Spontaneous phosphatidylcholine transfer by collision between vesicles at high lipid concentration

Abstract

The transfer kinetics of [3H]-1-palmitoyl-2-oleoylphosphatidylcholine ([3H]POPC) and 1-palmitoyl-2-(pyrenyldecanoyl)phosphatidylcholine (PyrPC) from POPC small unilamellar vesicles were examined at 37 degrees C with lipid concentrations ranging from 0.1 to 40 mM. The rate of [3H]POPC transfer was determined by analyzing the movement of this lipid from charged donor to neutral acceptor vesicles. The rate of decay of the ratio of the intensity of pyrene excimer fluorescence to that from the pyrene monomer (E/M) upon addition of an unlabeled vesicle population to a population containing PyrPC was used to evaluate PyrPC transfer. For both lipids, the kinetic data are best described by a model which assumes that transfer occurs by vesicle collisions as well as by desorption from the bilayer. For [3H]POPC, the off-rate constant is 0.014 h-1 while the collisional rate constant is 0.0016 mM-1 h-1. PyrPC has an off-rate constant of 0.023 h-1 and a collisional constant of 0.0015 mM-1 h-1. These numbers were calculated by assuming the rate of interbilayer transfer to be negligible relative to that of intervesicular transfer. The large transfer fluxes in the high vesicle concentration range where the collisional process dominates suggest that spontaneous transfer may be of importance in membrane biogenesis.

Spontaneous lipid transfer between organized lipid assemblies

“…23,26,57,66,[110][111][112][113][114][132][133][134][135]. Then, two different laboratories both reported increased spontaneous lipid transfer rates attributable to transient collisions between donor and acceptor surfaces [96][97][98][107][108][109]. Although similar claims had been reported previously [22,113], it was difficult to rule out fusion between vesicles [113] and protein-mediated lipid transfer [22,137] in these earlier reports.…”

“…Thus, potential mechanisms for minimizing random intracellular spontaneous lipid transfer do exist. In addition, recent reports indicate that the spontaneous transfer rates of long-chain diacyl PCs between bile salt micelles [96][97][98] as well as between phospholipid bilayers [107][108][109] can be increased significantly when micelle or vesicle concentrations are high. The mechanism by which these enhanced spontaneous lipid transfer rates are achieved is discussed in detail in section IV-B and represents a significant new advance in the field.…”

“…Meanwhile, Thompson and co-workers [107][108][109] observed that, under appropriate conditions. POPC spontaneous transfer between bilayer vesicles is characterized by two rate processes.…”

“…1A. Only recently has compelling evidence mounted to warrant serious consideration of other mechanisms [96][97][98][107][108][109]157]. Accordingly, a detailed discussion of alternative models for lipid transfer (e.g., Fig.…”

Nonvesicular Lipid Transfer from the Endoplasmic Reticulum

“…Nonvesicular lipid transport between membranes could be mediated by spontaneous lipid transport, in which a lipid monomer is diffused through the cytosol from a donor to the acceptor membrane. Given that most cellular lipids are highly hydrophobic, their diffusion through an aqueous phase is very slow and insufficient to support substantial transport of most lipids (Jones and Thompson 1989;Mesmin and Maxfield 2009). Nevertheless, spontaneous lipid transport can be greatly facilitated at membrane contact sites (MCSs) (Levine 2004;Holthuis and Levine 2005) and/or by lipid-transfer proteins (LTPs) (Lev 2010).…”