Exosome mediated communication within the tumor microenvironment

Journal of Controlled Release

Volumn 219, Issue , 2015, Pages 278-294

  Milane, Lara ^a   Singh, Amit ^a   Mattheolabakis, George ^a   Suresh, Megha ^a   Amiji, Mansoor M ^a  

^a NORTHEASTERN UNIVERSITY   (United States)

Author keywords

Cancer; Exosomes; Metastasis; MicroRNA; Signaling endosome

Indexed keywords

CELL MEMBRANES; CONTROLLED DRUG DELIVERY; CYTOLOGY; ENZYME ACTIVITY; NANOPARTICLES; PATHOLOGY; RNA; TARGETED DRUG DELIVERY;

CANCER; ENDOSOMES; EXOSOMES; METASTASIS; MICRORNAS;

DISEASES;

LIPID; MESSENGER RNA; MICRORNA; NANOPARTICLE; PROTEIN; TRANSCRIPTION FACTOR; ANTINEOPLASTIC AGENT; TUMOR MARKER;

ARTICLE; BIOGENESIS; CANCER CELL; CANCER IMMUNOTHERAPY; CANCER THERAPY; CELL COMMUNICATION; CELL MEMBRANE; CELL SELECTION; CELLULAR SECRETION; CLINICAL TRIAL (TOPIC); CYTOLOGY; DRUG RESISTANCE; ENDOCYTOSIS; ENDOSOME; EXOCYTOSIS; EXOSOME; HUMAN; IMMUNOMODULATION; MALIGNANT NEOPLASTIC DISEASE; METASTASIS; NONHUMAN; PRIORITY JOURNAL; TUMOR MICROENVIRONMENT; ANIMAL; DRUG DELIVERY SYSTEM; DRUG EFFECTS; METABOLISM; NEOPLASMS; PHYSIOLOGY;

ANIMALS; ANTINEOPLASTIC AGENTS; BIOMARKERS, TUMOR; CELL COMMUNICATION; DRUG DELIVERY SYSTEMS; EXOSOMES; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 85047700200     PISSN: 01683659     EISSN: 18734995     Source Type: Journal    
DOI: 10.1016/j.jconrel.2015.06.029     Document Type: Review

References (187)

