Hierarchical mesoscale domain organization of the plasma membrane

Kusumi, Akihiro; Suzuki, Kenichi; Kasai, Rinshi S.; Ritchie, Ken; Fujiwara, Takeshi

doi:10.1016/j.tibs.2011.08.001

Cited by 291 publications

(345 citation statements)

References 85 publications

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“…In eukaryotes, membrane partitioning is a well-described process with features at different length scales (41). In prokaryotes, it would also be envisaged that multiple mechanisms are at play, resulting in the coordination of processes from the molecular to the cellular level.…”

Section: Resultsmentioning

confidence: 99%

Supramolecular structure in the membrane of Staphylococcus aureus

García‐Lara

Weihs

et al. 2015

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

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All life demands the temporal and spatial control of essential biological functions. In bacteria, the recent discovery of coordinating elements provides a framework to begin to explain cell growth and division. Here we present the discovery of a supramolecular structure in the membrane of the coccal bacterium Staphylococcus aureus, which leads to the formation of a largescale pattern across the entire cell body; this has been unveiled by studying the distribution of essential proteins involved in lipid metabolism (PlsY and CdsA). The organization is found to require MreD, which determines morphology in rod-shaped cells. The distribution of protein complexes can be explained as a spontaneous pattern formation arising from the competition between the energy cost of bending that they impose on the membrane, their entropy of mixing, and the geometric constraints in the system. Our results provide evidence for the existence of a self-organized and nonpercolating molecular scaffold involving MreD as an organizer for optimal cell function and growth based on the intrinsic self-assembling properties of biological molecules.T he perpetuation of all cellular life requires the temporal and spatial management of essential biological functions, within the morphological framework characteristic of a specific organism. The underlying processes, which determine cell shape, are intimately intertwined with cell division and constitute pivotal issues for cell biology; their coordination in prokaryotes is mediated through counterparts of eukaryotic actin, tubulin, and intermediate filaments in addition to other specific components (1, 2). Several of these apparent cytoskeletal elements capitalize on their membrane binding properties, assembling along the longitudinal axis, between the poles of rod-shaped cells; they participate in many processes, including selection of the division site via the Min system and other components (3, 4); guidance and control of the cell wall biosynthetic machinery responsible for cell size, polarity, and shape through the actin-like protein MreB (5-11); and chromosome partitioning into daughter cells using another actin-like filament, ParM (12).Despite this set of highly coordinated mechanisms, it has recently been shown that otherwise rod-and cocci-shaped bacteria can exist as largely spherical wall-less forms known as L-forms, with the capacity to divide (13). Importantly, the division of L-forms of the rod-shaped bacterium Bacillus subtilis is freed from the requirement of the classical tubulin-like division component FtsZ (14). L-forms appear to divide by scission after blebbing, tabulation, or vesiculation dependent on an altered rate of membrane biosynthesis (15); this harks back perhaps to a more evolutionary primitive mechanism permitting cellular proliferation. Thus, are there underlying organizational mechanisms that exist, independent of apparent cytoskeletal elements? The fluid mosaic model proposing the free diffusion of membrane proteins through the lipids has been challenged by growing e...

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Section: Resultsmentioning

confidence: 99%

Supramolecular structure in the membrane of Staphylococcus aureus

García‐Lara

Weihs

et al. 2015

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

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“…Historically, monitoring the movement of a single molecule bearing a fluorescent marker was challenging, principally because the period in which the fluorophore could be tracked before photobleaching occurred was short and detectors lacked the sensitivity required. More recently however, the advent of new chromophores, allied to improvements in detector sensitivity, has made SFMT a F o r P e e r R e v i e w O n l y feasible process (Kusumi et al, 2011;Rolfe et al, 2011;Kusumi et al, 2010). A key requirement for SFMT is to track the movement of single molecules with a high enough frame rate to capture sufficient data for analysis (Skaug et al, 2011).…”

