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http://dx.doi.org/10.5483/BMBRep.2016.49.1.239

Emerging roles of exosomes in cancer invasion and metastasis  

Soung, Young Hwa (Department of Pathology, Stony Brook Medicine)
Nguyen, Thalia (Department of Physiology, University of Oklahoma Health Sciences Center)
Cao, Hans (Department of Physiology, University of Oklahoma Health Sciences Center)
Lee, Janet (Department of Physiology, University of Oklahoma Health Sciences Center)
Chung, Jun (Department of Pathology, Stony Brook Medicine)
Publication Information
BMB Reports / v.49, no.1, 2016 , pp. 18-25 More about this Journal
Abstract
Recent evidence has indicated that nano-sized vesicles called "exosomes" mediate the interaction between cancer cells and their microenvironment and play a critical role in the development of cancers. Exosomes contain cargo consisting of proteins, lipids, mRNAs, and microRNAs that can be delivered to different types of cells in nascent as well as distant locations. Cancer cell-derived exosomes (CCEs) have been identified in body fluids such as urine, plasma, and saliva from patients with cancer. Although their content depends on tumor type and stage, CCEs merit consideration as prognostic and diagnostic markers, as vehicles for drug delivery, and as potential therapeutic targets because they could transport various oncogenic elements. In this review, we summarize recent advances regarding the role of CCEs in cancer invasion and metastasis, as well as its potential clinical applications. [BMB Reports 2016; 49(1): 18-25]
Keywords
Exosomes; Invasion; Metastasis; Drug resistance; Biomarkers; Therapeutic application;
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1 Pitt JM, Charrier M, Viaud S et al (2014) Dendritic cell-derived exosomes as immunotherapies in the fight against cancer. J Immunol 193, 1006-1011   DOI
2 Chalmin F, Ladoire S, Mignot G et al (2010) Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 120, 457-471
3 Ohno S, Takanashi M, Sudo K et al (2013) Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells. Mol Ther 21, 185-191   DOI
4 Sun D, Zhuang X, Xiang X et al (2010) A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 18, 1606-1614   DOI
5 Escudier B, Dorval T, Chaput N et al (2005) Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 3, 10   DOI
6 Tian Y, Li S, Song J et al (2014) A doxorubicin delivery platform using engineered natural membrane vesicle exosomes for targeted tumor therapy. Biomaterials 35, 2383-2390   DOI
7 Skog J, Würdinger T, van Rijn S et al (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10, 1470-1476   DOI
8 Wang D and DuBois RN (2010) Eicosanoids and cancer. Nat Rev Cancer 10, 181-193   DOI
9 Esser J, Gehrmann U, D’Alexandri FL et al (2010) Exosomes from human macrophages and dendritic cells contain enzymes for leukotriene biosynthesis and promote granulocyte migration. J Allergy Clin Immunol 126, 1032-1040   DOI
10 Aung T, Chapuy B, Vogel D et al (2011) Exosomal evasion of humoral immunotherapy in aggressive B-cell lymphoma modulated by ATP-binding cassette transporter A3. Proc Natl Acad Sci U S A 108, 15336-15341   DOI
11 Silva J, Garcia V, Rodriguez M et al (2012) Analysis of exosome release and its prognostic value in human colorectal cancer. Genes Chromosomes Cancer 51, 409-418   DOI
12 He M, Qin H, Poon TCW et al (2015) Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs. Carcinogenesis 36, 1008-18   DOI
13 Rodríguez M, Silva J, Herrera A et al (2015) Exosomes enriched in stemness/metastatic-related mRNAS promote oncogenic potential in breast cancer. Oncotarget 6, 40575-40587   DOI
14 Merino AM, Hoogduijn MJ, Borras FE and Franquesa M (2014) Therapeutic potential of extracellular vesicles. Front Immunol 5, 658   DOI
15 Sahu R, Kaushik S, Clement CC et al (2011) Microautophagy of cytosolic proteins by late endosomes. Dev Cell 20, 131-139   DOI
16 Savina A, Furlán M, Vidal M, Colombo MI (2003) Exosome Release Is Regulated by a Calcium-dependent Mechanism in K562 Cells. J Biol Chem 278, 20083-20090   DOI
17 Record M, Carayon K, Poirot M and Silvente-Poirot S (2014) Exosomes as new vesicular lipid transporters involved in cell-cell communication and various pathophysiologies. Biochim Biophys Acta 184, 108-120   DOI
