Metabolic signature of extracellular vesicles depends on the cell culture conditions

References

• Yáñez-Mó M, Siljander PR, Andreu Z, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4(1):27066.
   PubMed Web of Science ®Google Scholar
• Di Vizio D, Kim J, Hager MH, et al. Oncosome formation in prostate cancer: Association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res. 2009;69(13):5601.
   PubMed Web of Science ®Google Scholar
• Höög JL, Lötvall J. Diversity of extracellular vesicles in human ejaculates revealed by cryo-electron microscopy. J Extracell Vesicles. 2015;4(1):28680.
   PubMed Web of Science ®Google Scholar
• Haraszti RA, Didiot M, Sapp E, et al. High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources. J Extracell Vesicles. 2016;5(1):32570.
   PubMed Web of Science ®Google Scholar
• Lázaro-Ibáñez E, Lunavat TR, Jang SC, et al. Distinct prostate cancer-related mRNA cargo in extracellular vesicle subsets from prostate cell lines. BMC Cancer. 2017;17(1):92.
   Web of Science ®Google Scholar
• Shephard AP, Yeung V, Clayton A, et al. Prostate cancer exosomes as modulators of the tumor microenvironment. J Cancer Metastasis Treat. 2017;3:289.
   Google Scholar
• Lázaro-Ibáñez, E., Neuvonen M, Takatalo M, et al. Metastatic state of parent cells influences the uptake and functionality of prostate cancer cell-derived extracellular vesicles. Journal of Extracellular Vesicles 2017;6(1):1354645.
   Google Scholar
• Théry C, Witwer KW, Aikawa E, et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the international society for extracellular vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles. 2018;7(1):1535750.
   PubMed Web of Science ®Google Scholar
• Mallat Z, Benamer H, Hugel B, et al. Elevated levels of shed membrane microparticles with procoagulant potential in the peripheral circulating blood of patients with acute coronary syndromes. Circulation. 2000;101(8):841.
   PubMed Web of Science ®Google Scholar
• Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470.
   PubMed Web of Science ®Google Scholar
• Sellam J, Proulle V, Jüngel A, et al. Increased levels of circulating microparticles in primary sjögren’s syndrome, systemic lupus erythematosus and rheumatoid arthritis and relation with disease activity. Arthritis Res Ther. 2009;11(5):R156.
   PubMed Web of Science ®Google Scholar
• Bruno S, Grange C, Collino F, et al. Microvesicles derived from mesenchymal stem cells enhance survival in a lethal model of acute kidney injury. PloS one. 2012;7(3):e33115.
   PubMed Web of Science ®Google Scholar
• Tian Y, Li S, Song J, et al. A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials. 2014;35(7):2383.
   PubMed Web of Science ®Google Scholar
• Saari H, Lázaro-Ibáñez E, Viitala T, et al. Microvesicle-and exosome-mediated drug delivery enhances the cytotoxicity of paclitaxel in autologous prostate cancer cells. J Control Release. 2015;220:727.
   Web of Science ®Google Scholar
• Watson DC, Bayik D, Srivatsan A, et al. Efficient production and enhanced tumor delivery of engineered extracellular vesicles. Biomaterials. 2016;105:195.
   PubMed Web of Science ®Google Scholar
• Guerreiro EM, Vestad B, Steffensen LA, et al. Efficient extracellular vesicle isolation by combining cell media modifications, ultrafiltration, and size-exclusion chromatography. PloS one. 2018;13(9):e0204276.
   PubMed Web of Science ®Google Scholar
• Shelke GV, Lässer C, Gho YS, et al. Importance of exosome depletion protocols to eliminate functional and RNA-containing extracellular vesicles from fetal bovine serum. J Extracell Vesicles. 2014;3(1):24783.
   Google Scholar
• Palomo L, Casal E, Royo F, et al. Considerations for applying metabolomics to the analysis of extracellular vesicles. Front Immunol. 2014;5:651.
   Web of Science ®Google Scholar
• Van Deun J, Mestdagh P, Agostinis P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228.
   PubMed Web of Science ®Google Scholar
• Puhka M, Nordberg M, Valkonen S, et al. KeepEX, a simple dilution protocol for improving extracellular vesicle yields from urine. Eur J Pharm Sci. 2017;98:30.
   PubMed Web of Science ®Google Scholar
• Tsugawa H, Cajka T, Kind T, et al. MS-DIAL: data-independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods. 2015;12(6):523.
