The biodistribution and immune suppressive effects of breast cancer-derived exosomes

Cancer Research

Volumn 76, Issue 23, 2016, Pages 6816-6827

  Wen, Shu Wen ^a   Sceneay, Jaclyn ^a,f   Lima, Luize Goncalves ^a   Wong, Christina S F ^a   Becker, Melanie ^a   Krumeich, Sophie ^a   Lobb, Richard J ^a   Castillo, Vanessa ^a   Wong, Ke Ni ^a   Ellis, Sarah ^b,c   Parker, Belinda S ^d   Möller, Andreas ^a,e  

^a QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^b PETER MACCALLUM CANCER CENTRE   (Australia)

^c UNIVERSITY OF MELBOURNE   (Australia)

^d LA TROBE UNIVERSITY   (Australia)

^e UNIVERSITY OF QUEENSLAND   (Australia)

^f BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD45 ANTIGEN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; BREAST CANCER; BREAST CANCER CELL LINE; CONTROLLED STUDY; EXOSOME; FEMALE; INTERNALIZATION; LIVER METASTASIS; LUNG METASTASIS; LYMPHOCYTE PROLIFERATION; METASTASIS POTENTIAL; MOUSE; MYELOID DERIVED SUPPRESSOR CELL; NATURAL KILLER CELL MEDIATED CYTOTOXICITY; NONHUMAN; PRIORITY JOURNAL; SUPPRESSOR CELL; T LYMPHOCYTE; TISSUE DISTRIBUTION; ANIMAL; BAGG ALBINO MOUSE; BREAST TUMOR; C57BL MOUSE; CELL PROLIFERATION; HUMAN; IMMUNOLOGY; IMMUNOSUPPRESSIVE TREATMENT; METABOLISM; PATHOLOGY; PROCEDURES;

ANIMALS; BREAST NEOPLASMS; CELL PROLIFERATION; EXOSOMES; FEMALE; HUMANS; IMMUNOSUPPRESSION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL;

EID: 85002758453     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-16-0868     Document Type: Article

References (55)

