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Original Research Articles

High-resolution proteomic and lipidomic analysis of exosomes and microvesicles from different cell sources

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Article: 32570 | Received 13 Jun 2016, Accepted 02 Oct 2016, Published online: 17 Nov 2016

References

  • Jia S, Zocco D, Samuels ML, Chou MF, Chammas R, Skog J, etal. Emerging technologies in extracellular vesicle-based molecular diagnostics. Expert Rev Mol Diagn. 2014; 14: 307–21.
  • Long JD, Sullivan TB, Humphrey J, Logvinenko T, Summerhayes KA, Kozinn S, etal. A non-invasive miRNA based assay to detect bladder cancer in cell-free urine. Am J Transl Res. 2015; 7: 2500–9.
  • Ben-Dov IZ, Whalen VM, Goilav B, Max KE, Tuschl T. Cell and microvesicle urine microRNA deep sequencing profiles from healthy individuals: observations with potential impact on biomarker studies. PLoS One. 2016; 11: e0147249.
  • Royo F, Zuñiga-Garcia P, Torrano V, Loizaga A, Sanchez-Mosquera P, Ugalde-Olano A, etal. Transcriptomic profiling of urine extracellular vesicles reveals alterations of CDH3 in prostate cancer. Oncotarget. 2016; 7: 6835–46.
  • Momen-Heravi F, Saha B, Kodys K, Catalano D, Satishchandran A, Szabo G. Increased number of circulating exosomes and their microRNA cargos are potential novel biomarkers in alcoholic hepatitis. J Transl Med. 2015; 13: 261.
  • Sohn W, Kim J, Kang SH, Yang SR, Cho JY, Cho HC, etal. Serum exosomal microRNAs as novel biomarkers for hepatocellular carcinoma. Exp Mol Med. 2015; 47: e184.
  • Quinn JF, Patel T, Wong D, Das S, Freedman JE, Laurent LC, etal. Extracellular RNAs: development as biomarkers of human disease. J Extracell Vesicles. 2015; 4: 27495.
  • Hornick NI, Huan J, Doron B, Goloviznina NA, Lapidus J, Chang BH, etal. Serum exosome microRNA as a minimally-invasive early biomarker of AML. Sci Rep. 2015; 5: 11295.
  • Didiot MC, Hall LM, Coles AH, Haraszti RA, Godinho BM, Chase K, etal. Exosome-mediated delivery of hydrophobically modified siRNA for Huntingtin mRNA silencing. Mol Ther. 2016; 126
  • Quesenberry PJ, Aliotta J, Deregibus MC, Camussi G. Role of extracellular RNA-carrying vesicles in cell differentiation and reprogramming. Stem Cell Res Ther. 2015; 6: 153.
  • Lener T, Gimona M, Aigner L, Borger V, Buzas E, Camussi G, etal. Applying extracellular vesicles based therapeutics in clinical trials – an ISEV position paper. J Extracell Vesicles. 2015; 4: 30087.
  • Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, Sixma JJ. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood. 1999; 94: 3791–9.
  • Holme PA, Brosstad F, Solum NO. The difference between platelet and plasma FXIII used to study the mechanism of platelet microvesicle formation. Thromb Haemost. 1993; 70: 681–6.
  • Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006. Chapter 3:Unit 3. 22.
  • Lobb RJ, Becker M, Wen SW, Wong CS, Wiegmans AP, Leimgruber A, etal. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015; 4: 27031.
  • Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, etal. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci USA. 2016; 113: E968–77.
  • Wubbolts R, Leckie RS, Veenhuizen PT, Schwarzmann G, Mobius W, Hoernschemeyer J, etal. Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Bio Chem. 2003; 278: 10963–72.
  • Aalberts M, van Dissel-Emiliani FM, van Adrichem NP, van Wijnen M, Wauben MH, Stout TA, etal. Identification of distinct populations of prostasomes that differentially express prostate stem cell antigen, annexin A1, and GLIPR2 in humans. Biol Reprod. 2012; 86: 82.
  • Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol Biol. 2015; 1295: 179–209.
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013; 200: 373–83.
  • Anderson JD, Johansson HJ, Graham CS, Vesterlund M, Pham MT, Bramlett CS, etal. Comprehensive proteomic analysis of mesenchymal stem cell exosomes reveals modulation of angiogenesis via nuclear factor-kappaB signaling. Stem Cells. 2016; 34: 601–13.
  • Kreimer S, Belov AM, Ghiran I, Murthy SK, Frank DA, Ivanov AR. Mass-spectrometry-based molecular characterization of extracellular vesicles: lipidomics and proteomics. J Proteome Res. 2015; 14: 2367–84.
  • Clark DJ, Fondrie WE, Liao Z, Hanson PI, Fulton A, Mao L, etal. Redefining the breast cancer exosome proteome by tandem mass tag quantitative proteomics and multivariate cluster analysis. Anal Chem. 2015; 87: 10462–9.
  • Wang Z, Hill S, Luther JM, Hachey DL, Schey KL. Proteomic analysis of urine exosomes by multidimensional protein identification technology (MudPIT). Proteomics. 2012; 12: 329–38.
  • Sinha A, Ignatchenko V, Ignatchenko A, Mejia-Guerrero S, Kislinger T. In-depth proteomic analyses of ovarian cancer cell line exosomes reveals differential enrichment of functional categories compared to the NCI 60 proteome. Biochem Biophys Res Commun. 2014; 445: 694–701.
