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Molecular Cancer
Published in: Molecular Cancer 1/2017

Open Access 01-12-2017 | Review

Role of exosomal proteins in cancer diagnosis

Authors: Weihua Li, Chuanyun Li, Tong Zhou, Xiuhong Liu, Xiaoni Liu, Xiuhui Li, Dexi Chen

Published in: Molecular Cancer | Issue 1/2017

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Abstract

Exosomes are emerging as a new type of cancer biomarkers. Exosome is a bilayered nano-sized vesicle secreted by various living cells in all body fluids. Based on the expanding albeit incomplete knowledge of their biogenesis, secretion by cells and cancer cell-specific molecular and genetic contents, exosomes are viewed as promising, clinically-relevant surrogates of cancer progression and response to therapy. Preliminary proteomic, genetic and functional profiling of cancer cell-derived or cancer plasma-derived exosomes confirms their unique characteristics. Alterations in protein or nucleic acid profiles of exosomes in plasma correlate with pathological processes of many diseases including cancer. However, previous studies on exosome application in cancer diagnosis and treatment mainly focussed on miRNAs. With the development of rapid large-scale production, purification, extraction and screening of exosomal contents, exosomal protein application can be explored for early stage cancer diagnosis, monitoring and prognosis evaluation. Here, we summarized the recent developments in application of exosomal proteins for cancer diagnosis.
Literature
1.
Mignot G, Roux S, Thery C, Segura E, Zitvogel L. Prospects for exosomes in immunotherapy of cancer. J Cell Mol Med. 2006;10:376–88.PubMedCrossRef
2.
Johnstone RM, Bianchini A, Teng K. Reticulocyte maturation and exosome release: transferrin receptor containing exosomes shows multiple plasma membrane functions. Blood. 1989;74:1844–51.PubMed
3.
Fader CM, Savina A, Sanchez D, Colombo MI. Exosome secretion and red cell maturation: exploring molecular components involved in the docking and fusion of multivesicular bodies in K562 cells. Blood Cells Mol Dis. 2005;35:153–7.PubMedCrossRef
4.
Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183:1161–72.PubMedCrossRef
5.
Clayton A, Turkes A, Navabi H, Mason MD, Tabi Z. Induction of heat shock proteins in B-cell exosomes. J Cell Sci. 2005;118:3631–8.PubMedCrossRef
6.
Chaput N, Flament C, Viaud S, Taieb J, Roux S, Spatz A, Andre F, LePecq JB, Boussac M, Garin J, et al. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukoc Biol. 2006;80:471–8.PubMedCrossRef
7.
Blanchard N, Lankar D, Faure F, Regnault A, Dumont C, Raposo G, Hivroz C. TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol. 2002;168:3235–41.PubMedCrossRef
8.
Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, Ricciardi-Castagnoli P, Raposo G, Amigorena S. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med. 1998;4:594–600.PubMedCrossRef
9.
Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F, Pageaux JF, Kobayashi T, Salles JP, Perret B, Bonnerot C, Record M. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J. 2004;380:161–71.PubMedPubMedCentralCrossRef
10.
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.PubMed
11.
Skokos D, Botros HG, Demeure C, Morin J, Peronet R, Birkenmeier G, Boudaly S, Mecheri S. 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.PubMedCrossRef
12.
Nguyen DG, Booth A, Gould SJ, Hildreth JE. Evidence that HIV budding in primary macrophages occurs through the exosome release pathway. J Biol Chem. 2003;278:52347–54.PubMedCrossRef
13.
14.
van Niel G, Heyman M. The epithelial cell cytoskeleton and intracellular trafficking. II. Intestinal epithelial cell exosomes: perspectives on their structure and function. Am J Physiol Gastrointest Liver Physiol. 2002;283:G251–5.PubMedCrossRef
15.
Van Niel G, Mallegol J, Bevilacqua C, Candalh C, Brugiere S, Tomaskovic-Crook E, Heath JK, Cerf-Bensussan N, Heyman M. Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice. Gut. 2003;52:1690–7.PubMedPubMedCentralCrossRef
16.
Taylor DD, Gercel-Taylor C. Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects. Br J Cancer. 2005;92:305–11.PubMedPubMedCentral
17.
Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7:297–303.PubMedCrossRef
18.
Riteau B, Faure F, Menier C, Viel S, Carosella ED, Amigorena S, Rouas-Freiss N. Exosomes bearing HLA-G are released by melanoma cells. Hum Immunol. 2003;64:1064–72.PubMedCrossRef
19.
