1,031
Views
95
CrossRef citations to date
0
Altmetric
Review

The potential of tumor-derived exosomes for noninvasive cancer monitoring

References

  • Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63(1):11-30
  • Cancer Research UK. Melanoma statistics and outlook. 2014. Available from: www.cancerresearchuk.org/about-cancer/type/melanoma/treatment/mela
  • Kohler BA, Sherman RL, Howlader N, et al. Annual report to the nation on the status of cancer, 1975-2011, featuring incidence of breast cancer subtypes by race/ethnicity, poverty, and state. J Natl Cancer Inst 2015;107(6):djv048
  • Parish CR. Cancer immunotherapy: the past, the present and the future. Immunol Cell Biol 2003;81(2):106-13
  • Beatty GL, Gladney WL. Immune escape mechanisms as a guide for cancer immunotherapy. Clin Cancer Res 2015;21(4):687-92
  • Patel SP, Kurzrock R. PD-L1 expression as a predictive biomarker in cancer immunotherapy. Mol Cancer Ther 2015;14(4):847-56
  • Mahoney KM, Freeman GJ, McDermott DF. The next immune-checkpoint inhibitors: PD-1/PD-L1 blockade in melanoma. Clin Ther 2015;37(4):764-82
  • McShane LM, Altman DG, Sauerbrei W, et al. Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 2005;97(16):1180-4
  • Shi Q, Mandrekar SJ, Sargent DJ. Predictive biomarkers in colorectal cancer: usage, validation, and design in clinical trials. Scand J Gastroenterol 2012;47(3):356-62
  • Taylor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 2011;33(5):441-54
  • Keller S, Ridinger J, Rupp AK, et al. Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 2011;9:86
  • Pan BT, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 1983;33(3):967-78
  • Harding C, Heuser J, Stahl P. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 1983;97(2):329-39
  • Pan BT, Teng K, Wu C, et al. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J Cell Biol 1985;101(3):942-8
  • Johnstone RM, Adam M, Hammond JR, et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987;262(19):9412-20
  • Cocucci E, Racchetti G, Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol 2009;19(2):43-51
  • Brinton LT, Sloane HS, Kester M, Kelly KA. Formation and role of exosomes in cancer. Cell Mol Life Sci 2015;72(4):659-71
  • Kowal J, Tkach M, Thery C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014;29:116-25
  • Marks MS, Heijnen HF, Raposo G. Lysosome-related organelles: unusual compartments become mainstream. Curr Opin Cell Biol 2013;25(4):495-505
  • Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013;200(4):373-83
  • Gould SJ, Raposo G. As we wait: coping with an imperfect nomenclature for extracellular vesicles. J Extracell Vesicles 2013;2. [Epub ahead of print]
  • van der Pol E, Boing AN, Harrison P, et al. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev 2012;64(3):676-705
  • Hemler ME. Tetraspanin functions and associated microdomains. Nat Rev Mol Cell Biol 2005;6(10):801-11
  • Rana S, Zoller M. Exosome target cell selection and the importance of exosomal tetraspanins: a hypothesis. Biochem Soc Trans 2011;39(2):559-62
  • Andreau Z, Yanez-Mo M. Tetraspanins in extracellular vesicle formation and function. Front Immunol 2014;5:1-12
  • Colombo M, Moita C, van Niel G, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 2013;126(Pt 24):5553-65
  • Park JE, Tan HS, Datta A, et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol Cell Proteomics 2010;9(6):1085-99
  • King HW, Michael MZ, Gleadle JM. Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 2012;12:421
  • Al-Nedawi K, Meehan B, Micallef J, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008;10(5):619-24
  • Dutta S, Warshall C, Bandyopadhyay C, et al. Interactions between exosomes from breast cancer cells and primary mammary epithelial cells leads to generation of reactive oxygen species which induce DNA damage response, stabilization of p53 and autophagy in epithelial cells. PLoS One 2014;9(5):e97580