   PubMed Web of Science ®Google Scholar
• Wishart DS, Feunang YD, Marcu A, et al. HMDB 4.0: the human metabolome database for 2018. Nucleic Acids Res. 2017;46(D1):D608–D617.
   Web of Science ®Google Scholar
• Fahy E, Subramaniam S, Murphy RC, et al. Update of the LIPID MAPS comprehensive classification system for lipids. J Lipid Res. 2009;50 Suppl:S9–S14.
   Web of Science ®Google Scholar
• Kanehisa M, Furumichi M, Tanabe M, et al. KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic Acids Res. 2017;45(D1):D353–D361.
   PubMed Web of Science ®Google Scholar
• Xia J, Wishart DS. Using metaboanalyst 3.0 for comprehensive metabolomics data analysis. Curr Protoc Bioinformatics. 2016;55:14.10.1–14.10.91.
   PubMedGoogle Scholar
• Mitchell JP, Court J, Mason MD, et al. Increased exosome production from tumour cell cultures using the integra CELLine culture system. J Immunol Methods. 2008;335(1):98.
   Web of Science ®Google Scholar
• Van Meer G, Voelker DR, Feigenson GW. Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol. 2008;9(2):112.
   PubMed Web of Science ®Google Scholar
• Bicalho B, Holovati JL, Acker JP. Phospholipidomics reveals differences in glycerophosphoserine profiles of hypothermically stored red blood cells and microvesicles. Biochimi Biophys Acta (BBA) Biomembr. 2013;1828(2):317.
   PubMed Web of Science ®Google Scholar
• Llorente A, Skotland T, Sylvänne T, et al. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids. 2013;1831(7):1302.
   PubMed Web of Science ®Google Scholar
• Gibellini F, Smith TK. The kennedy pathway—de novo synthesis of phosphatidylethanolamine and phosphatidylcholine. IUBMB Life. 2010;62(6):414.
   PubMed Web of Science ®Google Scholar
• Kennedy EP, Weiss SB. The function of cytidine coenzymes in the biosynthesis of phospholipides. The. J Biol Chem. 1956;222(1):193.
   PubMed Web of Science ®Google Scholar
• Yang JS, Lee JC, Byeon SK, et al. 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. 2017;89(4):2488.
   Web of Science ®Google Scholar
• Dang VD, Jella KK, Ragheb RRT, et al. Lipidomic and proteomic analysis of exosomes from mouse cortical collecting duct cells.. FASEB J. 2017;31(12):5399.
   PubMed Web of Science ®Google Scholar
• Deshane J, Hough K, Wilson L, et al. Airway exosomes from asthmatics modulate differential T helper responses. J Allergy Clin Immunol. 2017;139(2):AB375.
   Web of Science ®Google Scholar
• Lydic TA, Townsend S, Adda CG, et al. Rapid and comprehensive ‘shotgun’lipidome profiling of colorectal cancer cell derived exosomes. Methods. 2015;87:83.
   PubMed Web of Science ®Google Scholar
• Hosseini-Beheshti E, Pham S, Adomat H, et al. Exosomes as biomarker enriched microvesicles: characterization of exosomal proteins derived from a panel of prostate cell lines with distinct AR phenotypes. Mol Cell Proteomics. 2012;11(10):863.
   PubMed Web of Science ®Google Scholar
• Phuyal S, Skotland T, Hessvik NP, et al. The ether lipid precursor hexadecylglycerol stimulates the release and changes the composition of exosomes derived from PC-3 cells. J Biol Chem. 2015;290(7):4225.
   PubMed Web of Science ®Google Scholar
• Laurén E, Tigistu-Sahle F, Valkonen S, et al. Phospholipid composition of packed red blood cells and that of extracellular vesicles show a high resemblance and stability during storage. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids. 2018;1863(1):1.
   Web of Science ®Google Scholar
• Brzozowski JS, Jankowski H, Bond DR, et al. Lipidomic profiling of extracellular vesicles derived from prostate and prostate cancer cell lines. Lipids Health Dis. 2018;17(1):211.
   Web of Science ®Google Scholar
• Fuller N, Rand R. The influence of lysolipids on the spontaneous curvature and bending elasticity of phospholipid membranes. Biophys J. 2001;81(1):243.
