The biology of cancer exosomes: Insights and new perspectives

Cancer Research

Volumn 77, Issue 23, 2017, Pages 6480-6488

  Ruivo, Carolina F ^a,d   Adem, Barbara ^a,d   Silva, Miguel ^a,b,d   Melo, Sonia A ^a,c,d  

^a UNIVERSITY OF PORTO   (Portugal)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c University of Porto   (Portugal)

^d UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

EXOSOME; HUMAN; IMMUNE RESPONSE; LIVER METASTASIS; LUNG METASTASIS; MALIGNANT NEOPLASM; NONHUMAN; ORGANELLE BIOGENESIS; PERITONEUM METASTASIS; PRIORITY JOURNAL; REVIEW; TUMOR MICROENVIRONMENT; CD4+ T LYMPHOCYTE; CELL COMMUNICATION; DENDRITIC CELL; DISEASE EXACERBATION; IMMUNOLOGY; METASTASIS; NEOPLASM; PATHOLOGY; PHYSIOLOGY;

TUMOR MARKER;

BIOMARKERS, TUMOR; CD4-POSITIVE T-LYMPHOCYTES; CELL COMMUNICATION; DENDRITIC CELLS; DISEASE PROGRESSION; EXOSOMES; HUMANS; NEOPLASM METASTASIS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 85038637162     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-17-0994     Document Type: Review

References (83)

