Lipids in exosomes: Current knowledge and the way forward

Colombo, 2014, Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles, Annu Rev Cell Dev Biol, 30, 255, 10.1146/annurev-cellbio-101512-122326 Bobrie, 2011, Exosome secretion: molecular mechanisms and roles in immune responses, Traffic, 12, 1659, 10.1111/j.1600-0854.2011.01225.x György, 2011, Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles, Cell Mol Life Sci, 68, 2667, 10.1007/s00018-011-0689-3 Raposo, 2013, Extracellular vesicles: exosomes, microvesicles, and friends, J Cell Biol, 200, 373, 10.1083/jcb.201211138 Kalra, 2012, Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation, PLoS Biol, 10, 10.1371/journal.pbio.1001450 Kim, 2015, EVpedia: a community web resource for prokaryotic and eukaryotic extracellular vesicles research, Semin Cell Dev Biol, 40, 4, 10.1016/j.semcdb.2015.02.005 Yanez-Mo, 2015, Biological properties of extracellular vesicles and their physiological functions, J Extracell Vesicles, 4, 27066, 10.3402/jev.v4.27066 Fais, 2016, Evidence-based clinical use of nanoscale extracellular vesicles in nanomedicine, ACS Nano, 10, 3886, 10.1021/acsnano.5b08015 El Andaloussi, 2013, Extracellular vesicles: biology and emerging therapeutic opportunities, Nat Rev Drug Discov, 12, 347, 10.1038/nrd3978 Tkach, 2016, Communication by extracellular vesicles: where we are and where we need to go, Cell, 164, 1226, 10.1016/j.cell.2016.01.043 Vader, 2016, Extracellular vesicles for drug delivery, Adv Drug Deliv Rev, 106, 148, 10.1016/j.addr.2016.02.006 Maas, 2017, Extracellular vesicles: unique intercellular delivery vehicles, Trends Cell Biol, 27, 172, 10.1016/j.tcb.2016.11.003 Subra, 2007, Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies, Biochimie, 89, 205, 10.1016/j.biochi.2006.10.014 Record, 2014, Emerging concepts on the role of exosomes in lipid metabolic diseases, Biochimie, 96, 67, 10.1016/j.biochi.2013.06.016 Record, 2014, Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies, Biochim Biophys Acta, 1841, 108, 10.1016/j.bbalip.2013.10.004 Kavaliauskiene, 2014, Cell density-induced changes in lipid composition and intracellular trafficking, Cell Mol Life Sci, 71, 1097, 10.1007/s00018-013-1441-y Stoll, 1984, Changes in serum influence the fatty acid composition of established cell lines, In Vitro, 20, 732, 10.1007/BF02618879 Sodar, 2016, Low-density lipoprotein mimics blood plasma-derived exosomes and microvesicles during isolation and detection, Sci Rep, 6, 24316, 10.1038/srep24316 Thery, 2006, Isolation and characterization of exosomes from cell culture supernatants and biological fluids, 22 Li, 2017, Progress in Exosome Isolation Techniques Theranostics, 7, 789 van der Pol, 2016, Recent developments in the nomenclature, presence, isolation, detection and clinical impact of extracellular vesicles, J Thromb Haemost, 14, 56, 10.1111/jth.13190 Taylor, 2015, Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes, Methods, 87, 3, 10.1016/j.ymeth.2015.02.019 van Meer, 2008, Membrane lipids: where they are and how they behave, Nat Rev Mol Cell Biol, 9, 112, 10.1038/nrm2330 Khaldoun, 2014, Autophagosomes contribute to intracellular lipid distribution in enterocytes, Mol Biol Cell, 25, 118, 10.1091/mbc.e13-06-0324 Hessvik, 2016, PIKfyve inhibition increases exosome release and induces secretory autophagy, Cell Mol Life Sci, 73, 4717, 10.1007/s00018-016-2309-8 Koivusalo, 2001, Quantitative determination of phospholipid compositions by ESI-MS: effects of acyl chain length, unsaturation, and lipid concentration on instrument response, J Lipid Res, 42, 663, 10.1016/S0022-2275(20)31176-7 Han, 2005, Shotgun lipidomics: electrospray ionization mass spectrometric analysis and quantitation of cellular lipidomes directly from crude extracts of biological samples, Mass Spectrom Rev, 24, 367, 10.1002/mas.20023 Wenk, 2010, Lipidomics: new tools and applications, Cell, 143, 888, 10.1016/j.cell.2010.11.033 Jung, 2011, High