Spatial Relationship and Functional Relevance of Three Lipid Domain Populations at the Erythrocyte Surface

Conrard, Louise; Stommen, Amaury; Pollet, Hélène; Tyteca, Donatienne

doi:10.1016/j.bpj.2018.11.1192

Cited by 4 publications

(22 citation statements)

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“…All determinations were performed on isolated washed RBCs. Intracellular calcium was measured by fluorimetry using the Fluo-4 AM probe and normalized to the corresponding intracellular Hb content (detected by spectrophotometry as described above) as previously ( Conrard et al, 2018 ). Such method generated only qualitative measurements as the Fluo-4 fluorescence signal is not a linear function of the calcium concentration ( Kaestner et al, 2006 ).…”

Section: Methodsmentioning

confidence: 99%

“…For instance, it is not known whether the budding of EVs could occur from specific regions of the plasma membrane and if some specific lipid domains could represent the starting point of the vesiculation process. Three types of submicrometric lipid domains have been identified at the outer plasma membrane leaflet of resting RBCs (i.e., RBCs that are not in the deformation process): (i) those mainly enriched in cholesterol (hereafter referred as cholesterol-enriched domains), (ii) those co-enriched in the ganglioside GM1, phosphatidylcholine and cholesterol (hereafter referred as GM1-enriched domains), and (iii) those co-enriched in sphingomyelin, phosphatidylcholine and cholesterol (hereafter referred as sphingomyelin-enriched domains) ( Carquin et al, 2014 , 2015 , 2016 ; Conrard et al, 2018 ). During RBC deformation, cholesterol-enriched domains gather in high curvature areas, forming or stabilizing highly curved membrane regions.…”

Section: Introductionmentioning

confidence: 99%

“…During RBC deformation, cholesterol-enriched domains gather in high curvature areas, forming or stabilizing highly curved membrane regions. GM1- and sphingomyelin-enriched domains increase in abundance upon calcium influx and efflux respectively, thereby potentially participating to calcium exchanges, also essential for RBC deformation ( Leonard et al, 2017 , 2018 ; Conrard et al, 2018 ). Although those domains appeared to contribute to the RBC deformation process, their contribution to RBC vesiculation is not known.…”

Section: Introductionmentioning

confidence: 99%

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Interplay Between Plasma Membrane Lipid Alteration, Oxidative Stress and Calcium-Based Mechanism for Extracellular Vesicle Biogenesis From Erythrocytes During Blood Storage

et al. 2020

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The shedding of extracellular vesicles (EVs) from the red blood cell (RBC) surface is observed during senescence in vivo and RBC storage in vitro . Two main models for EV shedding, respectively based on calcium rise and oxidative stress, have been proposed in the literature but the role of the plasma membrane lipid composition and properties is not understood. Using blood in K + /EDTA tubes stored for up to 4 weeks at 4°C as a relevant RBC vesiculation model, we showed here that the RBC plasma membrane lipid composition, organization in domains and biophysical properties were progressively modified during storage and contributed to the RBC vesiculation. First, the membrane content in cholesterol and linoleic acid decreased whereas lipid peroxidation and spectrin:membrane occupancy increased, all compatible with higher membrane rigidity. Second, phosphatidylserine surface exposure showed a first rapid rise due to membrane cholesterol decrease, followed by a second calcium-dependent increase. Third, lipid domains mainly enriched in GM1 or sphingomyelin strongly increased from the 1st week while those mainly enriched in cholesterol or ceramide decreased during the 1st and 4th week, respectively. Fourth, the plasmatic acid sphingomyelinase activity considerably increased upon storage following the sphingomyelin-enriched domain rise and potentially inducing the loss of ceramide-enriched domains. Fifth, in support of the shedding of cholesterol- and ceramide-enriched domains from the RBC surface, the number of cholesterol-enriched domains lost and the abundance of EVs released during the 1st week perfectly matched. Moreover, RBC-derived EVs were enriched in ceramide at the 4th week but depleted in sphingomyelin. Then, using K + /EDTA tubes supplemented with glucose to longer preserve the ATP content, we better defined the sequence of events. Altogether, we showed that EV shedding from lipid domains only represents part of the global vesiculation mechanistics, for which we propose four successive events (cholesterol domain decrease, oxidative stress, sphingomyelin/sphingomyelinase/ceramide/calcium alteration and phosphatidylserine exposure).

