Exosomes: A novel pathway of local and distant intercellular communication that facilitates the growth and metastasis of neoplastic lesions

American Journal of Pathology

Volumn 184, Issue 1, 2014, Pages 28-41

  Zhang, Huang Ge ^a   Grizzle, William E ^b  

^a University of Louisville School of Medicine   (United States)

^b University of Alabama at Birmingham   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ARTICLE; AUTOCRINE EFFECT; CANCER GROWTH; CELL COMMUNICATION; CELL FUNCTION; CELL KINETICS; CHEMOTAXIS; EXOSOME; HUMAN; IMMUNE SYSTEM; IMMUNOSURVEILLANCE; METASTASIS; MOLECULAR WEIGHT; MOLECULE; PARACRINE SIGNALING; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TUMOR CELL; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR RESISTANCE;

ANIMALS; EXOME; HUMANS; NEOPLASMS;

EID: 84890408539     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2013.09.027     Document Type: Review

References (126)

1. B.J. Tauro, D.W. Greening, R.A. Mathias, S. Mathivanan, H. Ji, and R.J. Simpson Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids Mol Cell Proteomics 12 2013 587 598
2. K. Koga, K. Matsumoto, T. Akuyoshi, M. Kubo, N. Yamanaka, A. Tasaki, H. Nakashima, M. Makamura, S. Kuroki, M. Tanaka, and M. Katano Purification, characterization and biological significance of tumor-derived exosomes Anticancer Res 25 2005 3703 3707
3. E.G. Trams, C.J. Lauter, N. Salem Jr., and U. Heine Exfoliation of membrane ecto-enzymes in the form of microvesicles Biochim Biophys Acta 645 1981 63 70
4. R.M. Johnstone, J.R. Adam, L.O. Hammond, and C. Turbide Vesicle formation during reticulocyte maturation: association of plasma membrane activities with released vesicles (exosomes) J Biol Chem 262 1987 9412 9420
5. 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
6. A. Clayton, J. Court, H. Navabi, M. Adams, M.D. Mason, J.A. Hobot, G.R. Newman, and B. Jasani Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry J Immunol Methods 247 2001 163 174
7. 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
8. C. Thery, L. Zitvogel, and S. Amigorena Exosomes: composition, biogenesis and function Nat Rev Immunol 2 2002 569 579
9. J.M. Escoloa, M.J. Kleijmeer, W. Stoorvogel, J.M. Griffith, O. Yoshie, and H.J. Geuze Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B lymphocytes J Biol Chem 273 1998 20121
10. H.-G. Zhang, and W.E. Grizzle Exosomes and cancer: a newly described pathway of immune suppression Clin Cancer Res 17 2011 1 6
11. H.-G. Zhang, Y. Liu, Z.-B. Deng, C. Liu, X. Xiang, and W.E. Grizzle Exosomes and immune surveillance of neoplastic lesions: a review Biotech Histochem 87 2012 161 168
12. H.G. Zhang, and W.E. Grizzle The effects of exosomes and related vesicles on cancer development, progression and dissemination. Emerging Concepts of Tumor Exosomes-Mediated Cell-Cell Communication H.-G. Zhang, 2013 Springer Science New York 107 129
13. J.E. Park, H.S. Tan, A. Datta, R.C. Lai, H. Zhang, W. Meng, S.K. Lim, and S.K. Sze Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes Mol Cell Proteomics 9 2010 1085 1099
14. D. Castellana, F. Zobairi, M.C. Martinez, M.A. Panaro, V. Mitolo, J.M. Freyssinet, and C. Kunzelmann Membrane microvesicles as actors in the establishment of a favorable prostatic tumoral niche: a role for activated fibroblasts and CX3CL1-CX3CR1 axis Cancer Res 69 2009 785 793
