Molecular pathways: Tumor-derived microvesicles and their interactions with immune cells In vivo

Clinical Cancer Research

Volumn 19, Issue 10, 2013, Pages 2598-2604

  Pucci, Ferdinando ^a   Pittet, Mikael J ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMILORIDE; ANGIOPOIETIN RECEPTOR; CANCER ANTIBODY; CELL SURFACE RECEPTOR; DIANNEXIN; EPITHELIAL CELL ADHESION MOLECULE; HEAT SHOCK PROTEIN 72; LIPID; MESSENGER RNA; MICRORNA; PROTEIN; RAB27A PROTEIN; SCATTER FACTOR RECEPTOR; SPHINGOMYELIN PHOSPHODIESTERASE INHIBITOR; STAT3 PROTEIN; STEM CELL FACTOR; TEMOZOLOMIDE; TOLL LIKE RECEPTOR 2; UNCLASSIFIED DRUG;

ANTIANGIOGENIC ACTIVITY; ANTINEOPLASTIC ACTIVITY; APOPTOSIS; ARTICLE; BIOGENESIS; BLADDER CANCER; BONE MARROW CELL; CANCER DIAGNOSIS; CANCER IMMUNIZATION; CANCER IMMUNOLOGY; CELL COMMUNICATION; CELL FATE; CELL FUNCTION; CELL INTERACTION; CELL INVASION; CELL MOTION; CELL PROLIFERATION; CELL TRANSFER; CELL VIABILITY; CIRCULATING TUMOR CELL; COLORECTAL CANCER; COLORECTAL INVASIVE CANCER; CYTOKINE RESPONSE; CYTOTOXICITY; EFFECTOR CELL; EXOSOME; GLIOBLASTOMA; HUMAN; IMMUNE RESPONSE; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IN VITRO STUDY; IN VIVO STUDY; LUNG ADENOCARCINOMA; LYMPHOCYTIC INFILTRATION; MELANOMA CELL; NATURAL KILLER CELL; NONHUMAN; OVARY CANCER; PRIORITY JOURNAL; PROSTATE CANCER; REGULATORY T LYMPHOCYTE; SURVIVAL; T LYMPHOCYTE; TUMOR DERIVED MICROVESICLE; TUMOR GROWTH; ANIMAL; BIOLOGICAL MODEL; IMMUNOLOGY; MEMBRANE MICROPARTICLE; METABOLISM; NEOPLASMS; SIGNAL TRANSDUCTION; TUMOR MICROENVIRONMENT;

ANIMALS; CELL-DERIVED MICROPARTICLES; EXOSOMES; HUMANS; MODELS, IMMUNOLOGICAL; MYELOID CELLS; NEOPLASMS; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TUMOR MICROENVIRONMENT;

EID: 84878023280     PISSN: 10780432     EISSN: 15573265     Source Type: Journal    
DOI: 10.1158/1078-0432.CCR-12-0962     Document Type: Article

References (87)