  • Wieckowski E, Whiteside TL. Human tumor-derived vs dendritic cell-derived exosomes have distinct biologic roles and molecular profiles. Immunol Res 2006;36(1-3):247-54
  • Andreola G, Rivoltini L, Castelli C, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002;195(10):1303-16
  • Robbins PD, Morelli AE. Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 2014;14(3):195-208
  • Wieckowski EU, Visus C, Szajnik M, et al. Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 2009;183(6):3720-30
  • Kim JW, Wieckowski E, Taylor DD, et al. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res 2005;11(3):1010-20
  • Xiang X, Poliakov A, Liu C, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 2009;124(11):2621-33
  • Bobrie A, Thery C. Exosomes and communication between tumours and the immune system: are all exosomes equal? Biochem Soc Trans 2013;41(1):263-7
  • Gabrielsson S, Scheynius A. Exosomes in immunity and cancer–friends or foes? Semin Cancer Biol 2014;28:1-2
  • Saleem SN, Abdel-Mageed AB. Tumor-derived exosomes in oncogenic reprogramming and cancer progression. Cell Mol Life Sci 2015;72(1):1-10
  • Rak J, Guha A. Extracellular vesicles–vehicles that spread cancer genes. Bioessays 2012;34(6):489-97
  • Demory Beckler M, Higginbotham JN, Franklin JL, et al. Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics 2013;12(2):343-55
  • Kahlert C, Melo SA, Protopopov A, et al. Identification of double-stranded genomic DNA spanning all chromosomes with mutated KRAS and p53 DNA in the serum exosomes of patients with pancreatic cancer. J Biol Chem 2014;289(7):3869-75
  • Valadi H, Ekstrom K, Bossios A, et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9(6):654-9
  • 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):1470-6
  • Subra C, Grand D, Laulagnier K, et al. Exosomes account for vesicle-mediated transcellular transport of activatable phospholipases and prostaglandins. J Lipid Res 2010;51(8):2105-20
  • Record M, Subra C, Silvente-Poirot S, Poirot M. Exosomes as intercellular signalosomes and pharmacological effectors. Biochem Pharmacol 2011;81(10):1171-82
  • Martins VR, Dias MS, Hainaut P. Tumor-cell-derived microvesicles as carriers of molecular information in cancer. Curr Opin Oncol 2013;25(1):66-75
  • Atay S, Godwin AK. Tumor-derived exosomes: A message delivery system for tumor progression. Commun Integr Biol 2014;7(1):e28231
  • Vlassov AV, Magdaleno S, Setterquist R, Conrad R. Exosomes: current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta 2012;1820(7):940-8
  • Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183(3):1161-72
  • Blanchard N, Lankar D, Faure F, et al. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol 2002;168(7):3235-41
  • Lachenal G, Pernet-Gallay K, Chivet M, et al. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 2011;46(2):409-18
  • van Niel G, Raposo G, Candalh C, et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001;121(2):337-49
  • Peinado H, Aleckovic M, Lavotshkin S, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012;18(6):883-91
  • 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):816-26
  • Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011;71(11):3792-801
  • Iero M, Valenti R, Huber V, et al. Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 2008;15(1):80-8
  • Huber V, Fais S, Iero M, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 2005;128(7):1796-804
  • Whiteside TL. Immune modulation of T-cell and NK (natural killer) cell activities by TEXs (tumour-derived exosomes). Biochem Soc Trans 2013;41(1):245-51
  • Valenti R, Huber V, Iero M, et al. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007;67(7):2912-15
  • Webber J, Steadman R, Mason MD, et al. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010;70(23):9621-30
  • Webber JP, Spary LK, Sanders AJ, et al. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2015;34(3):290-302