Andre F, Schartz NE, Chaput N, Flament C, Raposo G, Amigorena S, Angevin E, Zitvogel L. Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine. 2002;20(Suppl 4):A28–31.PubMedCrossRef
20.
Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, Pomel C, Lhomme C, Escudier B, Le Chevalier T, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet. 2002;360:295–305.PubMedCrossRef
21.
van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, Heyman M. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology. 2001;121:337–49.PubMedCrossRef
22.
Faure J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, et al. Exosomes are released by cultured cortical neurones. Mol Cell Neurosci. 2006;31:642–8.PubMedCrossRef
23.
Ge R, Tan E, Sharghi-Namini S, Asada HH. Exosomes in cancer microenvironment and beyond: have we overlooked these extracellular messengers? Cancer Microenviron. 2012;5:323–32.PubMedPubMedCentralCrossRef
24.
Keller S, Rupp C, Stoeck A, Runz S, Fogel M, Lugert S, Hager HD, Abdel-Bakky MS, Gutwein P, Altevogt P. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 2007;72:1095–102.PubMedCrossRef
25.
Li QL, Bu N, Yu YC, Hua W, Xin XY. Exvivo experiments of human ovarian cancer ascites-derived exosomes presented by dendritic cells derived from umbilical cord blood for immunotherapy treatment. Clin Med Oncol. 2008;2:461–7.PubMedPubMedCentral
26.
Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol. 2008;110:13–21.PubMedCrossRef
27.
Almqvist N, Lonnqvist A, Hultkrantz S, Rask C, Telemo E. Serum-derived exosomes from antigen-fed mice prevent allergic sensitization in a model of allergic asthma. Immunology. 2008;125:21–7.PubMedPubMedCentralCrossRef
28.
Gallo A, Tandon M, Alevizos I, Illei GG. The majority of microRNAs detectable in serum and saliva is concentrated in exosomes. PLoS One. 2012;7:e30679.PubMedPubMedCentralCrossRef
29.
Ogawa Y, Kanai-Azuma M, Akimoto Y, Kawakami H, Yanoshita R. Exosome-like vesicles with dipeptidyl peptidase IV in human saliva. Biol Pharm Bull. 2008;31:1059–62.PubMedCrossRef
30.
Navabi H, Croston D, Hobot J, Clayton A, Zitvogel L, Jasani B, Bailey-Wood R, Wilson K, Tabi Z, Mason MD, Adams M. Preparation of human ovarian cancer ascites-derived exosomes for a clinical trial. Blood Cells Mol Dis. 2005;35:149–52.PubMedCrossRef
31.
Admyre C, Johansson SM, Qazi KR, Filen JJ, Lahesmaa R, Norman M, Neve EP, Scheynius A, Gabrielsson S. Exosomes with immune modulatory features are present in human breast milk. J Immunol. 2007;179:1969–78.PubMedCrossRef
32.
Saman S, Kim W, Raya M, Visnick Y, Miro S, Saman S, Jackson B, McKee AC, Alvarez VE, Lee NC, Hall GF. Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. J Biol Chem. 2012;287:3842–9.PubMedCrossRef
33.
Street JM, Barran PE, Mackay CL, Weidt S, Balmforth C, Walsh TS, Chalmers RT, Webb DJ, Dear JW. Identification and proteomic profiling of exosomes in human cerebrospinal fluid. J Transl Med. 2012;10:5.PubMedPubMedCentralCrossRef
34.
Qiu S, Duan X, Geng X, Xie J, Gao H. Antigen-specific activities of CD8+ T cells in the nasal mucosa of patients with nasal allergy. Asian Pac J Allergy Immunol. 2012;30:107–13.PubMed
35.
De Toro J, Herschlik L, Waldner C, Mongini C. Emerging roles of exosomes in normal and pathological conditions: new insights for diagnosis and therapeutic applications. Front Immunol. 2015;6:203.PubMedPubMedCentralCrossRef
36.
37.
Barteneva NS, Maltsev N, Vorobjev IA. Microvesicles and intercellular communication in the context of parasitism. Front Cell Infect Microbiol. 2013;3:49.PubMedPubMedCentralCrossRef
38.
Kucharzewska P, Belting M. Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress. J Extracell Vesicles. 2013;2
39.
40.