throughput quantitative molecular lipidomics, Biochim Biophys Acta, 1811, 925, 10.1016/j.bbalip.2011.06.025 Yang, 2011, Accurate quantification of lipid species by electrospray ionization mass spectrometry - meet a key challenge in lipidomics, Metabolites, 1, 21, 10.3390/metabo1010021 Wang, 2016, Novel advances in shotgun lipidomics for biology and medicine, Prog Lipid Res, 61, 83, 10.1016/j.plipres.2015.12.002 Hankins, 2015, Role of flippases, scramblases and transfer proteins in phosphatidylserine subcellular distribution, Traffic, 16, 35, 10.1111/tra.12233 Clark, 2011, Flippin' lipids, Nat Immunol, 12, 373, 10.1038/ni.2024 Llorente, 2013, Molecular lipidomics of exosomes released by PC-3 prostate cancer cells, Biochim Biophys Acta, 1831, 1302, 10.1016/j.bbalip.2013.04.011 Trajkovic, 2008, Ceramide triggers budding of exosome vesicles into multivesicular endosomes, Science, 319, 1244, 10.1126/science.1153124 Wubbolts, 2003, Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation, J Biol Chem, 278, 10963, 10.1074/jbc.M207550200 Laulagnier, 2004, Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization, Biochem J, 380, 161, 10.1042/bj20031594 Vidal, 1989, Asymmetric distribution of phospholipids in the membrane of vesicles released during in vitro maturation of guinea pig reticulocytes: evidence precluding a role for “aminophospholipid translocase”, J Cell Physiol, 140, 455, 10.1002/jcp.1041400308 Brouwers, 2013, Distinct lipid compositions of two types of human prostasomes, Proteomics, 13, 1660, 10.1002/pmic.201200348 Skotland, 2017, Molecular lipid species in urinary exosomes as potential prostate cancer biomarkers, Eur J Cancer, 70, 122, 10.1016/j.ejca.2016.10.011 Simbari, 2016, Plasmalogen enrichment in exosomes secreted by a nematode parasite versus those derived from its mouse host: implications for exosome stability and biology, J Extracell Vesicles, 5, 30741, 10.3402/jev.v5.30741 Hosseini-Beheshti, 2012, Exosomes as biomarker enriched microvesicles: characterization of exosomal proteins derived from a panel of prostate cell lines with distinct AR phenotypes, Mol Cell Proteomics, 11, 863, 10.1074/mcp.M111.014845 Phuyal, 2015, The ether lipid precursor hexadecylglycerol stimulates the release and changes the composition of exosomes derived from PC-3 cells, J Biol Chem, 290, 4225, 10.1074/jbc.M114.593962 Vidal, 1993, The small GTP-binding proteins Rab4 and ARF are associated with released exosomes during reticulocyte maturation, Eur J Cell Biol, 60, 261 Carayon, 2011, Proteolipidic composition of exosomes changes during reticulocyte maturation, J Biol Chem, 286, 34426, 10.1074/jbc.M111.257444 Lydic, 2015, Rapid and comprehensive ‘shotgun’ lipidome profiling of colorectal cancer cell derived exosomes, Methods, 87, 83, 10.1016/j.ymeth.2015.04.014 Haraszti, 2016, High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources, J Extracell. Vesicles, 5, 32570, 10.3402/jev.v5.32570 Petersen, 2010, Connecting Hsp70, sphingolipid metabolism and lysosomal stability, Cell Cycle, 9, 2305, 10.4161/cc.9.12.12052 Schulze, 2014, Sphingolipids and lysosomal pathologies, Biochim Biophys Acta, 1841, 799, 10.1016/j.bbalip.2013.10.015 Arienti, 1998, Fatty acid pattern of human prostasome lipid, Arch Biochem Biophys, 358, 391, 10.1006/abbi.1998.0876 Arienti, 2001, Lipid fatty acid and protein pattern of equine prostasome-like vesicles, Comp Biochem Physiol B Biochem Mol Biol, 128, 661, 10.1016/S1096-4959(00)00351-1 Piehl, 2006, Biochemical characterization and membrane fluidity of membranous vesicles isolated from boar seminal plasma, Anim Reprod Sci, 92, 401, 10.1016/j.anireprosci.2005.06.005 Huang, 1999, Maximum solubility of cholesterol in phosphatidylcholine and phosphatidylethanolamine bilayers, Biochim Biophys Acta, 1417, 89, 10.1016/S0005-2736(98)00260-0 Lorizate, 2013, Comparative lipidomics analysis of HIV-1 particles and their producer cell membrane in different cell lines, Cell Microbiol, 