1. C.V. Harding, J.E. Heuser, and P.D. Stahl Exosomes: looking back three decades and into the future J. Cell Biol. 200 2013 367 371
2. S.A. Melo, H. Sugimoto, J.T. O'Connell, N. Kato, A. Villanueva, A. Vidal, L. Qiu, E. Vitkin, L.T. Perelman, C.A. Melo, A. Lucci, C. Ivan, G.A. Calin, and R. Kalluri Cancer exosomes perform cell-independent microRNA biogenesis and promote tumorigenesis Cancer Cell 26 2014 707 721
3. B.H. Sung, T. Ketova, D. Hoshino, A. Zijlstra, and A.M. Weaver Directional cell movement through tissues is controlled by exosome secretion Nat. Commun. 6 2015 7164
4. A. Riches, E. Campbell, E. Borger, and S. Powis Regulation of exosome release from mammary epithelial and breast cancer cells - a new regulatory pathway Eur. J. Cancer 50 2014 1025 1034
5. M.T. Le, P. Hamar, C. Guo, E. Basar, R. Perdigao-Henriques, L. Balaj, and J. Lieberman Mir-200-containing extracellular vesicles promote breast cancer cell metastasis J. Clin. Invest. 124 2014 5109 5128
6. P. Kharaziha, S. Ceder, Q. Li, and T. Panaretakis Tumor cell-derived exosomes: a message in a bottle Biochim. Biophys. Acta 1826 2012 103 111
7. M. Colombo, C. Moita, G. van Niel, J. Kowal, J. Vigneron, P. Benaroch, N. Manel, L.F. Moita, C. Thery, and G. Raposo Analysis of escrt functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles J. Cell Sci. 126 2013 5553 5565
8. I. Parolini, C. Federici, C. Raggi, L. Lugini, S. Palleschi, A. De Milito, C. Coscia, E. Iessi, M. Logozzi, A. Molinari, M. Colone, M. Tatti, M. Sargiacomo, and S. Fais Microenvironmental pH is a key factor for exosome traffic in tumor cells J. Biol. Chem. 284 2009 34211 34222
9. D. Hanahan, and R.A. Weinberg Hallmarks of cancer: the next generation Cell 144 2011 646 674
10. L. Milane, Z. Duan, and M. Amiji Role of hypoxia and glycolysis in the development of multi-drug resistance in human tumor cells and the establishment of an orthotopic multi-drug resistant tumor model in nude mice using hypoxic pre-conditioning Cancer Cell Int. 11 2011 3
11. D.J. O'Shannessy, E.B. Somers, L.C. Wang, H. Wang, and R. Hsu Expression of folate receptors α and β in normal and cancerous gynecologic tissues: correlation of expression of the isoform with macrophage markers J. Ovarian Res. 8 2015 29
12. M.L. Taddei, E. Giannoni, G. Comito, and P. Chiarugi Microenvironment and tumor cell plasticity: an easy way out Cancer Lett. 341 2013 80 96
13. Y. Mosesson, G.B. Mills, and Y. Yarden Derailed endocytosis: an emerging feature of cancer Nat. Rev. Cancer 8 2008 835 850
14. L. Carrillo, B. Cucu, V. Bandmann, U. Homann, B. Hertel, S. Hillmer, G. Thiel, and A. Bertl High-resolution membrane capacitance measurements for studying endocytosis and exocytosis in yeast Traffic 16 7 2015 760 772
15. T. Tojima, R. Itofusa, and H. Kamiguchi Steering neuronal growth cones by shifting the imbalance between exocytosis and endocytosis J. Neurosci. 34 2014 7165 7178
16. R. Worthylake, L.K. Opresko, and H.S. Wiley Erbb-2 amplification inhibits down-regulation and induces constitutive activation of both erbb-2 and epidermal growth factor receptors J. Biol. Chem. 274 1999 8865 8874
17. P.A. Muller, P.T. Caswell, B. Doyle, M.P. Iwanicki, E.H. Tan, S. Karim, N. Lukashchuk, D.A. Gillespie, R.L. Ludwig, P. Gosselin, A. Cromer, J.S. Brugge, O.J. Sansom, J.C. Norman, and K.H. Vousden Mutant p53 drives invasion by promoting integrin recycling Cell 139 2009 1327 1341
18. T. Janas, M.M. Janas, K. Sapon, and T. Janas Mechanisms of RNA loading into exosomes FEBS Lett. 589 13 2015 1391 1398
19. N. Kosaka, H. Iguchi, Y. Yoshioka, F. Takeshita, Y. Matsuki, and T. Ochiya Secretory mechanisms and intercellular transfer of micrornas in living cells J. Biol. Chem. 285 2010 17442 17452
20. R. Dobrowolski, and E.M. De Robertis Endocytic control of growth factor signalling: multivesicular bodies as signalling organelles Nat. Rev. Mol. Cell Biol. 13 2012 53 60
21. G. Scita, and P.P. Di Fiore The endocytic matrix Nature 463 2010 464 473
22. A. Sorkin, and M. von Zastrow Endocytosis and signalling: intertwining molecular networks Nat. Rev. Mol. Cell Biol. 10 2009 609 622
23. J. Gruenberg The endocytic pathway: a mosaic of domains Nat. Rev. Mol. Cell Biol. 2 2001 721 730
24. O. Engebraaten, H.K. Vollan, and A.L. Borresen-Dale Triple-negative breast cancer and the need for new therapeutic targets Am. J. Pathol. 183 2013 1064 1074
25. S.S. Tan, Y. Yin, T. Lee, R.C. Lai, R.W. Yeo, B. Zhang, A. Choo, and S.K. Lim Therapeutic msc exosomes are derived from lipid raft microdomains in the plasma membrane J. Extracell Vesicles 2 2013
26. E. Cocucci, and J. Meldolesi Ectosomes and exosomes: shedding the confusion between extracellular vesicles Trends Cell Biol. 25 6 2015 364 372
27. J. Kowal, M. Tkach, and C. Thery Biogenesis and secretion of exosomes Curr. Opin. Cell Biol. 29 2014 116 125
28. C. Thery, M. Boussac, P. Veron, P. Ricciardi-Castagnoli, G. Raposo, J. Garin, and S. Amigorena Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles J. Immunol. 166 2001 7309 7318
29. W. Stoorvogel Resolving sorting mechanisms into exosomes Cell Res. 25 2015 531 532
30. D. Mazurov, L. Barbashova, and A. Filatov Tetraspanin protein CD9 interacts with metalloprotease CD10 and enhances its release via exosomes FEBS J. 280 2013 1200 1213
31. F.J. Verweij, M.A. van Eijndhoven, E.S. Hopmans, T. Vendrig, T. Wurdinger, E. Cahir-McFarland, E. Kieff, D. Geerts, R. van der Kant, J. Neefjes, J.M. Middeldorp, and D.M. Pegtel Lmp1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-κb activation EMBO J. 30 2011 2115 2129
