Lipid packing variations induced by pH in cardiolipin-containing bilayers: The driving force for the cristae-like shape instability

• Published in: Biochimica et biophysica acta Vol. 1808; no. 11; pp. 2724 - 2733
• Main Authors: Khalifat, Nada, Fournier, Jean-Baptiste, Angelova, Miglena I., Puff, Nicolas
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 01.11.2011; Elsevier
• Subjects: Cardiolipin; Cardiolipins - chemistry; Condensed Matter; Curvature instability; GUV; Hydrogen-Ion Concentration; Laurdan; Lipid Bilayers - chemistry; Microscopy; Mitochondrion; Physics; Soft Condensed Matter; Unilamellar Liposomes - chemistry; IMM; CL; GUV; GP; LUV; Mitochondrion; PC; PE; pH; Laurdan; Cardiolipin; Curvature instability; DPH
• ISSN: 0005-2736; 0006-3002; 1879-2642
• DOI: 10.1016/j.bbamem.2011.07.013

Cardiolipin is a four-tailed acidic lipid found predominantly within the inner membrane of mitochondria, and is thought to be a key component in determining inner membrane properties and potential. Thus, cardiolipin may be involved in the dynamics of the inner membrane characteristic invaginations (named cristae) that protrude into the matrix space. In previous studies, we showed the possibility to induce, by localized proton flow, a macroscopic cristae-like shape remodeling of an only-lipid model membrane mimicking the inner mitochondrial membrane. In addition, we reported a theoretical model describing the dynamics of a chemically driven membrane shape instability caused by a modification of the plane-shape equilibrium density of the lipids in the membrane. In the present work, we focus on the lipid-packing modifications observed in a model cardiolipin-containing lipid membrane submitted to pH decrease because this is the driving force of the instability. Laurdan fluorescence and ζ-potential measurements show that under pH decrease, membrane surface charge decreases, but that significant modification of the lipid packing is observed only for CL-containing membranes. Our giant unilamellar vesicle experiments also indicate that cristae-like morphologies are only observed for CL-containing lipid membranes. Taken together, these results highlight the fact that only a strong modulation of the lipid packing of the exposed monolayer leads to membrane shape instability and suggest that mitochondrial lipids, in particular the cardiolipin, play a specific role under pH modulation in inner mitochondrial membrane morphology and dynamics. [Display omitted] ► Cardiolipin is a key component of the inner mitochondrial membrane. ► pH induced significant lipid packing modifications only for cardiolipin-containing membranes. ► Asymmetry of the best preferred area per lipid leads to membrane shape instability. ► Cristae-like morphologies are only observed for cardiolipin-containing GUVs. ► Lipids play a specific role in inner mitochondrial membrane morphology and dynamics.