Glycoconjugates from extracellular vesicles: Structures, functions and emerging potential as cancer biomarkers

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1868, Issue 1, 2017, Pages 157-166

  Costa, Julia ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Cancer biomarkers; Exosomes; Extracellular vesicles; Glycoconjugates; Glycoproteins; Glycosylation

Indexed keywords

GLYCAN; GLYCOCONJUGATE; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; TUMOR MARKER;

ANALYTIC METHOD; CELL INTERACTION; CELL SELECTION; EXOSOME; FUCOSYLATION; GLYCOSYLATION; HUMAN; LIPID ANALYSIS; LIQUID CHROMATOGRAPHY; MASS SPECTROMETRY; MEMBRANE MICROPARTICLE; NONHUMAN; ORGANELLE BIOGENESIS; PROTEIN LOCALIZATION; PROTEIN MODIFICATION; PROTEIN STRUCTURE; REVIEW; SENSITIVITY AND SPECIFICITY; SEPARATION TECHNIQUE; TANDEM MASS SPECTROMETRY; TARGET CELL; ANIMAL; CELL MEMBRANE; METABOLISM; NEOPLASM;

ANIMALS; BIOMARKERS, TUMOR; CELL MEMBRANE; EXOSOMES; EXTRACELLULAR VESICLES; GLYCOCONJUGATES; GLYCOSYLATION; HUMANS; NEOPLASMS;

EID: 85016645896     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2017.03.007     Document Type: Review

References (103)

1. Tkach, M., Thery, C., Communication by extracellular vesicles: where we are and where we need to go. Cell 164 (2016), 1226–1232.
2. Becker, A., Thakur, B.K., Weiss, J.M., Kim, H.S., Peinado, H., Lyden, D., Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell 30 (2016), 836–848.
3. Nawaz, M., Fatima, F., Vallabhaneni, K.C., Penfornis, P., Valadi, H., Ekstrom, K., Kholia, S., Whitt, J.D., Fernandes, J.D., Pochampally, R., Squire, J.A., Camussi, G., Extracellular vesicles: evolving factors in stem cell biology. Stem Cells Int., 2016, 2016, 1073140.
4. Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., Wood, M.J., Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29 (2011), 341–345.
5. Kalluri, R., The biology and function of exosomes in cancer. J. Clin. Invest. 126 (2016), 1208–1215.
6. Krishnamoorthy, L., Bess, J.W. Jr., Preston, A.B., Nagashima, K., Mahal, L.K., HIV-1 and microvesicles from T cells share a common glycome, arguing for a common origin. Nat. Chem. Biol. 5 (2009), 244–250.
7. Batista, B.S., Eng, W.S., Pilobello, K.T., Hendricks-Munoz, K.D., Mahal, L.K., Identification of a conserved glycan signature for microvesicles. J. Proteome Res. 10 (2011), 4624–4633.
8. Escrevente, C., Grammel, N., Kandzia, S., Zeiser, J., Tranfield, E.M., Conradt, H.S., Costa, J., Sialoglycoproteins and N-glycans from secreted exosomes of ovarian carcinoma cells. PLoS One, 8, 2013, e78631.
9. Gerlach, J.Q., Griffin, M.D., Getting to know the extracellular vesicle glycome. Mol. BioSyst. 12 (2016), 1071–1081.
10. Fuster, M.M., Esko, J.D., The sweet and sour of cancer: glycans as novel therapeutic targets. Nat. Rev. Cancer 5 (2005), 526–542.
11. D'Angelo, G., Capasso, S., Sticco, L., Russo, D., Glycosphingolipids: synthesis and functions. FEBS J. 280 (2013), 6338–6353.
12. Marino, K., Bones, J., Kattla, J.J., Rudd, P.M., A systematic approach to protein glycosylation analysis: a path through the maze. Nat. Chem. Biol. 6 (2010), 713–723.