15. 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
16. B.S. Hong, J.H. Cho, H. Kim, E.J. Choi, S. Rho, J. Kim, J.H. Kim, D.S. Choi, Y.K. Kim, D. Hwang, and Y.S. Gho Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells BMC Genomics 10 2009 556
17. J.L. Hood, H. Pan, G.M. Lanza, S.A. Wickline Consortium for Translational Research in Advanced Imaging and Nanomedicine (C-TRAIN) Paracrine induction of endothelium by tumor exosomes Lab Invest 89 2009 1317 1328
18. S. Gesierich, I. Berezovskly, E. Ryschich, and M. Zöller Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029 Cancer Res 66 2006 7083 7094
19. 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
20. T. Jung, D. Castellana, P. Klingbell, I.C. Hernández, M. Vitacolonna, D.J. Orlicky, S.R. Roffler, P. Brodt, and M. Zöller CD44v6 dependence of premetastatic niche preparation by exosomes Neoplasia 11 2009 1093 1105
21. H. Péinado, M. Alečković, 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. Yuan, V.R. Martins, J. Skog, R.N. Kaplan, M.S. Brady, J.D. Wolchok, P.B. Chapman, Y. Kang, J. Bromberg, and D. Lyden Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET Nat Med 18 2012 883 891
22. H.G. Zhang, G. Garcia-Santos, H. Peinado, and D.C. Lyden Microenvironmental regulation of metastasis by exosomes H.-G. Zhang, Emerging Concepts of Tumor Exosome-Mediated Cell-Cell Communication 2013 Springer Science New York 181 201
23. 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
24. A. Poliakov, M. Spilman, T. Dokland, C.L. Amling, and J.A. Mobley Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen Prostate 69 2009 159 167
25. V. Palanisamy, S. Sharma, A. Deshpande, H. Zhou, J. Gimzewski, and D.T. Wong Nanostructural and transcriptomic analyses of human saliva derived exosomes PLoS One 5 2010 e8577
26. D.D. Taylor, and C. Gerçel-Taylor Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects Br J Cancer 92 2005 305 311
27. A. Clayton, A. Turkes, H. Navabi, M.D. Mason, and Z. Tabi Induction of heat shock proteins in B-cell exosomes J Cell Sci 118 2005 3631 3638
28. 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 Microenvironment pH is a key factor for exosomes traffic in tumor cells J Biol Chem 284 2009 34211 34222
29. G. Taraboletti, S. D'Ascenzo, I. Giusti, D. Marchetti, P. Borsotti, D. Millimaggi, R. Giavazzi, A. Pavan, and V. Dolo Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH Neoplasia 8 2006 96 103
30. A. Savina, M. Furlán, M. Vical, and M.I. Colombo Exosome release is regulated by a calcium-dependent mechanism in K562 cells J Biol Chem 278 2003 20083 20090
31. M.W. Graner, R.I. Cumming, and D.D. Bigner The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences J Neurosci 27 2007 11214 11227
32. R.B. Koumangoye, A.M. Sakwe, J.S. Goodwin, T. Patel, and J. Ochieng Detachment of breast tumor cells induces rapid secretion of exosomes which subsequently mediate cellular adhesion and spreading PLoS One 6 2011 e24234
33. + cells Traffic 11 2010 110 122
34. 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
35. A. Lespagnol, D. Duflaut, C. Beekman, L. Blanc, G. Fiucci, J.C. Marine, M. Vidal, R. Amson, and A. Telerman Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3-null mice Cell Death Differ 15 2008 1723 1733
36. A. Lo Cicero, and G. Raposo The cell biology of exosomes: historical and perspectives H.-G. Zhang, Emerging Concepts of Tumor Exosomes-Mediated Cell-Cell Communication 2013 Springer Science+Business Media New York 1 32