  • Gross JC, Chaudhary V, Bartscherer K, Boutros M. Active Wnt proteins are secreted on exosomes. Nat Cell Biol 2012;14(10):1036-45
  • Luga V, Zhang L, Viloria-Petit AM, et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012;151(7):1542-56
  • Safaei R, Larson BJ, Cheng TC, et al. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 2005;4(10):1595-604
  • Corcoran C, Rani S, O’Brien K, et al. Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PLoS One 2012;7(12):e50999
  • Beloribi S, Ristorcelli E, Breuzard G, et al. Exosomal lipids impact notch signaling and induce death of human pancreatic tumoral SOJ-6 cells. PLoS One 2012;7(10):e47480
  • Yu X, Harris SL, Levine AJ. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res 2006;66(9):4795-801
  • Putz U, Howitt J, Doan A, et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci Signal 2012;5(243):ra70
  • Putz U, Mah S, Goh CP, et al. PTEN secretion in exosomes. Methods 2015;77-78:157-63
  • Johnstone RM, Mathew A, Mason AB, Teng K. Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. J Cell Physiol 1991;147(1):27-36
  • Abd Elmageed ZY, Yang Y, Thomas R, et al. Neoplastic reprogramming of patient-derived adipose stem cells by prostate cancer cell-associated exosomes. Stem Cells 2014;32(4):983-97
  • Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 2014;3. [Epub ahead of print]
  • Feng D, Zhao WL, Ye YY, et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010;11(5):675-87
  • Nolte-’t Hoen EN, Buschow SI, Anderton SM, et al. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 2009;113(9):1977-81
  • Muller L, Hong CS, Stolz DB, et al. Isolation of biologically-active exosomes from human plasma. J Immunol Methods 2014;411:55-65
  • Taylor DD, Shah S. Methods of isolating extracellular vesicles impact down-stream analyses of their cargoes. Methods 2015. [Epub ahead of print]
  • Brownlee Z, Lynn KD, Thorpe PE, Schroit AJ. A novel “salting-out” procedure for the isolation of tumor-derived exosomes. J Immunol Methods 2014;407:120-6
  • Saenz-Cuesta M, Arbelaiz A, Oregi A, et al. Methods for extracellular vesicles isolation in a hospital setting. Front Immunol 2015;6:50
  • Hong CS, Muller L, Boyiadzis M, Whiteside TL. Isolation and characterization of CD34+ blast-derived exosomes in acute myeloid leukemia. PLoS One 2014;9(8):e103310
  • Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol Chapter 2006;3:Unit 3 22
  • Taylor DD, Doellgast GJ. Quantitation of peroxidase-antibody binding to membrane fragments using column chromatography. Anal Biochem 1979;98(1):53-9
  • Hong CS, Funk S, Muller L, et al. Isolation of biologically active and morphologically intact exosomes from human plasma. Submitted 2015. [Epub ahead of print]
  • Witwer KW, Buzas EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013. [Epub ahead of print]
  • Gyorgy B, Paloczi K, Kovacs A, et al. Improved circulating microparticle analysis in acid-citrate dextrose (ACD) anticoagulant tube. Thromb Res 2014;133(2):285-92
  • van der Meel R, Krawczyk-Durka M, van Solinge WW, Schiffelers RM. Toward routine detection of extracellular vesicles in clinical samples. Int J Lab Hematol 2014;36(3):244-53
  • Sokolova V, Ludwig AK, Hornung S, et al. Characterisation of exosomes derived from human cells by nanoparticle tracking analysis and scanning electron microscopy. Colloids Surf B Biointerfaces 2011;87(1):146-50
  • Jayachandran M, Miller VM, Heit JA, Owen WG. Methodology for isolation, identification and characterization of microvesicles in peripheral blood. J Immunol Methods 2012;375(1-2):207-14
  • 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
  • Hong CS, Muller L, Whiteside TL, Boyiadzis M. Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia. Front Immunol 2014;5:160
  • Szczepanski MJ, Szajnik M, Welsh A, et al. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica 2011;96(9):1302-9