13. Thaysen-Andersen, M., Packer, N.H., Schulz, B.L., Maturing glycoproteomics technologies provide unique structural insights into the N-glycoproteome and its regulation in health and disease. Mol. Cell. Proteomics 15 (2016), 1773–1790.
14. Silva, M.L., Cancer serum biomarkers based on aberrant post-translational modifications of glycoproteins: clinical value and discovery strategies. Biochim. Biophys. Acta 1856 (2015), 165–177.
15. Machado, E., Kandzia, S., Carilho, R., Altevogt, P., Conradt, H.S., Costa, J., N-glycosylation of total cellular glycoproteins from the human ovarian carcinoma SKOV3 cell line and of recombinantly expressed human erythropoietin. Glycobiology 21 (2011), 376–386.
16. Gomes, J., Gomes-Alves, P., Carvalho, S.B., Peixoto, C., Alves, P.M., Altevogt, P., Costa, J., Extracellular vesicles from ovarian carcinoma cells display specific glycosignatures. Biomol. Ther. 5 (2015), 1741–1761.
17. Ahn, Y.H., Kim, J.Y., Yoo, J.S., Quantitative mass spectrometric analysis of glycoproteins combined with enrichment methods. Mass Spectrom. Rev. 34 (2015), 148–165.
18. Stowell, S.R., Ju, T., Cummings, R.D., Protein glycosylation in cancer. Annu. Rev. Pathol. 10 (2015), 473–510.
19. Costa, J., Grabenhorst, E., Nimtz, M., Conradt, H.S., Stable expression of the Golgi form and secretory variants of human fucosyltransferase III from BHK-21 cells. Purification and characterization of an engineered truncated form from the culture medium. J. Biol. Chem. 272 (1997), 11613–11621.
20. Kudelka, M.R., Antonopoulos, A., Wang, Y., Duong, D.M., Song, X., Seyfried, N.T., Dell, A., Haslam, S.M., Cummings, R.D., Ju, T., Cellular O-glycome reporter/amplification to explore O-glycans of living cells. Nat. Methods 13 (2016), 81–86.
21. Gray, C.J., Thomas, B., Upton, R., Migas, L.G., Eyers, C.E., Barran, P.E., Flitsch, S.L., Applications of ion mobility mass spectrometry for high throughput, high resolution glycan analysis. Biochim. Biophys. Acta 1860 (2016), 1688–1709.
22. Lee, L.Y., Thaysen-Andersen, M., Baker, M.S., Packer, N.H., Hancock, W.S., Fanayan, S., Comprehensive N-glycome profiling of cultured human epithelial breast cells identifies unique secretome N-glycosylation signatures enabling tumorigenic subtype classification. J. Proteome Res. 13 (2014), 4783–4795.
23. Kobata, A., Exo- and endoglycosidases revisited. Proc. Jpn. Acad. Ser. B Phys. Biol. Sci. 89 (2013), 97–117.
24. Pinho, S.S., Reis, C.A., Glycosylation in cancer: mechanisms and clinical implications. Nat. Rev. Cancer 15 (2015), 540–555.
25. Kailemia, M.J., Park, D., Lebrilla, C.B., Glycans and glycoproteins as specific biomarkers for cancer. Anal. Bioanal. Chem., 2016.
26. Taniguchi, N., Kizuka, Y., Glycans and cancer: role of N-glycans in cancer biomarker, progression and metastasis, and therapeutics. Adv. Cancer Res. 126 (2015), 11–51.
27. Allam, H., Aoki, K., Benigno, B.B., McDonald, J.F., Mackintosh, S.G., Tiemeyer, M., Abbott, K.L., Glycomic analysis of membrane glycoproteins with bisecting glycosylation from ovarian cancer tissues reveals novel structures and functions. J. Proteome Res. 14 (2015), 434–446.
28. Anugraham, M., Jacob, F., Nixdorf, S., Everest-Dass, A.V., Heinzelmann-Schwarz, V., Packer, N.H., Specific glycosylation of membrane proteins in epithelial ovarian cancer cell lines: glycan structures reflect gene expression and DNA methylation status. Mol. Cell. Proteomics 13 (2014), 2213–2232.
