Host Immune Cell Membrane Deformability Governs the Uptake Route of Malaria-Derived Extracellular Vesicles

. 2025 Mar 18 ; 19 (10) : 9760-9778. [epub] 20250303

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid40030053

The malaria parasite, Plasmodium falciparum, secretes extracellular vesicles (EVs) to facilitate its growth and to communicate with the external microenvironment, primarily targeting the host's immune cells. How parasitic EVs enter specific immune cell types within the highly heterogeneous pool of immune cells remains largely unknown. Using a combination of imaging flow cytometry and advanced fluorescence analysis, we demonstrated that the route of uptake of parasite-derived EVs differs markedly between host T cells and monocytes. T cells, which are components of the adaptive immune system, internalize parasite-derived EVs mainly through an interaction with the plasma membrane, whereas monocytes, which function in the innate immune system, take up these EVs via endocytosis. The membranal/endocytic balance of EV internalization is driven mostly by the amount of endocytic incorporation. Integrating atomic force microscopy with fluorescence data analysis revealed that internalization depends on the biophysical properties of the cell membrane rather than solely on molecular interactions. In support of this, altering the cholesterol content in the cell membrane tilted the balance in favor of one uptake route over another. Our results provide mechanistic insights into how P. falciparum-derived EVs enter into diverse host cells. This study highlights the sophisticated cell-communication tactics used by the malaria parasite.

Zobrazit více v PubMed

World Malaria Report 2023. https://www.who.int/teams/global-malaria-programme/reports/world-malaria-report-2023. (accessed April 18, 2024).

Ofir-Birin Y.; Heidenreich M.; Regev-Rudzki N. Pathogen-Derived Extracellular Vesicles Coordinate Social Behaviour and Host Manipulation. Semin. Cell Dev. Biol. 2017, 67, 83–90. 10.1016/j.semcdb.2017.03.004. PubMed DOI

Mashburn L. M.; Whiteley M. Membrane Vesicles Traffic Signals and Facilitate Group Activities in a Prokaryote. Nature 2005, 437 (7057), 422–425. 10.1038/nature03925. PubMed DOI

van der Pol E.; Böing A. N.; Harrison P.; Sturk A.; Nieuwland R. Classification, Functions, and Clinical Relevance of Extracellular Vesicles. Pharmacol. Rev. 2012, 64 (3), 676–705. 10.1124/pr.112.005983. PubMed DOI

Sisquella X.; Ofir-Birin Y.; Pimentel M. A.; Cheng L.; Abou Karam P.; Sampaio N. G.; Penington J. S.; Connolly D.; Giladi T.; Scicluna B. J.; Sharples R. A.; Waltmann A.; Avni D.; Schwartz E.; Schofield L.; Porat Z.; Hansen D. S.; Papenfuss A. T.; Eriksson E. M.; Gerlic M.; Hill A. F.; Bowie A. G.; Regev-Rudzki N. Malaria Parasite DNA-Harbouring Vesicles Activate Cytosolic Immune Sensors. Nat. Commun. 2017, 8 (1), 1985.10.1038/s41467-017-02083-1. PubMed DOI PMC

De Gassart A.; Géminard C.; Février B.; Raposo G.; Vidal M. Lipid Raft-Associated Protein Sorting in Exosomes. Blood 2003, 102 (13), 4336–4344. 10.1182/blood-2003-03-0871. PubMed DOI

Thorsteinsson K.; Olsén E.; Schmidt E.; Pace H.; Bally M. FRET-Based Assay for the Quantification of Extracellular Vesicles and Other Vesicles of Complex Composition. Anal. Chem. 2020, 92 (23), 15336–15343. 10.1021/acs.analchem.0c02271. PubMed DOI PMC

Buzás E. I.; Tóth E.; Sódar B. W.; Szabó-Taylor K. Molecular Interactions at the Surface of Extracellular Vesicles. Semin. Immunopathol. 2018, 40 (5), 453–464. 10.1007/s00281-018-0682-0. PubMed DOI PMC

Dong G.; Filho A. L.; Olivier M. Modulation of Host-Pathogen Communication by Extracellular Vesicles (EVs) of the Protozoan Parasite Leishmania. Front. Cell. Infect. Microbiol. 2019, 9, 100.10.3389/fcimb.2019.00100. PubMed DOI PMC

Bonsergent E.; Grisard E.; Buchrieser J.; Schwartz O.; Théry C.; Lavieu G. Quantitative Characterization of Extracellular Vesicle Uptake and Content Delivery within Mammalian Cells. Nat. Commun. 2021, 12 (1), 1864.10.1038/s41467-021-22126-y. PubMed DOI PMC

Mantel P. Y.; Marti M. The Role of Extracellular Vesicles in Plasmodium and Other Protozoan Parasites. Cell Microbiol. 2014, 16 (3), 344–354. 10.1111/cmi.12259. PubMed DOI PMC

