Different isolation approaches lead to diverse glycosylated extracellular vesicle populations

References

• van Niel G, D’Angelo G, Raposo G. Shedding light on the cell biology of extracellular vesicles. Nat Rev Mol Cell Biol. 2018;19(4):213–17.
   PubMed Web of Science ®Google Scholar
• Rak J, Guha A. Extracellular vesicles–vehicles that spread cancer genes. Bioessays. 2012;34(6):489–497.
   PubMed Web of Science ®Google Scholar
• Tkach M, Thery C. Communication by extracellular vesicles: where we are and where we need to go. Cell. 2016;164(6):1226–1232.
   PubMed Web of Science ®Google Scholar
• Vader P, Breakefield XO, Wood MJ. Extracellular vesicles: emerging targets for cancer therapy. Trends Mol Med. 2014;20(7):385–393.
   PubMed Web of Science ®Google Scholar
• Zhang H, Freitas D, Kim HS, et al. Identification of distinct nanoparticles and subsets of extracellular vesicles by asymmetric flow field-flow fractionation. Nat Cell Biol. 2018;20(3):332–343.
   PubMed Web of Science ®Google Scholar
• Williams C, Royo F, Aizpurua-Olaizola O, et al. Glycosylation of extracellular vesicles: current knowledge, tools and clinical perspectives. J Extracell Vesicles. 2018;7(1):1442985.
   PubMed Web of Science ®Google Scholar
• Lin J, Li J, Huang B, et al. Exosomes: novel biomarkers for clinical diagnosis. ScientificWorldJournal. 2015;2015:657086.
   PubMedGoogle Scholar
• Pinho SS, Reis CA. Glycosylation in cancer: mechanisms and clinical implications. Nat Rev Cancer. 2015;15(9):540–555.
   PubMed Web of Science ®Google Scholar
• Chugh S, Barkeer S, Rachagani S, et al. Disruption of C1galt1 gene promotes development and metastasis of pancreatic adenocarcinomas in mice. Gastroenterology. 2018;155(5):1608–1624.
   Web of Science ®Google Scholar
• Ozaki H, Matsuzaki H, Ando H, et al. Enhancement of metastatic ability by ectopic expression of ST6GalNAcI on a gastric cancer cell line in a mouse model. Clin Exp Metastasis. 2012;29(3):229–238.
   Web of Science ®Google Scholar
• Nakagoe T, Sawai T, Tsuji T, et al. Pre-operative serum levels of sialyl Tn antigen predict liver metastasis and poor prognosis in patients with gastric cancer. Eur J Surg Oncol. 2001;27(8):731–739.
   PubMed Web of Science ®Google Scholar
• David L, Carneiro F, Sobrinho-Simoes M. Sialosyl Tn antigen expression is associated with the prognosis of patients with advanced gastric cancer. Cancer. 1996;78(1):177–178.
   Web of Science ®Google Scholar
• Victorzon M, Nordling S, Nilsson O, et al. Sialyl Tn antigen is an independent predictor of outcome in patients with gastric cancer. Int J Cancer. 1996;65(3):295–300.
   Web of Science ®Google Scholar
• Freitas D, Campos D, Gomes J, et al. O-glycans truncation modulates gastric cancer cell signaling and transcription leading to a more aggressive phenotype. EBioMedicine. 2019;40:349–362.
   Web of Science ®Google Scholar
• Marcos NT, Pinho S, Grandela C, et al. Role of the human ST6GalNAc-I and ST6GalNAc-II in the synthesis of the cancer-associated sialyl-Tn antigen. Cancer Res. 2004;64(19):7050–7057.
   PubMed Web of Science ®Google Scholar
• Marcos NT, Bennett EP, Gomes J, et al. ST6GalNAc-I controls expression of sialyl-Tn antigen in gastrointestinal tissues. Front Biosci (Elite Ed). 2011;3:1443–1455.
   PubMedGoogle Scholar
• Ju T, Lanneau GS, Gautam T, et al. Human tumor antigens Tn and sialyl Tn arise from mutations in Cosmc. Cancer Res. 2008;68(6):1636–1646.
   PubMed Web of Science ®Google Scholar
• Radhakrishnan P, Dabelsteen S, Madsen FB, et al. Immature truncated O-glycophenotype of cancer directly induces oncogenic features. Proc Natl Acad Sci U S A. 2014;111(39):E4066–75.
   PubMed Web of Science ®Google Scholar
• Baldus SE, Hanisch FG. Biochemistry and pathological importance of mucin-associated antigens in gastrointestinal neoplasia. Adv Cancer Res. 2000;79:201–248.