  • Wang Y, Sabbatino F, Wang X, Ferrone S. Detection of chondroitin sulfate proteoglycan 4 (CSPG4) in melanoma. Methods Mol Biol 2014;1102:523-35
  • Rodriguez M, Llanes L, Perez A, et al. Generation and characterization of an anti-idiotype monoclonal antibody related to GM3(NeuGc) ganglioside. Hybrid Hybridomics 2003;22(5):307-14
  • Pickhard A, Grober S, Haug AK, et al. Survivin and pAkt as potential prognostic markers in squamous cell carcinoma of the head and neck. Oral Surg Oral Med Oral Pathol Oral Radiol 2014;117(6):733-42
  • Szczepanski MJ, Whiteside TL. Elevated PRAME expression: what does this mean for treatment of head and neck squamous cell carcinoma? Biomark Med 2013;7(4):575-8
  • Taylor DD, Gercel-Taylor C. The origin, function, and diagnostic potential of RNA within extracellular vesicles present in human biological fluids. Front Genet 2013;4:142
  • Kalra H, Adda CG, Liem M, et al. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics 2013;13(22):3354-64
  • Nilsson J, Skog J, Nordstrand A, et al. Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer 2009;100(10):1603-7
  • Muller L, Muller-Haegele S, Mitsuhashi M, et al. Exosomes isolated from plasma of glioma patients enrolled in a vaccination trial reflect anti-tumor immune activity and might predict survival. Oncoimmunology 2015;4(6):e1008347
  • Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008;110(1):13-21
  • Santiago-Dieppa DR, Steinberg J, Gonda D, et al. Extracellular vesicles as a platform for ‘liquid biopsy’ in glioblastoma patients. Expert Rev Mol Diagn 2014;14(7):819-25
  • Kim DK, Kang B, Kim OY, et al. EVpedia: an integrated database of high-throughput data for systemic analyses of extracellular vesicles. J Extracell Vesicles 2013. [Epub ahead of print]
  • Kalra H, Simpson RJ, Ji H, et al. Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012;10(12):e1001450
  • Lasser C. Exosomes in diagnostic and therapeutic applications: biomarker, vaccine and RNA interference delivery vehicle. Expert Opin Biol Ther 2015;15(1):103-17
  • Nawaz M, Camussi G, Valadi H, et al. The emerging role of extracellular vesicles as biomarkers for urogenital cancers. Nat Rev Urol 2014;11(12):688-701
  • Roberson CD, Atay S, Gercel-Taylor C, Taylor DD. Tumor-derived exosomes as mediators of disease and potential diagnostic biomarkers. Cancer Biomark 2010;8(4-5):281-91
  • Rolfo C, Castiglia M, Hong D, et al. Liquid biopsies in lung cancer: the new ambrosia of researchers. Biochim Biophys Acta 2014;1846(2):539-46
  • Rabinowits G, Gercel-Taylor C, Day JM, et al. Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 2009;10(1):42-6
  • Henderson MC, Azorsa DO. The genomic and proteomic content of cancer cell-derived exosomes. Front Oncol 2012;2:38
  • Esquela-Kerscher A, Slack FJ. Oncomirs - microRNAs with a role in cancer. Nat Rev Cancer 2006;6(4):259-69
  • Chevillet JR, Kang Q, Ruf IK, et al. Quantitative and stoichiometric analysis of the microRNA content of exosomes. Proc Natl Acad Sci U S A 2014;111(41):14888-93
  • Zocco D, Ferruzzi P, Cappello F, et al. Extracellular vesicles as shuttles of tumor biomarkers and anti-tumor drugs. Front Oncol 2014;4:267
  • Nolte-’t Hoen EN, Buermans HP, Waasdorp M, et al. Deep sequencing of RNA from immune cell-derived vesicles uncovers the selective incorporation of small non-coding RNA biotypes with potential regulatory functions. Nucleic Acids Res 2012;40(18):9272-85
  • Ogata-Kawata H, Izumiya M, Kurioka D, et al. Circulating exosomal microRNAs as biomarkers of colon cancer. PLoS One 2014;9(4):e92921
  • Rosell R, Wei J, Taron M. Circulating MicroRNA Signatures of Tumor-Derived Exosomes for Early Diagnosis of Non-Small-Cell Lung Cancer. Clin Lung Cancer 2009;10(1):8-9
  • Corcoran C, Friel AM, Duffy MJ, et al. Intracellular and extracellular microRNAs in breast cancer. Clin Chem 2011;57(1):18-32