Regev-Rudzki N.; Wilson D. W.; Carvalho T. G.; Sisquella X.; Coleman B. M.; Rug M.; Bursac D.; Angrisano F.; Gee M.; Hill A. F.; Baum J.; Cowman A. F. Cell-Cell Communication between Malaria-Infected Red Blood Cells via Exosome-like Vesicles. Cell 2013, 153 (5), 1120–1133. 10.1016/j.cell.2013.04.029. PubMed DOI

Mantel P. Y.; Hoang A. N.; Goldowitz I.; Potashnikova D.; Hamza B.; Vorobjev I.; Ghiran I.; Toner M.; Irimia D.; Ivanov A. R.; Barteneva N.; Marti M. Malaria-Infected Erythrocyte-Derived Microvesicles Mediate Cellular Communication within the Parasite Population and with the Host Immune System. Cell Host Microbe 2013, 13 (5), 521–534. 10.1016/j.chom.2013.04.009. PubMed DOI PMC

Ofir-Birin Y.; Ben Ami Pilo H.; Cruz Camacho A.; Rudik A.; Rivkin A.; Revach O. Y.; Nir N.; Block Tamin T.; Abou Karam P.; Kiper E.; Peleg Y.; Nevo R.; Solomon A.; Havkin-Solomon T.; Rojas A.; Rotkopf R.; Porat Z.; Avni D.; Schwartz E.; Zillinger T.; Hartmann G.; Di Pizio A.; Quashie N.; Ben; Dikstein R.; Gerlic M.; Torrecilhas A. C.; Levy C.; Nolte-‘t Hoen E. N. M.; Bowie A. G.; Regev-Rudzki N. Malaria Parasites Both Repress Host CXCL10 and Use It as a Cue for Growth Acceleration. Nat. Commun. 2021, 12 (1), 4851.10.1038/s41467-021-24997-7. PubMed DOI PMC

Ye W.; Chew M.; Hou J.; Lai F.; Leopold S. J.; Loo H. L.; Ghose A.; Dutta A. K.; Chen Q.; Ooi E. E.; White N. J.; Dondorp A. M.; Preiser P.; Chen J. Microvesicles from Malaria-Infected Red Blood Cells Activate Natural Killer Cells via MDA5 Pathway. PLoS Pathog. 2018, 14 (10), e1007298.10.1371/JOURNAL.PPAT.1007298. PubMed DOI PMC

Abou Karam P.; Rosenhek-Goldian I.; Ziv T.; Ben Ami Pilo H.; Azuri I.; Rivkin A.; Kiper E.; Rotkopf R.; Cohen S. R.; Torrecilhas A. C.; Avinoam O.; Rojas A.; Morandi M. I.; Regev-Rudzki N. Malaria Parasites Release Vesicle Subpopulations with Signatures of Different Destinations. EMBO Rep. 2022, 23 (7), e54755.10.15252/embr.202254755. PubMed DOI PMC

Mantel P. Y.; Hjelmqvist D.; Walch M.; Kharoubi-Hess S.; Nilsson S.; Ravel D.; Ribeiro M.; Grüring C.; Ma S.; Padmanabhan P.; Trachtenberg A.; Ankarklev J.; Brancucci N. M.; Huttenhower C.; Duraisingh M. T.; Ghiran I.; Kuo W. P.; Filgueira L.; Martinelli R.; Marti M. Infected Erythrocyte-Derived Extracellular Vesicles Alter Vascular Function via Regulatory Ago2-MiRNA Complexes in Malaria. Nat. Commun. 2016, 7 (1), 12727.10.1038/ncomms12727. PubMed DOI PMC

Dekel E.; Yaffe D.; Rosenhek-Goldian I.; Ben-Nissan G.; Ofir-Birin Y.; Morandi M. I.; Ziv T.; Sisquella X.; Pimentel M. A.; Nebl T.; Kapp E.; Ohana Daniel Y.; Karam P. A.; Alfandari D.; Rotkopf R.; Malihi S.; Temin T. B.; Mullick D.; Revach O. Y.; Rudik A.; Gov N. S.; Azuri I.; Porat Z.; Bergamaschi G.; Sorkin R.; Wuite G. J. L.; Avinoam O.; Carvalho T. G.; Cohen S. R.; Sharon M.; Regev-Rudzki N. 20S Proteasomes Secreted by the Malaria Parasite Promote Its Growth. Nat. Commun. 2021, 12 (1), 1172.10.1038/s41467-021-21344-8. PubMed DOI PMC

