Abstract

H2O2 permeation through a cell membrane significantly affects living organisms, and permeation is controlled by the physico-chemical nature of lipids and other membrane components. We investigated the molecular relationship between H2O2 permeation and lipid membrane structure using three oxidized lipids. POVPC and PazePC act as intra- and inter-molecular permeation promoters, respectively; however, their underlying mechanisms were different. The former changed the partition equilibrium, while the latter changed the permeation pathway. PoxnoPC inhibited permeation under our experimental conditions via an intra-molecular configuration change. Thus, both intra- and inter-molecular processes were found to control the role of oxidized lipids as inhibitors and promoters towards H2O2 permeation with different mechanisms depending on structure and composition. Here, we identified two independent H2O2 permeation routes: (i) permeation through lipid membrane with increased partition coefficient by intra-molecular configurational change and (ii) diffusion through pores (water channels) formed by inter-molecular configurational change of oxidized lipids. We provide new insight into how biological cells control permeation of molecules through intra- and inter-molecular configurational changes in the lipid membrane. Thus, by employing a rational design for both oxidized lipids and other components, the permeation behaviour of H2O2 and other ions and molecules through a lipid membrane could be controlled.

Highlights

  • Cell membrane acts as a physical barrier that prevents the exchange of ions and molecules between a cell’s internal and external environments

  • H2O2 permeation rate P first increases from 0.007 to 0.015 with the addition of POVPC until its molar concentration exceeds 5 mol %, which indicates that the presence of POVPC below 5 mol % enhances passive permeation of H2O2 molecules (Fig. 2a)

  • POVPC showed an intra-molecular switching from nonlooped to looped configuration depending on its concentration in the dioleoyl-sn-glycero-3-p hosphocholine (DOPC) membrane, which changed the role of POVPC from permeation inhibitor to promoter

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Summary

Introduction

Cell membrane acts as a physical barrier that prevents the exchange of ions and molecules between a cell’s internal and external environments. Concerning passive permeation through cell membranes, an influence of the oxidized lipid has been investigated by both experiments and simulations[29,30,32,39,40,41], especially focusing on its effect on intra-molecular and an inter-molecular structural changes. The former involves the reorientation of the oxidized tails (sn-2 acyl chains) toward the water/ membrane interface to form hydrogen bonds with water and the polar headgroup of surrounding lipids[27,28,32,33]. The present study focused on permeation of the H2O2 molecule, our finding on the relation between permeation and structure can be applied to other ions and molecules as well

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