Novel insights into exosome-induced, tumor-associated inflammation and immunomodulation

Seminars in Cancer Biology

Volumn 28, Issue , 2014, Pages 51-57

  Altevogt, Peter ^a   Bretz, Niko P ^a   Ridinger, Johannes ^a,b   Utikal, Jochen ^a,b   Umansky, Viktor ^a,b  

^a GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Chemokines; Cytokines; Exosome signaling; Myeloid derived suppressor cells

Indexed keywords

INTERLEUKIN 1BETA; INTERLEUKIN 23P19; INTERLEUKIN 6; INTERLEUKIN 8; MYELOID DIFFERENTIATION FACTOR 88; RANTES; STAT3 PROTEIN; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 7; TOLL LIKE RECEPTOR 8; TUMOR ANTIGEN; TUMOR NECROSIS FACTOR ALPHA; CYTOKINE;

BONE MARROW CELL; BREAST CANCER; CANCER GROWTH; CANCER PATIENT; CELL ACTIVITY; COLORECTAL CANCER; CYTOKINE PRODUCTION; CYTOKINE RELEASE; DOWN REGULATION; EXOSOME; GLIOBLASTOMA; HEAD AND NECK CANCER; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; IMMUNOSTIMULATION; MELANOMA; MONOCYTE; NATURAL KILLER CELL; NON SMALL CELL LUNG CANCER; NONHUMAN; PHASE 3 CLINICAL TRIAL (TOPIC); PHASE 4 CLINICAL TRIAL (TOPIC); PHENOTYPE; PROTEIN EXPRESSION; REVIEW; STOMACH CANCER; T LYMPHOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; IMMUNOLOGY; INFLAMMATION; NEOPLASM;

ANIMALS; CYTOKINES; EXOSOMES; HUMANS; IMMUNOMODULATION; INFLAMMATION; NEOPLASMS;

EID: 84926247911     PISSN: 1044579X     EISSN: 10963650     Source Type: Journal    
DOI: 10.1016/j.semcancer.2014.04.008     Document Type: Review

References (94)