Abdi A.; Yu L.; Goulding D.; Rono M. K.; Bejon P.; Choudhary J.; Rayner J. Proteomic Analysis of Extracellular Vesicles from a Plasmodium Falciparum Kenyan Clinical Isolate Defines a Core Parasite Secretome. Wellcome Open Res. 2017, 2, 50.10.12688/wellcomeopenres.11910.1. PubMed DOI PMC

Kioko M.; Pance A.; Mwangi S.; Goulding D.; Kemp A.; Rono M.; Ochola-Oyier L. I.; Bull P. C.; Bejon P.; Rayner J. C.; Abdi A. I. Extracellular Vesicles Could Be a Putative Posttranscriptional Regulatory Mechanism That Shapes Intracellular RNA Levels in Plasmodium Falciparum. Nat. Commun. 2023, 14 (1), 6447.10.1038/s41467-023-42103-x. PubMed DOI PMC

Rivkin A.; Ben-Hur S.; Regev-Rudzki N. Malaria Parasites Distribute Subversive Messages across Enemy Lines. Trends Parasitol. 2017, 33 (1), 2–4. 10.1016/j.pt.2016.11.005. PubMed DOI

Escrevente C.; Keller S.; Altevogt P.; Costa J. Interaction and Uptake of Exosomes by Ovarian Cancer Cells. BMC Cancer 2011, 11 (1), 108.10.1186/1471-2407-11-108. PubMed DOI PMC

Gurung S.; Perocheau D.; Touramanidou L.; Baruteau J. The Exosome Journey: From Biogenesis to Uptake and Intracellular Signalling. Cell Commun. Signaling 2021, 19 (1), 47.10.1186/s12964-021-00730-1. PubMed DOI PMC

Friese C.; Yang J.. Extracellular Vesicle Transportation and Uptake by Recipient Cells Physiol. Behav. 2019; Vol. 46 (2), , pp 248–25610.3390/pr9020273.Extracellular. DOI

Raposo G.; Stoorvogel W. Extracellular Vesicles: Exosomes, Microvesicles, and Friends. J. Cell Biol. 2013, 200, 373–383. 10.1083/jcb.201211138. PubMed DOI PMC

Mulcahy L. A.; Pink R. C.; Carter D. R. F. Routes and Mechanisms of Extracellular Vesicle Uptake. J. Extracell. Vesicles 2014, 3 (1), 24641.10.3402/jev.v3.24641. PubMed DOI PMC

Horibe S.; Tanahashi T.; Kawauchi S.; Murakami Y.; Rikitake Y. Mechanism of Recipient Cell-Dependent Differences in Exosome Uptake. BMC Cancer 2018, 18 (1), 47.10.1186/s12885-017-3958-1. PubMed DOI PMC

Montecalvo A.; Larregina A. T.; Shufesky W. J.; Stolz D. B.; Sullivan M. L. G.; Karlsson J. M.; Baty C. J.; Gibson G. A.; Erdos G.; Wang Z.; Milosevic J.; Tkacheva O. A.; Divito S. J.; Jordan R.; Lyons-Weiler J.; Watkins S. C.; Morelli A. E. Mechanism of Transfer of Functional MicroRNAs between Mouse Dendritic Cells via Exosomes. Blood 2012, 119 (3), 756–766. 10.1182/blood-2011-02-338004. PubMed DOI PMC

Morelli A. E.; Larregina A. T.; Shufesky W. J.; Sullivan M. L. G.; Stolz D. B.; Papworth G. D.; Zahorchak A. F.; Logar A. J.; Wang Z.; Watkins S. C.; Falo L. D.; Thomson A. W. Endocytosis, Intracellular Sorting, and Processing of Exosomes by Dendritic Cells. Blood 2004, 104 (10), 3257–3266. 10.1182/blood-2004-03-0824. PubMed DOI

Joshi B. S.; de Beer M. A.; Giepmans B. N. G.; Zuhorn I. S. Endocytosis of Extracellular Vesicles and Release of Their Cargo from Endosomes. ACS Nano 2020, 14 (4), 4444–4455. 10.1021/acsnano.9b10033. PubMed DOI PMC

Eguchi S.; Takefuji M.; Sakaguchi T.; Ishihama S.; Mori Y.; Tsuda T.; Takikawa T.; Yoshida T.; Ohashi K.; Shimizu Y.; Hayashida R.; Kondo K.; Bando Y. K.; Ouchi N.; Murohara T. Cardiomyocytes Capture Stem Cell-Derived, Anti-Apoptotic MicroRNA-214 via Clathrin-Mediated Endocytosis in Acute Myocardial Infarction. J. Biol. Chem. 2019, 294 (31), 11665–11674. 10.1074/jbc.RA119.007537. PubMed DOI PMC

Zheng Y.; Tu C.; Zhang J.; Wang J. Inhibition of Multiple Myeloma-derived Exosomes Uptake Suppresses the Functional Response in Bone Marrow Stromal Cell. Int. J. Oncol. 2019, 54 (3), 1061–1070. 10.3892/ijo.2019.4685. PubMed DOI