18 Laulagnier K, Grand D, Dujardin A et al (2004) PLD2 is enriched on exosomes and its activity is correlated to the release of exosomes. FEBS Lett 572, 11-14   DOI
19 Dikic I (2004) ALIX-ing phospholipids with endosome biogenesis. BioEssays 26, 604-607   DOI
20 Matsuo H, Chevallier J, Mayran N et al (2004) Role of LBPA and Alix in Multivesicular Liposome Formation and Endosome Organization. Science 303, 531-534   DOI
21 Trajkovic K, Hsu C, Chiantia S et al (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247   DOI
22 Strauss K, Goebel C, Runz H et al (2010) Exosome Secretion Ameliorates Lysosomal Storage of Cholesterol in Niemann-Pick Type C Disease. J Biol Chem 285, 26279-26288   DOI
23 Ikonen E (2001) Roles of lipid rafts in membrane transport. Curr Opin Cell Biol 13, 470-477   DOI
24 Tan SS, Yin Y, Lee T et al (2013) Therapeutic MSC exosomes are derived from lipid raft microdomains in the plasma membrane. J Extracell Vesicles 2, 22614   DOI
25 Ogata-Kawata H, Izumiya M, Kurioka D et al (2014) Circulating Exosomal microRNAs as Biomarkers of Colon Cancer. PLoS One 9, e92921   DOI
26 Llorente A, Skotland T, Sylvänne T et al (2013) Molecular lipidomics of exosomes released by PC-3 prostate cancer cells. Biochim Biophys Acta 1831, 1302-1309   DOI
27 Lydic TA, Townsend S, Adda CG et al (2015) Rapid and comprehensive “shotgun” lipidome profiling of colorectal cancer cell derived exosomes. Methods 4, 014
28 Ohshima K, Inoue K, Fujiwara A et al (2010) Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PloS One 5, e13247   DOI
29 Anastasiadou E and Slack FJ (2014) Malicious exosomes. Science 346, 1459-1460   DOI
30 Madhavan B, Yue S, Galli U et al (2015) Combined evaluation of a panel of protein and miRNA serum-exosome biomarkers for pancreatic cancer diagnosis increases sensitivity and specificity. Int J Cancer 136, 2616-2627   DOI
31 Taylor DD and Gercel-Taylor C (2008) MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110, 13-21   DOI
32 Yang M, Chen J, Su F et al (2011) Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 10, 117   DOI
33 Wang M, Zhao C, Shi H et al (2014) Deregulated micro-RNAs in gastric cancer tissue-derived mesenchymal stem cells: novel biomarkers and a mechanism for gastric cancer. Br J Cancer 110, 1199-1210   DOI
34 Sidhu SS, Mengistab AT, Tauscher AN, LaVail J and Basbaum C (2004) The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 23, 956-963   DOI
35 Fabbri M, Paone A, Calore F et al (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 109, E2110-2116   DOI
36 Umezu T, Ohyashiki K, Kuroda M and Ohyashiki JH (2013) Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 32, 2747-2755   DOI
37 Zhou W, Fong MY, Min Y et al (2014) Cancer-Secreted miR-105 Destroys Vascular Endothelial Barriers to Promote Metastasis. Cancer Cell 25, 501-515   DOI
38 Théry C, Ostrowski M and Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9, 581-593   DOI
39 Luga V and Wrana JL (2013) Tumor-stroma interaction: Revealing fibroblast-secreted exosomes as potent regulators of Wnt-planar cell polarity signaling in cancer metastasis. Cancer Res 73, 6843-6847   DOI
40 Huber V, Fais S, Iero M et al (2005) Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 128, 1796-1804.   DOI
41 Klibi J, Niki T, Riedel A et al (2009) Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 113, 1957-1966   DOI
42 Wolfers J, Lozier A, Raposo G et al (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7, 297-303   DOI
43 Wieckowski EU, Visus C, Szajnik M, Szczepanski MJ, Storkus WJ and Whiteside TL (2009) Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 183, 3720-3730   DOI
44 Andre F, Schartz NEC, Movassagh M et al (2002) Malignant effusions and immunogenic tumour-derived exosomes. Lancet 360, 295-305   DOI
45 Andreola G, Rivoltini L, Castelli C et al (2002) Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 195, 1303-1316   DOI
46 Xiang X, Poliakov A, Liu C et al (2009) Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 124, 2621-2633   DOI
47 Hoshino A, Costa-Silva B, Shen T-L et al (2015) Tumour exosome integrins determine organotropic metastasis. Nature 28, 15756
48 Théry C, Boussac M, Véron P et al (2001) Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol Baltim Md 166, 7309-7318.