Hornick NI, Huan J, Doron B, Goloviznina NA, Lapidus J, Chang BH, Kurre P. Serum exosome MicroRNA as a minimally-invasive early biomarker of AML. Sci Rep. 2015;5:11295.PubMedPubMedCentralCrossRef
41.
Tang MK, Wong AS. Exosomes: emerging biomarkers and targets for ovarian cancer. Cancer Lett. 2015;367:26–33.PubMedCrossRef
42.
Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, LeBleu VS, Mittendorf EA, Weitz J, Rahbari N, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523:177–82.PubMedPubMedCentralCrossRef
43.
Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, Chen D, Gu J, He X, Huang S. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25:981–4.PubMedPubMedCentralCrossRef
44.
Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol. 2002;2:569–79.PubMed
45.
46.
Mathivanan S, Fahner CJ, Reid GE, Simpson RJ. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 2012;40:D1241–4.PubMedCrossRef
47.
Mathivanan S, Simpson RJ. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics. 2009;9:4997–5000.PubMedCrossRef
48.
Mathivanan S, Ji H, Simpson RJ. Exosomes: extracellular organelles important in intercellular communication. J Proteome. 2010;73:1907–20.CrossRef
49.
van Niel G, Porto-Carreiro I, Simoes S, Raposo G. Exosomes: a common pathway for a specialized function. J Biochem. 2006;140:13–21.PubMedCrossRef
50.
Michael A, Bajracharya SD, Yuen PS, Zhou H, Star RA, Illei GG, Alevizos I. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010;16:34–8.PubMedCrossRef
51.
Trams EG, Lauter CJ, Salem NJ, Heine U. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim Biophys Acta. 1981;645:63–70.PubMedCrossRef
52.
53.
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11:1143–9.PubMedCrossRef
54.
Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180.PubMedPubMedCentralCrossRef
55.
Salido-Guadarrama I, Romero-Cordoba S, Peralta-Zaragoza O, Hidalgo-Miranda A, Rodriguez-Dorantes M. MicroRNAs transported by exosomes in body fluids as mediators of intercellular communication in cancer. Onco Targets Ther. 2014;7:1327–38.PubMedPubMedCentral
56.
van der Pol E, Boing AN, Harrison P, Sturk A, Nieuwland R. Classification, functions, and clinical relevance of extracellular vesicles. Pharmacol Rev. 2012;64:676–705.PubMedCrossRef
57.
Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brugger B, Simons M. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319:1244–7.PubMedCrossRef
58.
Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14:677–85.PubMedCrossRef
59.
Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature. 2007;450:435–9.PubMedCrossRef
60.
Segura E, Nicco C, Lombard B, Veron P, Raposo G, Batteux F, Amigorena S, Thery C. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood. 2005;106:216–23.PubMedCrossRef
61.
62.
63.
Roma-Rodrigues C, Fernandes AR, Baptista PV. Exosome in tumour microenvironment: overview of the crosstalk between normal and cancer cells. Biomed Res Int. 2014;2014:179486.PubMedPubMedCentralCrossRef
64.
Minciacchi VR, Freeman MR, Di Vizio D. Extracellular vesicles in cancer: exosomes, microvesicles and the emerging role of large oncosomes. Semin Cell Dev Biol. 2015;40:41–51.PubMedPubMedCentralCrossRef
65.
Fraser KB, Moehle MS, Alcalay RN, West AB. Urinary LRRK2 phosphorylation predicts parkinsonian phenotypes in G2019S LRRK2 carriers. Neurology. 2016;86:994–9.PubMedPubMedCentralCrossRef
66.
Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, Morgelin M, Bourseau-Guilmain E, Bengzon J, Belting M. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A. 2013;110:7312–7.PubMedPubMedCentralCrossRef
67.
Khalyfa A, Almendros I, Gileles-Hillel A, Akbarpour M, Trzepizur W, Mokhlesi B, Huang L, Andrade J, Farre R, Gozal D. Circulating exosomes potentiate tumor malignant properties in a mouse model of chronic sleep fragmentation. Oncotarget. 2016;7:54676–90.PubMedPubMedCentralCrossRef
68.
Katoh M. Therapeutics targeting angiogenesis: genetics and epigenetics, extracellular miRNAs and signaling networks (review). Int J Mol Med. 2013;32:763–7.PubMedPubMedCentralCrossRef
69.