Feng D.; Zhao W. L.; Ye Y. Y.; Bai X. C.; Liu R. Q.; Chang L. F.; Zhou Q.; Sui S. F. Cellular Internalization of Exosomes Occurs through Phagocytosis. Traffic 2010, 11 (5), 675–687. 10.1111/j.1600-0854.2010.01041.x. PubMed DOI

Fabbri M.; Paone A.; Calore F.; Galli R.; Gaudio E.; Santhanam R.; Lovat F.; Fadda P.; Mao C.; Nuovo G. J.; Zanesi N.; Crawford M.; Ozer G. H.; Wernicke D.; Alder H.; Caligiuri M. A.; Nana-Sinkam P.; Perrotti D.; Croce C. M. MicroRNAs Bind to Toll-like Receptors to Induce Prometastatic Inflammatory Response. Proc. Natl. Acad. Sci. U.S.A. 2012, 109 (31), E2110–E2116. 10.1073/pnas.1209414109. PubMed DOI PMC

Parolini I.; Federici C.; Raggi C.; Lugini L.; Palleschi S.; De Milito A.; Coscia C.; Iessi E.; Logozzi M.; Molinari A.; Colone M.; Tatti M.; Sargiacomo M.; Fais S. Microenvironmental PH Is a Key Factor for Exosome Traffic in Tumor Cells. J. Biol. Chem. 2009, 284 (49), 34211–34222. 10.1074/jbc.M109.041152. PubMed DOI PMC

Carrera-Bravo C.; Koh E. Y.; Tan K. S. W. The Roles of Parasite-Derived Extracellular Vesicles in Disease and Host-Parasite Communication. Parasitol. Int. 2021, 83, 10237310.1016/j.parint.2021.102373. PubMed DOI

Dekel E.; Abou Karam P.; Ohana-daniel Y.; Biton M.; Regev-rudzki N. Antibody-free labeling of malaria-derived extracellular vesicles using flow cytometry. Biomedicines 2020, 8 (5), 98.10.3390/biomedicines8050098. PubMed DOI PMC

Alfandari D.; Ben Ami Pilo H.; Abou Karam P.; Dagan O.; Joubran C.; Rotkopf R.; Regev-Rudzki N.; Porat Z. Monitoring Distribution Dynamics of EV RNA Cargo Within Recipient Monocytes and Macrophages. Front. Cell. Infect. Microbiol. 2022, 11, 73962810.3389/fcimb.2021.739628. PubMed DOI PMC

Janmey P. A.; Kinnunen P. K. J. Biophysical Properties of Lipids and Dynamic Membranes. Trends Cell Biol. 2006, 16 (10), 538–546. 10.1016/j.tcb.2006.08.009. PubMed DOI

Joseph J. G.; Liu A. P. Mechanical Regulation of Endocytosis: New Insights and Recent Advances. Adv. Biosyst. 2020, 4 (5), 1900278.10.1002/adbi.201900278. PubMed DOI

Conca D. V.; Bano F.; Wirén J. von.; Scherrer L.; Svirelis J.; Thorsteinsson K.; Dahlin A.; Bally M.. Variant-Specific Interactions at the Plasma Membrane: Heparan Sulfate’s Impact on SARS-CoV-2 Binding Kinetics bioRxiv 2024, p 2024-01.10.1101/2024.01.10.574981. PubMed DOI PMC

Norling K.; Bernasconi V.; Agmo Hernández V.; Parveen N.; Edwards K.; Lycke N. Y.; Hoök F.; Bally M. Gel Phase 1,2-Distearoyl-Sn-Glycero-3-Phosphocholine-Based Liposomes Are Superior to Fluid Phase Liposomes at Augmenting Both Antigen Presentation on Major Histocompatibility Complex Class II and Costimulatory Molecule Display by Dendritic Cells in Vitro. ACS Infect. Dis. 2019, 5 (11), 1867–1878. 10.1021/acsinfecdis.9b00189. PubMed DOI

Ofir-Birin Y.; Abou karam P.; Rudik A.; Giladi T.; Porat Z.; Regev-Rudzki N. Monitoring Extracellular Vesicle Cargo Active Uptake by Imaging Flow Cytometry. Front. Immunol. 2018, 9, 1011.10.3389/fimmu.2018.01011. PubMed DOI PMC

Zuba-Surma E. K.; Kucia M.; Abdel-latif A. A.; Lillard J. W.; Ratajczak M. Z. The ImageStream System: A Key Step to a New Era in Imaging. Folia Histochem. Cytobiol. 2007, 45 (4), 279–290. PubMed