32. C. Villarroya-Beltri, F. Baixauli, C. Gutierrez-Vazquez, F. Sanchez-Madrid, and M. Mittelbrunn Sorting it out: regulation of exosome loading Semin. Cancer Biol. 28 2014 3 13
33. K. Trajkovic, C. Hsu, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, and et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes Science. 319 2008 1244 1247
34. A. Savina, M. Furlan, M. Vidal, and M.I. Colombo Exosome release is regulated by a calcium-dependent mechanism in k562 cells J. Biol. Chem. 278 2003 20083 20090
35. M. Ostrowski, N.B. Carmo, S. Krumeich, I. Fanget, G. Raposo, A. Savina, C.F. Moita, K. Schauer, A.N. Hume, R.P. Freitas, B. Goud, P. Benaroch, N. Hacohen, M. Fukuda, C. Desnos, M.C. Seabra, F. Darchen, S. Amigorena, L.F. Moita, and C. Thery Rab27a and rab27b control different steps of the exosome secretion pathway Nat. Cell Biol. 12 2010 11 13 (19-30; sup)
36. I. Nazarenko, S. Rana, A. Baumann, J. McAlear, A. Hellwig, M. Trendelenburg, G. Lochnit, K.T. Preissner, and M. Zoller Cell surface tetraspanin tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation Cancer Res. 70 2010 1668 1678
37. L. Alvarez-Erviti, Y. Seow, H. Yin, C. Betts, S. Lakhal, and M.J. Wood Delivery of sirna to the mouse brain by systemic injection of targeted exosomes Nat. Biotechnol. 29 2011 341 345
38. S. Hayes TGF-β receptor internalization into EEA1-enriched early endosomes: role in signaling to Smad2 J. Cell Biol. 158 2002 1239 1249
39. R. Zoncu, R.M. Perera, D.M. Balkin, M. Pirruccello, D. Toomre, and P. De Camilli A phosphoinositide switch controls the maturation and signaling properties of APPL endosomes Cell 136 2009 1110 1121
40. Z. Andreu, and M. Yanez-Mo Tetraspanins in extracellular vesicle formation and function Front. Immunol. 5 2014 442
41. C. Joffre, R. Barrow, L. Menard, V. Calleja, I.R. Hart, and S. Kermorgant A direct role for met endocytosis in tumorigenesis Nat. Cell Biol. 13 2011 827 837
42. H.W. King, M.Z. Michael, and J.M. Gleadle Hypoxic enhancement of exosome release by breast cancer cells BMC Cancer 12 2012 421
43. C.E. Meacham, and S.J. Morrison Tumour heterogeneity and cancer cell plasticity Nature 501 2013 328 337
44. I. Kawikova, and P.W. Askenase Diagnostic and therapeutic potentials of exosomes in CNS diseases Brain Res. 2014 10.1016/j.brainres.2014.09.070
45. http://www.Caltech.Edu/news/caltech-scientists-create-new-enzymes-biofuel-production-1519#sthash.Npaeqvzu.Dpuf, Last Accessed: May 26, 2015. Original Article: P. Heinzelman, C.D. Snow, I. Wu, C. Nguyen, A. Villalobos, S. Govindarajan, J. Minshull, and F.H. Arnold A family of thermostable fungal cellulases created by structure-guided recombination Proc. Natl. Acad. Sci. U. S. A. 106 2009 5610
46. M.A. Alonso, and J. Millán The role of lipid rafts in signalling and membrane trafficking in T lymphocytes J. Cell Sci. 114 2001 3957 3965
47. J.C. Pizarro, A.K. Wernimont, A. Hutchinson, H. Sullivan, J. Lew, A. Bochkarev, C.H. Arrowsmith, C. Bountra, J. Weigelt, A.M. Edwards, R. Hui, and T. Hills Structural Genomics Consortium, Crystal Structure of the n-Terminal Domain of hsp70 From Cryptosporidium Parvum (cgd2-20) http://www.Rcsb.Org/pdb/explore/explore.Do?Structureid=3l6q 10.2210/pdb3l6q/pdb (in, RCSB PDB Protein Data Bank; National Science Foundation, the National Institutes of Health, and the US Department of Energy)
48. Chapter 2: RNA and DNA revealed: new roles, new rules; small but powerful The New Genetics 2010 U.S. Department of Health and Human Services; National Institute of Health; National Institute of General Medical Sciences 24 39
49. A. Chow, W. Zhou, L. Liu, M.Y. Fong, J. Champer, D. Van Haute, A.R. Chin, X. Ren, B.G. Gugiu, Z. Meng, W. Huang, V. Ngo, M. Kortylewski, and S.E. Wang Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB Sci. Rep. 4 2014 5750
50. G. Falcone, A. Felsani, and I. D'Agnano Signaling by exosomal microRNAs in cancer J. Exp. Clin. Cancer Res. 34 2015 32
51. M.E. Cecilia Lässer, and Jan Lötvall The role of exosomal shuttle RNA (esRNA) in cell-to-cell communication Emerging Concepts of Tumor Exosome-mediated Cell-Cell Communication 2013 33 45
52. M. Yang, J. Chen, F. Su, B. Yu, F. Su, L. Lin, Y. Liu, J.D. Huang, and E. Song Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells Mol. Cancer 10 2011 117
53. D.M. Epstein Special delivery: microRNA-200-containing extracellular vesicles provide metastatic message to distal tumor cells J. Clin. Invest. 124 2014 5107 5108
54. Y. Bai, Y. Sun, J. Peng, H. Liao, H. Gao, Y. Guo, and L. Guo Overexpression of secretagogin inhibits cell apoptosis and induces chemoresistance in small cell lung cancer under the regulation of miR-494 Oncotarget 5 2014 7760 7775
55. S. Rana, K. Malinowska, and M. Zoller Exosomal tumor microrna modulates premetastatic organ cells Neoplasia 15 2013 281 295
56. X.J. Li, Z.J. Ren, and J.H. Tang Microrna-34a: a potential therapeutic target in human cancer Cell Death Dis. 5 2014 e1327
57. Q. Ji, X. Hao, M. Zhang, W. Tang, M. Yang, L. Li, D. Xiang, J.T. Desano, G.T. Bommer, D. Fan, E.R. Fearon, T.S. Lawrence, and L. Xu MicroRNA miR-34 inhibits human pancreatic cancer tumor-initiating cells PLoS One 4 2009 e6816
58. G. Yu, W. Yao, W. Xiao, H. Li, H. Xu, and B. Lang MicroRNA-34a functions as an anti-metastatic microRNA and suppresses angiogenesis in bladder cancer by directly targeting CD44 J. Exp. Clin. Cancer Res. 33 2014 779
59. M. Aga, G.L. Bentz, S. Raffa, M.R. Torrisi, S. Kondo, N. Wakisaka, T. Yoshizaki, J.S. Pagano, and J. Shackelford Exosomal HIF-1α supports invasive potential of nasopharyngeal carcinoma-associated LMP1-positive exosomes Oncogene 33 2014 4613 4622