Hood JL. Melanoma exosome induction of endothelial cell GM-CSF in pre-metastatic lymph nodes may result in different M1 and M2 macrophage mediated angiogenic processes. Med Hypotheses. 2016;94:118–22.PubMedCrossRef
70.
DeRita RM, Zerlanko B, Singh A, Lu H, Iozzo RV, Benovic JL, Languino LR. C-Src, insulin-like growth factor I receptor, G-protein-coupled receptor Kinases and focal adhesion Kinase are enriched into prostate cancer cell Exosomes. J Cell Biochem. 2017;118:66–73.PubMedCrossRef
71.
Wang J, De Veirman K, Faict S, Frassanito MA, Ribatti D, Vacca A, Menu E. Multiple myeloma exosomes establish a favourable bone marrow microenvironment with enhanced angiogenesis and immunosuppression. J Pathol. 2016;239:162–73.PubMedCrossRef
72.
Konstantinell A, Bruun JA, Olsen R, Aspar A, Skalko-Basnet N, Sveinbjornsson B, Moens U. Secretomic analysis of extracellular vesicles originating from polyomavirus-negative and polyomavirus-positive Merkel cell carcinoma cell lines. Proteomics. 2016;16:2587–91.PubMedCrossRef
73.
Thakur BK, Zhang H, Becker A, Matei I, Huang Y, Costa-Silva B, Zheng Y, Hoshino A, Brazier H, Xiang J, et al. Double-stranded DNA in exosomes: a novel biomarker in cancer detection. Cell Res. 2014;24:766–9.PubMedPubMedCentralCrossRef
74.
Zomer A, Maynard C, Verweij FJ, Kamermans A, Schafer R, Beerling E, Schiffelers RM, de Wit E, Berenguer J, Ellenbroek SI, et al. In vivo imaging reveals extracellular vesicle-mediated phenocopying of metastatic behavior. Cell. 2015;161:1046–57.PubMedPubMedCentralCrossRef
75.
Endres M, Kneitz S, Orth MF, Perera RK, Zernecke A, Butt E. Regulation of matrix metalloproteinases (MMPs) expression and secretion in MDA-MB-231 breast cancer cells by LIM and SH3 protein 1 (LASP1). Oncotarget. 2016;7:64244–59.PubMedPubMedCentralCrossRef
76.
Sanchez CA, Andahur EI, Valenzuela R, Castellon EA, Fulla JA, Ramos CG, Trivino JC. Exosomes from bulk and stem cells from human prostate cancer have a differential microRNA content that contributes cooperatively over local and pre-metastatic niche. Oncotarget. 2016;7:3993–4008.PubMedCrossRef
77.
Sceneay J, Smyth MJ, Moller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev. 2013;32:449–64.PubMedCrossRef
78.
Gu J, Qian H, Shen L, Zhang X, Zhu W, Huang L, Yan Y, Mao F, Zhao C, Shi Y, Xu W. Gastric cancer exosomes trigger differentiation of umbilical cord derived mesenchymal stem cells to carcinoma-associated fibroblasts through TGF-beta/Smad pathway. PLoS One. 2012;7:e52465.PubMedPubMedCentralCrossRef
79.
Tlsty TD, Hein PW. Know thy neighbor: stromal cells can contribute oncogenic signals. Curr Opin Genet Dev. 2001;11:54–9.PubMedCrossRef
80.
Orimo A, Gupta PB, Sgroi DC, Arenzana-Seisdedos F, Delaunay T, Naeem R, Carey VJ, Richardson AL, Weinberg RA. Stromal fibroblasts present in invasive human breast carcinomas promote tumor growth and angiogenesis through elevated SDF-1/CXCL12 secretion. Cell. 2005;121:335–48.PubMedCrossRef
81.
Antonyak MA, Li B, Boroughs LK, Johnson JL, Druso JE, Bryant KL, Holowka DA, Cerione RA. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci U S A. 2011;108:4852–7.PubMedPubMedCentralCrossRef
82.
Yang C, Ruffner MA, Kim SH, Robbins PD. Plasma-derived MHC class II+ exosomes from tumor-bearing mice suppress tumor antigen-specific immune responses. Eur J Immunol. 2012;42:1778–84.PubMedPubMedCentralCrossRef
83.
Chornoguz O, Grmai L, Sinha P, Artemenko KA, Zubarev RA, Ostrand-Rosenberg S. Proteomic pathway analysis reveals inflammation increases myeloid-derived suppressor cell resistance to apoptosis. Mol Cell Proteomics. 2011;10:M110–M2980.PubMedCrossRef
84.