Stegmann T.; Wey J.; Bartoldus I.; Schoen P.; Bron R.; Ortiz A.; Nieva J. L.; Wilschut J. Evaluation of Viral Membrane Fusion Assays. Comparison of the Octadecylrhodamine Dequenching Assay with the Pyrene Excimer Assay. Biochemistry 1993, 32 (42), 11330–11337. 10.1021/bi00093a009. PubMed DOI

MacDonald R. I. Characteristics of Self-Quenching of the Fluorescence of Lipid-Conjugated Rhodamine in Membranes. J. Biol. Chem. 1990, 265 (23), 13533–13539. 10.1016/S0021-9258(18)77380-8. PubMed DOI

Arbeloa F. L.; Ojeda P. R.; Arbeloa I. L. Flourescence Self-Quenching of the Molecular Forms of Rhodamine B in Aqueous and Ethanolic Solutions. J. Lumin. 1989, 44 (1–2), 105–112. 10.1016/0022-2313(89)90027-6. DOI

Zhao W.; Fogg D. K.; Kaplan M. J. A Novel Image-Based Quantitative Method for the Characterization of NETosis. J. Immunol. Methods 2015, 423, 104–110. 10.1016/j.jim.2015.04.027. PubMed DOI PMC

Lindner B.; Martin E.; Steininger M.; Bundalo A.; Lenter M.; Zuber J.; Schuler M. A Genome-Wide CRISPR/Cas9 Screen to Identify Phagocytosis Modulators in Monocytic THP-1 Cells. Sci. Rep. 2021, 11 (1), 12973.10.1038/s41598-021-92332-7. PubMed DOI PMC

Kurynina A. V.; Erokhina M. V.; Makarevich O. A.; Sysoeva V. Y.; Lepekha L. N.; Kuznetsov S. A.; Onishchenko G. E. Plasticity of Human THP–1 Cell Phagocytic Activity during Macrophagic Differentiation. Biochemistry 2018, 83 (3), 200–214. 10.1134/S0006297918030021. PubMed DOI

Mao Y.; Finnemann S. C. Regulation of Phagocytosis by Rho GTPases. Small GTPases 2015, 6 (2), 89–99. 10.4161/21541248.2014.989785. PubMed DOI PMC

Dean P.; Heunis T.; Härtlova A.; Trost M. Regulation of Phagosome Functions by Post-Translational Modifications: A New Paradigm. Curr. Opin. Chem. Biol. 2019, 48, 73–80. 10.1016/j.cbpa.2018.11.001. PubMed DOI

Cockram T. O. J.; Dundee J. M.; Popescu A. S.; Brown G. C. The Phagocytic Code Regulating Phagocytosis of Mammalian Cells. Front. Immunol. 2021, 12, 629979.10.3389/fimmu.2021.629979. PubMed DOI PMC

Richards D. M.; Endres R. G. The Mechanism of Phagocytosis: Two Stages of Engulfment. Biophys. J. 2014, 107 (7), 1542–1553. 10.1016/j.bpj.2014.07.070. PubMed DOI PMC

McKelvey K. J.; Powell K. L.; Ashton A. W.; Morris J. M.; McCracken S. A. Exosomes: Mechanisms of Uptake. J. Circ. Biomarkers 2015, 4, 7.10.5772/61186. PubMed DOI PMC

Chang M. Y.; Brune J. E.; Black M.; Altemeier W. A.; Frevert C. W. Multicompartmental Analysis of the Murine Pulmonary Immune Response by Spectral Flow Cytometry. Am. J. Physiol. Lung Cell. Mol. Physiol. 2023, 325 (4), L518–L535. 10.1152/ajplung.00317.2022. PubMed DOI PMC

Croce A. C.; Bottiroli G. Autofluorescence Spectroscopy and Imaging: A Tool for Biomedical Research and Diagnosis. Eur. J. Histochem. 2014, 58 (4), 320–337. 10.4081/ejh.2014.2461. PubMed DOI PMC

Thottacherry J. J.; Sathe M.; Prabhakara C.; Mayor S. Spoilt for Choice: Diverse Endocytic Pathways Function at the Cell Surface. Annu. Rev. Cell Dev. Biol. 2019, 35 (1), 55–84. 10.1146/annurev-cellbio-100617-062710. PubMed DOI PMC

Andronico L. A.; Jiang Y.; Carannante V.; Iskrak S.; Sandoz P. A.; Mikes J.; Klymchenko A.; Buggert M.; Österborg A.; Önfelt B.; Brodin P.; Sezgin E.. High-Throughput Analysis of Membrane Fluidity Unveils a Hidden Dimension in Immune Cell States bioRxiv 2024, p 2024-01.10.1101/2024.01.15.575649. DOI

