Curvature-driven lateral segregation of membrane constituents in Golgi cisternae

Derganc, Jure

doi:10.1088/1478-3975/4/4/008

Cited by 39 publications

(52 citation statements)

References 24 publications

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“…8). Indeed, in agreement with previous experimental and theoretical studies [19][20][21][22][23][24] , lipid sorting by membrane shape is not efficient when physiological radii are considered and does not correct significantly lipidpacking defects.…”

Section: Discussionsupporting

confidence: 91%

“…Most lipids are flexible molecules and, through shape adjustment, might minimize unfavourable exposure of their hydrocarbon chains to water. In addition, lipids with noncylindrical shape (for example, lysolipids or diacylglycerols) could distribute non-randomly within regions of different curvature to reduce geometrical mismatches, although the efficiency of such a mechanism has been questioned due to the propensity of lipids to readily mix through the entropic effect [19][20][21][22][23][24] .…”

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confidence: 99%

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A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment

et al. 2014

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Two parameters of biological membranes, curvature and lipid composition, direct the recruitment of many peripheral proteins to cellular organelles. Although these traits are often studied independently, it is their combination that generates the unique interfacial properties of cellular membranes. Here, we use a combination of in vivo, in vitro and in silico approaches to provide a comprehensive map of how these parameters modulate membrane adhesive properties. The correlation between the membrane partitioning of model amphipathic helices and the distribution of lipid-packing defects in membranes of different shape and composition explains how macroscopic membrane properties modulate protein recruitment by changing the molecular topography of the membrane interfacial region. Furthermore, our results suggest that the range of conditions that can be obtained in a cellular context is remarkably large because lipid composition and curvature have, under most circumstances, cumulative effects.

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Section: Discussionsupporting

confidence: 91%

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confidence: 99%

A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment

et al. 2014

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“…From Table 2, the curvature preference of all the NBD-labeled lipids would become very low (<10%) in SUVs with a diameter larger than 100 nm. These observations support predictions of coarse-grained molecular-dynamic simulations in SUVs (20,21) and theoretical studies (2,19).…”

Section: Discussionsupporting

confidence: 85%

“…Not all lipids form the H II phase; however, the spontaneous curvature of some other lipids can be estimated by analyzing the perturbation in the periodicity of the DOPE H II phase caused by the addition of the second lipid type (17,18). Theoretical studies based on these measurements (2,19) and molecular-dynamic simulations (20,21) suggested that the curvature preference of lipids is weaker than that observed in biological systems. Consistent with these studies, no significant sorting of lipids into membrane nanotubes was observed (22,23).…”

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confidence: 99%

Measurement of the membrane curvature preference of phospholipids reveals only weak coupling between lipid shape and leaflet curvature

Kamal

Mills

Grzybek

et al. 2009

Proc. Natl. Acad. Sci. U.S.A.

126

115

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In biological processes, such as fission, fusion and trafficking, it has been shown that lipids of different shapes are sorted into regions with different membrane curvatures. This lipid sorting has been hypothesized to be due to the coupling between the membrane curvature and the lipid's spontaneous curvature, which is related to the lipid's molecular shape. On the other hand, theoretical predictions and simulations suggest that the curvature preference of lipids, due to shape alone, is weaker than that observed in biological processes. To distinguish between these different views, we have directly measured the curvature preferences of several lipids by using a fluorescence-based method. We prepared small unilamellar vesicles of different sizes with a mixture of egg-PC and a small mole fraction of N-nitrobenzoxadiazole (NBD)-labeled phospholipids or lysophospholipids of different chain lengths and saturation, and measured the NBD equilibrium distribution across the bilayer. We observed that the transverse lipid distributions depended linearly on membrane curvature, allowing us to measure the curvature coupling coefficient. Our measurements are in quantitative agreement with predictions based on earlier measurements of the spontaneous curvatures of the corresponding nonfluorescent lipids using X-ray diffraction. We show that, though some lipids have high spontaneous curvatures, they nevertheless showed weak curvature preferences because of the low values of the lipid molecular areas. The weak curvature preference implies that the asymmetric lipid distributions found in biological membranes are not likely to be driven by the spontaneous curvature of the lipids, nor are lipids discriminating sensors of membrane curvature.curvature coupling | lipid spontaneous curvature | small unilamellar vesicle | fluorescence quenching I n biological membranes, lipids are not distributed homogeneously. The inhomogeneity of lipid distributions within a bilayer may be due to preferential association of particular lipid types with membrane proteins (1, 2), domain formation as a result of the interactions between lipids and sterols (3) or due to the preferences of lipids of different shapes toward regions of matching membrane curvature (4). Membrane regions in which the lipid inhomogeneity or sorting is observed are often highly curved. For example, (i) during mating in the protozoon Tetrahymena thermophila, the pore-containing membrane regions, which become highly negatively curved during fusion, are enriched in coneshaped 2-aminoethylphosphonolipids (5); (ii) in Ca 2+ -dependent exocytosis and in regulated synaptic vesicle fusion, cone-shaped phosphatidylinositol-4,5-bisphosphate lipids are important (6, 7), and are thought to facilitate the formation of an intermediate fusion structure by localizing at the fusion site (8); and (iii) lipids of different shapes are differently sorted in the tubules and vesicles in the endosomal pathway (9). These observations have raised the possibility that the distribution of the lipids may be de...

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“…Both C 0 and k depend on the composition of the curved patch. If this patch is more curved than its surroundings, the bending energy can be lowered by adjusting the composition to reduce k and/or to have C 0 match C. This idea has been explored theoretically, with special emphasis on the interplay between lipid inhomogeneity and the mechanical properties of vesicles (Markin 1981;Seifert 1993;Derganc 2007;Jiang and Powers 2008;Sorre et al 2009). …”

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confidence: 99%

Curvature-Driven Lipid Sorting in Biomembranes

Callan-Jones¹,

Sorre²,

Bassereau³

2011

Cold Spring Harbor Perspectives in Biology

125

128

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It has often been suggested that the high curvature of transport intermediates in cells may be a sufficient means to segregate different lipid populations based on the relative energy costs of forming bent membranes. In this review, we present in vitro experiments that highlight the essential physics of lipid sorting at thermal equilibrium: It is driven by a trade-off between bending energy, mixing entropy, and interactions between species. We collect evidence that lipid sorting depends strongly on lipid -lipid and protein-lipid interactions, and hence on the underlying composition of the membrane and on the presence of bound proteins.

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Curvature-driven lateral segregation of membrane constituents in Golgi cisternae

Cited by 39 publications

References 24 publications

A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment

A sub-nanometre view of how membrane curvature and composition modulate lipid packing and protein recruitment

Measurement of the membrane curvature preference of phospholipids reveals only weak coupling between lipid shape and leaflet curvature

Curvature-Driven Lipid Sorting in Biomembranes

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