60. H.G. Zhang, and W.E. Grizzle Exosomes and cancer: a newly described pathway of immune suppression Clin. Cancer Res. 17 2011 959 964
61. M.W. Graner, O. Alzate, A.M. Dechkovskaia, J.D. Keene, J.H. Sampson, D.A. Mitchell, and D.D. Bigner Proteomic and immunologic analyses of brain tumor exosomes FASEB J. 23 2009 1541 1557
62. H. Valadi, K. Ekstrom, A. Bossios, M. Sjostrand, J.J. Lee, and J.O. Lotvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat. Cell Biol. 9 2007 654 659
63. T.H. Ung, H.J. Madsen, J.E. Hellwinkel, A.M. Lencioni, and M.W. Graner Exosome proteomics reveals transcriptional regulator proteins with potential to mediate downstream pathways Cancer Sci. 105 2014 1384 1392
64. J. Skog, T. Wurdinger, S. van Rijn, D.H. Meijer, L. Gainche, M. Sena-Esteves, W.T. Curry Jr., B.S. Carter, A.M. Krichevsky, and X.O. Breakefield Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers Nat. Cell Biol. 10 2008 1470 1476
65. Z. Deng, Z. Cheng, X. Xiang, J. Yan, X. Zhuang, C. Liu, H. Jiang, S. Ju, L. Zhang, W. Grizzle, J. Mobley, J. Roman, D. Miller, and H.G. Zhang Tumor cell cross talk with tumor-associated leukocytes leads to induction of tumor exosomal fibronectin and promotes tumor progression Am. J. Pathol. 180 2012 390 398
66. J.N. Higginbotham, M. Demory Beckler, J.D. Gephart, J.L. Franklin, G. Bogatcheva, G.J. Kremers, D.W. Piston, G.D. Ayers, R.E. McConnell, M.J. Tyska, and R.J. Coffey Amphiregulin exosomes increase cancer cell invasion Curr. Biol. 21 2011 779 786
67. S. Khan, J.R. Aspe, M.G. Asumen, F. Almaguel, O. Odumosu, S. Acevedo-Martinez, M. De Leon, W.H. Langridge, and N.R. Wall Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential Br. J. Cancer 100 2009 1073 1086
68. J. Webber, R. Steadman, M.D. Mason, Z. Tabi, and A. Clayton Cancer exosomes trigger fibroblast to myofibroblast differentiation Cancer Res. 70 2010 9621 9630
69. B.K. Thakur, H. Zhang, A. Becker, I. Matei, Y. Huang, B. Costa-Silva, Y. Zheng, A. Hoshino, H. Brazier, J. Xiang, C. Williams, R. Rodriguez-Barrueco, J.M. Silva, W. Zhang, S. Hearn, O. Elemento, N. Paknejad, K. Manova-Todorova, K. Welte, J. Bromberg, H. Peinado, and D. Lyden Double-stranded DNA in exosomes: a novel biomarker in cancer detection Cell Res. 24 2014 766 769
70. S.H. Huang, Y. Li, J. Zhang, J. Rong, and S. Ye Epidermal growth factor receptor-containing exosomes induce tumor-specific regulatory T cells Cancer Invest. 31 2013 330 335
71. B. Fevrier, and G. Raposo Exosomes: endosomal-derived vesicles shipping extracellular messages Curr. Opin. Cell Biol. 16 2004 415 421
72. W. Stoorvogel, M.J. Kleijmeer, H.J. Geuze, and G. Raposo The biogenesis and functions of exosomes Traffic 3 2002 321 330
73. G.R. Alessandra Lo Cicero The cell biology of exosomes: historical and perspectives Emerging Concepts of Tumor Exosome-mediated Cell-Cell Communication 2013 1 32
74. G. van Niel, I. Porto-Carreiro, S. Simoes, and G. Raposo Exosomes: a common pathway for a specialized function J. Biochem. 140 2006 13 21
75. L. Rajendran, M. Honsho, T.R. Zahn, P. Keller, K.D. Geiger, P. Verkade, and K. Simons Alzheimer's disease β-amyloid peptides are released in association with exosomes Proc. Natl. Acad. Sci. U. S. A. 103 2006 11172 11177
76. E. Emmanouilidou, K. Melachroinou, T. Roumeliotis, S.D. Garbis, M. Ntzouni, L.H. Margaritis, L. Stefanis, and K. Vekrellis Cell-produced α-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival J. Neurosci. 30 2010 6838 6851
77. C. Gomes, S. Keller, P. Altevogt, and J. Costa Evidence for secretion of Cu, Zn superoxide dismutase via exosomes from a cell model of amyotrophic lateral sclerosis Neurosci. Lett. 428 2007 43 46
78. J. Yang, F. Wei, C. Schafer, and D.T. Wong Detection of tumor cell-specific mRNA and protein in exosome-like microvesicles from blood and saliva PLoS One 9 2014 e110641
79. E. Odintsova, T. Sugiura, and F. Berditchevski Attenuation of EGF receptor signaling by a metastasis suppressor, the tetraspanin cd82/kai-1 Curr. Biol. 10 2000 1009 1012
80. V. Luga, L. Zhang, A.M. Viloria-Petit, A.A. Ogunjimi, M.R. Inanlou, E. Chiu, M. Buchanan, A.N. Hosein, M. Basik, and J.L. Wrana Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration Cell 151 2012 1542 1556
81. M.Z. Sanyukta Rana The functional importance of tetraspanins in exosomes Emerging Concepts of Tumor Exosome-mediated Cell-Cell Communication 2013 69 106
82. S. Matzku, D. Komitowski, M. Mildenberger, and M. Zoller Characterization of bsp73, a spontaneous rat tumor and its in vivo selected variants showing different metastasizing capacities Invasion Metastasis 3 1983 109 123
83. M.A. Lafleur, D. Xu, and M.E. Hemler Tetraspanin proteins regulate membrane type-1 matrix metalloproteinase-dependent pericellular proteolysis Mol. Biol. Cell 20 2009 2030 2040
84. M. Yanez-Mo, O. Barreiro, P. Gonzalo, A. Batista, D. Megias, L. Genis, N. Sachs, M. Sala-Valdes, M.A. Alonso, M.C. Montoya, A. Sonnenberg, A.G. Arroyo, and F. Sanchez-Madrid Mt1-mmp collagenolytic activity is regulated through association with tetraspanin CD151 in primary endothelial cells Blood 112 2008 3217 3226
85. J. Gong, R. Jaiswal, J.M. Mathys, V. Combes, G.E. Grau, and M. Bebawy Microparticles and their emerging role in cancer multidrug resistance Cancer Treat. Rev. 38 2012 226 234
86. J. Hakulinen, L. Sankkila, N. Sugiyama, K. Lehti, and J. Keski-Oja Secretion of active membrane type 1 matrix metalloproteinase (MMP-14) into extracellular space in microvesicular exosomes J. Cell. Biochem. 105 2008 1211 1218