1. Crescitelli R., Lasser C., Szabo T.G., Kittel A., Eldh M., Dianzani I., et al. Distinct RNA profiles in subpopulations of extracellular vesicles: apoptotic bodies, microvesicles and exosomes. J Extracell Vesicles 2013, 2.
2. Witwer K.W., Buzas E.I., Bemis L.T., Bora A., Lasser C., Lotvall J., et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles 2013, 2.
3. Wickman G., Julian L., Olson M.F. How apoptotic cells aid in the removal of their own cold dead bodies. Cell Death Differ 2012, 19:735-742.
4. Thery C., Zitvogel L., Amigorena S. Exosomes: composition, biogenesis and function. Nat Rev Immunol 2002, 2:569-579.
5. Andre F., Schartz N.E., Movassagh M., Flament C., Pautier P., Morice P., et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002, 360:295-305.
6. Hendrix A., Westbroek W., Bracke M., Wever O.D. An ex(o)citing machinery for invasive tumor growth. Cancer Res 2010, 70:9533-9537.
7. Ginestra A., La Placa M.D., Saladino F., Cassara D., Nagase H., Vittorelli M.L. The amount and proteolytic content of vesicles shed by human cancer cell lines correlates with their in vitro invasiveness. Anticancer Res 1998, 18:3433-3437.
8. Keller S., Sanderson M.P., Stoeck A., Altevogt P. Exosomes: from biogenesis and secretion to biological function. Immunol Lett 2006, 107:102-108.
9. Valadi H., Ekstrom K., Bossios A., Sjostrand M., Lee J.J., Lotvall J.O. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
10. Lotvall J., Valadi H. Cell to cell signalling via exosomes through esRNA. Cell Adhes Migr 2007, 1:156-158.
11. Gutierrez-Vazquez C., Villarroya-Beltri C., Mittelbrunn M., Sanchez-Madrid F. Transfer of extracellular vesicles during immune cell-cell interactions. Immunol Rev 2013, 251:125-142.
12. Fruhbeis C., Frohlich D., Kuo W.P., Amphornrat J., Thilemann S., Saab A.S., et al. Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol 2013, 11:e1001604.
13. Luga V., Zhang L., Viloria-Petit A.M., Ogunjimi A.A., Inanlou M.R., Chiu E., et al. Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 2012, 151:1542-1556.
14. Webber J.P., Spary L.K., Sanders A.J., Chowdhury R., Jiang W.G., Steadman R., et al. Differentiation of tumour-promoting stromal myofibroblasts by cancer exosomes. Oncogene 2014, 10.1038/onc.2013.560.
15. Li J., Liu K., Liu Y., Xu Y., Zhang F., Yang H., et al. Exosomes mediate the cell-to-cell transmission of IFN-alpha-induced antiviral activity. Nat Immunol 2013, 14:793-803.
16. 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.
17. Dai S., Wan T., Wang B., Zhou X., Xiu F., Chen T., et al. More efficient induction of HLA-A*0201-restricted and carcinoembryonic antigen (CEA)-specific CTL response by immunization with exosomes prepared from heat-stressed CEA-positive tumor cells. Clin Cancer Res 2005, 11:7554-7563.
18. 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.
19. Hsu D.H., Paz P., Villaflor G., Rivas A., Mehta-Damani A., Angevin E., et al. Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides. J Immunother 2003, 26:440-450.
20. Whiteside T.L. Tumour-derived exosomes or microvesicles: another mechanism of tumour escape from the host immune system. Br J Cancer 2005, 92:209-211.
21. Valenti R., Huber V., Iero M., Filipazzi P., Parmiani G., Rivoltini L. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007, 67:2912-2915.
22. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009, 9:581-593.
23. Zhang H.G., Grizzle W.E. Exosomes and cancer: a newly described pathway of immune suppression. Clin Cancer Res 2011, 17:959-964.
24. Clayton A. Cancer cells use exosomes as tools to manipulate immunity and the microenvironment. Oncoimmunology 2012, 1:78-80.
25. Filipazzi P., Burdek M., Villa A., Rivoltini L., Huber V. Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin Cancer Biol 2012, 22:342-349.
26. Chalmin F., Ladoire S., Mignot G., Vincent J., Bruchard M., Remy-Martin J.P., 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, 120:457-471.
27. Xiang X., Liu Y., Zhuang X., Zhang S., Michalek S., Taylor D.D., et al. TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. Am J Pathol 2010, 177:1606-1610.
28. Bretz N.P., Ridinger J., Rupp A.K., Rimbach K., Keller S., Rupp C., et al. Body fluid exosomes promote secretion of inflammatory cytokines in monocytic cells via toll-like receptor signaling. J Biol Chem 2013, 288:36691-36702.
29. Zhang B., Yin Y., Lai R.C., Tan S.S., Choo A.B., Lim S.K. Mesenchymal stem cell secretes immunologically active exosomes. Stem Cells Dev 2014, [Epub ahead of print].
30. Danesh A., Inglis H.C., Jackman R.P., Wu S., Deng X., Muench M.O., et al. Exosomes from RBC units bind to monocytes and induce pro-inflammatory cytokines, boosting T cell responses in vitro. Blood 2014, 123:687-696.
31. Nazarenko I., Rupp A.K., Altevogt P. Exosomes as a potential tool for a specific delivery of functional molecules. Methods Mol Biol 2013, 1049:495-511.
32. Runz S., Keller S., Rupp C., Stoeck A., Issa Y., Koensgen D., et al. Malignant ascites-derived exosomes of ovarian carcinoma patients contain CD24 and EpCAM. Gynecol Oncol 2007, 107:563-571.
