Interplay between Structure and Fluidity of Model Lipid Membranes under Oxidative Attack

Abstract

A proper regulation of membrane fluidity is critical for cellular activities such as communication between cells, mitosis, and endocytosis. Unsaturated lipids, a main component of biological membranes, are particularly susceptible to oxidative attack of reactive oxygen species. The oxidation of lipids can produce structural derangement of membranes and eventually alter the membrane fluidity. We have applied fluorescence correlation spectroscopy (FCS) and Raman spectroscopy to investigate the fluidity and structure of model membranes subject to oxidative attack. Hydrogen peroxide has little effect on the lateral fluidity of membranes, whereas hydroxyl radical causes a significantly increased fluidity. The latter is rationalized with the cleavage of the acyl chains of lipids caused by hydroxyl radical; this interpretation is founded on the diminished intensities of lines in Raman spectra associated with -CH(2) and C═C moieties in lipids and supported by mass-spectral measurements. The same approach provides a mechanistic account of the inhibitory capability of vitamins C and E against the increased membrane fluidity resulting from an oxidative attack. Membranes with much cholesterol exhibit a novel resistance against altered membrane fluidity induced with oxidative attack; this finding has biological implications. Our approach combining FCS and Raman measurements reveals the interplay between the structure and fluidity of membranes and provides insight into the pathophysiology of cellular oxidative injury.

High revivability of vitrified–warmed bovine mature oocytes after recovery culture with α-tocopherol

“…These differences might be associated with the affinity of antioxidants, as the hydrophobic a-tocopherol protects the lipid bilayer of the plasma membrane from oxidative stress (Gutnisky et al 2013). Oxidative stress increases membrane fluidity through cleavage of the lipid acyl chain (Tai et al 2010). Such alterations in membrane property might disturb uptake of extracellular components essential for supporting physiological aster formation.…”

Effect of head group and lipid tail oxidation in the cell membrane revealed through integrated simulations and experiments

“…The latter can then alter the structural and dynamic properties of the membrane, which can lead to an increase in the permeability, a change in the lipid order and bilayer thickness as well as in its fluidity 15–23 .…”

“…There are already several experimental studies 15–18, 24, 25 and a few simulation papers 20–22, 26 devoted to a detailed investigation of the effect of lipid oxidation on the properties of the lipid membrane. Tai et al .…”

“…Tai et al . studied the fluidity and structure of model membranes (i.e., giant unilaminar vesicles) under oxidative attack, using fluorescence correlation spectroscopy and Raman spectroscopy 15 . They found that OH radicals cause a significantly higher lateral fluidity of the membranes, while hydrogen peroxide has little effect 15 .…”

“…studied the fluidity and structure of model membranes (i.e., giant unilaminar vesicles) under oxidative attack, using fluorescence correlation spectroscopy and Raman spectroscopy 15 . They found that OH radicals cause a significantly higher lateral fluidity of the membranes, while hydrogen peroxide has little effect 15 . An increase of the membrane disordering was observed in 16, 17 , while in 18, 24 , the opposite effect was reported, i.e., an increase of the lipid order and a drop in the membrane fluidity.…”