87. K. Al-Nedawi, B. Meehan, J. Micallef, V. Lhotak, L. May, A. Guha, and J. Rak Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells Nat. Cell Biol. 10 2008 619 624
88. H. Sheldon, E. Heikamp, H. Turley, R. Dragovic, P. Thomas, C.E. Oon, R. Leek, M. Edelmann, B. Kessler, R.C. Sainson, I. Sargent, J.L. Li, and A.L. Harris New mechanism for notch signaling to endothelium at a distance by delta-like 4 incorporation into exosomes Blood 116 2010 2385 2394
89. E. van der Pol, and A. Sturk Overview of extracellular vesicles in health and disease P. Harrison, C. Gardiner, I.L. Sargent, Extracellular Vesicles in Health and Disease 2014 Pan Stanford Publications Singapore 1 46
90. S. Taverna, A. Flugy, L. Saieva, E.C. Kohn, A. Santoro, S. Meraviglia, G. De Leo, and R. Alessandro Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis Int. J. Cancer 130 2012 2033 2043
91. G. Wang, M. Dinkins, Q. He, G. Zhu, C. Poirier, A. Campbell, M. Mayer-Proschel, and E. Bieberich Astrocytes secrete exosomes enriched with proapoptotic ceramide and prostate apoptosis response 4 (PAR-4): potential mechanism of apoptosis induction in Alzheimer disease (AD) J. Biol. Chem. 287 2012 21384 21395
92. C. Subra, K. Laulagnier, B. Perret, and M. Record Exosome lipidomics unravels lipid sorting at the level of multivesicular bodies Biochimie 89 2007 205 212
93. R. Wubbolts, R.S. Leckie, P.T. Veenhuizen, G. Schwarzmann, W. Mobius, J. Hoernschemeyer, J.W. Slot, H.J. Geuze, and W. Stoorvogel Proteomic and biochemical analyses of human b cell-derived exosomes. Potential implications for their function and multivesicular body formation J. Biol. Chem. 278 2003 10963 10972
94. K. Laulagnier, C. Motta, S. Hamdi, S. Roy, F. Fauvelle, J.F. Pageaux, T. Kobayashi, J.P. Salles, B. Perret, C. Bonnerot, and M. Record Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization Biochem. J. 380 2004 161 171
95. A. Llorente, T. Skotland, T. Sylvanne, D. Kauhanen, T. Rog, A. Orlowski, I. Vattulainen, K. Ekroos, and K. Sandvig Molecular lipidomics of exosomes released by pc-3 prostate cancer cells Biochim. Biophys. Acta 1831 2013 1302 1309
96. M. Record Exosomal lipids in cell-cell communication Emerging Concepts of Tumor Exosome-mediated Cell-Cell Communication 2013 47 68
97. Y. Toda, K. Takata, Y. Nakagawa, H. Kawakami, S. Fujioka, K. Kobayashi, Y. Hattori, Y. Kitamura, K. Akaji, and E. Ashihara Effective internalization of U251-MG-secreted exosomes into cancer cells and characterization of their lipid components Biochem. Biophys. Res. Commun. 456 2015 768 773
98. S. Boukouris, and S. Mathivanan Exosomes in bodily fluids are a highly stable resource of disease biomarkers Proteomics Clin. Appl. 9 2015 358 367
99. R.J. Simpson, J.W. Lim, R.L. Moritz, and S. Mathivanan Exosomes: proteomic insights and diagnostic potential Expert Rev. Proteomics 6 2009 267 283
100. H. Kalra, C.G. Adda, M. Liem, C.S. Ang, A. Mechler, R.J. Simpson, M.D. Hulett, and S. Mathivanan Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma Proteomics 13 2013 3354 3364
101. Q. Ge, Y. Zhou, J. Lu, Y. Bai, X. Xie, and Z. Lu Mirna in plasma exosome is stable under different storage conditions Molecules 19 2014 1568 1575
102. S.M. Hanash, S.J. Pitteri, and V.M. Faca Mining the plasma proteome for cancer biomarkers Nature 452 2008 571 579
103. E.P. Diamandis The failure of protein cancer biomarkers to reach the clinic: why, and what can be done to address the problem? BMC Med. 10 2012 87
104. D. Duijvesz, K.E. Burnum-Johnson, M.A. Gritsenko, A.M. Hoogland, M.S. Vredenbregt-van den Berg, R. Willemsen, T. Luider, L. Pasa-Tolic, and G. Jenster Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer PLoS One 8 2013 e82589
105. E. Hosseini-Beheshti, S. Pham, H. Adomat, N. Li, and E.S. Tomlinson Guns Exosomes as biomarker enriched microvesicles: characterization of exosomal proteins derived from a panel of prostate cell lines with distinct ar phenotypes Mol. Cell. Proteomics 11 2012 863 885
106. J. Nilsson, J. Skog, A. Nordstrand, V. Baranov, L. Mincheva-Nilsson, X. Breakefield, and A. Widmark Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer Br. J. Cancer 100 2009 1603 1607
107. R.J. Bryant, T. Pawlowski, J.W. Catto, G. Marsden, R.L. Vessella, B. Rhees, C. Kuslich, T. Visakorpi, and F.C. Hamdy Changes in circulating microrna levels associated with prostate cancer Br. J. Cancer 106 2012 768 774
108. R. Nishikawa, T. Sugiyama, Y. Narita, F. Furnari, W.K. Cavenee, and M. Matsutani Immunohistochemical analysis of the mutant epidermal growth factor, deltaEGFR, in glioblastoma Brain Tumor Pathol. 21 2004 53 56
109. I.K. Mellinghoff, M.Y. Wang, I. Vivanco, D.A. Haas-Kogan, S. Zhu, E.Q. Dia, K.V. Lu, K. Yoshimoto, J.H. Huang, D.J. Chute, B.L. Riggs, S. Horvath, L.M. Liau, W.K. Cavenee, P.N. Rao, R. Beroukhim, T.C. Peck, J.C. Lee, W.R. Sellers, D. Stokoe, M. Prados, T.F. Cloughesy, C.L. Sawyers, and P.S. Mischel Molecular determinants of the response of glioblastomas to EGFR kinase inhibitors N. Engl. J. Med. 353 2005 2012 2024
110. H. Shao, J. Chung, L. Balaj, A. Charest, D.D. Bigner, B.S. Carter, F.H. Hochberg, X.O. Breakefield, R. Weissleder, and H. Lee Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy Nat. Med. 18 2012 1835 1840
111. J.C. Akers, V. Ramakrishnan, R. Kim, J. Skog, I. Nakano, S. Pingle, J. Kalinina, W. Hua, S. Kesari, Y. Mao, X.O. Breakefield, F.H. Hochberg, E.G. Van Meir, B.S. Carter, and C.C. Chen Mir-21 in the extracellular vesicles (EVs) of cerebrospinal fluid (CSF): a platform for glioblastoma biomarker development PLoS One 8 2013 e78115