Section: Model Systems and Methods For Studying Lateral Diffusionmentioning

confidence: 99%

“…When monitored at low frequency, molecules appear to diffuse normally. In contrast, when monitored for sufficient periods at high frequency, the trajectories are divided in to small localized regions (diameter ~30-300 nm) within which diffusion is normal (D L = 0.1-0.6 µm 2 s -1 for lipids and transmembrane proteins at 37 °C), with relatively infrequent 'hops' between adjacent regions (Kusumi et al, 2011;Valentine and Haggie, 2011;Crane and Verkmann, 2010;Kusumi et al, 2010 been accounted for by picket-fence models, which include transmembrane proteins anchored to the cytoskeleton as the 'pickets' and membrane cytoskeletal proteins such as actin filaments as the 'fence' (Golebiewska et al, 2011;Kusumi, et al 2011). Lipid rafts may also account for some instances of anomalous diffusion and it is notable that the compartment size in the picket-fence models are of the same order of magnitude as lipid rafts (Kusumi, et al 2010;Kusumi, et al 2011).…”

Section: Measurements Of D L In Biogenic Membranesmentioning

confidence: 99%

“…Whether lipid diffusion between compartments is related to the formation of rafts is the subject of some debate (Kusumi 2010, Kusumi 2011, Mueller 2011. A major role of cholesterol appears to be the regulation of membrane fluidity and lipid dynamics (Owen et al, 2010), respectively retarding or accelerating the lateral diffusion of unsaturated and saturated lipids, as seen for PFG-NMR studies with binary cholesterol-PC mixtures (Day and Kenworthy, 2009;Kahya et al, 2006;Fillipov et al, 2003;Kahya et al, 2003).…”

Section: Measurements Of D L In Biogenic Membranesmentioning

confidence: 99%

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Resolving the kinetics of lipid, protein and peptide diffusion in membranes

Sanderson

2012

Molecular Membrane Biology

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“…However, the contemporary view of cell membranes includes lateral heterogeneity, which is created by lipids organization into functional domains rich in sphingolipids and cholesterol (Simons and Ikonen 1997;Goñi 2014). These highly dynamic domains, also called lipid rafts, with sizes in the nanometer order are thought to be involved in membrane phenomena such as signal transduction, parasite infection, and intracellular trafficking of lipids and protein (Simons and Toomre 2000;Simons and Ehehalt 2002;Regen 2002;Kusumi et al 2011). The rafts theory appeared in the nineties and became as popular as controversial (Munro 2003;Lichtenberg et al 2005;Hancock 2006;Levental and Veatch 2016) by the way it addresses the well-known and biophysically-based concept of lipid heterogeneity.…”

Section: Introductionmentioning

confidence: 99%

Biophysical approaches in the study of biomembrane solubilization: quantitative assessment and the role of lateral inhomogeneity

et al. 2017

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Detergents are amphiphilic molecules widely used to solubilize biological membranes and/or extract their components. Nevertheless, because of the complex composition of biomembranes, their solubilization by detergents has not been systematically studied. In this review, we address the solubilization of erythrocytes, which provide a relatively simple, robust and easy to handle biomembrane, and of biomimetic models, to stress the role of the lipid composition on the solubilization process. First, results of a systematic study on the solubilization of human erythrocyte membranes by different series of non-ionic (Triton, CxEy, Brij, Renex, Tween), anionic (bile salts) and zwitterionic (ASB, CHAPS) detergents are shown. Such quantitative approach allowed us to propose R e sat -the effective detergent/lipid molar ratio in the membrane for the onset of hemolysis as a new parameter to classify the solubilization efficiency of detergents. Second, detergent-resistant membranes (DRMs) obtained as a result of the partial solubilization of erythrocytes by TX-100, C 12 E 8 and Brij detergents are examined. DRMs were characterized by their cholesterol, sphingolipid and specific proteins content, as well as lipid packing. Finally, lipid bilayers of tuned lipid composition forming liposomes were used to investigate the solubilization process of membranes of different compositions/phases induced by Triton X-100. Optical microscopy of giant unilamellar vesicles revealed that pure phospholipid membranes are fully solubilized, whereas the presence of cholesterol renders the mixture partially or even fully insoluble, depending on the composition. Additionally, Triton X-100 induced phase separation in raft-like mixtures, and selective solubilization of the fluid phase only.

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Hierarchical mesoscale domain organization of the plasma membrane

Cited by 291 publications

References 85 publications

Supramolecular structure in the membrane of Staphylococcus aureus

Supramolecular structure in the membrane of Staphylococcus aureus

Resolving the kinetics of lipid, protein and peptide diffusion in membranes

Biophysical approaches in the study of biomembrane solubilization: quantitative assessment and the role of lateral inhomogeneity

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