Lateral phase separation in tense membranes

Hamada, Tsutomu; Kishimoto, Yuko; Nagasaki, Takeshi; Takagi, Masahiro

doi:10.1039/c1sm05948c

Cited by 99 publications

(126 citation statements)

References 48 publications

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“…Application of shear stress to GUVs consisting of phospholipids and cholesterol caused a marked decrease in their membrane lipid order, indicating that the lipid order response is a physical phenomenon that does not involve participation by any membrane proteins, the cytoskeleton, or biological activities of living cells. Membrane tension induced by the application of osmotic pressure has recently been shown to induce lateral phase separation in the homogeneous membranes of GUVs which had the same composition as our own (Hamada et al, 2011). The effects of tension and shear stress on the order of membrane lipid phases seem to be the opposite, i.e.…”

Section: Discussionmentioning

confidence: 49%

Endothelial cell and model membranes respond to shear stress by rapidly decreasing the order of their lipid phases

Yamamoto

Ando

2013

Journal of Cell Science

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SummaryEndothelial cells (ECs) sense shear stress and transduce blood flow information into functional responses that play important roles in vascular homeostasis and pathophysiology. A unique feature of shear-stress-sensing is the involvement of many different types of membrane-bound molecules, including receptors, ion channels and adhesion proteins, but the mechanisms remain unknown. Because cell membrane properties affect the activities of membrane-bound proteins, shear stress might activate various membrane-bound molecules by altering the physical properties of EC membranes. To determine how shear stress influences the cell membrane, cultured human pulmonary artery ECs were exposed to shear stress and examined for changes in membrane lipid order and fluidity by Laurdan two-photon imaging and FRAP measurements. Upon shear stress stimulation, the lipid order of EC membranes rapidly decreased in an intensity-dependent manner, and caveolar membrane domains changed from the liquid-ordered state to the liquid-disordered state. Notably, a similar decrease in lipid order occurred when the artificial membranes of giant unilamellar vesicles were exposed to shear stress, suggesting that this is a physical phenomenon. Membrane fluidity increased over the entire EC membranes in response to shear stress. Addition of cholesterol to ECs abolished the effects of shear stress on membrane lipid order and fluidity and markedly suppressed ATP release, which is a well-known EC response to shear stress and is involved in shear-stress Ca 2+ signaling. These findings indicate that EC membranes directly respond to shear stress by rapidly decreasing their lipid phase order and increasing their fluidity; these changes could be linked to shear-stress-sensing and response mechanisms.

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Section: Discussionmentioning

confidence: 49%

Endothelial cell and model membranes respond to shear stress by rapidly decreasing the order of their lipid phases

Yamamoto

Ando

2013

Journal of Cell Science

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“…As a result, the percentage of pore-formed structure increases with the DPPG (-) concentration (Fig.5). At a lower cholesterol concentration, a saturated lipid-rich region shows an So phase [7,46]. With 10% cholesterol, the rate of pore formation was significantly increased (Fig.6).…”