Schneider J.; Dufrêne Y. F.; Barger W. R.; Lee G. U. Atomic Force Microscope Image Contrast Mechanisms on Supported Lipid Bilayers. Biophys. J. 2000, 79 (2), 1107–1118. 10.1016/S0006-3495(00)76364-8. PubMed DOI PMC

Garcia-Manyes S.; Sanz F. Nanomechanics of Lipid Bilayers by Force Spectroscopy with AFM: A Perspective. Biochim. Biophys. Acta, Biomembr. 2010, 1798 (4), 741–749. 10.1016/j.bbamem.2009.12.019. PubMed DOI

Dufrêne Y. F.; Boland T.; Schneider J. W.; Barger W. R.; Lee G. U. Characterization of the Physical Properties of Model Biomembranes at the Nanometer Scale with the Atomic Force Microscope. Faraday Discuss. 1999, 111 (0), 79–94. 10.1039/a807637e. PubMed DOI

Raucher D.; Sheetz M. P. Membrane Expansion Increases Endocytosis Rate during Mitosis. J. Cell Biol. 1999, 144 (3), 497–506. 10.1083/jcb.144.3.497. PubMed DOI PMC

Djakbarova U.; Madraki Y.; Chan E. T.; Kural C. Dynamic Interplay between Cell Membrane Tension and Clathrin-Mediated Endocytosis. Biol. Cell 2021, 113 (8), 344–373. 10.1111/boc.202000110. PubMed DOI PMC

Rodal S. K.; Skretting G.; Garred Ø.; Vilhardt F.; Van Deurs B.; Sandvig K. Extraction of Cholesterol with Methyl-β-Cyclodextrin Perturbs Formation of Clathrin-Coated Endocytic Vesicles. Mol. Biol. Cell 1999, 10 (4), 961–974. 10.1091/mbc.10.4.961. PubMed DOI PMC

Hissa B.; Pontes B.; Roma P. M. S.; Alves A. P.; Rocha C. D.; Valverde T. M.; Aguiar P. H. N.; Almeida F. P.; Guimarães A. J.; Guatimosim C.; Silva A. M.; Fernandes M. C.; Andrews N. W.; Viana N. B.; Mesquita O. N.; Agero U.; Andrade L. O. Membrane Cholesterol Removal Changes Mechanical Properties of Cells and Induces Secretion of a Specific Pool of Lysosomes. PLoS One 2013, 8 (12), e8298810.1371/journal.pone.0082988. PubMed DOI PMC

Biswas A.; Kashyap P.; Datta S.; Sengupta T.; Sinha B. Cholesterol Depletion by MβCD Enhances Cell Membrane Tension and Its Variations-Reducing Integrity. Biophys. J. 2019, 116 (8), 1456–1468. 10.1016/j.bpj.2019.03.016. PubMed DOI PMC

Yáñez-Mó M.; Siljander P.R.; Andreu Z.; Zavec A.B.; Borràs F.E.; Buzas E.I.; Buzas K.; Casal E.; Cappello F.; Carvalho J.; et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles 2015, 14 (4), 27066.10.3402/jev.v4.27066. PubMed DOI PMC

Owen D. M.Methods in Membrane Lipids, 2nd ed.; Humana Press, 2015; Vol. 1232, pp 1–327.

Park D.; Don A. S.; Massamiri T.; Karwa A.; Warner B.; MacDonald J.; Hemenway C.; Naik A.; Kuan K. T.; Dilda P. J.; Wong J. W. H.; Camphausen K.; Chinen L.; Dyszlewski M.; Hogg P. J. Noninvasive Imaging of Cell Death Using an Hsp90 Ligand. J. Am. Chem. Soc. 2011, 133 (9), 2832–2835. 10.1021/ja110226y. PubMed DOI PMC

Krylova S. V.; Feng D. The Machinery of Exosomes: Biogenesis, Release, and Uptake. Int. J. Mol. Sci. 2023, 24 (2), 1337.10.3390/ijms24021337. PubMed DOI PMC

Rai A. K.; Johnson P. J. Trichomonas Vaginalis Extracellular Vesicles Are Internalized by Host Cells Using Proteoglycans and Caveolin-Dependent Endocytosis. Proc. Natl. Acad. Sci. U.S.A. 2019, 116 (43), 21354–21360. 10.1073/pnas.1912356116. PubMed DOI PMC

Grant B. D.; Donaldson J. G. Pathways and Mechanisms of Endocytic Recycling. Nat. Rev. Mol. Cell Biol. 2009, 10 (9), 597–608. 10.1038/nrm2755. PubMed DOI PMC

Cocucci E.; Aguet F.; Boulant S.; Kirchhausen T. The First Five Seconds in the Life of a Clathrin-Coated Pit. Cell 2012, 150 (3), 495–507. 10.1016/j.cell.2012.05.047. PubMed DOI PMC