49 Blanchard N, Lankar D, Faure F et al (2002) TCR activation of human T cells induces the production of exosomes bearing the TCR/CD3/zeta complex. J Immunol Baltim Md 168, 3235-3241
50 Montecalvo A, Larregina AT, Shufesky WJ et al (2012) Mechanism of transfer of functional microRNAs between mouse dendritic cells via exosomes. Blood 119, 756-766   DOI
51 Kahlert C and Kalluri R (2013) Exosomes in tumor microenvironment influence cancer progression and metastasis. J Mol Med 91, 431-437   DOI
52 Peinado H, Alečković M, Lavotshkin S et al (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18, 883-891   DOI
53 Al-Nedawi K, Meehan B, Micallef J et al (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10, 619-624   DOI
54 Demory Beckler M, Higginbotham JN, Franklin JL et al (2013) Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS. Mol Cell Proteomics 12, 343-355   DOI
55 Corcoran C, Rani S, O’Brien K et al (2012) Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes. PloS One 7, e50999   DOI
56 Hood JL, San RS and Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71, 3792-3801   DOI
57 Robbins PD and Morelli AE (2014) Regulation of immune responses by extracellular vesicles. Nat Rev Immunol 14, 195-208   DOI
58 Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ and Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9, 654-659   DOI
59 Milane L, Singh A, Mattheolabakis G, Suresh M and Amiji MM (2015) Exosome mediated communication within the tumor microenvironment. J Control Release 219, 278-294   DOI
60 Théry C, Zitvogel L and Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2, 569-579
61 Edidin M (2001) Shrinking patches and slippery rafts: scales of domains in the plasma membrane. Trends Cell Biol 11, 492-496   DOI
62 Hanson PI and Cashikar A (2012) Multivesicular body morphogenesis. Annu Rev Cell Dev Biol 28, 337-362   DOI
63 Stuffers S, Sem Wegner C, Stenmark H, Brech A (2009) Multivesicular Endosome Biogenesis in the Absence of ESCRTs. Traffic 10, 925-937   DOI
64 Hemler ME (2001) Specific tetraspanin functions. J Cell Biol 155, 1103-1107   DOI
65 Pant S, Hilton H and Burczynski ME (2012) The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem Pharmacol 83, 1484-1494   DOI
66 King HW, Michael MZ and Gleadle JM (2012) Hypoxic enhancement of exosome release by breast cancer cells. BMC Cancer 12, 421   DOI
67 Nazarenko I, Rana S, Baumann A et al (2010) Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70, 1668-1678   DOI
68 Vlassov AV, Magdaleno S, Setterquist R and Conrad R (2012) Exosomes: Current knowledge of their composition, biological functions, and diagnostic and therapeutic potentials. Biochim Biophys Acta 1820, 940-948   DOI
69 Raposo G and Stoorvogel W (2013) Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 200, 373-383   DOI
70 EL Andaloussi S, Mäger I, Breakefield XO and Wood MJ (2013) Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Discov 12, 347-357   DOI
71 Kharaziha P, Ceder S, Li Q and Panaretakis T (2012) Tumor cell-derived exosomes: A message in a bottle. Biochim Biophys Acta 1826, 103-111
72 Johnstone RM, Adam M, Hammond JR, Orr L and Turbide C (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 262, 9412-9420