37. M.F. Baietti, Z. Zhang, E. Mortier, A. Melchio, G. Degeest, A. Geeraerts, Y. Ivarsson, F. Depoortere, C. Coomans, E. Vermeiren, P. Zimmermann, and G. David Syndecan-syntenin-ALIX regulates the biogenesis of exosomes Nat Cell Biol 14 2012 677 685
38. T. Wollert, and J.H. Hurley Molecular mechanism of multivesciular body biopsies by ESCRT complexes Nature 464 2010 864 869
39. K. Trajkovic, C. Hsh, S. Chiantia, L. Rajendran, D. Wenzel, F. Wieland, P. Schwille, B. Brügger, and M. Simons Ceramide triggers budding of exosome vesicles into multivesicular endosomes Science 319 2008 1244 1247
40. C.A. Thompson, A. Purushothaman, V.C. Ramani, I. Vlodavsky, and R.D. Sanderson Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes J Biol Chem 288 2013 10093 10099
41. D. Skokos, H.G. Botros, C. Demeure, J. Morin, R. Peronet, G. Birkenmeier, S. Boudaly, and S. Mécheri Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo J Immunol 170 2003 3037 3045
42. A.E. Morelli, A.T. Larregina, W.J. Shufesky, M.M.L.G. Sullivan, D.B.S. Sullivan, 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
43. G. Van Niel, J. Mallegol, C. Bevilacqua, C. Candalh, S. Brugière, E. Tomaskovic-Crook, J.K. Heath, N. Cerf-Besussan, and M. Heyman Intestinal epithelial exosomes carry MHC class II/peptides able to inform the immune system in mice Gut 52 2003 1690 1697
44. I. Nazarenko, S. Rana, A. Baumann, J. McAlear, A. Hellwig, M. Trendelenburg, G. Lochnit, K.L. Preissner, and M. Zöller Cell surface tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation Cancer Res 70 2010 1668 1678
45. M.P. Caby, D. Lankar, C. Vincendeau-Scherrer, G. Raposo, and C. Bonnerot Exosomal-like vesicles are present in human blood plasma Int Immunol 17 2005 879 887
46. M. Logozzi, A. De Milito, L. Lugini, M. Borghi, L. Calabrò, 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
47. S. Rana, and M. Zöller The Functional Importance of Tetraspanins in Exosomes Emerging Concepts of Tumor Exosomes-Mediated Cell-Cell Communication Z.-H. Zhang, 2013 Springer Science+Business Media New York 69 106
48. L. Blanc, A. De Gassart, C. Geminard, P. Bette-Bobillo, and M. Vidal Exosome release by reticulocytes - an integral part of the red blood cell differentiation system Blood Cells Mol Dis 35 2005 21 26
49. 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
50. C. Barrės, L. Blanc, P. Bette-Bobillo, S. André, R. Marmoun, H.-J. Gabius, and M. Vidal Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages Blood 115 2010 696 705
51. C. Lässer, V.S. Alikhani, K. Ekström, M. Eldh, P.T. Paredes, A. Bossios, M. Sjöstrand, S. Gabrielsson, J. Lötvall, and H. Valadi Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages J Transl Med 9 2011 9
52. H. Valadi, K. Ekström, A. Bossios, M. Sjöstrand, J.J. Lee, and J.O. Lötvall Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells Nat Cell Biol 9 2007 654 659
53. A. Zomer, T. Vendrig, E.S. Hopmans, M. van Eijndhoven, J.M. Middeldorp, and D.M. Pegtel Exosomes: fit to deliver small RNA Commun Integr Biol 3 2010 447 450
54. J.L. Welton, S. Khanna, P.J. Giles, P. Brennan, I.A. Brewis, J. Staffurth, M.D. Mason, and A. Clayton Proteomics analysis of bladder cancer exosomes Mol Cell Proteomics 9 2010 1324 1338