François-Martin C.; Pincet F. Actual Fusion Efficiency in the Lipid Mixing Assay - Comparison between Nanodiscs and Liposomes. Sci. Rep. 2017, 7 (1), 43860.10.1038/srep43860. PubMed DOI PMC

Cho Y. Y.; Kwon O. H.; Chung S. Preferred Endocytosis of Amyloid Precursor Protein from Cholesterol-Enriched Lipid Raft Microdomains. Molecules 2020, 25 (23), 5490.10.3390/molecules25235490. PubMed DOI PMC

Watts C.; Marsh M. Endocytosis: What Goes in and How?. J. Cell Sci. 1992, 103 (1), 1–8. 10.1242/JCS.103.1.1A. PubMed DOI

Morandi M. I.; Busko P.; Ozer-Partuk E.; Khan S.; Zarfati G.; Elbaz-Alon Y.; Abou Karam P.; Napso Shogan T.; Ginini L.; Gil Z.; Regev-Rudzki N.; Avinoam O. Extracellular Vesicle Fusion Visualized by Cryo-Electron Microscopy. PNAS Nexus 2022, 1 (4), pgac156.10.1093/pnasnexus/pgac156. PubMed DOI PMC

Ben Ami Pilo H.; Khan Khilji S.; Lühle J.; Biskup K.; Levy Gal B.; Rosenhek Goldian I.; Alfandari D.; Revach O.; Kiper E.; Morandi M. I.; Rotkopf R.; Porat Z.; Blanchard V.; Seeberger P. H.; Regev-Rudzki N.; Moscovitz O. Sialylated N -glycans Mediate Monocyte Uptake of Extracellular Vesicles Secreted from Plasmodium Falciparum -infected Red Blood Cells. J. Extracell. Biol. 2022, 1 (2), e33.10.1002/jex2.33. PubMed DOI PMC

Näslund T. I.; Paquin-Proulx D.; Paredes P. T.; Vallhov H.; Sandberg J. K.; Gabrielsson S. Exosomes from Breast Milk Inhibit HIV-1 Infection of Dendritic Cells and Subsequent Viral Transfer to CD4+ T Cells. Aids 2014, 28 (2), 171–180. 10.1097/QAD.0000000000000159. PubMed DOI

Rana S.; Yue S.; Stadel D.; Zöller M. Toward Tailored Exosomes: The Exosomal Tetraspanin Web Contributes to Target Cell Selection. Int. J. Biochem. Cell Biol. 2012, 44 (9), 1574–1584. 10.1016/j.biocel.2012.06.018. PubMed DOI

Zech D.; Rana S.; Büchler M. W.; Zöller M. Tumor-Exosomes and Leukocyte Activation: An Ambivalent Crosstalk. Cell Commun. Signaling 2012, 10, 37.10.1186/1478-811X-10-37. PubMed DOI PMC

Groza R.; Schmidt K. V.; Müller P. M.; Ronchi P.; Schlack-Leigers C.; Neu U.; Puchkov D.; Dimova R.; Matthaeus C.; Taraska J.; Weikl T. R.; Ewers H. Adhesion Energy Controls Lipid Binding-Mediated Endocytosis. Nat. Commun. 2024, 15 (1), 2767.10.1038/s41467-024-47109-7. PubMed DOI PMC

Martin-Jaular L.; Nakayasu E. S.; Ferrer M.; Almeida I. C.; del Portillo H. A. Exosomes from Plasmodium Yoelii-Infected Reticulocytes Protect Mice from Lethal Infections. PLoS One 2011, 6 (10), e26588.10.1371/journal.pone.0026588. PubMed DOI PMC

Trager W.; Jensen J. B. Human Malaria Parasites in Continuous Culture. J. Parasitol. 2005, 91 (3), 484–486. 10.1645/0022-3395(2005)091[0484:HMPICC]2.0.CO;2. PubMed DOI

Unterholzner L.; Keating S. E.; Baran M.; Horan K. A.; Jensen S. B.; Sharma S.; Sirois C. M.; Jin T.; Latz E.; Xiao T. S.; Fitzgerald K. A.; Paludan S. R.; Bowie A. G. IFI16 Is an Innate Immune Sensor for Intracellular DNA. Nat. Immunol. 2010, 11 (11), 997–1004. 10.1038/ni.1932. PubMed DOI PMC

Cladera J.; Martin I.; O’Shea P. The Fusion Domain of HIV Gp41 Interacts Specifically with Heparan Sulfate on the T-Lymphocyte Cell Surface. EMBO J. 2001, 20 (1–2), 19–26. 10.1093/emboj/20.1.19. PubMed DOI PMC