   PubMed Web of Science ®Google Scholar
• Blanc L, Barres C, Bette-Bobillo P, et al. Reticulocyte-secreted exosomes bind natural IgM antibodies: involvement of a ROS-activatable endosomal phospholipase iPLA2. Blood. 2007;110(9):3407.
   Web of Science ®Google Scholar
• Coutant F, Perrin-Cocon L, Agaugue S, et al. Mature dendritic cell generation promoted by lysophosphatidylcholine. J Immunol. 2002;169(4):1688.
   Web of Science ®Google Scholar
• Subra C, Laulagnier K, Perret B, et al. Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies. Biochimie. 2007;89(2):205.
   PubMed Web of Science ®Google Scholar
• Thery C, Boussac M, Veron P, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001;166(12):7309.
   PubMed Web of Science ®Google Scholar
• Braverman NE, Moser AB. Functions of plasmalogen lipids in health and disease. Biochim Biophys Acta Mol Basis Dis. 2012;1822(9):1442.
   PubMed Web of Science ®Google Scholar
• Paltauf F. Ether lipids in biomembranes. Chem Phys Lipids. 1994;74(2):101.
   Web of Science ®Google Scholar
• Han X, Gross RW. Plasmenylcholine and phosphatidylcholine membrane bilayers possess distinct conformational motifs. Biochem. 1990;29(20):4992.
   Web of Science ®Google Scholar
• Glaser PE, Gross RW. 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. Biochem. 1994;33(19):5805.
   PubMed Web of Science ®Google Scholar
• Lohner K, Balgavy P, Hermetter A, et al. Stabilization of non-bilayer structures by the etherlipid ethanolamine plasmalogen. Biochimi Biophys Acta (BBA) Biomembr. 1991;1061(2):132.
   Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113(8):E968.
   PubMed Web of Science ®Google Scholar
• Xia J, Wishart DS. MSEA: A web-based tool to identify biologically meaningful patterns in quantitative metabolomic data. Nucleic Acids Res. 2010;38(suppl_2):W71.
   PubMed Web of Science ®Google Scholar
• Zhao H, Yang L, Baddour J, et al. Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism. Elife. 2016;5:e10250.
   PubMed Web of Science ®Google Scholar
• Gudbergsson JM, Johnsen KB, Skov MN, et al. Systematic review of factors influencing extracellular vesicle yield from cell cultures. Cytotechnology. 2016;68(4):579.
   PubMed Web of Science ®Google Scholar
• Gal D, MacDonald PC, Porter JC, et al. Effect of cell density and confluency on cholesterol metabolism in cancer cells in monolayer culture. Cancer Res. 1981;41(2):473.
   PubMed Web of Science ®Google Scholar
• Bereiter-Hahn J, Münnich A, Woiteneck P. Dependence of energy metabolism on the density of cells in culture. Cell Struct Funct. 1998;23(2):85.
   Web of Science ®Google Scholar
• Chance K. Design and implementation of successful regulatory strategies in biosimilar development. In: Gutka H., Yang H., Kakar S. (eds). Biosimilars. AAPS Advances in the Pharmaceutical Sciences Series. Cham: Springer; 2018. p. 107.
   Google Scholar
• Brühlmann D, Sokolov M, Butté A, et al. Parallel experimental design and multivariate analysis provides efficient screening of cell culture media supplements to improve biosimilar product quality. Biotechnol Bioeng. 2017;114(7):1448.
   Web of Science ®Google Scholar
• Puhka M, Takatalo M, Nordberg M, et al. Metabolomic profiling of extracellular vesicles and alternative normalization methods reveal enriched metabolites and strategies to study prostate cancer-related changes. Theranostics. 2017;7:3824.
   Web of Science ®Google Scholar
• Altadill T, Campoy I, Lanau L, et al. Enabling metabolomics based biomarker discovery studies using molecular phenotyping of exosome-like vesicles. PLoS One. 2016;11(3):e0151339.
   PubMed Web of Science ®Google Scholar
• Iraci N, Gaude E, Leonardi T, et al. Extracellular vesicles are independent metabolic units with asparaginase activity. Nat Chem Biol. 2017;13(9):951.
   Web of Science ®Google Scholar
• Clos-Garcia M, Loizaga-Iriarte A, Zuñiga-Garcia P, et al. Metabolic alterations in urine extracellular vesicles are associated to prostate cancer pathogenesis and progression. J Extracell Vesicles. 2018;7(1):1470442.
   PubMed Web of Science ®Google Scholar