1. Thery C. Exosomes: secreted vesicles and intercellular communications. F1000 Biol Rep 2011;3:15.
2. Kalluri R. The biology and function of exosomes in cancer. J Clin Invest 2016;126:1208–15.
3. 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.
4. Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, et al. Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 2011;46: 409–18.
5. Bahrini I, Song J-h, Diez D, Hanayama R. Neuronal exosomes facilitate synaptic pruning by up-regulating complement factors in microglia. Sci Rep 2015;5:7989.
6. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001;7:297–303.
7. Meehan K, Vella LJ. The contribution of tumour-derived exosomes to the hallmarks of cancer. Crit Rev Clin Lab Sci 2016;53:121–31.
8. Fong MY, Zhou W, Liu L, Alontaga AY, Chandra M, Ashby J, et al. Breast cancer-secreted miR-122 reprograms glucose metabolism in pre-metastatic niche to promote metastasis. Nat Cell Biol 2015;17:183–94.
9. Skog J, Wurdinger T, van Rijn S, Meijer D, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and protein that promote tumor growth and provide diagnostic biomarkers. Nat Cell Biol 2008; 10:1470–6.
10. Mu W, Rana S, Zoller € M. Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 2013;15:875–87.
11. Sung BH, Ketova T, Hoshino D, Zijlstra A, Weaver AM. Directional cell movement through tissues is controlled by exosome secretion. Nat Commun 2015;6:7164.
12. Zitvogel L, Regnault A, Lozier A, Wolfers J, Flament C, Tenza D, et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. Nat Med 1998;4:594–600.
13. Abusamra AJ, Zhong Z, Zheng X, Li M, Ichim TE, Chin JL, et al. Tumor exosomes expressing Fas ligand mediate CD8þ T-cell apoptosis. Blood Cells Mol Dis 2005;35:169–73.
14. Kamerkar S, LeBleu VS, Sugimoto H, Yang S, Ruivo CF, Melo SA, et al. Exosomes facilitate therapeutic targeting of oncogenic KRAS in pancreatic cancer. Nature 2017;546:498–503.
15. Johnstone RM, Adam M, Pan BT. The fate of the transferrin receptor during maturation of sheep reticulocytes in vitro. Can J Biochem Cell Biol 1984;62:1246–54.
16. Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014;30:255–89.
17. Ostrowski M, Carmo NB, Krumeich S, Fanget I, Raposo G, Savina A, et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 2010;12:19–30.
18. Kowal J, Arras G, Colombo M, Jouve M, Morath JP, Primdal-Bengtson B, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A 2016;113:E968–77.
19. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654–9.
20. Melo Sonia A, Sugimoto H, O'Connell Joyce T, Kato N, Villanueva A, Vidal A, et al. Cancer exosomes perform cell-independent MicroRNA biogenesis and promote tumorigenesis. Cancer Cell 2014;26:707–21.
21. Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm 2009;117:1.
22. Balaj L, Lessard R, Dai L, Cho Y-J, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011;2:180.
23. Kahlert C, Melo SA, Protopopov A, Tang J, Seth S, Koch M, 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;289:3869–75.
24. Consortium E-T, Van Deun J, Mestdagh P, Agostinis P, Akay O, Anand S, et al. EV-TRACK: transparent reporting and centralizing knowledge in extracellular vesicle research. Nat Meth 2017;14:228–32.
25. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996;183:1161–72.
26. Holling TM, Schooten E, van Den Elsen PJ. Function and regulation of MHC class II molecules in T-lymphocytes: of mice and men. Hum Immunol 2004;65:282–90.
27. VincentSchneider H, Stumptner-Cuvelette P, Lankar D, Pain S, Raposo G, Benaroch P, et al. Exosomes bearing HLADR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int Immunol 2002;14:713–22.
28. Mayordomo JI, Zorina T, Storkus WJ, Zitvogel L, Celluzzi C, Falo LD, et al. Bone marrow-derived dendritic cells pulsed with synthetic tumour peptides elicit protective and therapeutic antitumour immunity. Nat Med 1995;1:1297–302.
29. Andre F, Schartz NEC, Movassagh M, Flament C, Pautier P, Morice P, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002;360:295–305.
30. Hiltbrunner S, Larssen P, Eldh M, Martinez-Bravo M-J, Wagner AK, Karlsson MCI, et al. Exosomal cancer immunotherapy is independent of MHC molecules on exosomes. Oncotarget 2016;7:38707–17.
31. Qazi KR, Gehrmann U, Domange Jordo€ E, Karlsson MCI, Gabrielsson S. Antigen-loaded exosomes alone induce Th1-type memory through a B cell–dependent mechanism. Blood 2009;113:2673–83.
32. Escudier B, Dorval T, Chaput N, Andre F, Caby M-P, Novault S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of thefirst phase I clinical trial. J Transl Med 2005;3:10.
33. Morse MA, Garst J, Osada T, Khan S, Hobeika A, Clay TM, et al. A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer. J Transl Med 2005;3:9.
34. Dai S, Wei D, Wu Z, Zhou X, Wei X, Huang H, et al. Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer. Mol Ther 2008;16:782–90.
35. Bell BM, Kirk ID, Hiltbrunner S, Gabrielsson S, Bultema JJ. Designer exosomes as next-generation cancer immunotherapy. Nanomedicine 2016;12:163–9.
36. Liu C, Yu S, Zinn K, Wang J, Zhang L, Jia Y, et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 2006;176:1375–85.
37. Yu S, Liu C, Su K, Wang J, Liu Y, Zhang L, et al. Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol 2007;178: 6867–75.
38. Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity 2014;41:49–61.
39. Chow A, Zhou W, Liu L, Fong MY, Champer J, Van Haute D, et al. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-kB. Sci Rep 2014;4:5750.
40. Pattabiraman DR, Weinberg RA. Tackling the cancer stem cells [mdash] what challenges do they pose? Nat Rev Drug Discov 2014;13:497–512.
41. Lu P, Weaver VM, Werb Z. The extracellular matrix: a dynamic niche in cancer progression. J Cell Biol 2012;196:395–406.
42. Webber J, Steadman R, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010;70: 9621–30.
43. Kalluri R, Zeisberg M. Fibroblasts in cancer. Nat Rev Cancer 2006;6: 392–401.
44. Cho JA, Park H, Lim EH, Lee KW. Exosomes from breast cancer cells can convert adipose tissue-derived mesenchymal stem cells into myofibroblast-like cells. Int J Oncol 2012;40:130–8.
45. Baglio SR, Lagerweij T, Perez-Lanzon M, Ho XD, Leveille N, Melo SA, et al. Blocking tumor-educated MSC paracrine activity halts osteosarcoma progression. Clin Cancer Res 2017;23:3721–33.