55. M.G. Harrington, A.H. Fonteh, E. Oberins, P. Lise, R.P. Cowan, G. McComb, J.N. Chavez, J. Rush, R.G. Biringer, and A.F. Hühmer The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid Cerebrospinal Fluid Res 6 2009 10
56. L.R. McNally, U. Manne, and W.E. Grizzle Post-transcriptional processing of genetic information and its relation to cancer Biotech Histochem 88 2013 365 372
57. J. Jones, W.E. Grizzle, H. Wang, and C. Yates MicroRNAs that affect prostate cancer: emphasis on prostate cancer in African Americans Biotech Histochem 88 2013 410 424
58. A. Turchinovich, L. Weiz, A. Langheinz, and B. Burwinkel Characterization of extracelluar circulating microRNA Nucleic Acids Res 39 2011 7223 7233
59. J.D. Arroyo, J.R. Chevillet, E.M. Kroh, I.K. Ruf, C.C. Pritchard, D.F. Gibson, P.S. Mitchell, C.F. Bennett, E.L. Pogosova-Agadjanyan, D.L. Stirewalt, J.F. Tait, and M. Tewari Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma Proc Natl Acad Sci U S A 108 2011 5003 5008
60. A. Gallo, M. Tandon, I. Alevizos, and G.G. Illei The majority of microRNAs detectable in serum and saliva is concentrated in exosomes PLoS One 7 2012 e30679
61. M. Belting, and A. Wittrup Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease J Cell Biol 183 2008 1187 1191
62. J.P. Hegmans, M.P.L. Bard, A. Hemmes, T.M. Luider, M.J. Klejimeer, J.-B. Prins, L. Zitvogel, S.A. Burgers, H.C. Hoogsteden, and B.N. Lambrecht Proteomic analysis of exosomes secreted by human mesothelioma cells Am J Pathol 164 2004 1807 1815
63. C. Montpellier, B.A. Tews, J. Poitrimole, V. Rocha-Perugini, V. D'Arienzo, J. Potel, X.A. Zhang, E. Rubinstein, J. Dubuisson, and L. Cocquerel Interacting region of CD81 and two of its partners, EWI-2 and EWI-2wint, and their effect on hepatitis C virus infection J Biol Chem 286 2011 13954 13965
64. Y. Liu, S.V. Shah, X. Xiang, J. Wang, Z.B. Deng, C. Liu, L. Zhang, J. Wu, T. Edmonds, C. Jambor, J.C. Kappes, and H.G. Zhang COP9-associated CSN5 regulates exosomal protein deubiquitination and sorting Am J Pathol 174 2009 1415 1425
65. Z. Deng, R. Pardi, W. Cheadle, X. Xiang, S. Zhang, S.V. Shah, W. Grizzle, D. Miller, J. Mountz, and H-G. Zhang Plant homologue constitutive photomorphogenesis 9 (COP9) signalosome subunit CSN5 regulates innate immune responses in macrophages Blood 117 2011 4796 4804
66. C. Admyre, J. Grunewald, S. Thyberg, S. Gripenbäck, 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
67. K. Skriner, K. Adolph, P.R. Jungblut, and G.R. Burmester Association of citrullinated proteins with synovial exosomes Arthritis Rheum 54 2006 3809 3814
68. 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
69. S. Chang, D.T. Lau, and W. Wong Breast cancer exosome-like microvesicles and salivary gland cells interplay alters salivary gland cell-derived exosome-like microvesicles in vitro PLoS One 7 2012 e33037
70. A. Sabapatha, C. Gerçel-Taylor, and D.D. Taylor Specific isolation of placenta-derived exosomes from the circulation of pregnant women and their immunoregulatory consequences Am J Reprod Immunol 56 2006 345 355
71. D.D. Taylor, S. Akyol, and C. Gerçel-Taylor Pregnancy-associated exosomes and their modulation of T cell signaling J Immunol 176 2006 1534 1542
72. M. Hedlund, A.-C. Stenqvist, O. Nagaeva, L. Kjellberg, M. Wulff, V. Baranov, and L. Mincheva-Nilsson Human placenta expresses and secretes NKG2D ligands via exosomes that down-modulate the cognate receptor expression: evidence for immunosuppressive function J Immunol 183 2009 340 351