Taylor DD, Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol. 2011;33:441–54.PubMedCrossRef
85.
Condamine T, Gabrilovich DI. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 2011;32:19–25.PubMedCrossRef
86.
Wang T, Diaz AJ, Yen Y. The role of peroxiredoxin II in chemoresistance of breast cancer cells. Breast Cancer (Dove Med Press). 2014;6:73–80.
87.
Chen WX, Liu XM, Lv MM, Chen L, Zhao JH, Zhong SL, Ji MH, Hu Q, Luo Z, Wu JZ, Tang JH. Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs. PLoS One. 2014;9:e95240.PubMedPubMedCentralCrossRef
88.
Bebawy M, Combes V, Lee E, Jaiswal R, Gong J, Bonhoure A, Grau GE. Membrane microparticles mediate transfer of P-glycoprotein to drug sensitive cancer cells. Leukemia. 2009;23:1643–9.PubMedCrossRef
89.
Safaei R, Larson BJ, Cheng TC, Gibson MA, Otani S, Naerdemann W, Howell SB. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther. 2005;4:1595–604.PubMedCrossRef
90.
Boelens MC, Wu TJ, Nabet BY, Xu B, Qiu Y, Yoon T, Azzam DJ, Twyman-Saint VC, Wiemann BZ, Ishwaran H, et al. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell. 2014;159:499–513.PubMedPubMedCentralCrossRef
91.
Penfornis P, Vallabhaneni KC, Whitt J, Pochampally R. Extracellular vesicles as carriers of microRNA, proteins and lipids in tumor microenvironment. Int J Cancer. 2016;138:14–21.PubMedCrossRef
92.
93.
94.
Frydrychowicz M, Kolecka-Bednarczyk A, Madejczyk M, Yasar S, Dworacki G. Exosomes - structure, biogenesis and biological role in non-small-cell lung cancer. Scand J Immunol. 2015;81:2–10.PubMedCrossRef
95.
Azmi AS, Bao B, Sarkar FH. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev. 2013;32:623–42.PubMedCrossRef
96.
Grange C, Tapparo M, Collino F, Vitillo L, Damasco C, Deregibus MC, Tetta C, Bussolati B, Camussi G. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011;71:5346–56.PubMedCrossRef
97.
Li J, Sherman-Baust CA, Tsai-Turton M, Bristow RE, Roden RB, Morin PJ. Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer. BMC Cancer. 2009;9:244.PubMedPubMedCentralCrossRef
98.
Rolfo C, Castiglia M, Hong D, Alessandro R, Mertens I, Baggerman G, Zwaenepoel K, Gil-Bazo I, Passiglia F, Carreca AP, et al. Liquid biopsies in lung cancer: the new ambrosia of researchers. Biochim Biophys Acta. 1846;2014:539–46.
99.
Clark DJ, Fondrie WE, Yang A, Mao L. Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes. J Proteome. 2016;133:161–9.CrossRef
100.
Jakobsen KR, Paulsen BS, Baek R, Varming K, Sorensen BS, Jorgensen MM. Exosomal proteins as potential diagnostic markers in advanced non-small cell lung carcinoma. J Extracell Vesicles. 2015;4:26659.PubMedCrossRef
101.
Li Y, Zhang Y, Qiu F, Qiu Z. Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis. 2011;32:1976–83.PubMedCrossRef
102.
Sandfeld-Paulsen B, Jakobsen KR, Baek R, Folkersen BH, Rasmussen TR, Meldgaard P, Varming K, Jorgensen MM, Sorensen BS. Exosomal proteins as diagnostic biomarkers in lung cancer. J Thorac Oncol. 2016;11:1701–10.PubMedCrossRef
103.
Keryer-Bibens C, Pioche-Durieu C, Villemant C, Souquere S, Nishi N, Hirashima M, Middeldorp J, Busson P. Exosomes released by EBV-infected nasopharyngeal carcinoma cells convey the viral latent membrane protein 1 and the immunomodulatory protein galectin 9. BMC Cancer. 2006;6:283.PubMedPubMedCentralCrossRef
104.
Klibi J, Niki T, Riedel A, Pioche-Durieu C, Souquere S, Rubinstein E, Le Moulec S, Guigay J, Hirashima M, Guemira F, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood. 2009;113:1957–66.PubMedCrossRef
105.
