The dual effect of oxidation on lipid bilayer structure

Abstract

Sphingomyelin membranes were prepared with different levels of oxidative damage caused by tert-butyl hydroperoxide (TBH). Temperature-induced changes in membrane hydrocarbon chain packing (phase transitions) were monitored using infrared spectroscopy. Lipid phase transition characteristics were evaluated from thermodynamic parameters fitted to the experimental transition curve data. At temperatures below the lipid phase transition Tc, hydrocarbon chains pack in an ordered state whereas above the Tc the hydrocarbon chains pack in a disordered state. Compared to the non-oxidized control, the packing of the hydrocarbon chains of mildly oxidized sphingomyelin (less than 10 nmol TBH/mg lipid) was no different at all temperatures below the Tc, and was more ordered above the Tc. The hydrocarbon chains of strongly oxidized sphingomyelin (greater than 10 nmol TBH/mg lipid) were more disordered at temperatures above and below the Tc compared to the control samples. These results suggest that lipid oxidation has a dual effect on lipid order. A more ordered or disordered state may result depending on the degree of oxidation and the state of lipid order prior to oxidation. These results could be important for explaining the structural changes in oxidized membranes high in sphingomyelin such as those found in the ocular lens and liver plasma membranes.

Sphingolipids in human lens membranes: an update on their composition and possible biological implications

“…Beyond the studies reviewed in 1984, multiple reports have demonstrated the relevance of lens lipid oxidation with age and cataract formation (Ahuja et al, 1999;Borchman et al, 1992Borchman et al, , 2000Borchman and Yappert, 1998;Girao et al, 1998;Jernigan et al, 1993;Ogiso et al, 1993;Simonelli et al, 1996;Zhang et al, 1999). This topic will not be discussed in detail, but many studies have demonstrated that the propensity of lens mammalian membranes toward degradation is inversely related to the contents of sphingolipids (Babizhayev et al, 1988;Bhuyan and Bhuyan, 1994;Bhuyan et al, 1991Bhuyan et al, , 1996Borchman et al, 2000;Borchman and Yappert, 1998;Girao et al, 1998;Reddy et al, 1999;Simonelli et al, 1996;Varma et al, 1994).…”

Lipids and the ocular lens

“…Oxidized lipids contain hydrophilic groups such as hydroxyl and hydroperoxyl moieties located on the hydrophobic hydrocarbon chains that disrupt lipid-lipid interactions, causing structural irregularities in the membrane ( 60 ). Phospholipase A2 degrades lipids at points in the membrane that exhibit such structural irregularities ( 61 ).…”

Peroxidation of polyunsaturated phosphatidyl-choline lipids during electroformation

“…This then alters the lipid composition and mechanical packing of the vesicle that subsequently forms [16][17][18][19]. As a result, there could be changes in liposomal permeability [20][21][22] and the subtle interactions between lipids and membrane proteins and/or other amphiphilic molecules [16].…”