33. Keller S., Konig A.K., Marme F., Runz S., Wolterink S., Koensgen D., et al. Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett 2009, 278:73-81.
34. Keller S., Ridinger J., Rupp A.K., Janssen J.W., Altevogt P. Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 2011, 9:86.
35. Rupp A.K., Rupp C., Keller S., Brase J.C., Ehehalt R., Fogel M., et al. Loss of EpCAM expression in breast cancer derived serum exosomes: role of proteolytic cleavage. Gynecol Oncol 2011, 122:437-446.
36. Torregrosa Paredes P., Esser J., Admyre C., Nord M., Rahman Q.K., Lukic A., et al. Bronchoalveolar lavage fluid exosomes contribute to cytokine and leukotriene production in allergic asthma. Allergy 2012, 67:911-919.
37. Gardella S., Andrei C., Ferrera D., Lotti L.V., Torrisi M.R., Bianchi M.E., et al. The nuclear protein HMGB1 is secreted by monocytes via a non-classical, vesicle-mediated secretory pathway. EMBO Rep 2002, 3:995-1001.
38. Ji H., Greening D.W., Barnes T.W., Lim J.W., Tauro B.J., Rai A., et al. Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components. Proteomics 2013, 13:1672-1686.
39. Burke M., Choksawangkarn W., Edwards N., Ostrand-Rosenberg S., Fenselau C. Exosomes from myeloid-derived suppressor cells carry biologically active proteins. J Proteome Res 2014, 13:836-843.
40. 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 USA 2012, 109:E2110-E2116.
41. Andre F., Schartz N.E., Chaput N., Flament C., Raposo G., Amigorena S., et al. Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine 2002, 20(Suppl. 4):A28-A31.
42. Zeelenberg I.S., Ostrowski M., Krumeich S., Bobrie A., Jancic C., Boissonnas A., et al. Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res 2008, 68:1228-1235.
43. Chaput N., Flament C., Viaud S., Taieb J., Roux S., Spatz A., et al. Dendritic cell derived-exosomes: biology and clinical implementations. J Leukocyte Biol 2006, 80:471-478.
44. Viaud S., Thery C., Ploix S., Tursz T., Lapierre V., Lantz O., et al. Dendritic cell-derived exosomes for cancer immunotherapy: what's next. Cancer Res 2010, 70:1281-1285.
45. 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.
46. Azmi A.S., Bao B., Sarkar F.H. Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review. Cancer Metastasis Rev 2013, 32:623-642.
47. 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, 66:9290-9298.
48. Gabrilovich D.I., Ostrand-Rosenberg S., Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012, 12:253-268.
49. Ostrand-Rosenberg S. Immune surveillance: a balance between protumor and antitumor immunity. Curr Opin Genet Dev 2008, 18:11-18.
50. Peranzoni E., Zilio S., Marigo I., Dolcetti L., Zanovello P., Mandruzzato S., et al. Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 2010, 22:238-244.
51. Brandau S., Moses K., Lang S. The kinship of neutrophils and granulocytic myeloid-derived suppressor cells in cancer: cousins, siblings or twins. Semin Cancer Biol 2013, 23:171-182.
52. Umansky V., Sevko A. Melanoma-induced immunosuppression and its neutralization. Semin Cancer Biol 2012, 22:319-326.
53. Youn J.I., Nagaraj S., Collazo M., Gabrilovich D.I. Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 2008, 181:5791-5802.
54. Filipazzi P., Huber V., Rivoltini L. Phenotype, function and clinical implications of myeloid-derived suppressor cells in cancer patients. Cancer Immunol Immunother 2012, 61:255-263.
55. Poschke I., Kiessling R. On the armament and appearances of human myeloid-derived suppressor cells. Clin Immunol 2012, 144:250-268.
56. Baniyash M. Chronic inflammation, immunosuppression and cancer: new insights and outlook. Semin Cancer Biol 2006, 16:80-88.
57. Wu L., Yan C., Czader M., Foreman O., Blum J.S., Kapur R., et al. Inhibition of PPARgamma in myeloid-lineage cells induces systemic inflammation, immunosuppression, and tumorigenesis. Blood 2012, 119:115-126.
58. Condamine T., Gabrilovich D.I. Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 2011, 32:19-25.
59. Lu T., Gabrilovich D.I. Molecular pathways: tumor-infiltrating myeloid cells and reactive oxygen species in regulation of tumor microenvironment. Clin Cancer Res 2012, 18:4877-4882.
60. Nagaraj S., Schrum A.G., Cho H.I., Celis E., Gabrilovich D.I. Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J Immunol 2010, 184:3106-3116.
61. Bronte V., Zanovello P. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 2005, 5:641-654.
62. Li H., Han Y., Guo Q., Zhang M., Cao X. Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-beta 1. J Immunol 2009, 182:240-249.
63. Ostrand-Rosenberg S., Sinha P. Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 2009, 182:4499-4506.
64. Serafini P., Mgebroff S., Noonan K., Borrello I. Myeloid-derived suppressor cells promote cross-tolerance in B-cell lymphoma by expanding regulatory T cells. Cancer Res 2008, 68:5439-5449.
65. Pan P.Y., Ma G., Weber K.J., Ozao-Choy J., Wang G., Yin B., et al. Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer. Cancer Res 2010, 70:99-108.
66. Qu P., Yan C., Du H. Matrix metalloproteinase 12 overexpression in myeloid lineage cells plays a key role in modulating myelopoiesis, immune suppression, and lung tumorigenesis. Blood 2011, 117:4476-4489.