   PubMed Web of Science ®Google Scholar
• Werther JL, Rivera-MacMurray S, Bruckner H, et al. Mucin-associated sialosyl-Tn antigen expression in gastric cancer correlates with an adverse outcome. Br J Cancer. 1994;69(3):613–616.
   PubMed Web of Science ®Google Scholar
• Itzkowitz S, Kjeldsen T, Friera A, et al.. Expression of Tn, sialosyl Tn, and T antigens in human pancreas. Gastroenterology. 1991;100(6):1691–1700.
   PubMed Web of Science ®Google Scholar
• Inoue M, Ton SM, Ogawa H, et al. Expression of Tn and sialyl-Tn antigens in tumor tissues of the ovary. Am J Clin Pathol. 1991;96(6):711–716.
   PubMed Web of Science ®Google Scholar
• Itzkowitz SH, Yuan M, Montgomery CK, et al. Expression of Tn, sialosyl-Tn, and T antigens in human colon cancer. Cancer Res. 1989;49(1):197–204.
   PubMed Web of Science ®Google Scholar
• Yonezawa S, Tachikawa T, Shin S, et al. Sialosyl-Tn antigen. Am J Clin Pathol. 1992;98(2):167–174.
   Web of Science ®Google Scholar
• Julien S, Picco G, Sewell R, et al. Sialyl-Tn vaccine induces antibody-mediated tumour protection in a relevant murine model. Br J Cancer. 2009;100(11):1746–1754.
   Web of Science ®Google Scholar
• Kjeldsen T, Clausen H, Hirohashi S, et al. Preparation and characterization of monoclonal antibodies directed to the tumor-associated O-linked sialosyl-2—-6 alpha-N-acetylgalactosaminyl (sialosyl-Tn) epitope. Cancer Res. 1988;48(8):2214–2220.
   PubMed Web of Science ®Google Scholar
• Baietti MF, Zhang Z, Mortier E, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14(7):677–685.
   PubMed Web of Science ®Google Scholar
• Liang Y, Eng WS, Colquhoun DR, et al. Complex N-linked glycans serve as a determinant for exosome/microvesicle cargo recruitment. J Biol Chem. 2014;289(47):32526–32537.
   PubMed Web of Science ®Google Scholar
• Saunderson SC, Dunn AC, Crocker PR, et al. CD169 mediates the capture of exosomes in spleen and lymph node. Blood. 2014;123(2):208–216.
   PubMed Web of Science ®Google Scholar
• Hao S, Bai O, Li F, et al. Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology. 2007;120(1):90–102.
   Web of Science ®Google Scholar
• Christianson HC, Svensson KJ, van Kuppevelt TH, et al. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci U S A. 2013;110(43):17380–17385.
   PubMed Web of Science ®Google Scholar
• Purushothaman A, Bandari SK, Liu J, et al. Fibronectin on the surface of myeloma cell-derived exosomes mediates exosome-cell interactions. J Biol Chem. 2016;291(4):1652–1663.
   PubMed Web of Science ®Google Scholar
• Menard JA, Cerezo-Magana M, Belting M. Functional role of extracellular vesicles and lipoproteins in the tumour microenvironment. Philos Trans R Soc Lond B Biol Sci. 2018;373:1737.
   Web of Science ®Google Scholar
• Gerlach JQ, Griffin MD. Getting to know the extracellular vesicle glycome. Mol Biosyst. 2016;12(4):1071–1081.
   PubMedGoogle Scholar
• Van Deun J, Mestdagh P, Sormunen R, et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J Extracell Vesicles. 2014;3:10.3402/jev.v3.24858.
   Google Scholar
• Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4:27031.
   PubMed Web of Science ®Google Scholar
• Witwer KW, Buzas EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2.
   PubMedGoogle Scholar
• Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods. 2015;87:3–10.
   PubMed 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):E968–77.
   PubMed Web of Science ®Google Scholar
• Campos D, Freitas D, Gomes J, et al. Probing the O-glycoproteome of gastric cancer cell lines for biomarker discovery. Mol Cell Proteomics. 2015;14(6):1616–1629.
   PubMed Web of Science ®Google Scholar
• Thery C, Amigorena S, Raposo G, et al. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol 2006;30:3.22.1-3.22.29. Chapter 3:Unit 3 22.
   PubMedGoogle Scholar
• Tauro BJ, Greening DW, Mathias RA, et al. Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods. 2012;56(2):293–304.
   PubMed Web of Science ®Google Scholar
• Gomes C, Almeida A, Ferreira JA, et al. Glycoproteomic analysis of serum from patients with gastric precancerous lesions. J Proteome Res. 2013;12(3):1454–1466.
