Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork

Tsuji, Akihiko; Kawasaki, Kazunori; Ohnishi, Shun‐ichi; Merkle, Hellmut; Kusumi, Akihiro

doi:10.1021/bi00419a041

Cited by 124 publications

(111 citation statements)

References 32 publications

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“…1a). Indeed, FRAP measurements on erythrocytes membrane (see also [19]) suggested that membrane proteins are confined by steric interaction of their cytoplasmic part with spectrin cytoskeleton. This model was reinforced by electron microscopy imaging of the sub-membrane region that showed unambiguously that spectrin forms a meshgrid tightly attached to the membrane via transmembrane band-3 proteins [20].…”

Section: The Cytoskeleton Meshwork Is a Barrier To Diffusionmentioning

confidence: 99%

What do diffusion measurements tell us about membrane compartmentalisation? Emergence of the role of interprotein interactions

2008

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The techniques of diffusion analysis based on optical microscopy approaches have revealed a great diversity of the dynamic organisation of cell membranes. For a long period, two frameworks have dominated the way of representing the membrane structure: the membrane skeleton fences and the lipid raft models. Progresses in the methods of data analysis have shed light on the features and consequently the possible origin of membrane domains: Inter-protein interactions play a role in confinement. Innovative developments pushing forward the spatiotemporal resolution limits are currently emerging, which are likely to provide in the future a detailed understanding of the intimate functional dynamic organisation of the cell membrane. Keywords Membrane domain . Diffusion . Protein interaction OverviewThe main function of membranes is to generate close compartments: The cell itself (by the plasma membrane) and also the nucleus (by nuclear envelope), the Golgi apparatus, the endoplasmic reticulum, various organelles or the vesicles which are involved in transport processes. Membranes delimit these structures and allow them to have a different composition from the rest of the cell by restricting the diffusion of ions and macromolecules. The specific transport of molecules or information across the membrane is devoted to membrane proteins. Membranes are essentially composed of lipid and proteins, each of them representing about 50% in weight. Lipids are amphiphilic molecules that spontaneously form a bilayer in water. Among the variety of lipids, cholesterol has a specific place since it is particularly abundant in eukaryotic cells. Cholesterol can modify the lipid molecular order [1] and is presumed to participate in lipid micro-phase separation (rafts) [2][3][4][5].Since the structure of biological membranes is maintained by non-covalent bonds, they have first been considered as a fluid lipid bilayer in which embedded proteins are free to diffuse [6]. After the advent of this fluid mosaic model postulating a random distribution of membrane molecules [6], experimental evidence showed that the proteins and lipids are distributed heterogeneously in the membrane. For example, incomplete recoveries were systematically observed in fluorescence recovery after photobleaching (FRAP; see "Appendix 1") experiments. The first indication of the presence of micrometer-sized domains was obtained by FRAP. Yechiel and Edidin found a decrease of the mobile fraction with increasing radius of the bleaching spot ([7, 8] and see "Appendix 1").The huge diversity of lipids and proteins implies that a very large number of combinatorial interactions can occur between them [9]. Since all lipids and proteins do not J Chem Biol (2008) [14,15]. Interactions of membrane proteins with the cytoskeleton or with the glycocalyx can also affect the membrane organisation and are likely to play a confining role [16]. A significant challenge of cell biology is to characterise and to understand not only the origin but also the role of these micrometric ...

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Section: The Cytoskeleton Meshwork Is a Barrier To Diffusionmentioning

confidence: 99%

What do diffusion measurements tell us about membrane compartmentalisation? Emergence of the role of interprotein interactions

2008

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“…Abundant evidence implicates the RBC membrane skeleton in controlling band 3 lateral mobility. Disruption of spectrin-ankyrin and ankyrin-band 3 linkages causes band 3 mobility to increase (21)(22)(23)(24), as does treatment with proteases to remove the cytoplasmic domain of band 3 (25,26) or treatment with ATP or 2,3-DPG (27) at levels that are sufficient to destabilize isolated RBC membrane skeletons (28) Band 3 rotational mobility has been studied in normal RBC ghosts (26,(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44), abnormal RBC ghosts (45,46), and intact RBCs (19,31,37).2 Rapidly rotating, slowly rotating, and rotationally immobile forms of band 3 appear to coexist in the membrane. At 37°C in normal RBC membranes, 20-25% of band 3 molecules rotate with correlation times (r) < 250 Ms, 50-75% rotate with r 1-3 ms, and 5-25% are rotationally immobile on the time scale of the experiment (19,37,40 About half of the rapidly rotating band 3 molecules may rotate with correlation times of 25-30 ,ts; this population could represent band 3 dimers rotating free of constraints other than the viscosity of the lipid bilayer (37).…”