15, 292, 10.1111/cmi.12101 Szempruch, 2016, Sending a message: extracellular vesicles of pathogenic protozoan parasites, Nat Rev Microbiol, 14, 669, 10.1038/nrmicro.2016.110 Kimura, 2016, Roles of specific lipid species in the cell and their molecular mechanism, Prog Lipid Res, 62, 75, 10.1016/j.plipres.2016.02.001 Róg, 2015, Interdigitation of long-chain sphingomyelin induces coupling of membrane leaflets in a cholesterol dependent manner, Biochim Biophys Acta, 1858, 281, 10.1016/j.bbamem.2015.12.003 Marquardt, 2016, Cholesterol's location in lipid bilayers, Chem Phys Lipids, 199, 17, 10.1016/j.chemphyslip.2016.04.001 Segawa, 2015, An apoptotic ‘eat me’ signal: phosphatidylserine exposure, Trends Cell Biol, 25, 639, 10.1016/j.tcb.2015.08.003 Hoshino, 2015, Tumour exosome integrins determine organotropic metastasis, Nature, 525, 329, 10.1038/nature15756 Wei, 2016, Surface phosphatidylserine is responsible for the internalization on microvesicles derived from hypoxia-induced human bone marrow mesenchymal stem cells into human endothelial cells, PLoS One, 11 Nakai, 2016, A novel affinity-based method for the isolation of highly purified extracellular vesicles, Sci Rep, 6, 33935, 10.1038/srep33935 Lai, 2016, MSC secretes at least 3 EV types each with a unique permutation of membrane lipid, protein and RNA, J Extracell Vesicles, 5, 29828, 10.3402/jev.v5.29828 Gentile, 1994, Determination of the size of HIV using adenovirus type 2 as an internal length marker, J Virol Methods, 48, 43, 10.1016/0166-0934(94)90087-6 Chamberlain, 2004, Detergents as tools for the purification and classification of lipid rafts, FEBS Lett, 559, 1, 10.1016/S0014-5793(04)00050-X Sonnino, 2013, Membrane domains and the “lipid raft” concept, Curr Med Chem, 20, 4 Pike, 2002, Lipid rafts are enriched in arachidonic acid and plasmenylethanolamine and their composition is independent of caveolin-1 expression: a quantitative electrospray ionization/mass spectrometric analysis, Biochemistry, 41, 2075, 10.1021/bi0156557 Manni, 2015, Lipids that determine detergent resistance of MDCK cell membrane fractions, Chem Phys Lipids, 191, 68, 10.1016/j.chemphyslip.2015.08.011 Martin, 2005, Detailed characterization of the lipid composition of detergent-resistant membranes from photoreceptor rod outer segment membranes, Invest Ophthalmol Vis Sci, 46, 1147, 10.1167/iovs.04-1207 van Gestel, 2016, Ultrastructure and lipid composition of detergent-resistant membranes derived from mammalian sperm and two types of epithelial cells, Cell Tissue Res, 363, 129, 10.1007/s00441-015-2272-y Schuck, 2003, Resistance of cell membranes to different detergents, Proc Natl Acad Sci, 100, 5795, 10.1073/pnas.0631579100 Babiychuk, 2006, Biochemical characterization of detergent-resistant membranes: a systematic approach, Biochem J, 397, 407, 10.1042/BJ20060056 Chen, 2009, Isolation at physiological temperature of detergent-resistant membranes with properties expected of lipid rafts: the influence of buffer composition, Biochem J, 417, 525, 10.1042/BJ20081385 Brugger, 2006, The HIV lipidome: a raft with an unusual composition, Proc Natl Acad Sci, 103, 2641, 10.1073/pnas.0511136103 Kosaka, 2010, Secretory mechanisms and intercellular transfer of microRNAs in living cells, J Biol Chem, 285, 17442, 10.1074/jbc.M110.107821 Mittelbrunn, 2011, Unidirectional transfer of microRNA-loaded exosomes from T cells to antigen-presenting cells, Nat Commun, 2, 282, 10.1038/ncomms1285 van Niel, 2011, The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis, Dev Cell, 21, 708, 10.1016/j.devcel.2011.08.019 Colombo, 2013, Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles, J Cell Sci, 126, 5553 Phuyal, 2014, Regulation of exosome release by glycosphingolipids and flotillins, FEBS J, 281, 2214, 10.1111/febs.12775 Milhas, 2010, Anterograde and retrograde transport of neutral sphingomyelinase-2 between the Golgi and the plasma membrane, Biochim Biophys Acta, 1801, 1361, 