Houali K, Wang X, Shimizu Y, Djennaoui D, Nicholls J, Fiorini S, Bouguermouh A, Ooka T. 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;13:4993–5000.PubMedCrossRef
106.
Meckes DJ, Shair KH, Marquitz AR, Kung CP, Edwards RH, Raab-Traub N. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci U S A. 2010;107:20370–5.PubMedPubMedCentralCrossRef
107.
Ye SB, Li ZL, Luo DH, Huang BJ, Chen YS, Zhang XS, Cui J, Zeng YX, Li J. Tumor-derived exosomes promote tumor progression and T-cell dysfunction through the regulation of enriched exosomal microRNAs in human nasopharyngeal carcinoma. Oncotarget. 2014;5:5439–52.PubMedPubMedCentralCrossRef
108.
109.
Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, Forman D, Bray F. Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer. 2013;49:1374–403.PubMedCrossRef
110.
Wu L, Zhang X, Zhang B, Shi H, Yuan X, Sun Y, Pan Z, Qian H, Xu W. Exosomes derived from gastric cancer cells activate NF-kappaB pathway in macrophages to promote cancer progression. Tumour Biol. 2016;37:12169–80.PubMedCrossRef
111.
Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K, Mochizuki T. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One. 2010;5:e13247.PubMedPubMedCentralCrossRef
112.
Li C, Liu DR, Li GG, Wang HH, Li XW, Zhang W, Wu YL, Chen L. CD97 promotes gastric cancer cell proliferation and invasion through exosome-mediated MAPK signaling pathway. World J Gastroenterol. 2015;21:6215–28.PubMedPubMedCentralCrossRef
113.
Qu JL, Qu XJ, Qu JL, Qu XJ, Zhao MF, Teng YE, Zhang Y, Hou KZ, Jiang YH, Yang XH, Liu YP. The role of cbl family of ubiquitin ligases in gastric cancer exosome-induced apoptosis of Jurkat T cells. Acta Oncol. 2009;48:1173–80.PubMedCrossRef
114.
Anami K, Oue N, Noguchi T, Sakamoto N, Sentani K, Hayashi T, Naito Y, Oo HZ, Yasui W. TSPAN8, identified by Escherichia Coli ampicillin secretion trap, is associated with cell growth and invasion in gastric cancer. Gastric Cancer. 2016;19:370–80.PubMedCrossRef
115.
Welton JL, Khanna S, Giles PJ, Brennan P, Brewis IA, Staffurth J, Mason MD, Clayton A. Proteomics analysis of bladder cancer exosomes. Mol Cell Proteomics. 2010;9:1324–38.PubMedPubMedCentralCrossRef
116.
Toth B, Nieuwland R, Liebhardt S, Ditsch N, Steinig K, Stieber P, Rank A, Gohring P, Thaler CJ, Friese K, Bauerfeind I. Circulating microparticles in breast cancer patients: a comparative analysis with established biomarkers. Anticancer Res. 2008;28:1107–12.PubMed
117.
Meehan K, Vella LJ. The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit Rev Clin Lab Sci. 2016;53:121–31.PubMedCrossRef
118.
Khan S, Bennit HF, Turay D, Perez M, Mirshahidi S, Yuan Y, Wall NR. Early diagnostic value of survivin and its alternative splice variants in breast cancer. BMC Cancer. 2014;14:176.PubMedPubMedCentralCrossRef
119.
Baran J, Baj-Krzyworzeka M, Weglarczyk K, Szatanek R, Zembala M, Barbasz J, Czupryna A, Szczepanik A, Zembala M. Circulating tumour-derived microvesicles in plasma of gastric cancer patients. Cancer Immunol Immunother. 2010;59:841–50.PubMedCrossRef
120.
Lim JW, Mathias RA, Kapp EA, Layton MJ, Faux MC, Burgess AW, Ji H, Simpson RJ. Restoration of full-length APC protein in SW480 colon cancer cells induces exosome-mediated secretion of DKK-4. Electrophoresis. 2012;33:1873–80.PubMedCrossRef
121.
Silva J, Garcia V, Rodriguez M, Compte M, Cisneros E, Veguillas P, Garcia JM, Dominguez G, Campos-Martin Y, Cuevas J, et al. Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer. 2012;51:409–18.PubMedCrossRef
122.