1. Siegel R, Ma J, Zou Z, Jemal A. Cancer statistics, 2014. CA Cancer J Clin 2014;64:9-29.
2. Sledge GW, Mamounas EP, Hortobagyi GN, Burstein HJ, Goodwin PJ, Wolff AC. Past, present, and future challenges in breast cancer treatment. J Clin Oncol 2014;32:1979-86.
3. McAllister SS, Weinberg RA. The tumour-induced systemic environment as a critical regulator of cancer progression and metastasis. Nat Cell Biol 2014;16:717-27.
4. Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011;144:646-74.
5. Thery C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002;2:569-79.
6. 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;1820:940-8.
7. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A 2009;106:3794-9.
8. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 2008;10:619-24.
9. Ciravolo V, Huber V, Ghedini GC, Venturelli E, Bianchi F, Campiglio M, et al. Potential role of HER2-overexpressing exosomes in countering trastuzumab-based therapy. J Cell Physiol 2012;227:658-67.
10. 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.
11. Wen S, Lobb R, Möller A. Exosomes in cancer metastasis: novel targets for diagnosis and therapy? Cancer Forum, Cancer Council Australia 2014;38:116-9.
12. 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.
13. Sceneay J, Parker BS, Smyth MJ, Moller A. Hypoxia-driven immunosuppression contributes to the pre-metastatic niche. Oncoimmunology 2013;2:e22355.
14. Sceneay J, Smyth MJ, Moller A. The pre-metastatic niche: finding common ground. Cancer Metastasis Rev 2013;32:449-64.
15. 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.
16. Taylor DD, Gercel-Taylor C, Lyons KS, Stanson J, Whiteside TL. T-cell apoptosis and suppression of T-cell receptor/CD3-zeta by Fas ligand-containing membrane vesicles shed from ovarian tumors. Clin Cancer Res 2003;9:5113-9.
17. Xiang X, Poliakov A, Liu C, Liu Y, Deng ZB, Wang J, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 2009;124:2621-33.
18. Bidwell BN, Slaney CY, Withana NP, Forster S, Cao Y, Loi S, et al. Silencing of Irf7 pathways in breast cancer cells promotes bone metastasis through immune escape. Nat Med 2012;18:1224-31.
19. Casey AE, Laster WRJr., Ross GL. Sustained enhanced growth of carcinoma EO771 in C57 black mice. Exp Biol Med 1951;77:358-62.
20. Moller A, House CM, Wong CS, Scanlon DB, Liu MC, Ronai Z, et al. Inhibition of Siah ubiquitin ligase function. Oncogene 2009;28:289-96.
21. Pulaski BA, Ostrand-Rosenberg S. Mouse 4T1 breast tumor model. Current protocols in immunology/edited by John E Coligan [et al] 2001;Chapter 20:Unit202.
22. Sceneay J, Liu MC, Chen A, Wong CS, Bowtell DD, Moller A. The antioxidant N-acetylcysteine prevents HIF-1 stabilization under hypoxia in vitro but does not affect tumorigenesis in multiple breast cancer models in vivo. PloS ONE 2013;8:e66388.
23. Lobb RJ, Becker M, Wen SW, Wong CS, Wiegmans AP, Leimgruber A, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracellular Vesicles 2015;4:27031.
24. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015;527:329-35.
25. Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol Cell Proteomics 2010;9:197-208.
26. de Vrij J, Maas SL, van Nispen M, Sena-Esteves M, Limpens RW, Koster AJ, et al. Quantification of nanosized extracellular membrane vesicles with scanning ion occlusion sensing. Nanomedicine 2013;8:1443-58.
27. Roberts GS, Kozak D, Anderson W, Broom MF, Vogel R, Trau M. Tunable nano/micropores for particle detection and discrimination: scanning ion occlusion spectroscopy. Small 2010;6:2653-8.
28. Lyons AB, Parish CR. Determination of lymphocyte division by flow cytometry. J Immunol Methods 1994;171:131-7.
29. Chan CJ, Andrews DM, McLaughlin NM, Yagita H, Gilfillan S, Colonna M, et al. DNAM-1/CD155 interactions promote cytokine and NK cell-mediated suppression of poorly immunogenic melanoma metastases. J Immunol 2010;184:902-11.
30. Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, et al. Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res 2012;72:3906-11.
31. Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PloS One 2009;4:e5219.
32. Taylor DD, Lyons KS, Gercel-Taylor C. Shed membrane fragment-associated markers for endometrial and ovarian cancers. Gynecol Oncol 2002;84:443-8.
33. Raber PL, Thevenot P, Sierra R, Wyczechowska D, Halle D, Ramirez ME, et al. Subpopulations of myeloid-derived suppressor cells impair T cell responses through independent nitric oxide-related pathways. Int J Cancer 2014;134:2853-64.
34. Talmadge JE, Gabrilovich DI. History of myeloid-derived suppressor cells. Nat Rev Cancer 2013;13:739-52.
35. Gupta GP, Massague J. Cancer metastasis: building a framework. Cell 2006;127:679-95.
36. Hoshino A, Costa-Silva B, Shen TL, Rodrigues G, Hashimoto A, Tesic Mark M, et al. Tumour exosome integrins determine organotropic metastasis. Nature 2015;527:329-35.
37. Wiklander OP, Nordin JZ, O'Loughlin A, Gustafsson Y, Corso G, Mager I, et al. Extracellular vesicle in vivo biodistribution is determined by cell source, route of administration and targeting. J Extracellular Vesicles 2015;4:26316.
38. Sun D, Zhuang X, Xiang X, Liu Y, Zhang S, Liu C, et al. A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes. Mol Ther 2010;18:1606-14.
39. Zhuang X, Xiang X, Grizzle W, Sun D, Zhang S, Axtell RC, et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol Ther 2011;19:1769-79.
40. Kim R, Emi M, Tanabe K. Cancer immunoediting from immune surveillance to immune escape. Immunology 2007;121:1-14.
41. Mallegol J, Van Niel G, Lebreton C, Lepelletier Y, Candalh C, Dugave C, et al. T84-intestinal epithelial exosomes bear MHC class II/peptide complexes potentiating antigen presentation by dendritic cells. Gastroenterology 2007;132:1866-76.
42. Rana S, Yue S, Stadel D, Zoller M. Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol 2012;44:1574-84.
43. Segura E, Guerin C, Hogg N, Amigorena S, Thery C. CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo. J Immunol 2007;179:1489-96.
44. Isin M, Uysaler E, Ozgur E, Koseoglu H, Sanli O, Yucel OB, et al. Exosomal lncRNA-p21 levels may help to distinguish prostate cancer from benign disease. Front Genet 2015;6:168.
45. Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008;10:1470-6.
46. Taylor DD, Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008;110:13-21.
47. Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, Bronte V, Mandruzzato S. Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J Immunother 2012;35:107-15.
48. Chafe SC, Lou Y, Sceneay J, Vallejo M, Hamilton MJ, McDonald PC, et al. Carbonic anhydrase IX promotes myeloid-derived suppressor cell mobilization and establishment of a metastatic niche by stimulating G-CSF production. Cancer Res 2015;75:996-1008.
49. Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest 2010;120:457-71.
50. Liu Y, Xiang X, Zhuang X, Zhang S, Liu C, Cheng Z, et al. Contribution of MyD88 to the tumor exosome-mediated induction of myeloid derived suppressor cells. Am J Pathol 2010;176:2490-9.
51. Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res 2006;66:9290-8.
52. Jiang Y, Li Y, Zhu B. T-cell exhaustion in the tumor microenvironment. Cell Death Dis 2015;6:e1792.
53. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002;195:1303-16.
54. Wieckowski EU, Visus C, Szajnik M, Szczepanski MJ, Storkus WJ, Whiteside TL. Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 2009;183:3720-30.
55. Ichim TE, Zhong Z, Kaushal S, Zheng X, Ren X, Hao X, et al. Exosomes as a tumor immune escape mechanism: possible therapeutic implications. J Translat Med 2008;6:37.