10.1016/j.bbalip.2010.08.001 Hannun, 2002, The ceramide-centric universe of lipid-mediated cell regulation: stress encounters of the lipid kind, J Biol Chem, 277, 25847, 10.1074/jbc.R200008200 Ghossoub, 2014, Syntenin-ALIX exosome biogenesis and budding into multivesicular bodies are controlled by ARF6 and PLD2, Nat Commun, 5, 3477, 10.1038/ncomms4477 Laulagnier, 2004, PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes, FEBS Lett, 572, 11, 10.1016/j.febslet.2004.06.082 Alonso, 2005, Diacylglycerol kinase alpha regulates the secretion of lethal exosomes bearing Fas ligand during activation-induced cell death of T lymphocytes, J Biol Chem, 280, 28439, 10.1074/jbc.M501112200 Glaser, 1994, Plasmenylethanolamine facilitates rapid membrane fusion: a stopped-flow kinetic investigation correlating the propensity of a major plasma membrane constituent to adopt an HII phase with its ability to promote membrane fusion, Biochemistry, 33, 5805, 10.1021/bi00185a019 Li, 2016, A molecular mechanism to regulate lysosome motility for lysosome positioning and tubulation, Nat Cell Biol, 18, 404, 10.1038/ncb3324 Niemela, 2007, Assessing the nature of lipid raft membranes, PLoS Comput Biol, 3, 10.1371/journal.pcbi.0030034 Dupuy, 2008, Protein area occupancy at the center of the red blood cell membrane, Proc Natl Acad Sci, 105, 2848, 10.1073/pnas.0712379105 Fuhrmann, 2015, Active loading into extracellular vesicles significantly improves the cellular uptake and photodynamic effect of porphyrins, J Control Release, 205, 35, 10.1016/j.jconrel.2014.11.029 Johnsen, 2014, A comprehensive overview of exosomes as drug delivery vehicles - endogenous nanocarriers for targeted cancer therapy, Biochim Biophys Acta, 1846, 75 Batrakova, 2016, Development and regulation of exosome-based therapy products, Wiley Interdiscip Rev Nanomed Nanobiotechnol, 8, 744, 10.1002/wnan.1395 Ingato, 2016, Good things come in small packages: overcoming challenges to harness extracellular vesicles for therapeutic delivery, J Control Release, 241, 174, 10.1016/j.jconrel.2016.09.016 Abrami, 2013, Hijacking multivesicular bodies enables long-term and exosome-mediated long-distance action of anthrax toxin, Cell Rep, 5, 986, 10.1016/j.celrep.2013.10.019 Huebner, 2015, Exosomes in urine biomarker discovery, Adv Exp Med Biol, 845, 43, 10.1007/978-94-017-9523-4_5 Rak, 2013, Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer, Front Pharmacol, 4, 21, 10.3389/fphar.2013.00021 Stremersch, 2016, Therapeutic and diagnostic applications of extracellular vesicles, J Control Release, 244, 167, 10.1016/j.jconrel.2016.07.054 Simpson, 2009, Exosomes: proteomic insights and diagnostic potential, Expert Rev Proteomics, 6, 267, 10.1586/epr.09.17 Wang, 2017, Exosomal proteins as prostate cancer biomarkers in urine: from mass spectrometry discovery to immunoassay-based validation, Eur J Pharm Sci, 98, 80, 10.1016/j.ejps.2016.09.023 Nameta, 2016, Disruption of membranes of extracellular vesicles is necessary for ELISA determination of urine AQP2: proof of disruption and epitopes of AQP2 antibodies, Int J Mol Sci, 17, 1634, 10.3390/ijms17101634 Del Boccio, 2012, A hyphenated microLC-Q-TOF-MS platform for exosomal lipidomics investigations: application to RCC urinary exosomes, Electrophoresis, 33, 689, 10.1002/elps.201100375 Min, 2011, Shotgun lipidomics for candidate biomarkers of urinary phospholipids in prostate cancer, Anal Bioanal Chem, 399, 823, 10.1007/s00216-010-4290-7 Kim, 2009, Quantitative analysis of phosphatidylcholines and phosphatidylethanolamines in urine of patients with breast cancer by nanoflow liquid chromatography/tandem mass spectrometry, Anal Bioanal Chem, 393, 1649, 10.1007/s00216-009-2621-3 Yang, 2017, Size dependent lipidomic analysis of urinary exosomes from patients with prostate cancer by flow field-flow fractionation and nanoflow liquid chromatography-tandem mass spectrometry, Anal Chem, 89, 2488, 10.1021/acs.analchem.6b04634