  • Vallejo MC, Nakayasu ES, Longo LV, Ganiko L, Lopes FG, Matsuo AL, etal. Lipidomic analysis of extracellular vesicles from the pathogenic phase of Paracoccidioides brasiliensis . PLoS One. 2012; 7: e39463.
  • Del Boccio P, Raimondo F, Pieragostino D, Morosi L, Cozzi G, Sacchetta P, etal. A hyphenated microLC-Q-TOF-MS platform for exosomal lipidomics investigations: application to RCC urinary exosomes. Electrophoresis. 2012; 33: 689–96.
  • Llorente A, Skotland T, Sylvanne T, Kauhanen D, Rog T, Orlowski A, etal. Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta. 2013; 1831: 1302–9.
  • Duijvesz D, Burnum-Johnson KE, Gritsenko MA, Hoogland AM, Vredenbregt-van den Berg MS, Willemsen R, etal. Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer. PLoS One. 2013; 8: e82589.
  • Kalra H, Adda CG, Liem M, Ang CS, Mechler A, Simpson RJ, etal. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics. 2013; 13: 3354–64.
  • Ji H, Greening DW, Barnes TW, Lim JW, Tauro BJ, Rai A, etal. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics. 2013; 13: 1672–86.
  • Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA, etal. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009; 23: 1541–57.
  • Choi DS, Kim DK, Kim YK, Gho YS. Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics. 2013; 13: 1554–71.
  • Carayon K, Chaoui K, Ronzier E, Lazar I, Bertrand-Michel J, Roques V, etal. Proteolipidic composition of exosomes changes during reticulocyte maturation. J Biol Chem. 2011; 286: 34426–39.
  • Evans SM, Putt M, Yang XY, Lustig RA, Martinez-Lage M, Williams D, etal. Initial evidence that blood-borne microvesicles are biomarkers for recurrence and survival in newly diagnosed glioblastoma patients. J Neurooncol. 2016; 127: 391–400.
  • Kiebish MA, Bell R, Yang K, Phan T, Zhao Z, Ames W, etal. Dynamic simulation of cardiolipin remodeling: greasing the wheels for an interpretative approach to lipidomics. J Lipid Res. 2010; 51: 2153–70.
  • Simons B, Kauhanen D, Sylvanne T, Tarasov K, Duchoslav E, Ekroos K. Shotgun lipidomics by sequential precursor ion fragmentation on a hybrid quadrupole time-of-flight mass spectrometer. Metabolites. 2012; 2: 195–213.
  • Wilhelm M, Schlegl J, Hahne H, Moghaddas Gholami A, Lieberenz M, Savitski MM, etal. Mass-spectrometry-based draft of the human proteome. Nature. 2014; 509: 582–7.
  • Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 2009; 37: 1–13.
  • Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009; 4: 44–57.
  • Keerthikumar S, Chisanga D, Ariyaratne D, Al Saffar H, Anand S, Zhao K, etal. ExoCarta: a web-based compendium of exosomal cargo. J Mol Biol. 2016; 428: 688–92.
  • Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics. 2010; 73: 1907–20.
  • Lai CP, Kim EY, Badr CE, Weissleder R, Mempel TR, Tannous BA, etal. Visualization and tracking of tumour extracellular vesicle delivery and RNA translation using multiplexed reporters. Nat Commun. 2015; 6: 7029.
  • Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, etal. Tumour exosome integrins determine organotropic metastasis. Nature. 2015; 527: 329–35.
  • Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, etal. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol. 2010; 12 19–30; sup pp 1–13.
  • Balaj L, Atai NA, Chen W, Mu D, Tannous BA, Breakefield XO, etal. Heparin affinity purification of extracellular vesicles. Sci Rep. 2015; 5: 10266.
  • Skokos D, Botros HG, Demeure C, Morin J, Peronet R, Birkenmeier G, etal. Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo . J Immunol. 2003; 170: 3037–45.
  • Kalra H, Drummen GP, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci. 2016; 17: 170.
  • Zhang B, Asadi S, Weng Z, Sismanopoulos N, Theoharides TC. Stimulated human mast cells secrete mitochondrial components that have autocrine and paracrine inflammatory actions. PLoS One. 2012; 7: e49767.
  • Sebastiani GD, Iuliano A, Cantarini L, Galeazzi M. Genetic aspects of the antiphospholipid syndrome: an update. Autoimmun Rev. 2016; 15: 433–9.
  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, etal. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008; 319: 1244–7.
  • Guo BB, Bellingham SA, Hill AF. The neutral sphingomyelinase pathway regulates packaging of the prion protein into exosomes. J Biol Chem. 2015; 290: 3455–67.
  • Yuyama K, Sun H, Mitsutake S, Igarashi Y. Sphingolipid-modulated exosome secretion promotes clearance of amyloid-beta by microglia. J Biol Chem. 2012; 287: 10977–89.
  • Phuyal S, Hessvik NP, Skotland T, Sandvig K, Llorente A. Regulation of exosome release by glycosphingolipids and flotillins. FEBS J. 2014; 281: 2214–27.