Lipid Composition of the Cell Membrane Outer Leaflet Regulates Endocytosis of Nanomaterials through Alterations in Scavenger Receptor Activity

Nazemidashtarjandi, Saeed; Sharma, Vishva Mitra; Puri, Vishwajeet; Farnoud, Amir M.; Burdick, Monica M.

doi:10.1021/acsnano.1c08344

Cited by 9 publications

(4 citation statements)

References 72 publications

(137 reference statements)

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“…The effect of LEX on particular plasma membrane-localized processes also can be tested. Examples include stimulated phosphorylation of insulin receptor in CHO cells (40), endocytosis of model nanoparticles in A549 cells (66), and stimulated Syk recruitment during mast cell signaling (this study). This demonstrates the robustness and usefulness of this strategy.…”

Section: Discussionmentioning

confidence: 99%

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Lipid Driven Inter-leaflet Coupling of Plasma Membrane Order Regulates FcεRI Signaling in Mast Cells

Yang

Wagenknecht-Wiesner

Yin

et al. 2022

Preprint

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Engagement of high affinity immunoglobulin E (IgE) receptor FcεRI with extracellular, multivalent antigen (Ag) stabilizes co-existing ordered and disordered phases in the inner leaflet of the plasma membrane. This optimally controls biochemical interactions between signaling components required for transmembrane (TM) signaling in mast cells. The biophysical organization of the resting inner leaflet is poised to respond appropriately to this extracellular stimulation. The resting inner leaflet is generally less ordered than the outer leaflet, with a lipid composition that does not spontaneously phase separate in model membranes. We proposed that coupling between the two leaflets mediates separation into different phase-like domains in the inner leaflet. To test this hypothesis in live cells, we first established a straightforward approach to evaluate changes in membrane order due to inter-leaflet coupling by measuring inner leaflet diffusion of phase-specific lipid probes with Imaging Fluorescence Correlation Spectroscopy (ImFCS) before and after methyl-α-cyclodextrin (mαCD)-catalyzed exchange of outer leaflet lipids (LEX) with exogenous order- or disorder-promoting phospholipids. We examined the functional impact of LEX by monitoring two Ag-stimulated cellular responses, namely early-stage recruitment of Syk kinase to the inner leaflet and late-stage exocytosis of secretory granules (degranulation). Based on changes in probe diffusion, we observed global increase or decrease of inner leaflet order when outer leaflet is exchanged with order or disorder promoting lipids, respectively, in unstimulated cells. Furthermore, the degree of stimulated Syk recruitment and degranulation correlates with the inner leaflet order of the resting cells, which was varied using LEX. Overall, combined LEX and ImFCS platform provides strong evidence of lipid-based control of stimulated TM signaling in live mast cells. In addition, our functional results imply that resting-state lipid composition and ordering of the outer leaflet sets the ordering of the inner leaflet, likely via interleaflet coupling, and correspondingly modulates TM signaling initiated by antigen-activated IgE-FcεRI.

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Section: Discussionmentioning

confidence: 99%

“…Therefore, the degree of lipid exchange should be quantified, for example by TLC as in Fig. S1 or mass spectrometry (66), as part of interpreting the biophysical and functional results.…”

Section: Lex Is a Useful Approach For Studying Inter-leaflet Coupling...mentioning

confidence: 99%

Lipid Driven Inter-leaflet Coupling of Plasma Membrane Order Regulates FcεRI Signaling in Mast Cells

Yang

Wagenknecht-Wiesner

Yin

et al. 2022

Preprint

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“…Thus, erythrocytes are a kind of natural “innate carrier” with many unique advantages in drug delivery ( 6 ). Erythrocyte membranes can be used as an encapsulating material to decorate nanoparticles as delivery vehicle systems with the advantages of long circulation, high membrane flexibility and stability ( 7 ), good biocompatibility ( 8 ), the retention of basic cellular functions, and functional groups that can be modified on the membrane surface ( 9 ). Owing to these special advantages, the use of erythrocytes as biomimetic drug nanomaterials to treat diseases and modulate immune function shows great potential.…”

Section: Introductionmentioning

confidence: 99%

Mannose-modified erythrocyte membrane-encapsulated chitovanic nanoparticles as a DNA vaccine carrier against reticuloendothelial tissue hyperplasia virus

Feng

Tang

et al. 2023

Front. Immunol.