   PubMed Web of Science ®Google Scholar
• Oliveros JC. Venny. An interactive tool for comparing lists with Venn’s diagrams. 2007–2015. http://bioinfogpcnbcsices/tools/venny/indexhtml
   Google Scholar
• Steentoft C, Vakhrushev SY, Joshi HJ, et al. Precision mapping of the human O-GalNAc glycoproteome through SimpleCell technology. Embo J. 2013;32(10):1478–1488.
   PubMed Web of Science ®Google Scholar
• Consortium E-T, Van Deun J, Mestdagh P, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Methods. 2017;14(3):228–232.
   PubMed Web of Science ®Google Scholar
• Rosa-Fernandes L, Rocha VB, Carregari VC, et al. A perspective on extracellular vesicles proteomics. Front Chem. 2017;5:102.
   PubMed Web of Science ®Google Scholar
• Becker A, Thakur BK, Weiss JM, et al. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30(6):836–848.
   PubMed Web of Science ®Google Scholar
• Costa-Silva B, Aiello NM, Ocean AJ, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17(6):816–826.
   PubMed Web of Science ®Google Scholar
• Hoshino A, Costa-Silva B, Shen TL, et al. Tumour exosome integrins determine organotropic metastasis. Nature. 2015;527(7578):329–335.
   PubMed Web of Science ®Google Scholar
• Peinado H, Zhang H, Matei IR, et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer. 2017;17(5):302–317.
   PubMed Web of Science ®Google Scholar
• Costa J. Glycoconjugates from extracellular vesicles: structures, functions and emerging potential as cancer biomarkers. Biochim Biophys Acta. 2017;1868(1):157–166.
   Web of Science ®Google Scholar
• Tkach M, Kowal J, Thery C. Why the need and how to approach the functional diversity of extracellular vesicles. Philos Trans R Soc Lond B Biol Sci. 2018;373:1737.
   Web of Science ®Google Scholar
• Konoshenko MY, Lekchnov EA, Vlassov AV, et al. Isolation of extracellular vesicles: general methodologies and latest trends. Biomed Res Int. 2018;2018:8545347.
   PubMed Web of Science ®Google Scholar
• Campos D, Freitas D, Gomes J, et al. Glycoengineered cell models for the characterization of cancer O-glycoproteome: an innovative strategy for biomarker discovery. Expert Rev Proteomics. 2015;12(4):337–342.
   PubMed Web of Science ®Google Scholar
• Pinho S, Marcos NT, Ferreira B, et al. Biological significance of cancer-associated sialyl-Tn antigen: modulation of malignant phenotype in gastric carcinoma cells. Cancer Lett. 2007;249(2):157–170.
   Web of Science ®Google Scholar
• Lotvall J, Hill AF, Hochberg F, et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the international society for extracellular vesicles. J Extracell Vesicles. 2014;3:26913.
   PubMedGoogle Scholar
• Sinha A, Alfaro J, Kislinger T. Characterization of protein content present in exosomes isolated from conditioned media and urine. Curr Protoc Protein Sci. 2017;87:24.9.1‐ 24.9.12.
   Google Scholar
• Stolk M, Seifert M. Protein contaminations impact quantification and functional analysis of extracellular vesicle preparations from mesenchymal stromal cells. J Stem Cells Regen Med. 2015;11(2):44–47.
   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):579–592.
   PubMed Web of Science ®Google Scholar
• Royo F, Zuniga-Garcia P, Sanchez-Mosquera P, et al. Different EV enrichment methods suitable for clinical settings yield different subpopulations of urinary extracellular vesicles from human samples. J Extracell Vesicles. 2016;5:29497.
   PubMed Web of Science ®Google Scholar
• Gerlach JQ, Maguire CM, Kruger A, et al. Urinary nanovesicles captured by lectins or antibodies demonstrate variations in size and surface glycosylation profile. Nanomedicine (Lond). 2017;12(11):1217–1229.
   PubMed Web of Science ®Google Scholar
• Escrevente C, Grammel N, Kandzia S, et al. Sialoglycoproteins and N-glycans from secreted exosomes of ovarian carcinoma cells. PLoS One. 2013;8(10):e78631.
   PubMed Web of Science ®Google Scholar
• Escrevente C, Keller S, Altevogt P, et al. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer. 2011;11:108.
   PubMed Web of Science ®Google Scholar
• Malloci M, Perdomo L, Veerasamy M, et al. Extracellular vesicles: mechanisms in human health and disease. Antioxid Redox Signal. 2019;30(6):813–856.
   Web of Science ®Google Scholar
• Katsuda T, Kosaka N, Ochiya T. The roles of extracellular vesicles in cancer biology: toward the development of novel cancer biomarkers. Proteomics. 2014;14(4–5):412–425.
   PubMed Web of Science ®Google Scholar