29. Nakagawa, T., Miyoshi, E., Yakushijin, T., Hiramatsu, N., Igura, T., Hayashi, N., Taniguchi, N., Kondo, A., Glycomic analysis of alpha-fetoprotein L3 in hepatoma cell lines and hepatocellular carcinoma patients. J. Proteome Res. 7 (2008), 2222–2233.
30. Harduin-Lepers, A., Krzewinski-Recchi, M.A., Colomb, F., Foulquier, F., Groux-Degroote, S., Delannoy, P., Sialyltransferases functions in cancers. Front. Biosci. (Elite Ed.) 4 (2012), 499–515.
31. Carvalho, A.S., Harduin-Lepers, A., Magalhaes, A., Machado, E., Mendes, N., Costa, L.T., Matthiesen, R., Almeida, R., Costa, J., Reis, C.A., Differential expression of alpha-2,3-sialyltransferases and alpha-1,3/4-fucosyltransferases regulates the levels of sialyl Lewis a and sialyl Lewis x in gastrointestinal carcinoma cells. Int. J. Biochem. Cell Biol. 42 (2010), 80–89.
32. Couchman, J.R., Multhaupt, H., Sanderson, R.D., Recent insights into cell surface heparan sulphate proteoglycans and cancer. F1000Res, 5, 2016.
33. Ahmed, M., Cheung, N.K., Engineering anti-GD2 monoclonal antibodies for cancer immunotherapy. FEBS Lett. 588 (2014), 288–297.
34. Colombo, M., Raposo, G., Thery, C., Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu. Rev. Cell Dev. Biol. 30 (2014), 255–289.
35. Kowal, J., Arras, G., Colombo, M., Jouve, M., Morath, J.P., Primdal-Bengtson, B., Dingli, F., Loew, D., Tkach, M., Thery, C., Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc. Natl. Acad. Sci. U. S. A. 113 (2016), E968–E977.
36. Kim, D.K., Kang, B., Kim, O.Y., Choi, D.S., Lee, J., Kim, S.R., Go, G., Yoon, Y.J., Kim, J.H., Jang, S.C., Park, K.S., Choi, E.J., Kim, K.P., Desiderio, D.M., Kim, Y.K., Lotvall, J., Hwang, D., Gho, Y.S., EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J. Extracell. Vesicles, 2, 2013.
37. Kalra, H., Simpson, R.J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., Bond, V.C., Borras, F.E., Breakefield, X., Budnik, V., Buzas, E., Camussi, G., Clayton, A., Cocucci, E., Falcon-Perez, J.M., Gabrielsson, S., Gho, Y.S., Gupta, D., Harsha, H.C., Hendrix, A., Hill, A.F., Inal, J.M., Jenster, G., Kramer-Albers, E.M., Lim, S.K., Llorente, A., Lotvall, J., Marcilla, A., Mincheva-Nilsson, L., Nazarenko, I., Nieuwland, R., Nolte-'t Hoen, E.N., Pandey, A., Patel, T., Piper, M.G., Pluchino, S., Prasad, T.S., Rajendran, L., Raposo, G., Record, M., Reid, G.E., Sanchez-Madrid, F., Schiffelers, R.M., Siljander, P., Stensballe, A., Stoorvogel, W., Taylor, D., Thery, C., Valadi, H., van Balkom, B.W., Vazquez, J., Vidal, M., Wauben, M.H., Yanez-Mo, M., Zoeller, M., Mathivanan, S., Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol., 10, 2012, e1001450.
38. Simpson, R.J., Kalra, H., Mathivanan, S., ExoCarta as a resource for exosomal research. J. Extracell. Vesicles, 1, 2012.
39. Andreu, Z., Yanez-Mo, M., Tetraspanins in extracellular vesicle formation and function. Front. Immunol., 5, 2014, 442.