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Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Interplay Between Plasma Membrane Lipid Alteration, Oxidative Stress and Calcium-Based Mechanism for Extracellular Vesicle Biogenesis From Erythrocytes During Blood Storage

et al. 2020

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“…They also differentially associate to high and low RBC membrane curvature areas and exhibit a different response to RBC mechanical stimulation [ 224 ]. Altogether, our data suggest the coexistence at the RBC surface of at least three types of domains (i) those mostly enriched in chol, which gather in high-curvature membranes during the RBC deformation, (ii) those mostly enriched in GM1 which might be associated with the Ca 2+ entry regulation during deformation, and (iii) those mostly enriched in SM and chol, which might regulate the Ca 2+ efflux during the shape restoration after deformation [ 183 , 203 , 206 , 210 , 220 , 224 , 225 ]. Using other probes (e.g., cholera toxin B subunit conjugates, antibodies or treatment with PlcHR2, a phospholipase C/SMase from Pseudomonas aeruginosa ) and techniques (e.g., SDS-digested freeze-fracture replica labeling), other groups have evidenced stable domains enriched in GM1 [ 226 ], GM3 [ 227 ] or Cer [ 228 ].…”

Section: Microvesicle Biogenesis and Shedding—role Of Plasma Membrmentioning

confidence: 99%

“…( f ) HeLa cell labeled for chol with Theta-D4-DRONPA and processed by photoactivated localization microscopy (PALM). Adapted from ( a ) [ 225 ]; ( b ) [ 229 ]; ( c ) [ 230 ]; ( d ) [ 231 ]; ( e ) [ 232 ]; ( f ) [ 233 ].…”

Section: Figurementioning

confidence: 99%

Plasma Membrane Lipid Domains as Platforms for Vesicle Biogenesis and Shedding?

et al. 2018

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Extracellular vesicles (EVs) contribute to several pathophysiological processes and appear as emerging targets for disease diagnosis and therapy. However, successful translation from bench to bedside requires deeper understanding of EVs, in particular their diversity, composition, biogenesis and shedding mechanisms. In this review, we focus on plasma membrane-derived microvesicles (MVs), far less appreciated than exosomes. We integrate documented mechanisms involved in MV biogenesis and shedding, focusing on the red blood cell as a model. We then provide a perspective for the relevance of plasma membrane lipid composition and biophysical properties in microvesiculation on red blood cells but also platelets, immune and nervous cells as well as tumor cells. Although only a few data are available in this respect, most of them appear to converge to the idea that modulation of plasma membrane lipid content, transversal asymmetry and lateral heterogeneity in lipid domains may play a significant role in the vesiculation process. We suggest that lipid domains may represent platforms for inclusion/exclusion of membrane lipids and proteins into MVs and that MVs could originate from distinct domains during physiological processes and disease evolution.

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Modeling of full-length Piezo1 suggests importance of the proximal N-terminus for dome structure

Chong

Vecchis

Hyman

et al. 2021

Biophysical Journal

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Piezo1 forms a mechanically activated calcium-permeable nonselective cation channel that is functionally important in many cell types. Structural data exist for C-terminal regions, but we lack information about N-terminal regions and how the entire channel interacts with the lipid bilayer. Here, we use computational approaches to predict the three-dimensional structure of the full-length Piezo1 and simulate it in an asymmetric membrane. A number of novel insights are suggested by the model: 1) Piezo1 creates a trilobed dome in the membrane that extends beyond the radius of the protein, 2) Piezo1 changes the lipid environment in its vicinity via preferential interactions with cholesterol and phosphatidylinositol 4,5-bisphosphate (PIP 2 ) molecules, and 3) cholesterol changes the depth of the dome and PIP 2 binding preference. In vitro alteration of cholesterol concentration inhibits Piezo1 activity in a manner complementing some of our computational findings. The data suggest the importance of N-terminal regions of Piezo1 for dome structure and membrane cholesterol and PIP 2 interactions.

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Spatial Relationship and Functional Relevance of Three Lipid Domain Populations at the Erythrocyte Surface

Cited by 4 publications

References 0 publications

Interplay Between Plasma Membrane Lipid Alteration, Oxidative Stress and Calcium-Based Mechanism for Extracellular Vesicle Biogenesis From Erythrocytes During Blood Storage

Interplay Between Plasma Membrane Lipid Alteration, Oxidative Stress and Calcium-Based Mechanism for Extracellular Vesicle Biogenesis From Erythrocytes During Blood Storage

Plasma Membrane Lipid Domains as Platforms for Vesicle Biogenesis and Shedding?

Modeling of full-length Piezo1 suggests importance of the proximal N-terminus for dome structure

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