  • Liu J, Sun H, Wang X, et al. Increased exosomal microRNA-21 and microRNA-146a levels in the cervicovaginal lavage specimens of patients with cervical cancer. Int J Mol Sci 2014;15(1):758-73
  • Silva J, Garcia V, Zaballos A, et al. Vesicle-related microRNAs in plasma of nonsmall cell lung cancer patients and correlation with survival. Eur Respir J 2011;37(3):617-23
  • Hong BS, Cho JH, Kim H, et al. Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 2009;10:556
  • Whiteside TL. Immune responses to cancer: are they potential biomarkers of prognosis? Front Oncol 2013;3:107
  • Whiteside TL. Induced regulatory T cells in inhibitory microenvironments created by cancer. Expert Opin Biol Ther 2015;14(10):1411-25
  • Schuler PJ, Saze Z, Hong CS, et al. Human CD4(+) CD39(+) regulatory T cells produce adenosine upon co-expression of surface CD73 or contact with CD73(+) exosomes or CD73(+) cells. Clin Exp Immunol 2014;177(2):531-43
  • Szajnik M, Czystowska M, Szczepanski MJ, et al. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS ONE 2010;5(7):e11469
  • Filipazzi P, Burdek M, Villa A, et al. Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin Cancer Biol 2012;22(4):342-9
  • Clayton A, Mitchell JP, Court J, et al. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 2008;180(11):7249-58
  • Clayton A, Mitchell JP, Court J, et al. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res 2007;67(15):7458-66
  • Abusamra AJ, Zhong Z, Zheng X, et al. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis 2005;35(2):169-73
  • Chang S, Kohrt H, Maecker HT. Monitoring the immune competence of cancer patients to predict outcome. Cancer Immunol Immunother 2014;63(7):713-19
  • Grange C, Collino F, Tapparo M, Camussi G. Oncogenic micro-RNAs and Renal Cell Carcinoma. Front Oncol 2014;4:49
  • Geddings JE, Mackman N. Tumor-derived tissue factor-positive microparticles and venous thrombosis in cancer patients. Blood 2013;122(11):1873-80
  • Al-Nedawi K, Meehan B, Kerbel RS, et al. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 2009;106(10):3794-9
  • Nazarenko I, Rana S, Baumann A, et al. Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 2010;70(4):1668-78
  • Zhuang G, Wu X, Jiang Z, et al. Tumour-secreted miR-9 promotes endothelial cell migration and angiogenesis by activating the JAK-STAT pathway. EMBO J 2012;31(17):3513-23
  • van Niel G, Charrin S, Simoes S, et al. The tetraspanin CD63 regulates ESCRT-independent and -dependent endosomal sorting during melanogenesis. Dev Cell 2011;21(4):708-21
  • Jakobsen KR, Paulsen BS, Baek R, et al. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J Extracell Vesicles 2015;4:26659
  • Baietti MF, Zhang Z, Mortier E, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 2012;14(7):677-85
  • Ostrowski M, Carmo NB, Krumeich S, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010;12(1):19-30. sup pp 11-13
  • Hsu C, Morohashi Y, Yoshimura S, et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 2010;189(2):223-32
  • Logozzi M, De Milito A, Lugini L, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One 2009;4(4):e5219
  • Klibi J, Niki T, Riedel A, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 2009;113(9):1957-66
  • Shao H, Chung J, Balaj L, et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 2012;18(12):1835-40
  • Graner MW, Alzate O, Dechkovskaia AM, et al. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J 2009;23(5):1541-57
  • Epple LM, Griffiths SG, Dechkovskaia AM, et al. Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS One 2012;7(7):e42064
  • Redzic JS, Ung TH, Graner MW. Glioblastoma extracellular vesicles: reservoirs of potential biomarkers. Pharmgenomics Pers Med 2014;7:65-77
  • Higginbotham JN, Demory Beckler M, Gephart JD, et al. Amphiregulin exosomes increase cancer cell invasion. Curr Biol 2011;21(9):779-86
  • Khan S, Bennit HF, Turay D, et al. Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer 2014;14:176