73. L. Mincheva-Nilsson Immune cells and molecules in pregnancy: friends or foes to the fetus? Exp Rev Clin Immunol 2 2006 457 470
74. B. Toth, C.A. Lok, A. Böing, J.A. van der Post, K. Friese, and R. Nieuwland Microparticles and exosomes: impact on normal and complicated pregnancy Am J Reprod Immunol 58 2007 389 402
75. J. Bullerdiek, and I. Flor Exosome-delivered microRNAs of "chromosome 19 microRNA cluster" as immunomodulation in pregnancy and tumorigenesis Mol Cytogenet 5 2012 27
76. R. Donker, J.F. Mouillet, T. Chu, C.A. Hubel, D.B. Stolz, A.E. Morelli, and Y. Sadovsky The expression profile of C19MC microRNAs in primary human trophoblast cells and exosomes Mol Hum Reprod 18 2012 417 424
77. S.H. Kim, N. Bianco, R. Menon, E.R. Lechman, W.J. Shufesky, A.E. Morelli, and P.D. Robbins Exosomes derived from genetically modified DC expressing FasL are anti-inflammatory and immunosuppressive Mol Ther 13 2006 289 300
78. A.J. Abusamra, Z. Zhong, X. Zheng, M. Li, T.E. Ichim, J.L. Chin, and W.P. Min Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis Blood Cells Mol Dis 35 2005 169 173
79. D.D. Taylor, C. Gerçel-Taylor, K.S. Lyons, J. Stanson, and T.L. Whiteside T-cell apoptosis and suppression of T-cell receptor/CD3-ζ by fas ligand-containing membrane vesicles shed from ovarian tumors Clin Cancer Res 9 2003 5113 5119
80. + T cells by dendritic cell-derived exosomes Nat Immunol 3 2002 1156 1162
81. 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
82. F. Andre, N. Chaput, N.E.C. 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 are potent cell-free peptide-based vaccine, I: dendritic cell-derived exosomes transfer functional MHC class 1/peptide complexes to dendritic cells Blood 172 2004 2126 2136
83. N. Chaput, N.E.C. Schartz, F. André, J. Taïeb, 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 naïve Tc1 lymphocytes leading to tumor rejection J Immunol 172 2004 2137 2146
84. K.R. Qazo, U. Gehrmann, E.D. Jordö, M.C.I. Karlsson, and S. Gabrielsson Antigen-loaded exosomes alone induce Th 1-type memory through a B cell-dependent mechanism Blood 113 2009 2673 2683
85. G.J. Wang, Y. Liu, A. Qin, S.V. Shah, Z.B. Deng, X. Xiang, Z. Cheng, C. Liu, J. Wang, L. Zhang, W.E. Grizzle, and H.G. Zhang Thymus exosomes-like particles induce regulatory T cells J Immunol 181 2008 5242 5248
86. H.G. Zhang, C. Liu, K. Su, S. Yu, L. Zhang, S. Zhang, J. Wang, X. Cao, W. Grizzle, and R.P. Kimberly A membrane form of TNF-alpha presented by exosomes delays T cell activation-induced cell death J Immunol 176 2006 7385 7393
87. H.G. Zhang, and W.E. Grizzle The effects of exosomes and related vesicles on cancer development, progression and dissemination H.G. Zhang, Emerging Concepts for Tumor Exosome-Mediated Cell-Cell Communication 2013 Springer Science New York, New York 107 129
88. S.-H. Kim, E.R. Lechman, N. Bianco, R. Menon, A. Keravala, J. Nash, Z. Mi, S.C. Watkins, A. Gambotto, and P.D. Robbins Exosomes derived from IL-10-treated dendritic cells can suppress inflammation and collagen-induced arthritis J Immunol 174 2005 6440 6448
89. Z. Cai, W. Zhang, F. Yang, L. Yu, Z. Yu, J.H. Pan, L. Wang, X. Cao, and J. Wang Immunosuppressive exosomes from TGF-β1 gene-modified dendritic cells attenuate Th17-mediated inflammatory autoimmune disease by inducing regulatory T cells Cell Res 22 2012 607 610