40. Perez-Hernandez, D., Gutierrez-Vazquez, C., Jorge, I., Lopez-Martin, S., Ursa, A., Sanchez-Madrid, F., Vazquez, J., Yanez-Mo, M., The intracellular interactome of tetraspanin-enriched microdomains reveals their function as sorting machineries toward exosomes. J. Biol. Chem. 288 (2013), 11649–11661.
41. Vella, L.J., Sharples, R.A., Lawson, V.A., Masters, C.L., Cappai, R., Hill, A.F., Packaging of prions into exosomes is associated with a novel pathway of PrP processing. J. Pathol. 211 (2007), 582–590.
42. Escrevente, C., Keller, S., Altevogt, P., Costa, J., Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer, 11, 2011, 108.
43. Saraswat, M., Joenvaara, S., Musante, L., Peltoniemi, H., Holthofer, H., Renkonen, R., N-linked (N-) glycoproteomics of urinary exosomes. [corrected]. Mol. Cell. Proteomics 14 (2015), 263–276.
44. Staubach, S., Schadewaldt, P., Wendel, U., Nohroudi, K., Hanisch, F.G., Differential glycomics of epithelial membrane glycoproteins from urinary exovesicles reveals shifts toward complex-type N-glycosylation in classical galactosemia. J. Proteome Res. 11 (2012), 906–916.
45. Gerlach, J.Q., Kruger, A., Gallogly, S., Hanley, S.A., Hogan, M.C., Ward, C.J., Joshi, L., Griffin, M.D., Surface glycosylation profiles of urine extracellular vesicles. PLoS One, 8, 2013, e74801.
46. Echevarria, J., Royo, F., Pazos, R., Salazar, L., Falcon-Perez, J.M., Reichardt, N.C., Microarray-based identification of lectins for the purification of human urinary extracellular vesicles directly from urine samples. Chembiochem 15 (2014), 1621–1626.
47. Llorente, A., Skotland, T., Sylvanne, T., Kauhanen, D., Rog, T., Orlowski, A., Vattulainen, I., Ekroos, K., Sandvig, K., Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim. Biophys. Acta 1831 (2013), 1302–1309.
48. Christianson, H.C., Svensson, K.J., van Kuppevelt, T.H., Li, J.P., Belting, M., Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc. Natl. Acad. Sci. U. S. A. 110 (2013), 17380–17385.
49. Zeringer, E., Barta, T., Li, M., Vlassov, A.V., Strategies for isolation of exosomes. Cold Spring Harb. Protoc. 2015 (2015), 319–323.
50. Pocsfalvi, G., Stanly, C., Fiume, I., Vekey, K., Chromatography and its hyphenation to mass spectrometry for extracellular vesicle analysis. J. Chromatogr. A 1439 (2016), 26–41.
51. Escrevente, C., Morais, V.A., Keller, S., Soares, C.M., Altevogt, P., Costa, J., Functional role of N-glycosylation from ADAM10 in processing, localization and activity of the enzyme. Biochim. Biophys. Acta 1780 (2008), 905–913.
52. Hong, C.S., Funk, S., Muller, L., Boyiadzis, M., Whiteside, T.L., Isolation of biologically active and morphologically intact exosomes from plasma of patients with cancer. J. Extracell. Vesicles, 5, 2016, 29289.
53. Royo, F., Zuniga-Garcia, P., Sanchez-Mosquera, P., Egia, A., Perez, A., Loizaga, A., Arceo, R., Lacasa, I., Rabade, A., Arrieta, E., Bilbao, R., Unda, M., Carracedo, A., Falcon-Perez, J.M., Different EV enrichment methods suitable for clinical settings yield different subpopulations of urinary extracellular vesicles from human samples. J. Extracell. Vesicles, 5, 2016, 29497.
54. Balaj, L., Atai, N.A., Chen, W., Mu, D., Tannous, B.A., Breakefield, X.O., Skog, J., Maguire, C.A., Heparin affinity purification of extracellular vesicles. Sci. Rep., 5, 2015, 10266.