112. C.H. Lawrie, S. Gal, H.M. Dunlop, B. Pushkaran, A.P. Liggins, K. Pulford, A.H. Banham, F. Pezzella, J. Boultwood, J.S. Wainscoat, C.S. Hatton, and A.L. Harris Detection of elevated levels of tumour-associated microRNAs in serum of patients with diffuse large B-cell lymphoma Br. J. Haematol. 141 2008 672 675
113. Y. Tanaka, H. Kamohara, K. Kinoshita, J. Kurashige, T. Ishimoto, M. Iwatsuki, M. Watanabe, and H. Baba Clinical impact of serum exosomal microRNA-21 as a clinical biomarker in human esophageal squamous cell carcinoma Cancer 119 2013 1159 1167
114. D.D. Taylor, and C. Gercel-Taylor Microrna signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer Gynecol. Oncol. 110 2008 13 21
115. H. Im, H. Shao, Y.I. Park, V.M. Peterson, C.M. Castro, R. Weissleder, and H. Lee Label-free detection and molecular profiling of exosomes with a nano-plasmonic sensor Nat. Biotechnol. 32 2014 490 495
116. K. Sugimachi, T. Matsumura, H. Hirata, R. Uchi, M. Ueda, H. Ueo, Y. Shinden, T. Iguchi, H. Eguchi, K. Shirabe, T. Ochiya, Y. Maehara, and K. Mimori Identification of a bona fide microrna biomarker in serum exosomes that predicts hepatocellular carcinoma recurrence after liver transplantation Br. J. Cancer 112 2015 532 538
117. G. Rabinowits, C. Gercel-Taylor, J.M. Day, D.D. Taylor, and G.H. Kloecker Exosomal microRNA: a diagnostic marker for lung cancer Clin. Lung Cancer 10 2009 42 46
118. Y. Li, Y. Zhang, F. Qiu, and Z. Qiu Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC Electrophoresis 32 2011 1976 1983
119. C. Lau, Y. Kim, D. Chia, N. Spielmann, G. Eibl, D. Elashoff, F. Wei, Y.L. Lin, A. Moro, T. Grogan, S. Chiang, E. Feinstein, C. Schafer, J. Farrell, and D.T. Wong Role of pancreatic cancer-derived exosomes in salivary biomarker development J. Biol. Chem. 288 2013 26888 26897
120. S. Klein-Scory, M.M. Tehrani, C. Eilert-Micus, K.A. Adamczyk, N. Wojtalewicz, M. Schnolzer, S.A. Hahn, W. Schmiegel, and I. Schwarte-Waldhoff New insights in the composition of extracellular vesicles from pancreatic cancer cells: implications for biomarkers and functions Proteome Sci. 12 2014 50
121. B.J. Tauro, D.W. Greening, R.A. Mathias, H. Ji, S. Mathivanan, A.M. Scott, and R.J. Simpson Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes Methods 56 2012 293 304
122. M. Logozzi, A. De Milito, L. Lugini, M. Borghi, L. Calabro, M. Spada, M. Perdicchio, M.L. Marino, C. Federici, E. Iessi, D. Brambilla, G. Venturi, F. Lozupone, M. Santinami, V. Huber, M. Maio, L. Rivoltini, and S. Fais High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients PLoS One 4 2009 e5219
123. D. Hoshino, K.C. Kirkbride, K. Costello, E.S. Clark, S. Sinha, N. Grega-Larson, M.J. Tyska, and A.M. Weaver Exosome secretion is enhanced by invadopodia and drives invasive behavior Cell Rep. 5 2013 1159 1168
124. W. Mu, S. Rana, and M. Zöller Host matrix modulation by tumor exosomes promotes motility and invasiveness Neoplasia 15 2013 875-IN874
125. H. Peinado, S. Lavotshkin, and D. Lyden The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts Semin. Cancer Biol. 21 2011 139 146
126. M.Y. Fong, W. Zhou, L. Liu, A.Y. Alontaga, M. Chandra, J. Ashby, A. Chow, S.T. O'Connor, S. Li, A.R. Chin, G. Somlo, M. Palomares, Z. Li, J.R. Tremblay, A. Tsuyada, G. Sun, M.A. Reid, X. Wu, P. Swiderski, X. Ren, Y. Shi, M. Kong, W. Zhong, Y. Chen, and S.E. Wang Breast-cancer-secreted mir-122 reprograms glucose metabolism in premetastatic niche to promote metastasis Nat. Cell Biol. 17 2015 183 194
127. J.L. Hood, H. Pan, G.M. Lanza, and S.A. Wickline Paracrine induction of endothelium by tumor exosomes Lab. Invest. 89 2009 1317 1328
128. H. Peinado, M. Aleckovic, S. Lavotshkin, I. Matei, B. Costa-Silva, G. Moreno-Bueno, M. Hergueta-Redondo, C. Williams, G. Garcia-Santos, C.M. Ghajar, A. Nitadori-Hoshino, C. Hoffman, K. Badal, B.A. Garcia, M.K. Callahan, J.D. Yuan, V.R. Martins, J. Skog, R.N. Kaplan, M.S. Brady, M.S. Brady, J.D. Wolchok, P.B. Chapman, Y.B. Kang, J. Bromberg, and D. Lyden Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through met Nat. Med. 18 2012 (883-+)
129. J.L. Hood, R.S. San, and S.A. Wickline Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis Cancer Res. 71 2011 3792 3801
130. M.B. Meads, R.A. Gatenby, and W.S. Dalton Environment-mediated drug resistance: a major contributor to minimal residual disease Nat. Rev. Cancer 9 2009 665 674
131. A.S. Azmi, B. Bao, and F.H. Sarkar Exosomes in cancer development, metastasis, and drug resistance: a comprehensive review Cancer Metastasis Rev. 32 2013 623 642
132. K. Shedden, X.T. Xie, P. Chandaroy, Y.T. Chang, and G.R. Rosania Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles Cancer Res. 63 2003 4331 4337
133. F. Luciani, M. Spada, A. De Milito, A. Molinari, L. Rivoltini, A. Montinaro, M. Marra, L. Lugini, M. Logozzi, F. Lozupone, C. Federici, E. Iessi, G. Parmiani, G. Arancia, F. Belardelli, and S. Fais Effect of proton pump inhibitor pretreatment on resistance of solid tumors to cytotoxic drugs J. Natl. Cancer Inst. 96 2004 1702 1713
134. K.G. Chen, J.C. Valencia, B. Lai, G. Zhang, J.K. Paterson, F. Rouzaud, W. Berens, S.M. Wincovitch, S.H. Garfield, R.D. Leapman, V.J. Hearing, and M.M. Gottesman Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas Proc. Natl. Acad. Sci. U. S. A. 103 2006 9903 9907
135. R. Safaei, A.K. Holzer, K. Katano, G. Samimi, and S.B. Howell The role of copper transporters in the development of resistance to Pt drugs J. Inorg. Biochem. 98 2004 1607 1613
136. R. Safaei, B.J. Larson, T.C. Cheng, M.A. Gibson, S. Otani, W. Naerdemann, and S.B. Howell Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells Mol. Cancer Ther. 4 2005 1595 1604