Section: Introductionmentioning

confidence: 99%

“…At 37°C in normal RBC membranes, 20-25% of band 3 molecules rotate with correlation times (r) < 250 Ms, 50-75% rotate with r 1-3 ms, and 5-25% are rotationally immobile on the time scale of the experiment (19,37,40 About half of the rapidly rotating band 3 molecules may rotate with correlation times of 25-30 ,ts; this population could represent band 3 dimers rotating free of constraints other than the viscosity of the lipid bilayer (37). A number of experiments on RBC ghost membranes suggest that band 3 rotational mobility, like band 3 lateral mobility, is controlled by the RBC membrane skeleton (26,36,37,43). In addition, SAO RBCs exhibit a very large fraction of rotationally immobile band 3 (30,31,46).…”

Section: Introductionmentioning

confidence: 99%

Differential control of band 3 lateral and rotational mobility in intact red cells.

Corbett¹,

Agre²,

Palek³

et al. 1994

J. Clin. Invest.

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Measurements of integral membrane protein lateral mobility and rotational mobility have been separately used to investigate dynamic protein-protein and protein-lipid interactions that underlie plasma membrane structure and function. In model bilayer membranes, the mobilities of reconstituted proteins depend on the size of the diffusing molecule and the viscosity of the lipid bilayer. There are no direct tests, however, of the relationship between mechanisms that control protein lateral mobility and rotational mobility in intact biological membranes. We have measured the lateral and rotational mobility of band 3 in spectrin-deficient red blood cells from patients with hereditary spherocytosis and hereditary pyropoikilocytosis. Our data suggest that band 3 lateral mobility is regulated by the spectrin content of the red cell membrane. In contrast, band 3 rotational mobility is unaffected by changes in spectrin content. Band 3 lateral mobility and rotational mobility must therefore be controlled by different molecular mechanisms. (J. Clin. Invest. 1994. 94:683-688.) Key words: erythrocyte membrane * hereditary spherocytosis -hereditary pyropoikilocytosis fluorescence photobleaching recovery polarized fluorescence depletion

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“…Glycophorin A, present in -5 x 105 copies per cell (5), is the major sialoglycoprotein. The membrane skeleton determines RBC stability, deformability, and shape (6-9) and appears to regulate lateral and rotational mobility of band 3 and glycophorin A in the plane ofthe membrane (10)(11)(12)(13)(14)(15)(16)(17)(18). The major skeletal protein, spectrin, is attached to the overlying bilayer through interactions involving: ankyrin, which links spectrin to a portion ( 10-15%) of band 3; protein 4.1, which links spectrin to glycophorin C and possibly to glycophorin A and band 3; and, possibly, inner leaflet aminophospholipids, including phosphatidylserine and phosphatidylethanolamine (2).…”

Section: Introductionmentioning

confidence: 99%

Band 3 and glycophorin are progressively aggregated in density-fractionated sickle and normal red blood cells. Evidence from rotational and lateral mobility studies.

Corbett¹,

Golan²

1993

J. Clin. Invest.

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Band 3 aggregation in the plane of the red blood cell (RBC) membrane is postulated to be important in the pathophysiology of hemolysis of dense sickle and normal RBCs. We used the fluorescence photobleaching recovery and polarized fluorescence depletion techniques to measure the lateral and rotational mobility of band 3, glycophorins, and phospholipid analogues in membranes of density-separated intact RBCs from seven patients with sickle cell disease and eight normal controls. The fractions of laterally mobile band 3 and glycophorin decreased progressively as sickle RBC density increased. Normal RBCs also showed a progressive decrease in band 3 fractional mobility with increasing buoyant density. Rapidly rotating, slowly rotating, and rotationally immobile forms of band 3 were observed in both sickle and normal RBC membranes. The fraction of rapidly rotating band 3 progressively decreased and the fraction of rotationally immobile band 3 progressively increased with increasing sickle RBC density. Changes in the fraction of rotationally immobile band 3 were not reversible upon hypotonic swelling of dense sickle RBCs, and normal RBCs osmotically shrunken in sucrose buffers failed to manifest band 3 immobilization at median cell hemoglobin concentration values characteristic of dense sickle RBCs. We conclude that dense sickle and normal RBCs acquire irreversible membrane abnormalities that cause transmembrane protein immobilization and band 3 aggregation. Band 3 aggregates could serve as cell surface sites of autologous antibody binding and thereby lead to removal of dense sickle and normal (senescent)

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Regulation of band 3 mobilities in erythrocyte ghost membranes by protein association and cytoskeletal meshwork

Cited by 124 publications

References 32 publications

What do diffusion measurements tell us about membrane compartmentalisation? Emergence of the role of interprotein interactions

What do diffusion measurements tell us about membrane compartmentalisation? Emergence of the role of interprotein interactions

Differential control of band 3 lateral and rotational mobility in intact red cells.

Band 3 and glycophorin are progressively aggregated in density-fractionated sickle and normal red blood cells. Evidence from rotational and lateral mobility studies.

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