55. Friand, V., David, G., Zimmermann, P., Syntenin and syndecan in the biogenesis of exosomes. Biol. Cell. 107 (2015), 331–341.
56. Thompson, C.A., Purushothaman, A., Ramani, V.C., Vlodavsky, I., Sanderson, R.D., Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes. J. Biol. Chem. 288 (2013), 10093–10099.
57. Roucourt, B., Meeussen, S., Bao, J., Zimmermann, P., David, G., Heparanase activates the syndecan-syntenin-ALIX exosome pathway. Cell Res. 25 (2015), 412–428.
58. Liang, Y., Eng, W.S., Colquhoun, D.R., Dinglasan, R.R., Graham, D.R., Mahal, L.K., Complex N-linked glycans serve as a determinant for exosome/microvesicle cargo recruitment. J. Biol. Chem. 289 (2014), 32526–32537.
59. Welton, J.L., Khanna, S., Giles, P.J., Brennan, P., Brewis, I.A., Staffurth, J., Mason, M.D., Clayton, A., Proteomics analysis of bladder cancer exosomes. Mol. Cell. Proteomics 9 (2010), 1324–1338.
60. Barres, C., Blanc, L., Bette-Bobillo, P., Andre, S., Mamoun, R., Gabius, H.J., Vidal, M., Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 115 (2010), 696–705.
61. Honig, E., Schneider, K., Jacob, R., Recycling of galectin-3 in epithelial cells. Eur. J. Cell Biol. 94 (2015), 309–315.
62. Lener, T., Gimona, M., Aigner, L., Borger, V., Buzas, E., Camussi, G., Chaput, N., Chatterjee, D., Court, F.A., Del Portillo, H.A., O'Driscoll, L., Fais, S., Falcon-Perez, J.M., Felderhoff-Mueser, U., Fraile, L., Gho, Y.S., Gorgens, A., Gupta, R.C., Hendrix, A., Hermann, D.M., Hill, A.F., Hochberg, F., Horn, P.A., de Kleijn, D., Kordelas, L., Kramer, B.W., Kramer-Albers, E.M., Laner-Plamberger, S., Laitinen, S., Leonardi, T., Lorenowicz, M.J., Lim, S.K., Lotvall, J., Maguire, C.A., Marcilla, A., Nazarenko, I., Ochiya, T., Patel, T., Pedersen, S., Pocsfalvi, G., Pluchino, S., Quesenberry, P., Reischl, I.G., Rivera, F.J., Sanzenbacher, R., Schallmoser, K., Slaper-Cortenbach, I., Strunk, D., Tonn, T., Vader, P., van Balkom, B.W., Wauben, M., Andaloussi, S.E., Thery, C., Rohde, E., Giebel, B., Applying extracellular vesicles based therapeutics in clinical trials - an ISEV position paper. J. Extracell. Vesicles, 4, 2015, 30087.
63. Skog, J., Wurdinger, T., van Rijn, S., Meijer, D.H., Gainche, L., Sena-Esteves, M., Curry, W.T. Jr., Carter, B.S., Krichevsky, A.M., Breakefield, X.O., Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10 (2008), 1470–1476.
64. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., Rak, J., Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 10 (2008), 619–624.
65. Peinado, H., Aleckovic, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., Garcia-Santos, G., Ghajar, C., Nitadori-Hoshino, A., Hoffman, C., Badal, K., Garcia, B.A., Callahan, M.K., Yuan, J., Martins, V.R., Skog, J., Kaplan, R.N., Brady, M.S., Wolchok, J.D., Chapman, P.B., Kang, Y., Bromberg, J., Lyden, D., Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18 (2012), 883–891.