1. Swartz MA, Lund AW. Lymphatic and interstitial flow in the tumour microenvironment: linking mechanobiology with immunity. Nat Rev Cancer 2012;12:210-9.
2. Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 2009;9:581-93.
3. Simons M, Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr Opin Cell Biol 2009;21:575-81.
4. Cocucci E, Meldolesi J. Ectosomes. Curr Biol 2011;21:R940-1.
5. Hawari FI, Rouhani FN, Cui X, Yu ZX, Buckley C, Kaler M, et al. Release of full-length 55-kDa TNF receptor 1 in exosome-like vesicles: a mechanism for generation of soluble cytokine receptors. Proc Natl Acad Sci U S A 2004;101:1297-302.
6. Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JE, Gould SJ. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol 2006;172:923-35.
7. Thery C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol 2001;166:7309-18.
8. Bobrie A, Colombo M, Raposo G, Thery C. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 2011;12:1659-68.
9. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q. Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci 2012;109:4146-51.
10. Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 2012;14:677-85.
11. Wurdinger T, Gatson NN, Balaj L, Kaur B, Breakefield XO, Pegtel DM. Extracellular vesicles and their convergence with viral pathways. Adv Virol 2012;2012:767694.
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. Miyanishi M, Tada K, Koike M, Uchiyama Y, Kitamura T, Nagata S. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007;450:435-9.
14. Montecalvo A, Larregina AT, Shufesky WJ, Stolz DB, Sullivan MLG, Karlsson JM, et al. Mechanism of transfer of functional micro RNAs between mouse dendritic cells via exosomes. Blood 2012;119: 756-66.
15. Dainiak N, Sorba S. Intracellular regulation of the production and release of human erythroid-directed lymphokines. J Clin Invest 1991;87:213-20.
16. MacKenzie A, Wilson HL, Kiss-Toth E, Dower SK, North RA, Surprenant A. Rapid secretion of interleukin-1beta by microvesicle shedding. Immunity 2001;15:825-35.
17. Sidhu SS, Mengistab AT, Tauscher AN, LaVail J, Basbaum C. The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004;23:956-63.
18. Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 2009;284:34211-22.
19. Svensson KJ, Kucharzewska P, Christianson HC, Sköld S, Löfstedt T, Johansson MC, et al. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2 mediated heparinbinding EGF signaling in endothelial cells. Proc Natl Acad Sci 2011;108:13147-52.
20. Gasser O, Schifferli JA. Activated polymorphonuclear neutrophils disseminate anti-inflammatory microparticles by ectocytosis. Blood 2004;104:2543-8.
21. 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.
22. 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.
23. Nolte-'t Hoen EN, Buschow SI, Anderton SM, Stoorvogel W, Wauben MH. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 2009;113:1977-81.
24. Baj-Krzyworzeka M, Szatanek R, Weglarczyk K, Baran J, Urbanowicz B, Branski P, et al. Tumour-derived microvesicles carry several surface determinants and mRNA of tumour cells and transfer some of these determinants to monocytes. Cancer Immunol Immunother 2006;55: 808-18.
25. Putz U, Howitt J, Doan A, Goh C-P, Low L-H, Silke J, et al. The tumor suppressor PTEN is exported in exosomes and has phosphatase activity in recipient cells. Sci Signal 2012;5:ra70.
26. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and micro RNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007;9:654-9.
27. Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 2010;39: 133-44.
28. Russell TB, Skinner AM, Kurre P. Programmed vesicle transfer of green fluorescent protein from a stably transduced cell line to primary hematopoietic cells. Blood 2012;119:5330-2.
29. Skog J, Wurdinger T, Rijn Sv, Meijer DH, Gainche L, Curry WT, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008;10:1470-6.
30. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011;331:1565-70.
31. Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pages C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science 2006;313: 1960-4.
32. Curiel TJ, Coukos G, Zou L, Alvarez X, Cheng P, Mottram P, et al. Specific recruitment of regulatory T cells in ovarian carcinoma fosters immune privilege and predicts reduced survival. Nat Med 2004;10: 942-9.
33. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010;141:39-51.
34. Albanese J, Meterissian S, Kontogiannea M, Dubreuil C, Hand A, Sorba S, et al. Biologically active Fas antigen and its cognate ligand are expressed on plasma membrane-derived extracellular vesicles. Blood 1998;91:3862-74.
35. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, et al. Induction of lymphocyte apoptosis by tumor cell secretion of Fas Lbearing microvesicles. J Exp Med 2002;195:1303-16.
36. Kim JW, Wieckowski E, Taylor DD, Reichert TE, Watkins S, Whiteside TL. Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes. Clin Cancer Res 2005;11:1010-20.
37. Abusamra AJ, Zhong Z, Zheng X, Li M, Ichim TE, Chin JL, et al. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis 2005;35:169-73.
38. Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 2005;128:1796-804.
39. Taylor DD, Akyol S, Gercel-Taylor C. Pregnancy-associated exosomes and their modulation of T cell signaling. J Immunol 2006;176:1534-42.
40. Clayton A, Tabi Z. Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis 2005;34:206-13.
41. Liu C, Yu S, Zinn K, Wang J, Zhang L, Jia Y, et al. Murine mammary carcinoma exosomes promote tumor growth by suppression of NKcell function. J Immunol 2006;176:1375-85.
42. 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.
43. 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.
44. 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.
45. 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.
46. Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M, Whiteside TL. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS One 2010;5:e11469.
47. Wang GJ, Liu Y, Qin A, Shah SV, Deng ZB, Xiang X, et al. Thymus exosomes-like particles induce regulatory T cells. J Immunol 2008; 181:5242-8.
48. Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z. Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 2011;187:676-83.
49. Hakulinen J, Sankkila L, Sugiyama N, Lehti K, Keski-Oja J. Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes. J Cell Biochem 2008;105:1211-8.
50. 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.
51. Webber J, Steadman R, Mason MD, Tabi Z, Clayton A. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res 2010;70:9621-30.
52. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRv III by microvesicles derived from tumour cells. Nat Cell Biol 2008;10:619-24.
53. 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;22:342-9.
54. Shedden K, Xie XT, Chandaroy P, Chang YT, Rosania GR. Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 2003;63: 4331-7.
55. Sverdlov ED. Amedeo Avogadro's cry: what is 1 microg of exosomes? Bioessays 2012;34:873-5.
56. Weissleder R, Pittet MJ. Imaging in the era of molecular oncology. Nature 2008;452:580-9.
57. 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 2012. [Epub ahead of print].
58. 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.
59. Mazzieri R, Pucci F, Moi D, Zonari E, Ranghetti A, Berti A, et al. Targeting the ANG2/TIE2 axis inhibits tumor growth and metastasis by impairing angiogenesis and disabling rebounds of proangiogenic myeloid cells. Cancer Cell 2011;19:512-26.
60. Boccaccio C, Comoglio PM. Invasive growth: a MET-driven genetic programme for cancer and stem cells. Nat Rev Cancer 2006;6: 637-45.
61. Tesio M, Golan K, Corso S, Giordano S, Schajnovitz A, Vagima Y, et al. Enhanced c-Met activity promotes G-CSF-induced mobilization of hematopoietic progenitor cells via ROS signaling. Blood 2011;117: 419-28.
62. Acharyya S, Oskarsson T, Vanharanta S, Malladi S, Kim J, Morris PG, et al. A CXCL1 paracrine network links cancer chemoresistance and metastasis. Cell 2012;150:165-78.
63. Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, et al. Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci U S A 2012;109:2491-6.
64. McAllister SS, Gifford AM, Greiner AL, Kelleher SP, Saelzler MP, Ince TA, et al. Systemic endocrine instigation of indolent tumor growth requires osteopontin. Cell 2008;133:994-1005.
65. Marrony S, Bassilana F, Seuwen K, Keller H. Bone morphogenetic protein 2 induces placental growth factor in mesenchymal stem cells. Bone 2003;33:426-33.
66. Ding Y, Huang Y, Song N, Gao X, Yuan S, Wang X, et al. NFAT1 mediates placental growth factor-induced myelomonocytic cell recruitment via the induction of TNF-alpha. J Immunol 2010;184: 2593-601.
67. Martelli F, Verrucci M, Migliaccio G, Zingariello M, Rana RA, Vannucchi AM, et al. Removal of the spleen in mice alters the cytokine expression profile of the marrow micro-environment and increases bone formation. Ann N Y Acad Sci 2009;1176:77-86.
68. Cortez-Retamozo V, Etzrodt M, Newton A, Ryan R, Pucci F, Sio SW, et al. Angiotensin II drives the production of tumor-promoting macrophages. Immunity 2013;38:296-308.
69. Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008;319:1244-7.
70. Shao H, Chung J, Balaj L, Charest A, Bigner DD, Carter BS, et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med 2012;18:1835-40.
71. Ceccarelli S, Visco V, Raffa S, Wakisaka N, Pagano JS, Torrisi MR. Epstein-Barr virus latent membrane protein 1 promotes concentration in multivesicular bodies of fibroblast growth factor 2 and its release through exosomes. Int J Cancer 2007;121:1494-506.
72. Cullen BR. Enhancing and confirming the specificity of RNAi experiments. Nat Methods 2006;3:677-81.
73. Mignot G, Chalmin F, Ladoire S, Rebe C, Ghiringhelli F, Xiang X, et al. Tumor exosome-mediated MDSC activation. Am J Pathol 2011;178: 1403-5.
74. Sadallah S, Eken C, Martin PJ, Schifferli JA. Microparticles (ectosomes) shed by stored human platelets downregulate macrophages and modify the development of dendritic cells. J Immunol 2011;186: 6543-52.
75. Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, et al. Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 2006;20:847-56.
76. Hoekstra D, de Boer T, Klappe K, Wilschut J. Fluorescence method for measuring the kinetics of fusion between biological membranes. Biochemistry 1984;23:5675-81.
77. Vallhov H, Gutzeit C, Johansson SM, Nagy N, Paul M, Li Q, et al. Exosomes containing glycoprotein 350 released by EBV-transformed B cells selectively target B cells through CD21 and block EBV infection in vitro. J Immunol 2011;186:73-82.
78. Balaj L, Lessard R, Dai L, Cho YJ, Pomeroy SL, Breakefield XO, et al. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2011;2:180.
79. Rabinowits G, Gercel-Taylor C, Day JM, Taylor DD, Kloecker GH. Exosomal micro RNA: a diagnostic marker for lung cancer. Clin Lung Cancer 2009;10:42-6.
80. Taylor DD, Gercel-Taylor C. Micro RNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008;110:13-21.
81. Chen CL, Lai YF, Tang P, Chien KY, Yu JS, Tsai CH, et al. Comparative and targeted proteomic analyses of urinary microparticles from bladder cancer and hernia patients. J Proteome Res 2012;11:5611-29.
82. Bryant RJ, Pawlowski T, Catto JW, Marsden G, Vessella RL, Rhees B, et al. Changes in circulating micro RNA levels associated with prostate cancer. Br J Cancer 2012;106:768-74.
83. Choi DS, Park JO, Jang SC, Yoon YJ, Jung JW, Choi DY, et al. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 2011;11:2745-51.
84. Balic M, Williams A, Lin H, Datar R, Cote RJ. Circulating tumor cells: from bench to bedside. Annu Rev Med 2013;64:31-44.
85. Escudier B, Dorval T, Chaput N, Andre F, Caby MP, Novault S, et al. Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial. J Transl Med 2005;3:10.
86. Garaude J, Kent A, van Rooijen N, Blander JM. Simultaneous targeting of toll-and nod-like receptors induces effective tumor-specific immune responses. Sci Transl Med 2012;4:120ra16.
87. Marleau AM, Chen CS, Joyce JA, Tullis RH. Exosome removal as a therapeutic adjuvant in cancer. J Transl Med 2012;10:134.