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      • Record: found
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      Lipidomic Analysis of Extracellular Vesicles from the Pathogenic Phase of Paracoccidioides brasiliensis

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          Abstract

          Background

          Fungal extracellular vesicles are able to cross the cell wall and transport molecules that help in nutrient acquisition, cell defense, and modulation of the host defense machinery.

          Methodology/Principal Findings

          Here we present a detailed lipidomic analysis of extracellular vesicles released by Paracoccidioides brasiliensis at the yeast pathogenic phase. We compared data of two representative isolates, Pb3 and Pb18, which have distinct virulence profiles and phylogenetic background. Vesicle lipids were fractionated into different classes and analyzed by either electrospray ionization- or gas chromatography-mass spectrometry. We found two species of monohexosylceramide and 33 phospholipid species, including phosphatidylcholine, phosphatidylethanolamine, phosphatidic acid, phosphatidylserine, phosphatidylinositol, and phosphatidylglycerol. Among the phospholipid-bound fatty acids in extracellular vesicles, C18 1 predominated in Pb3, whereas C18:2 prevailed in Pb18. The prevalent sterol in Pb3 and Pb18 vesicles was brassicasterol, followed by ergosterol and lanosterol. Inter-isolate differences in sterol composition were observed, and also between extracellular vesicles and whole cells.

          Conclusions/Significance

          The extensive lipidomic analysis of extracellular vesicles from two P. brasiliensis isolates will help to understand the composition of these fungal components/organelles and will hopefully be useful to study their biogenesis and role in host-pathogen interactions.

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          Most cited references41

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          Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation.

          Richard Wubbolts, Rachel Leckie, Peter Veenhuizen … (2003)
          Exosomes are 60-100-nm membrane vesicles that are secreted into the extracellular milieu as a consequence of multivesicular body fusion with the plasma membrane. Here we determined the protein and lipid compositions of highly purified human B cell-derived exosomes. Mass spectrometric analysis indicated the abundant presence of major histocompatibility complex (MHC) class I and class II, heat shock cognate 70, heat shock protein 90, integrin alpha 4, CD45, moesin, tubulin (alpha and beta), actin, G(i)alpha(2), and a multitude of other proteins. An alpha 4-integrin may direct B cell-derived exosomes to follicular dendritic cells, which were described previously as potential target cells. Clathrin, heat shock cognate 70, and heat shock protein 90 may be involved in protein sorting at multivesicular bodies. Exosomes were also enriched in cholesterol, sphingomyelin, and ganglioside GM3, lipids that are typically enriched in detergent-resistant membranes. Most exosome-associated proteins, including MHC class II and tetraspanins, were insoluble in 3-[(3-cholamidopropyl)dimethylammonio]-1-propanesulfonic acid (CHAPS)-containing buffers. Multivesicular body-linked MHC class II was also resistant to CHAPS whereas plasma membrane-associated MHC class II was solubilized readily. Together, these data suggest that recruitment of membrane proteins from the limiting membranes into the internal vesicles of multivesicular bodies may involve their incorporation into tetraspanin-containing detergent-resistant membrane domains.
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            Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies.

            Caroline Subra, Karine Laulagnier, Bertrand Perret … (2007)
            Exosomes are part of the family of "bioactive vesicles" and appear to be involved in distal communications between cells. They vehiculate bioactive lipids and lipolytic enzymes and their biogenesis require specific lipids and a membrane reorganisation. Their biogenesis pathway could be a way to secrete enzymes involved in lipid signalling and to generate "particulate agonists". However, this pathway seems also to be used by pathogens such as HIV. This review will consider several aspects of lipidomics studies which might help to understand the fate and role of these fascinating vesicles.
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              Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization.

              Karine Laulagnier, Claude Motta, Safouane Hamdi … (2004)
              Exosomes are small vesicles secreted from multivesicular bodies, which are able to stimulate the immune system leading to tumour cell eradication. We have analysed lipids of exosomes secreted either upon stimulation from rat mast cells (RBL-2H3 cells), or constitutively from human dendritic cells. As compared with parent cells, exosomes displayed an enrichment in sphingomyelin, but not in cholesterol. Phosphatidylcholine content was decreased, but an enrichment was noted in disaturated molecular species as in phosphatidylethanolamines. Lyso(bis)phosphatidic acid was not enriched in exosomes as compared with cells. Fluorescence anisotropy demonstrated an increase in exosome-membrane rigidity from pH 5 to 7, suggesting their membrane reorganization between the acidic multivesicular body compartment and the neutral outer cell medium. NMR analysis established a bilayer organization of exosome membrane, and ESR studies using 16-doxyl stearic acid demonstrated a higher flip-flop of lipids between the two leaflets as compared with plasma membrane. In addition, the exosome membrane exhibited no asymmetrical distribution of phosphatidylethanolamines. Therefore exosome membrane displays a similar content of the major phospholipids and cholesterol, and is organized as a lipid bilayer with a random distribution of phosphatidylethanolamines. In addition, we observed tight lipid packing at neutral pH and a rapid flip-flop between the two leaflets of exosome membranes. These parameters could be used as a hallmark of exosomes.
              Article 0 comments Cited 222 times – based on 0 reviews     Review now
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                Author and article information

                Contributors
                : Role: Editor
                Journal
                Journal ID (nlm-ta): PLoS One
                Journal ID (iso-abbrev): PLoS ONE
                Journal ID (publisher-id): plos
                Journal ID (pmc): plosone
                Title: PLoS ONE
                Publisher: Public Library of Science (San Francisco, USA )
                ISSN (Electronic): 1932-6203
                Publication date Collection: 2012
                Publication date (Electronic): 22 June 2012
                Volume: 7
                Issue: 6
                Electronic Location Identifier: e39463
                Affiliations
                [1 ]Departamento de Microbiologia, Imunologia e Parasitologia, Universidade Federal de São Paulo, UNIFESP, São Paulo, São Paulo, Brazil
                [2 ]Border Biomedical Research Center, Department of Biological Sciences, University of Texas at El Paso (UTEP), El Paso, Texas, United States of America
                Montana State University, United States of America
                Author notes

                Conceived and designed the experiments: MCV ESN LG ALM ICA RP. Performed the experiments: MCV ESN LG LVGL FGL. Analyzed the data: MCV ESN LVGL LG FGL ALM ICA RP. Contributed reagents/materials/analysis tools: ICA RP. Wrote the paper: MCV ESN ICA RP.

                [¤]

                Current address: Biological Science Division, Pacific Northwest National Laboratory, Richland, Washington, United States of America

                Article
                Publisher ID: PONE-D-12-08838
                DOI: 10.1371/journal.pone.0039463
                PMC ID: 3382159
                PubMed ID: 22745761
                SO-VID: 132149cb-6256-4b1b-97a7-2141ad7670c6
                Copyright © Vallejo et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
                History
                Date received : 27 March 2012
                Date accepted : 21 May 2012
                Page count
                Pages: 10
                Categories
                Subject: Research Article
                Subject: Biology
                Subject: Biochemistry
                Subject: Lipids
                Subject: Fatty Acids
                Subject: Lipid Structure
                Subject: Neutral Lipids
                Subject: Sterols
                Subject: Microbiology
                Subject: Mycology
                Subject: Fungal Biochemistry
                Subject: Microbial Pathogens
                Subject: Medicine
                Subject: Infectious Diseases
                Subject: Fungal Diseases
                Subject: Paracoccidiomycosis
                Subject: Neglected Tropical Diseases
                Subject: Paracoccidiomycosis

                ScienceOpen disciplines: Uncategorized
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                ScienceOpen disciplines: Uncategorized

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