukui et al, 1992), and that some organisms (nematodes) have been shown to be extremely temperature sensitive, exhibiting thermotaxis up temperature gradients as small as 10 −4 • C/cm (Pline et al, 1988). It also seems that depolarization of the neuronal membrane is highly dependent on small variations in thermodynamic variables like temperature (Wunderlich et al, 2009;Blicher et al, 2009;Andersen et al, 2009;Wodzinska et al, 2009).…”

“…It has been shown that chemical guidance of growth cones is mediated by an asymmetric influx of calcium ions Ca 2+ ) and the neuronal transient receptor potential (TRP) channels appear to be the key sensors and mediators in the process (Wang and Poo, 2005;Talavera et al, 2008;Li et al, 2005;Sappington et al, 2009). It is know that TRP channels can be activated by depolarization of the cell using chemical guidance factors or by an increase in temperature (Talavera et al, 2008;Caterina et al, 1997) and highly localized heating (Huang et al, 2010), and there is strong evidence in general that depolarization of the neuronal membrane is highly sensitive to small variations in thermodynamic variables like temperature and pressure (Wunderlich et al, 2009;Blicher et al, 2009;Andersen et al, 2009;Wodzinska et al, 2009). We therefore propose the hypothesis that the optical neuronal guidance is mediated by laser-induced heating, in particular by influx of Ca 2+ -ions due to heat-induced activation of neuronal TRP channels, discussed more thoroughly in Section 4.1.…”

Ion-channel-like behavior in lipid bilayer membranes at the melting transition

“…For further details the reader is referred to Refs. [8] and [9]. Our bilayer membrane was made up of dioleoyl-phosphatidylcholine (DOPC) and dipalmitoyl phosphatidylcholine (DPPC) in a 2:1 ratio.…”