  • Marimpietri D, Petretto A, Raffaghello L, et al. Proteome profiling of neuroblastoma-derived exosomes reveal the expression of proteins potentially involved in tumor progression. PLoS ONE 2013;8(9):e75054
  • Flanagan J, Middeldorp J, Sculley T. Localization of the Epstein-Barr virus protein LMP 1 to exosomes. J Gen Virol 2003;84(Pt 7):1871-9
  • Staubach S, Razawi H, Hanisch FG. Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 2009;9(10):2820-35
  • Mears R, Craven RA, Hanrahan S, et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004;4(12):4019-31
  • Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 2010;73(10):1907-20
  • Mizutani K, Terazawa R, Kameyama K, et al. Isolation of prostate cancer-related exosomes. Anticancer Res 2014;34(7):3419-23
  • Li J, Sherman-Baust CA, Tsai-Turton M, et al. Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer 2009;9:244
  • Houali K, Wang X, Shimizu Y, et al. A new diagnostic marker for secreted Epstein-Barr virus encoded LMP1 and BARF1 oncoproteins in the serum and saliva of patients with nasopharyngeal carcinoma. Clin Cancer Res 2007;13(17):4993-5000
  • Bergmann C, Strauss L, Wieckowski E, et al. Tumor-derived microvesicles in sera of patients with head and neck cancer and their role in tumor progression. Head Neck 2009;31(3):371-80
  • Szajnik M, Derbis M, Lach M, et al. Exosomes in Plasma of Patients with Ovarian Carcinoma: Potential Biomarkers of Tumor Progression and Response to Therapy. Gynecol Obstet (Sunnyvale) 2013(Suppl 4):3
  • Mitchell PJ, Welton J, Staffurth J, et al. Can urinary exosomes act as treatment response markers in prostate cancer? J Transl Med 2009;7:4
  • Principe S, Jones EE, Kim Y, et al. In-depth proteomic analyses of exosomes isolated from expressed prostatic secretions in urine. Proteomics 2013;13(10-11):1667-71
  • Raimondo F, Morosi L, Corbetta S, et al. Differential protein profiling of renal cell carcinoma urinary exosomes. Mol Biosyst 2013;9(6):1220-33
  • Welton JL, Khanna S, Giles PJ, et al. Proteomics analysis of bladder cancer exosomes. Mol Cell Proteomics 2010;9(6):1324-38
  • Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis 2011;32(15):1976-83
  • Chiba M, Kimura M, Asari S. Exosomes secreted from human colorectal cancer cell lines contain mRNAs, microRNAs and natural antisense RNAs, that can transfer into the human hepatoma HepG2 and lung cancer A549 cell lines. Oncol Rep 2012;28(5):1551-8
  • Ogawa Y, Kanai-Azuma M, Akimoto Y, et al. Exosome-like vesicles with dipeptidyl peptidase IV in human saliva. Biol Pharm Bull 2008;31(6):1059-62
  • Xiao H, Wong DT. Proteomic analysis of microvesicles in human saliva by gel electrophoresis with liquid chromatography-mass spectrometry. Anal Chim Acta 2012;723:61-7
  • EVpedia. Available from: http://evpedia.info/ [cited 7 October 2014]
  • Roth P, Wischhusen J, Happold C, et al. A specific miRNA signature in the peripheral blood of glioblastoma patients. J Neurochem 2011;118(3):449-57
  • Manterola L, Guruceaga E, Gallego Perez-Larraya J, et al. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro Oncol 2014;16(4):520-7
  • Cazzoli R, Buttitta F, Di Nicola M, et al. microRNAs derived from circulating exosomes as noninvasive biomarkers for screening and diagnosing lung cancer. J Thorac Oncol 2013;8(9):1156-62
  • Bryant RJ, Pawlowski T, Catto JW, et al. Changes in circulating microRNA levels associated with prostate cancer. Br J Cancer 2012;106(4):768-74
  • Brase JC, Johannes M, Schlomm T, et al. Circulating miRNAs are correlated with tumor progression in prostate cancer. Int J Cancer 2011;128(3):608-16
  • Kogure T, Lin WL, Yan IK, et al. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011;54(4):1237-48
  • Huan J, Hornick NI, Shurtleff MJ, et al. RNA trafficking by acute myelogenous leukemia exosomes. Cancer Res 2013;73(2):918-29

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.