Klug Y. A.; Schwarzer R.; Rotem E.; Charni M.; Nudelman A.; Gramatica A.; Zarmi B.; Rotter V.; Shai Y. The HIV Gp41 Fusion Protein Inhibits T-Cell Activation through the Lentiviral Lytic Peptide 2 Motif. Biochemistry 2019, 58 (6), 818–832. 10.1021/acs.biochem.8b01175. PubMed DOI

Coleman B. M.; Hanssen E.; Lawson V. A.; Hill A. F. Prion-Infected Cells Regulate the Release of Exosomes with Distinct Ultrastructural Features. FASEB J. 2012, 26 (10), 4160–4173. 10.1096/fj.11-202077. PubMed DOI

Gerstle Z.; Desai R.; Veatch S. L. Giant Plasma Membrane Vesicles: An Experimental Tool for Probing the Effects of Drugs and Other Conditions on Membrane Domain Stability. Methods Enzymol. 2018, 603, 129–150. 10.1016/bs.mie.2018.02.007. PubMed DOI PMC

Filipe V.; Hawe A.; Jiskoot W. Critical Evaluation of Nanoparticle Tracking Analysis (NTA) by NanoSight for the Measurement of Nanoparticles and Protein Aggregates. Pharm. Res. 2010, 27 (5), 796–810. 10.1007/s11095-010-0073-2. PubMed DOI PMC

Fendl B.; Weiss R.; Fischer M. B.; Spittler A.; Weber V. Characterization of Extracellular Vesicles in Whole Blood: Influence of Pre-Analytical Parameters and Visualization of Vesicle-Cell Interactions Using Imaging Flow Cytometry. Biochem. Biophys. Res. Commun. 2016, 478 (1), 168–173. 10.1016/j.bbrc.2016.07.073. PubMed DOI

Nečas D.; Klapetek P. Gwyddion: An Open-Source Software for SPM Data Analysis. Open Phys. 2012, 10 (1), 181–188. 10.2478/s11534-011-0096-2. DOI

Virtanen P.; Gommers R.; Oliphant T. E.; Haberland M.; Reddy T.; Cournapeau D.; Burovski E.; Peterson P.; Weckesser W.; Bright J.; van der Walt S. J.; Brett M.; Wilson J.; Millman K. J.; Mayorov N.; Nelson A. R. J.; Jones E.; Kern R.; Larson E.; Carey C. J.; Polat İ.; Feng Y.; Moore E. W.; VanderPlas J.; Laxalde D.; Perktold J.; Cimrman R.; Henriksen I.; Quintero E. A.; Harris C. R.; Archibald A. M.; Ribeiro A. H.; Pedregosa F.; van Mulbregt P.; Vijaykumar A.; Bardelli A. Pietro.; Rothberg A.; Hilboll A.; Kloeckner A.; Scopatz A.; Lee A.; Rokem A.; Woods C. N.; Fulton C.; Masson C.; Häggström C.; Fitzgerald C.; Nicholson D. A.; Hagen D. R.; Pasechnik D. V.; Olivetti E.; Martin E.; Wieser E.; Silva F.; Lenders F.; Wilhelm F.; Young G.; Price G. A.; Ingold G. L.; Allen G. E.; Lee G. R.; Audren H.; Probst I.; Dietrich J. P.; Silterra J.; Webber J. T.; Slavič J.; Nothman J.; Buchner J.; Kulick J.; Schönberger J. L.; de Miranda Cardoso J. V.; Reimer J.; Harrington J.; Rodríguez J. L. C.; Nunez-Iglesias J.; Kuczynski J.; Tritz K.; Thoma M.; Newville M.; Kümmerer M.; Bolingbroke M.; Tartre M.; Pak M.; Smith N. J.; Nowaczyk N.; Shebanov N.; Pavlyk O.; Brodtkorb P. A.; Lee P.; McGibbon R. T.; Feldbauer R.; Lewis S.; Tygier S.; Sievert S.; Vigna S.; Peterson S.; More S.; Pudlik T.; Oshima T.; Pingel T. J.; Robitaille T. P.; Spura T.; Jones T. R.; Cera T.; Leslie T.; Zito T.; Krauss T.; Upadhyay U.; Halchenko Y. O.; Vázquez-Baeza Y. SciPy 1.0: Fundamental Algorithms for Scientific Computing in Python. Nat. Methods 2020, 17 (3), 261–272. 10.1038/s41592-019-0686-2. PubMed DOI PMC

Pedregosa F.; Michel V.; Grisel O.; Blondel M.; Prettenhofer P.; Weiss R.; Vanderplas J.; Cournapeau D.; Pedregosa F.; Varoquaux G.; Gramfort A.; Thirion B.; Grisel O.; Dubourg V.; Passos A.; Brucher M. Scikit-Learn: Machine Learning in Python. J. Mach. Learn. Res. 2011, 12 (85), 2825–2830.

Najít záznam

Citační ukazatele

Možnosti archivace