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IntroductionThe erythrocyte membranes used in nanovaccines include high membrane stability, long circulation life, adaptability and extremely good bio compatibility. Nanoparticles encapsulated by erythrocyte membranes are widely used as ideal drug delivery vehicles because of their high drug loading, long circulation time, and excellent biocompatibility. The mannose modification of delivery materials can help target mannose receptors (MRs) to deliver antigens to antigen-presenting cells (APCs).MethodsIn this study, the antigen gene gp90 of avian reticuloendotheliosis virus (REV) was encapsulated with carboxymethyl chitosan (CS) to obtain CSgp90 nanoparticles, which were coated with mannose-modied fowl erythrocyte membranes to yield CS-gp90@M-M nanoparticles. The physicochemical characterization and immune response of the CS-gp90@M-M nanoparticles were investigated in vitro and in vivo.ResultsCS-gp90@M-M nanoparticles were rapidly phagocytized in vitro by macrophages to induce the production of cytokines and nitric oxide. In vivo, CS-gp90@M-M nanoparticles increased cytokine levels, the CD4+/8+ ratio, REV-specific antibodies in the peripheral blood of chicks, and the mRNA levels of immune-related genes in the spleen and bursa of immunized chicks. CS-gp90@M-M nanoparticles could be targeted to lymphoid organs to prolong the retention time of the nanoparticles at the injection site and lymphatic organs, leading to a strong, sustained immune response. Moreover, the CS-gp90@M-M nano-vaccine showed a lasting immunoprotective effect and improved the body weight of chicks after the challenge.ConclusionOverall, CS-gp90@M-M nanoparticles can be used in vaccine designs as an effective delivery carrier with immune response-enhancing effects.

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“…A well-flowing membrane lipid bilayer is also an important structure for bacteria to resist a harsh external environment [ 9 ]. Some exogenously added substances, such as β-carotene [ 5 , 10 , 11 ], cyclodextrins [ 12 ], vitamin E [ 13 ], vitamin K1 [ 14 , 15 ], cholesterol [ 16 ], sterols [ 17 ] and melatonin [ 16 , 18 ], can be anchored to the membrane lipid bilayer, where they interact with the lipids to form a new lipid raft-like structure that improves the fluidity of the membrane and the viability of bacteria in harsh environments. For example, β-carotene and cyclodextrins can regulate the lipid phase of the membrane and anchor their polar groups to the opposite polar region of the membrane [ 19 ].…”

Section: Introductionmentioning

confidence: 99%

Improvement of Freeze-Dried Survival of Lactiplantibacillus plantarum Based on Cell Membrane Regulation

Cui

Qian

et al. 2022

Microorganisms

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The cell membrane of Lactiplantibacillus plantarum is a key structure for cell survival. In this study, we aimed to improve the lyophilization resistance of L. plantarum by regulating the cell membrane structure. Unsaturated fatty acids or cell membrane-regulating substances were added during culturing to determine their effect on the composition of cell membrane fatty acids and the survival rate of the cells after freeze-drying. The results showed that Tween 80, β-carotene and melatonin increased the lyophilization survival rate of L. plantarum by 9.44, 14.53, and 18.34%, respectively. After adding a lyophilization protective agent at a concentration of 21.49% at a 1:1 ratio, a combination of Tween 80, melatonin, and β-carotene was added to regulate the cell membrane, which increased the lyophilization survival rate by 32.08–86.05%. This study proposes new research directions and ideas for improving the survival rate of probiotics for industrial production.

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Lipid Composition of the Cell Membrane Outer Leaflet Regulates Endocytosis of Nanomaterials through Alterations in Scavenger Receptor Activity

Cited by 9 publications

References 72 publications

Lipid Driven Inter-leaflet Coupling of Plasma Membrane Order Regulates FcεRI Signaling in Mast Cells

Lipid Driven Inter-leaflet Coupling of Plasma Membrane Order Regulates FcεRI Signaling in Mast Cells

Mannose-modified erythrocyte membrane-encapsulated chitovanic nanoparticles as a DNA vaccine carrier against reticuloendothelial tissue hyperplasia virus

Improvement of Freeze-Dried Survival of Lactiplantibacillus plantarum Based on Cell Membrane Regulation

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