137. X. Yu, S.L. Harris, and A.J. Levine The regulation of exosome secretion: a novel function of the p53 protein Cancer Res. 66 2006 4795 4801
138. M.C. Boelens, T.J. Wu, B.Y. Nabet, B. Xu, Y. Qiu, T. Yoon, D.J. Azzam, C. Twyman-Saint Victor, B.Z. Wiemann, H. Ishwaran, P.J. Ter Brugge, J. Jonkers, J. Slingerland, and A.J. Minn Exosome transfer from stromal to breast cancer cells regulates therapy resistance pathways Cell 159 2014 499 513
139. M.M. Lv, X.Y. Zhu, W.X. Chen, S.L. Zhong, Q. Hu, T.F. Ma, J. Zhang, L. Chen, J.H. Tang, and J.H. Zhao Exosomes mediate drug resistance transfer in MCF-7 breast cancer cells and a probable mechanism is delivery of P-glycoprotein Tumour Biol. 35 2014 10773 10779
140. C. Corcoran, S. Rani, K. O'Brien, A. O'Neill, M. Prencipe, R. Sheikh, G. Webb, R. McDermott, W. Watson, J. Crown, and L. O'Driscoll Docetaxel-resistance in prostate cancer: evaluating associated phenotypic changes and potential for resistance transfer via exosomes PLoS One 7 2012 e50999
141. W.X. Chen, X.M. Liu, M.M. Lv, L. Chen, J.H. Zhao, S.L. Zhong, M.H. Ji, Q. Hu, Z. Luo, J.Z. Wu, and J.H. Tang Exosomes from drug-resistant breast cancer cells transmit chemoresistance by a horizontal transfer of microRNAs PLoS One 9 2014 e95240
142. X. Xiao, S. Yu, S. Li, J. Wu, R. Ma, H. Cao, Y. Zhu, and J. Feng Exosomes: decreased sensitivity of lung cancer A549 cells to cisplatin PLoS One 9 2014 e89534
143. G. Raposo, H.W. Nijman, W. Stoorvogel, R. Liejendekker, C.V. Harding, C.J. Melief, and H.J. Geuze B lymphocytes secrete antigen-presenting vesicles J. Exp. Med. 183 1996 1161 1172
144. H. Vincent-Schneider, P. Stumptner-Cuvelette, D. Lankar, S. Pain, G. Raposo, P. Benaroch, and C. Bonnerot Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells Int. Immunol. 14 2002 713 722
145. P.D. Robbins, and A.E. Morelli Regulation of immune responses by extracellular vesicles Nat. Rev. Immunol. 14 2014 195 208
146. D.H. Hsu, P. Paz, G. Villaflor, A. Rivas, A. Mehta-Damani, E. Angevin, L. Zitvogel, and J.B. Le Pecq Exosomes as a tumor vaccine: enhancing potency through direct loading of antigenic peptides J. Immunother. 26 2003 440 450
147. K.R. Qazi, U. Gehrmann, E. Domange Jordo, M.C. Karlsson, and S. Gabrielsson Antigen-loaded exosomes alone induce Th1-type memory through a B-cell-dependent mechanism Blood 113 2009 2673 2683
148. A.E. Morelli, A.T. Larregina, W.J. Shufesky, M.L. Sullivan, D.B. Stolz, G.D. Papworth, A.F. Zahorchak, A.J. Logar, Z. Wang, S.C. Watkins, L.D. Falo Jr., and A.W. Thomson Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells Blood 104 2004 3257 3266
149. A. Montecalvo, W.J. Shufesky, D.B. Stolz, M.G. Sullivan, Z. Wang, S.J. Divito, G.D. Papworth, S.C. Watkins, P.D. Robbins, A.T. Larregina, and A.E. Morelli Exosomes as a short-range mechanism to spread alloantigen between dendritic cells during T cell allorecognition J. Immunol. 180 2008 3081 3090
150. + T cells by dendritic cell-derived exosomes Nat. Immunol. 3 2002 1156 1162
151. J. Wolfers, A. Lozier, G. Raposo, A. Regnault, C. Thery, C. Masurier, C. Flament, S. Pouzieux, F. Faure, T. Tursz, E. Angevin, S. Amigorena, and L. Zitvogel Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming Nat. Med. 7 2001 297 303
152. R. Mears, R.A. Craven, S. Hanrahan, N. Totty, C. Upton, S.L. Young, P. Patel, P.J. Selby, and R.E. Banks Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry Proteomics 4 2004 4019 4031
153. P. Filipazzi, M. Burdek, A. Villa, L. Rivoltini, and V. Huber Recent advances on the role of tumor exosomes in immunosuppression and disease progression Semin. Cancer Biol. 22 2012 342 349
154. D.D. Poutsiaka, E.W. Schroder, D.D. Taylor, E.M. Levy, and P.H. Black Membrane vesicles shed by murine melanoma cells selectively inhibit the expression of Ia antigen by macrophages J. Immunol. 134 1985 138 144
155. G. Andreola, L. Rivoltini, C. Castelli, V. Huber, P. Perego, P. Deho, P. Squarcina, P. Accornero, F. Lozupone, L. Lugini, A. Stringaro, A. Molinari, G. Arancia, M. Gentile, G. Parmiani, and S. Fais Induction of lymphocyte apoptosis by tumor cell secretion of fasl-bearing microvesicles J. Exp. Med. 195 2002 1303 1316
156. + CTL responses through downregulation of peptide/MHC Class I and FAS ligand-mediated cytotoxicity J. Immunol. 185 2010 5268 5278
157. C. Liu, S. Yu, K. Zinn, J. Wang, L. Zhang, Y. Jia, J.C. Kappes, S. Barnes, R.P. Kimberly, W.E. Grizzle, and H.G. Zhang Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function J. Immunol. 176 2006 1375 1385
158. R. Valenti, V. Huber, P. Filipazzi, L. Pilla, G. Sovena, A. Villa, A. Corbelli, S. Fais, G. Parmiani, and L. Rivoltini Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes Cancer Res. 66 2006 9290 9298
159. S.A. Rollins, and P.J. Sims The complement-inhibitory activity of CD59 resides in its capacity to block incorporation of C9 into membrane C5b-9 J. Immunol. 144 1990 3478 3483
160. A. Clayton, C.L. Harris, J. Court, M.D. Mason, and B.P. Morgan Antigen-presenting cell exosomes are protected from complement-mediated lysis by expression of CD55 and CD59 Eur. J. Immunol. 33 2003 522 531
161. I. Salido-Guadarrama, S. Romero-Cordoba, O. Peralta-Zaragoza, A. Hidalgo-Miranda, and M. Rodriguez-Dorantes Micrornas transported by exosomes in body fluids as mediators of intercellular communication in cancer Onco Targets Ther. 7 2014 1327 1338
162. B.S. Batista, W.S. Eng, K.T. Pilobello, K.D. Hendricks-Munoz, and L.K. Mahal Identification of a conserved glycan signature for microvesicles J. Proteome Res. 10 2011 4624 4633
163. C. Kahlert, and R. Kalluri Exosomes in tumor microenvironment influence cancer progression and metastasis J. Mol. Med. 91 2013 431 437