Section: ⅳ Discussionmentioning

confidence: 94%

Coupling between pore formation and phase separation in charged lipid membranes

et al. 2015

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We investigated the effect of charge on the membrane morphology of giant unilamellar vesicles (GUVs) composed of various mixtures containing charged lipids. We observed the membrane morphologies by fluorescent and confocal laser microscopy in lipid mixtures consisting of a neutral unsaturated lipid [dioleoylphosphatidylcholine (DOPC)], a neutral saturated lipid [dipalmitoylphosphatidylcholine (DPPC)], a charged unsaturated lipid [dioleoylphosphatidylglycerol (DOPG (-) )], a charged saturated lipid[dipalmitoylphosphatidylglycerol (DPPG (-) )], and cholesterol (Chol). In binary mixtures of neutral DOPC/DPPC and charged DOPC/DPPG (-) , spherical vesicles were formed. On the other hand, pore formation was often observed with GUVs consisting of DOPG (-) and DPPC.In a DPPC/DPPG (-) /Chol ternary mixture, pore-formed vesicles were also frequently observed. The percentage of pore-formed vesicles increased with the DPPG (-) concentration.Moreover, when the head group charges of charged lipids were screened by the addition of salt, pore-formed vesicles were suppressed in both the binary and ternary charged lipid mixtures. We discuss the mechanisms of pore formation in charged lipid mixtures and the relationship between phase separation and the membrane morphology. Finally, we reproduce the results seen in experimental systems by using coarse-grained molecular dynamics simulations. Ⅰ. INTRODUCTIONThe basic structure of a biomembrane is a lipid bilayer that is composed of various types of phospholipids. Biomembranes not only separate the inner and outer environments of living cells, but also play a role in a wide range of life-related phenomena through dynamic structural changes. In biomembranes, the components are not uniformly dispersed, and it is believed that such compositional heterogeneity emerges spontaneously. This heterogeneous structure is known as a "lipid raft" [1][2][3]. Lipid rafts, which are enriched with saturated lipids, cholesterol, or various membrane proteins, are expected to function as platforms to which proteins are attached during signal transduction and membrane trafficking [4,5].Synthetic lipid vesicles consisting of several lipid molecules are commonly used as models of biomembranes to investigate the physicochemical properties of lipid membranes. In particular, ternary lipid mixtures consisting of a saturated lipid, unsaturated lipid, and cholesterol exhibit phase separation between the saturated lipid and the cholesterol-rich phase (the liquid-ordered (Lo) phase) and the unsaturated lipid-rich phase (the liquid-disordered (Ld) phase) [6,7]. The spontaneous domain formation that results from this phase separation has attracted great attention in connection to raft formation in biomembranes.Most previous studies have investigated the primary physical properties of lipid membranes composed of electrically neutral lipids [6,8]. However, biomembranes also contain negatively charged lipids. For instance, the membranes of prokaryotes such asStaphylococcus aureus and Escherichia co...

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“…13 Our membranes are adhesively tensed. If increasing membrane tension causes the liquid-ordered phase to transition to a gel phase, the diffusion in the gel phase will be many orders of magnitude slower than in a liquid phase.…”

Section: Discussionmentioning

confidence: 99%

Specific adhesion of membranes simultaneously supports dual heterogeneities in lipids and proteins

Shindell

Mica

Ritzer

et al. 2015

Phys. Chem. Chem. Phys.

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Membrane adhesion is a vital component of many biological processes. Heterogeneities in lipid and protein composition are often associated with the adhesion site. These heterogeneities are thought to play functional roles in facilitating signalling. Here we experimentally examine this phenomenon using model membranes made of a mixture of lipids that is near a phase boundary at room temperature. Non-adherent model membranes are in a well-mixed, disordered-fluid lipid phase indicated by homogeneous distribution of a fluorescent dye that is a marker for the fluid-disordered (L d ) phase. We specifically adhere membranes to a flat substrate bilayer using biotin-avidin binding. Adhesion produces two types of coexisting heterogeneities: an ordered lipid phase that excludes binding proteins and the fluorescent membrane dye, and a disordered lipid phase that is enriched in both binding proteins and membrane dye compared with the non-adhered portion of the same membrane. Thus, a single type of adhesion interaction (biotin-avidin binding), in an initially-homogeneous system, simultaneously stabilizes both ordered-phase and disordered-phase heterogeneities that are compositionally distinct from the non-adhered portion of the vesicle. These heterogeneities are long-lived and unchanged upon increased temperature.

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Lateral phase separation in tense membranes

Cited by 99 publications

References 48 publications

Endothelial cell and model membranes respond to shear stress by rapidly decreasing the order of their lipid phases

Endothelial cell and model membranes respond to shear stress by rapidly decreasing the order of their lipid phases

Coupling between pore formation and phase separation in charged lipid membranes

Specific adhesion of membranes simultaneously supports dual heterogeneities in lipids and proteins

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