66. Costa-Silva, B., Aiello, N.M., Ocean, A.J., Singh, S., Zhang, H., Thakur, B.K., Becker, A., Hoshino, A., Mark, M.T., Molina, H., Xiang, J., Zhang, T., Theilen, T.M., Garcia-Santos, G., Williams, C., Ararso, Y., Huang, Y., Rodrigues, G., Shen, T.L., Labori, K.J., Lothe, I.M., Kure, E.H., Hernandez, J., Doussot, A., Ebbesen, S.H., Grandgenett, P.M., Hollingsworth, M.A., Jain, M., Mallya, K., Batra, S.K., Jarnagin, W.R., Schwartz, R.E., Matei, I., Peinado, H., Stanger, B.Z., Bromberg, J., Lyden, D., Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat. Cell Biol. 17 (2015), 816–826.
67. Hoshino, A., Costa-Silva, B., Shen, T.L., Rodrigues, G., Hashimoto, A., Tesic Mark, M., Molina, H., Kohsaka, S., Di Giannatale, A., Ceder, S., Singh, S., Williams, C., Soplop, N., Uryu, K., Pharmer, L., King, T., Bojmar, L., Davies, A.E., Ararso, Y., Zhang, T., Zhang, H., Hernandez, J., Weiss, J.M., Dumont-Cole, V.D., Kramer, K., Wexler, L.H., Narendran, A., Schwartz, G.K., Healey, J.H., Sandstrom, P., Labori, K.J., Kure, E.H., Grandgenett, P.M., Hollingsworth, M.A., de Sousa, M., Kaur, S., Jain, M., Mallya, K., Batra, S.K., Jarnagin, W.R., Brady, M.S., Fodstad, O., Muller, V., Pantel, K., Minn, A.J., Bissell, M.J., Garcia, B.A., Kang, Y., Rajasekhar, V.K., Ghajar, C.M., Matei, I., Peinado, H., Bromberg, J., Lyden, D., Tumour exosome integrins determine organotropic metastasis. Nature 527 (2015), 329–335.
68. Mulcahy, L.A., Pink, R.C., Carter, D.R., Routes and mechanisms of extracellular vesicle uptake. J. Extracell. Vesicles, 3, 2014.
69. Chen, L., Brigstock, D.R., Integrins and heparan sulfate proteoglycans on hepatic stellate cells (HSC) are novel receptors for HSC-derived exosomes. FEBS Lett. 590 (2016), 4263–4274.
70. Franzen, C.A., Simms, P.E., Van Huis, A.F., Foreman, K.E., Kuo, P.C., Gupta, G.N., Characterization of uptake and internalization of exosomes by bladder cancer cells. Biomed. Res. Int., 2014, 2014, 619829.
71. Purushothaman, A., Bandari, S.K., Liu, J., Mobley, J.A., Brown, E.E., Sanderson, R.D., Fibronectin on the surface of myeloma cell-derived exosomes mediates exosome-cell interactions. J. Biol. Chem. 291 (2016), 1652–1663.
72. Hao, S., Bai, O., Li, F., Yuan, J., Laferte, S., Xiang, J., Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology 120 (2007), 90–102.
73. Saunderson, S.C., Dunn, A.C., Crocker, P.R., McLellan, A.D., CD169 mediates the capture of exosomes in spleen and lymph node. Blood 123 (2014), 208–216.
74. Hung, M.E., Leonard, J.N., Stabilization of exosome-targeting peptides via engineered glycosylation. J. Biol. Chem. 290 (2015), 8166–8172.
75. Katsuda, T., Kosaka, N., Ochiya, T., The roles of extracellular vesicles in cancer biology: toward the development of novel cancer biomarkers. Proteomics 14 (2014), 412–425.
76. Boukouris, S., Mathivanan, S., Exosomes in bodily fluids are a highly stable resource of disease biomarkers. Proteomics Clin. Appl. 9 (2015), 358–367.
77. Nawaz, M., Camussi, G., Valadi, H., Nazarenko, I., Ekstrom, K., Wang, X., Principe, S., Shah, N., Ashraf, N.M., Fatima, F., Neder, L., Kislinger, T., The emerging role of extracellular vesicles as biomarkers for urogenital cancers. Nat. Rev. Urol. 11 (2014), 688–701.