164. M. Ostrowski, N.B. Carmo, S. Krumeich, I. Fanget, G. Raposo, A. Savina, C.F. Moita, K. Schauer, A.N. Hume, R.P. Freitas, B. Goud, P. Benaroch, N. Hacohen, M. Fukuda, C. Desnos, M.C. Seabra, F. Darchen, S. Amigorena, L.F. Moita, and C. Thery Rab27a and rab27b control different steps of the exosome secretion pathway Nat. Cell Biol. 12 2010 11 13 (19-30; sup)
165. A. Savina, M. Furlan, M. Vidal, and M.I. Colombo Exosome release is regulated by a calcium-dependent mechanism in K562 cells J. Biol. Chem. 278 2003 20083 20090
166. M. Iero, R. Valenti, V. Huber, P. Filipazzi, G. Parmiani, S. Fais, and L. Rivoltini Tumour-released exosomes and their implications in cancer immunity Cell Death Differ. 15 2008 80 88
167. F. Chalmin, S. Ladoire, G. Mignot, J. Vincent, M. Bruchard, J.P. Remy-Martin, W. Boireau, A. Rouleau, B. Simon, D. Lanneau, A. De Thonel, G. Multhoff, A. Hamman, F. Martin, B. Chauffert, E. Solary, L. Zitvogel, C. Garrido, B. Ryffel, C. Borg, L. Apetoh, C. Rebe, and F. Ghiringhelli Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells J. Clin. Investig. 120 2010 457 471
168. J. Wahlgren, T.D. Karlson, M. Brisslert, F.V. Sani, E. Telemo, P. Sunnerhagen, and H. Valadi Plasma exosomes can deliver exogenous short interfering RNA to monocytes and lymphocytes Nucleic Acids Res. 40 2012
169. L. Zitvogel, A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes Nat. Med. 4 1998 594 600
170. J.N. Blattman, and P.D. Greenberg Cancer immunotherapy: a treatment for the masses Science 305 2004 200 205
171. F. Andre, N. Chaput, N.E. Schartz, C. Flament, N. Aubert, J. Bernard, F. Lemonnier, G. Raposo, B. Escudier, D.H. Hsu, T. Tursz, S. Amigorena, E. Angevin, and L. Zitvogel Exosomes as potent cell-free peptide-based vaccine. I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells J. Immunol. 172 2004 2126 2136
172. C. Admyre, J. Grunewald, J. Thyberg, S. Gripenback, G. Tornling, A. Eklund, A. Scheynius, and S. Gabrielsson Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid Eur. Respir. J. 22 2003 578 583
173. N. Chaput, N.E. Schartz, F. Andre, J. Taieb, S. Novault, P. Bonnaventure, N. Aubert, J. Bernard, F. Lemonnier, M. Merad, G. Adema, M. Adams, M. Ferrantini, A.F. Carpentier, B. Escudier, T. Tursz, E. Angevin, and L. Zitvogel Exosomes as potent cell-free peptide-based vaccine. II. Exosomes in CPG adjuvants efficiently prime naive TC1 lymphocytes leading to tumor rejection J. Immunol. 172 2004 2137 2146
174. E. Segura, S. Amigorena, and C. Thery Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses Blood Cells Mol. Dis. 35 2005 89 93
175. F. Guo, C.K. Chang, H.H. Fan, X.X. Nie, Y.N. Ren, Y.Y. Liu, and L.H. Zhao Anti-tumour effects of exosomes in combination with cyclophosphamide and polyinosinic-polycytidylic acid J. Int. Med. Res. 36 2008 1342 1353
176. L. Zitvogel, A. Regnault, A. Lozier, J. Wolfers, C. Flament, D. Tenza, P. Ricciardi-Castagnoli, G. Raposo, and S. Amigorena Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes Nat. Med. 4 1998 594 600
177. H.G. Zhang, H. Kim, C. Liu, S. Yu, J. Wang, W.E. Grizzle, R.P. Kimberly, and S. Barnes Curcumin reverses breast tumor exosomes mediated immune suppression of NK cell tumor cytotoxicity Biochim. Biophys. Acta 1773 2007 1116 1123
178. N. Bu, Q.L. Li, Q. Feng, and B.Z. Sun Immune protection effect of exosomes against attack of l1210 tumor cells Leuk. Lymphoma 47 2006 913 918
179. F. Andre, N.E. Schartz, M. Movassagh, C. Flament, P. Pautier, P. Morice, C. Pomel, C. Lhomme, B. Escudier, T. Le Chevalier, T. Tursz, S. Amigorena, G. Raposo, E. Angevin, and L. Zitvogel Malignant effusions and immunogenic tumour-derived exosomes Lancet 360 2002 295 305
180. J. Wolfers, A. Lozier, G. Raposo, A. Regnault, C. Thery, C. Masurier, C. Flament, S. Pouzieux, F. Faure, T. Tursz, E. Angevin, S. Amigorena, and L. Zitvogel Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming Nat. Med. 7 2001 297 303
181. + cytotoxic T cells in patients with glioma J. Neuro-Oncol. 104 2011 659 667
182. W. Chen, J. Wang, C. Shao, S. Liu, Y. Yu, Q. Wang, and X. Cao Efficient induction of antitumor T cell immunity by exosomes derived from heat-shocked lymphoma cells Eur. J. Immunol. 36 2006 1598 1607
183. + CTL- and Nk-mediated antitumour immunity than exosomes released from heat-shocked tumour cells expressing cytoplasmic Hsp70 J. Cell. Mol. Med. 14 2010 2655 2666
184. H.G. Lamparski, A. Metha-Damani, J.Y. Yao, S. Patel, D.H. Hsu, C. Ruegg, and J.B. Le Pecq Production and characterization of clinical grade exosomes derived from dendritic cells J. Immunol. Methods 270 2002 211 226
185. B. Escudier, T. Dorval, N. Chaput, F. Andre, M.P. Caby, S. Novault, C. Flament, C. Leboulaire, C. Borg, S. Amigorena, C. Boccaccio, C. Bonnerot, O. Dhellin, M. Movassagh, S. Piperno, C. Robert, V. Serra, N. Valente, J.B. Le Pecq, A. Spatz, O. Lantz, T. Tursz, E. Angevin, and L. Zitvogel Vaccination of metastatic melanoma patients with autologous dendritic cell (DC) derived-exosomes: results of the first phase I clinical trial J. Transl. Med. 3 2005 10
186. M.A. Morse, J. Garst, T. Osada, S. Khan, A. Hobeika, T.M. Clay, N. Valente, R. Shreeniwas, M.A. Sutton, A. Delcayre, D.H. Hsu, J.B. Le Pecq, and H.K. Lyerly A phase I study of dexosome immunotherapy in patients with advanced non-small cell lung cancer J. Transl. Med. 3 2005 9
187. S. Dai, D. Wei, Z. Wu, X. Zhou, X. Wei, H. Huang, and G. Li Phase I clinical trial of autologous ascites-derived exosomes combined with GM-CSF for colorectal cancer Mol. Ther. 16 2008 782 790