Fraser KB, Rawlins AB, Clark RG, Alcalay RN, Standaert DG, Liu N, West AB. Ser(P)-1292 LRRK2 in urinary exosomes is elevated in idiopathic Parkinson's disease. Mov Disord. 2016;31:1543–50.PubMedCrossRef
123.
Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WJ, Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10:1470–6.PubMedPubMedCentralCrossRef
124.
Shao H, Chung J, Balaj L, Charest A, Bigner DD, Carter BS, Hochberg FH, Breakefield XO, Weissleder R, Lee H. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med. 2012;18:1835–40.PubMedPubMedCentralCrossRef
125.
Raimondo F, Morosi L, Corbetta S, Chinello C, Brambilla P, Della MP, Villa A, Albo G, Battaglia C, Bosari S, et al. Differential protein profiling of renal cell carcinoma urinary exosomes. Mol BioSyst. 2013;9:1220–33.PubMedCrossRef
126.
Chen CL, Lai YF, Tang P, Chien KY, Yu JS, Tsai CH, Chen HW, Wu CC, Chung T, Hsu CW, et al. Comparative and targeted proteomic analyses of urinary microparticles from bladder cancer and hernia patients. J Proteome Res. 2012;11:5611–29.PubMedCrossRef
127.
Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, Breakefield XO, Widmark A. Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Br J Cancer. 2009;100:1603–7.PubMedPubMedCentralCrossRef
128.
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. 2007;107:563–71.PubMedCrossRef
129.
Szajnik M, Derbis M, Lach M, Patalas P, Michalak M, Drzewiecka H, Szpurek D, Nowakowski A, Spaczynski M, Baranowski W, Whiteside TL. Exosomes in plasma of patients with ovarian carcinoma: potential biomarkers of tumor progression and response to therapy. Gynecol Obstet (Sunnyvale). 2013;Suppl 4:3.
130.
Liang B, Peng P, Chen S, Li L, Zhang M, Cao D, Yang J, Li H, Gui T, Li X, Shen K. Characterization and proteomic analysis of ovarian cancer-derived exosomes. J Proteome. 2013;80:171–82.CrossRef
131.
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.PubMedCrossRef
132.
Melo SA, Sugimoto H, O'Connell JT, Kato N, Villanueva A, Vidal A, Qiu L, Vitkin E, Perelman LT, Melo CA, et al. Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis. Cancer Cell. 2014;26:707–21.PubMedPubMedCentralCrossRef
133.
Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, Hergueta-Redondo M, Williams C, Garcia-Santos G, Ghajar C, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med. 2012;18:883–91.PubMedPubMedCentralCrossRef
134.
Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, Perdicchio M, Marino ML, Federici C, Iessi E, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One. 2009;4:e5219.PubMedPubMedCentralCrossRef
135.
136.
Belov L, Matic KJ, Hallal S, Best OG, Mulligan SP, Christopherson RI. Extensive surface protein profiles of extracellular vesicles from cancer cells may provide diagnostic signatures from blood samples. J Extracell Vesicles. 2016;5:25355.PubMedCrossRef
137.
Yamashita T, Kamada H, Kanasaki S, Maeda Y, Nagano K, Abe Y, Inoue M, Yoshioka Y, Tsutsumi Y, Katayama S, et al. Epidermal growth factor receptor localized to exosome membranes as a possible biomarker for lung cancer diagnosis. Pharmazie. 2013;68:969–73.PubMed
138.
Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, Becker A, Hoshino A, Mark MT, Molina H, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol. 2015;17:816–26.PubMedCrossRef
139.
Revenfeld AL, Baek R, Nielsen MH, Stensballe A, Varming K, Jorgensen M. Diagnostic and prognostic potential of extracellular vesicles in peripheral blood. Clin Ther. 2014;36:830–46.PubMedCrossRef
140.
Gamez-Valero A, Lozano-Ramos SI, Bancu I, Lauzurica-Valdemoros R, Borras FE. Urinary extracellular vesicles as source of biomarkers in kidney diseases. Front Immunol. 2015;6:6.PubMedPubMedCentralCrossRef
Metadata
Title
Role of exosomal proteins in cancer diagnosis
Authors
Weihua Li
Chuanyun Li
Tong Zhou
Xiuhong Liu
Xiaoni Liu
Xiuhui Li
Dexi Chen
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Molecular Cancer / Issue 1/2017
Electronic ISSN: 1476-4598
DOI
https://doi.org/10.1186/s12943-017-0706-8

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