78. Cappello, F., Logozzi, M., Campanella, C., Bavisotto, C.C., Marcilla, A., Properzi, F., Fais, S., Exosome levels in human body fluids: a tumor marker by themselves?. Eur. J. Pharm. Sci. 96 (2017), 93–98.
79. Shao, H., Chung, J., Balaj, L., Charest, A., Bigner, D.D., Carter, B.S., Hochberg, F.H., Breakefield, X.O., Weissleder, R., Lee, H., Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat. Med. 18 (2012), 1835–1840.
80. Sethi, M.K., Kim, H., Park, C.K., Baker, M.S., Paik, Y.K., Packer, N.H., Hancock, W.S., Fanayan, S., Thaysen-Andersen, M., In-depth N-glycome profiling of paired colorectal cancer and non-tumorigenic tissues reveals cancer-, stage- and EGFR-specific protein N-glycosylation. Glycobiology 25 (2015), 1064–1078.
81. Im, H., Shao, H., Park, Y.I., Peterson, V.M., Castro, C.M., Weissleder, R., Lee, H., Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor. Nat. Biotechnol. 32 (2014), 490–495.
82. Runz, S., Keller, S., Rupp, C., Stoeck, A., Issa, Y., Koensgen, D., Mustea, A., Sehouli, J., Kristiansen, G., Altevogt, P., Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol. Oncol. 107 (2007), 563–571.
83. Salnikov, A.V., Bretz, N.P., Perne, C., Hazin, J., Keller, S., Fogel, M., Herr, I., Schlange, T., Moldenhauer, G., Altevogt, P., Antibody targeting of CD24 efficiently retards growth and influences cytokine milieu in experimental carcinomas. Br. J. Cancer 108 (2013), 1449–1459.
84. Kristiansen, G., Machado, E., Bretz, N., Rupp, C., Winzer, K.J., Konig, A.K., Moldenhauer, G., Marme, F., Costa, J., Altevogt, P., Molecular and clinical dissection of CD24 antibody specificity by a comprehensive comparative analysis. Lab. Investig. 90 (2010), 1102–1116.
85. Everest-Dass, A.V., Briggs, M.T., Kaur, G., Oehler, M.K., Hoffmann, P., Packer, N.H., N-glycan MALDI imaging mass spectrometry on formalin-fixed paraffin-embedded tissue enables the delineation of ovarian cancer tissues. Mol. Cell. Proteomics 15 (2016), 3003–3016.
86. Hurwitz, S.N., Rider, M.A., Bundy, J.L., Liu, X., Singh, R.K., Meckes, D.G. Jr., Proteomic profiling of NCI-60 extracellular vesicles uncovers common protein cargo and cancer type-specific biomarkers. Oncotarget, 2016.
87. Kunzli, B.M., Berberat, P.O., Zhu, Z.W., Martignoni, M., Kleeff, J., Tempia-Caliera, A.A., Fukuda, M., Zimmermann, A., Friess, H., Buchler, M.W., Influences of the lysosomal associated membrane proteins (lamp-1, lamp-2) and mac-2 binding protein (mac-2-BP) on the prognosis of pancreatic carcinoma. Cancer 94 (2002), 228–239.
88. Hu, J., He, J., Kuang, Y., Wang, Z., Sun, Z., Zhu, H., Liu, X., Expression and significance of 90K/Mac-2BP in prostate cancer. Exp. Ther. Med. 5 (2013), 181–184.
89. Menck, K., Scharf, C., Bleckmann, A., Dyck, L., Rost, U., Wenzel, D., Dhople, V.M., Siam, L., Pukrop, T., Binder, C., Klemm, F., Tumor-derived microvesicles mediate human breast cancer invasion through differentially glycosylated EMMPRIN. J. Mol. Cell Biol. 7 (2015), 143–153.
90. Chaiyawat, P., Weeraphan, C., Netsirisawan, P., Chokchaichamnankit, D., Srisomsap, C., Svasti, J., Champattanachai, V., Elevated O-GlcNAcylation of extracellular vesicle proteins derived from metastatic colorectal cancer cells. Cancer Genomics Proteomics 13 (2016), 387–398.