67. Tartour E., Pere H., Maillere B., Terme M., Merillon N., Taieb J., et al. Angiogenesis and immunity: a bidirectional link potentially relevant for the monitoring of antiangiogenic therapy and the development of novel therapeutic combination with immunotherapy. Cancer Metastasis Rev 2011, 30:83-95.
68. Meyer C., Sevko A., Ramacher M., Bazhin A.V., Falk C.S., Osen W., et al. Chronic inflammation promotes myeloid-derived suppressor cell activation blocking antitumor immunity in transgenic mouse melanoma model. Proc Natl Acad Sci USA 2011, 108:17111-17116.
69. Sade-Feldman M., Kanterman J., Ish-Shalom E., Elnekave M., Horwitz E., Baniyash M. Tumor necrosis factor-alpha blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity 2013, 38:541-554.
70. Mantovani A. Molecular pathways linking inflammation and cancer. Curr Mol Med 2010, 10:369-373.
71. Grivennikov S.I., Greten F.R., Karin M. Immunity, inflammation, and cancer. Cell 2010, 140:883-899.
72. Coussens L.M., Zitvogel L., Palucka A.K. Neutralizing tumor-promoting chronic inflammation: a magic bullet. Science 2013, 339:286-291.
73. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 2012, 22:33-40.
74. Allavena P., Germano G., Marchesi F., Mantovani A. Chemokines in cancer related inflammation. Exp Cell Res 2011, 317:664-673.
75. Joyce J.A., Pollard J.W. Microenvironmental regulation of metastasis. Nat Rev Cancer 2009, 9:239-252.
76. Bunt S.K., Yang L., Sinha P., Clements V.K., Leips J., Ostrand-Rosenberg S. Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res 2007, 67:10019-10026.
77. Haverkamp J.M., Crist S.A., Elzey B.D., Cimen C., Ratliff T.L. In vivo suppressive function of myeloid-derived suppressor cells is limited to the inflammatory site. Eur J Immunol 2011, 41:749-759.
78. Sevko A., Sade-Feldman M., Kanterman J., Michels T., Falk C.S., Umansky L., et al. Cyclophosphamide promotes chronic inflammation-dependent immunosuppression and prevents antitumor response in melanoma. J Investig Dermatol 2013, 133:1610-1619.
79. Mikyskova R., Indrova M., Pollakova V., Bieblova J., Simova J., Reinis M. Cyclophosphamide-induced myeloid-derived suppressor cell population is immunosuppressive but not identical to myeloid-derived suppressor cells induced by growing TC-1 tumors. J Immunother 2012, 35:374-384.
80. Chornoguz O., Grmai L., Sinha P., Artemenko K.A., Zubarev R.A., Ostrand-Rosenberg S. Proteomic pathway analysis reveals inflammation increases myeloid-derived suppressor cell resistance to apoptosis. Mol Cell Proteomics 2011, 10. M110.002980.
81. Taylor D.D., Gercel-Taylor C. Exosomes/microvesicles: mediators of cancer-associated immunosuppressive microenvironments. Semin Immunopathol 2011, 33:441-454.
82. Sheng H., Hassanali S., Nugent C., Wen L., Hamilton-Williams E., Dias P., et al. Insulinoma-released exosomes or microparticles are immunostimulatory and can activate autoreactive T cells spontaneously developed in nonobese diabetic mice. J Immunol 2011, 187:1591-1600.
83. Kato M., Takahashi M., Akhand A.A., Liu W., Dai Y., Shimizu S., et al. Transgenic mouse model for skin malignant melanoma. Oncogene 1998, 17:1885-1888.
84. Umansky V., Abschuetz O., Osen W., Ramacher M., Zhao F., Kato M., et al. Melanoma-specific memory T cells are functionally active in Ret transgenic mice without macroscopic tumors. Cancer Res 2008, 68:9451-9458.
85. Rodriguez P.C., Ochoa A.C. T cell dysfunction in cancer: role of myeloid cells and tumor cells regulating amino acid availability and oxidative stress. Semin Cancer Biol 2006, 16:66-72.
86. Taylor D.D., Gercel-Taylor C., Lyons K.S., Stanson J., Whiteside T.L. 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, 9:5113-5119.
87. Klibi J., Niki T., Riedel A., Pioche-Durieu C., Souquere S., Rubinstein E., et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood 2009, 113:1957-1966.
88. Clayton A., Al-Taei S., Webber J., Mason M.D., Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 2011, 187:676-683.
89. Wieckowski E.U., Visus C., Szajnik M., Szczepanski M.J., Storkus W.J., Whiteside T.L. Tumor-derived microvesicles promote regulatory T cell expansion and induce apoptosis in tumor-reactive activated CD8+ T lymphocytes. J Immunol 2009, 183:3720-3730.
90. Szajnik M., Czystowska M., Szczepanski M.J., Mandapathil M., Whiteside T.L. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS ONE 2010, 5:e11469.
91. 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, 176:1375-1385.
92. Clayton A., Mitchell J.P., Court J., Linnane S., Mason M.D., Tabi Z. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 2008, 180:7249-7258.
93. Ashiru O., Boutet P., Fernandez-Messina L., Aguera-Gonzalez S., Skepper J.N., Vales-Gomez M., et al. Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res 2010, 70:481-489.
94. Hedlund M., Nagaeva O., Kargl D., Baranov V., Mincheva-Nilsson L. Thermal- and oxidative stress causes enhanced release of NKG2D ligand-bearing immunosuppressive exosomes in leukemia/lymphoma T and B cells. PLoS ONE 2011, 6:e16899.