46. Borges FT, Melo SA, Ozdemir BC, Kato N, Revuelta I, Miller CA, et al. TGF-beta1-containing exosomes from injured epithelial cells activate fibroblasts to initiate tissue regenerative responses and fibrosis. J Am Soc Nephrol 2013;24:385–92.
47. Ribeiro MF, Zhu H, Millard RW, Fan G-C. Exosomes function in pro- and anti-angiogenesis. Curr Angiogenes 2013;2:54–9.
48. Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringner M, et al. 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.
49. Luga V, Zhang L, Viloria-Petit Alicia M, Ogunjimi Abiodun A, Inanlou Mohammad R, Chiu E, et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012; 151:1542–56.
50. Boelens MC, Wu TJ, Nabet BY, Xu B, Qiu Y, Yoon T, et al. Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways. Cell 2014;159:499–513.
51. Richards KE, Zeleniak AE, Fishel ML, Wu J, Littlepage LE, Hill R. Cancer-associated fibroblast exosomes regulate survival and proliferation of pancreatic cancer cells. Oncogene 2017;36:1770–8.
52. Hanahan D, Weinberg Robert A. Hallmarks of cancer: the next generation. Cell 2011;144:646–74.
53. Hoshino D, Kirkbride KC, Costello K, Clark ES, Sinha S, Grega-Larson N, et al. Exosome secretion is enhanced by invadopodia and drives invasive behavior. Cell Rep 2013;5:1159–68.
54. McCready J, Sims JD, Chan D, Jay DG. Secretion of extracellular hsp90a via exosomes increases cancer cell motility: a role for plasminogen activation. BMC Cancer 2010;10:294.
55. Zhou W, Fong MY, Min Y, Somlo G, Liu L, Palomares MR, et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell 2014;25:501–15.
56. Deng G, Qu J, Zhang Y, Che X, Cheng Y, Fan Y, et al. Gastric cancer-derived exosomes promote peritoneal metastasis by destroying the mesothelial barrier. FEBS Lett 2017;591:2167–79.
57. Lu X, Kang Y. Organotropism of breast cancer metastasis. J Mammary Gland Biol Neoplasia 2007;12:153.
58. Hoshino A, Costa-Silva B, Shen T-L, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015;527:329–35.
59. Sceneay J, Smyth MJ, Moller € A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev 2013;32:449–64.
60. Hood JL, San RS, Wickline SA. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 2011; 71:3792–801.
61. Hu L, Wickline SA, Hood JL. Magnetic resonance imaging of melanoma exosomesinlymphnodes.MagnResonMed2014.doi:10.1002/mrm.25376.
62. Peinado H, Aleckovic M, Lavotshkin S, Matei I, Costa-Silva B, Moreno-Bueno G, et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 2012;18: 883–91.
63. Costa-Silva B, Aiello NM, Ocean AJ, Singh S, Zhang H, Thakur BK, et al. Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver. Nat Cell Biol 2015;17:816–26.
64. Zhang H, Deng T, Liu R, Bai M, Zhou L, Wang X, et al. Exosome-delivered EGFR regulates liver microenvironment to promote gastric cancer liver metastasis. Nat Commun 2017;8:15016.
65. Zomer A, Steenbeek SC, Maynard C, van Rheenen J. Studying extracellular vesicle transfer by a Cre-loxP method. Nat Protoc 2016;11:87–101.
66. Zomer A, Maynard C, Verweij Frederik J, Kamermans A, Sch€afer R, Beerling E, et al. In vivo imaging reveals extracellular vesicle-mediated phenocopy-ing of metastatic behavior. Cell 2015;161:1046–57.
67. Rahman MA, Barger JF, Lovat F, Gao M, Otterson GA, Nana-Sinkam P. Lung cancer exosomes as drivers of epithelial mesenchymal transition. Oncotarget 2016;7:54852–66.
68. Adem B, Melo SA. Animal models in exosomes research: what the future holds. In: Wang J, editor. Novel implications of exosomes in diagnosis and treatment of cancer and infectious diseases. Rijeka, Croatia: InTech; 2017.
69. Suetsugu A, Honma K, Saji S, Moriwaki H, Ochiya T, Hoffman RM. Imaging exosome transfer from breast cancer cells to stroma at metastatic sites in orthotopic nude-mouse models. Adv Drug Deliv Rev 2013;65:383–90.
70. Wiklander OPB, Nordin JZ, Loughlin A, Gustafsson Y, Corso G, M€ager I, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracell Vesicles 2015; 4:26316.
71. Yoshimura A, Kawamata M, Yoshioka Y, Katsuda T, Kikuchi H, Nagai Y, et al. Generation of a novel transgenic rat model for tracing extracellular vesicles in body fluids. Sci Rep 2016;6:31172.
72. Amano T, Furuno T, Hirashima N, Ohyama N, Nakanishi M. Dynamics of intracellular granules with CD63-GFP in rat basophilic leukemia cells. J Biochem 2001;129:739–44.
73. Yang X, Wei L, Tang C, Slack R, Montgomery E, Lippman M. KAI1 protein is down-regulated during the progression of human breast cancer. Clin Cancer Res 2000;6:3424–9.
74. Funakoshi T, Tachibana I, Hoshida Y, Kimura H, Takeda Y, Kijima T, et al. Expression of tetraspanins in human lung cancer cells: frequent downregulation of CD9 and its contribution to cell motility in small cell lung cancer. Oncogene 0000;22:674–87.
75. Radford KJ, Thorne RF, Hersey P. Regulation of tumor cell motility and migration by CD63 in a human melanoma cell line. J Immunol 1997; 158:3353.
76. Sho M, Adachi M, Taki T, Hashida H, Konishi T, Huang CL, et al. Trans-membrane 4 superfamily as a prognostic factor in pancreatic cancer. Int J Cancer 1998;79:509–16.
77. Luberto C, Hassler DF, Signorelli P, Okamoto Y, Sawai H, Boros E, et al. Inhibition of tumor necrosis factor-induced cell death in MCF7 by a novel inhibitor of neutral sphingomyelinase. J Biol Chem 2002;277:41128–39.
78. Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of MicroRNAs in living cells. J Biol Chem 2010;285:17442–52.
79. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 2012;109:E2110–6.
80. Nakamura K, Sawada K, Kinose Y, Yoshimura A, Toda A, Nakatsuka E, et al. Exosomes promote ovarian cancer cell invasion through transfer of CD44 to peritoneal mesothelial cells. Mol Cancer Res 2017;15:78.
81. Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic MicroRNAs regulate cancer cell metastasis. J Biol Chem 2013;288: 10849–59.
82. Bobrie A, Krumeich S, Reyal F, Recchi C, Moita LF, Seabra MC, et al. Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 2012;72:4920–30.
83. Schultze M. Ein heizbarer Objecttisch und seine Verwendung bei Unter-suchungen des Blutes. Archiv fur € mikroskopische Anatomie 1865;1:1–42.