91. Staubach, S., Razawi, H., Hanisch, F.G., Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 9 (2009), 2820–2835.
92. Kamisawa, T., Wood, L.D., Itoi, T., Takaori, K., Pancreatic cancer. Lancet 388 (2016), 73–85.
93. O'Brien, D.P., Sandanayake, N.S., Jenkinson, C., Gentry-Maharaj, A., Apostolidou, S., Fourkala, E.O., Camuzeaux, S., Blyuss, O., Gunu, R., Dawnay, A., Zaikin, A., Smith, R.C., Jacobs, I.J., Menon, U., Costello, E., Pereira, S.P., Timms, J.F., Serum CA19-9 is significantly upregulated up to 2 years before diagnosis with pancreatic cancer: implications for early disease detection. Clin. Cancer Res. 21 (2015), 622–631.
94. Javeed, N., Sagar, G., Dutta, S.K., Smyrk, T.C., Lau, J.S., Bhattacharya, S., Truty, M., Petersen, G.M., Kaufman, R.J., Chari, S.T., Mukhopadhyay, D., Pancreatic cancer-derived exosomes cause paraneoplastic beta-cell dysfunction. Clin. Cancer Res. 21 (2015), 1722–1733.
95. Su, Z., Graybill, W.S., Zhu, Y., Detection and monitoring of ovarian cancer. Clin. Chim. Acta 415 (2013), 341–345.
96. Ricardo, S., Marcos-Silva, L., Pereira, D., Pinto, R., Almeida, R., Soderberg, O., Mandel, U., Clausen, H., Felix, A., Lunet, N., David, L., Detection of glyco-mucin profiles improves specificity of MUC16 and MUC1 biomarkers in ovarian serous tumours. Mol. Oncol. 9 (2015), 503–512.
97. Zhao, Z., Yang, Y., Zeng, Y., He, M., A microfluidic ExoSearch chip for multiplexed exosome detection towards blood-based ovarian cancer diagnosis. Lab Chip 16 (2016), 489–496.
98. Duffy, M.J., Lamerz, R., Haglund, C., Nicolini, A., Kalousova, M., Holubec, L., Sturgeon, C., Tumor markers in colorectal cancer, gastric cancer and gastrointestinal stromal cancers: European group on tumor markers 2014 guidelines update. Int. J. Cancer 134 (2014), 2513–2522.
99. Huber, V., Fais, S., Iero, M., Lugini, L., Canese, P., Squarcina, P., Zaccheddu, A., Colone, M., Arancia, G., Gentile, M., Seregni, E., Valenti, R., Ballabio, G., Belli, F., Leo, E., Parmiani, G., Rivoltini, L., Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 128 (2005), 1796–1804.
100. Lugini, L., Valtieri, M., Federici, C., Cecchetti, S., Meschini, S., Condello, M., Signore, M., Fais, S., Exosomes from human colorectal cancer induce a tumor-like behavior in colonic mesenchymal stromal cells. Oncotarget 7 (2016), 50086–50098.
101. Montemurro, F., Scaltriti, M., Biomarkers of drugs targeting HER-family signalling in cancer. J. Pathol. 232 (2014), 219–229.
102. Song, X., Ding, Y., Liu, G., Yang, X., Zhao, R., Zhang, Y., Zhao, X., Anderson, G.J., Nie, G., Cancer cell-derived exosomes induce mitogen-activated protein kinase-dependent monocyte survival by transport of functional receptor tyrosine kinases. J. Biol. Chem. 291 (2016), 8453–8464.
103. Ciravolo, V., Huber, V., Ghedini, G.C., Venturelli, E., Bianchi, F., Campiglio, M., Morelli, D., Villa, A., Della Mina, P., Menard, S., Filipazzi, P., Rivoltini, L., Tagliabue, E., Pupa, S.M., Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy. J. Cell. Physiol. 227 (2012), 658–667.