TY - JOUR
T1 - Structure and pH Dependence of Membranolytic Mechanisms by Truncated Oxidized Phospholipids
AU - Xie, Min
AU - Derks, Maik G.N.
AU - Koch, Eveline H.W.
AU - van Boven, C. Bjorn
AU - Janlad, Minchakarn
AU - Bagheri, Behnaz
AU - Xu, Zexi
AU - Kovryzhenko, Daria
AU - van Walree, Cornelis A.
AU - Sobota, Ana
AU - Weingarth, Markus
AU - Wong-Ekkabut, Jirasak
AU - Karttunen, Mikko
AU - Breukink, Eefjan
AU - Killian, J. Antoinette
AU - Sonnen, Andreas F.P.
AU - Lorent, Joseph H.
N1 - Publisher Copyright:
© 2025 American Chemical Society.
PY - 2025/3/19
Y1 - 2025/3/19
N2 - Membrane lipid oxidation is a universal process that occurs in situations of oxidative stress and is encountered in numerous physiological and pathological situations. Oxidized truncated phospholipids make up a large part of the oxidation products and alter the membrane properties in a way that can lead to cell death. However, the underlying mechanisms are not well understood nor is it clear whether environmental factors, such as pH, can modulate these effects. Using model membranes, we investigate how individual lipid aldehydes and carboxylic acids with truncated acyl chains alter the membrane structure. Our data shows that lipid aldehydes and carboxylic acids have different permeabilization efficiencies towards molecules of varying charge and size and that ΔC9 truncated lipids are usually more efficient in permeabilizing membranes than ΔC5. In terms of physical mechanisms, the ΔC9 truncated lipid carboxylic acid induces permeabilization and membrane curvature in a pH-dependent fashion. This is explained by ionization-dependent exposure of the carboxyl group to the water-bilayer interface, which increases the intrinsic molecular curvature of the oxidized lipid. Conversely, ΔC9 truncated lipid aldehydes and nonionized carboxyls do not induce curved structures but are more efficient in increasing permeability toward larger molecules. We further show that truncated lipids can escape the bilayer and accumulate at interfaces, implying that they might act on neighboring cells. This study indicates that oxidized phospholipids with truncated acyl chains disrupt membrane structure, depending on their specific molecular structure and the pH of the environment, opening a possible route for the design of lipid nanoparticles with pH-dependent drug release.
AB - Membrane lipid oxidation is a universal process that occurs in situations of oxidative stress and is encountered in numerous physiological and pathological situations. Oxidized truncated phospholipids make up a large part of the oxidation products and alter the membrane properties in a way that can lead to cell death. However, the underlying mechanisms are not well understood nor is it clear whether environmental factors, such as pH, can modulate these effects. Using model membranes, we investigate how individual lipid aldehydes and carboxylic acids with truncated acyl chains alter the membrane structure. Our data shows that lipid aldehydes and carboxylic acids have different permeabilization efficiencies towards molecules of varying charge and size and that ΔC9 truncated lipids are usually more efficient in permeabilizing membranes than ΔC5. In terms of physical mechanisms, the ΔC9 truncated lipid carboxylic acid induces permeabilization and membrane curvature in a pH-dependent fashion. This is explained by ionization-dependent exposure of the carboxyl group to the water-bilayer interface, which increases the intrinsic molecular curvature of the oxidized lipid. Conversely, ΔC9 truncated lipid aldehydes and nonionized carboxyls do not induce curved structures but are more efficient in increasing permeability toward larger molecules. We further show that truncated lipids can escape the bilayer and accumulate at interfaces, implying that they might act on neighboring cells. This study indicates that oxidized phospholipids with truncated acyl chains disrupt membrane structure, depending on their specific molecular structure and the pH of the environment, opening a possible route for the design of lipid nanoparticles with pH-dependent drug release.
UR - http://www.scopus.com/inward/record.url?scp=86000188314&partnerID=8YFLogxK
U2 - 10.1021/jacs.4c12543
DO - 10.1021/jacs.4c12543
M3 - Article
C2 - 40041982
AN - SCOPUS:86000188314
SN - 0002-7863
VL - 147
SP - 9175
EP - 9189
JO - Journal of the American Chemical Society
JF - Journal of the American Chemical Society
IS - 11
ER -