90. J. Skog, T. Würdinger, S. van Rijn, D.H. Meijer, L. Gainche, M. SenaEsteves, 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
91. 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
92. D. Xiao, J. Ohlendorf, Y. Chan, D.D. Taylor, S.N. Rai, S. Weigel, W. Zacharias, H. Hao, and K.M. McMasters Identifying mRNA, microRNA and protein profiles of melanoma exosomes PLoS One 7 2012 e46874
93. C. Liu, S. Yu, K. Zinn, J. Wang, L. Zhang, J. Yujiang, J.C. Kappes, S. Barnes, R.P. Kimberly, W.E. Grizzle, and H-G. Zhang Murine mammary carcinomas exosomes promote tumor growth by suppression of NK cell function J Immunol 176 2006 1375 1385
94. 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
95. J.W. Kim, E. Wieckowski, D.D. Taylor, T.E. Reichert, S. Watkins, and T.L. Whiteside Fas ligand-positive membranous vesicles isolated from sera of patients with oral cancer induce apoptosis of activated T lymphocytes Cancer Res 11 2005 1010 1020
96. A. Clayton, J.P. Mitchell, J. Court, S. Linnane, M.D. Mason, and Z. Taby Human tumor-derived exosomes down-modulate NKG2D expression J Immunol 180 2008 7249 7258
97. 2D-mediated functions 97 2012 1295 1303
98. S. Yu, C. Liu, K. Su, J. Wang, Y. Liu, L. Zhang, C. Li, Y. Cong, R. Kimberly, W.E. Grizzle, C. Falkson, and H.G. Zhang Tumor exosomes inhibit differentiation of bone marrow dendritic cells J Immunol 178 2007 6867 6875
99. 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-β-mediated suppressive activity on T lymphocytes Cancer Res 66 2006 9290 9298
100. R. Valenti, V. Huber, M. Ieor, P. Filipazzi, G. Parmiani, and L. Rivoltini Tumor-released microvesicles as vehicles of immunosuppression Cancer Res 67 2007 2912 2915
101. X. Xiang, A. Poliakov, C. Liu, Y. Liu, Z.B. Deng, J. Wang, Z. Cheng, S.V. Shah, G.J. Wang, L. Zhang, W.E. Grizzle, J. Mobley, and H.G. Zhang Induction of myeloid-derived suppressor cells by tumor exosomes Int J Cancer 124 2009 2621 2633
102. C. Liu, S. Yu, J. Kappes, J. Wang, W.E. Grizzle, K.R. Zinn, and H.G. Zhang Expansion of spleen myeloid suppressor cells represses NK cell cytotoxicity in tumor-bearing host Blood 109 2007 4336 4342
103. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
104. A.C. Ochoa, A.H. Zea, C. Hernandez, and P.C. Rodriguez Arginase, prostaglandins and myeloid-derived suppressor cells in renal cell carcinoma Clin Cancer Res 13 2007 721s 736s
105. Y. Liu, X. Xiang, X. Zhang, S. Zhang, C. Liu, Z. Cheng, S.M. Michalek, W.E. Grizzle, and H.G. Zhang Contribution of MyD88 to the tumor exosome-mediated induction of myeloid derived suppressor cells Am J Pathol 176 2010 2490 2499
106. X. Xiang, Y. Liu, X. Zhuang, S. Zhang, S. Michalek, D.D. Taylor, W. Grizzle, and H-G. Zhang TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes Am J Pathol 177 2010 1606 1610
107. M. Szajnik, M. Czystowska, M.J. Szczepanski, M. Mandapathil, and T.L. Whiteside Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg) PLoS One 5 2010 e11469
108. 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
109. K. Al-Nedawi, B. Meehan, R.S. Kerbel, A.C. Allison, and J. Rak Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR Proc Natl Acad Sci U S A 106 2009 3794 3799
110. E. Ristorcelli, E. Beraud, P. Verrando, C. Villard, D. Lafitte, V. Sbarra, D. Lombardo, and A. Verine Human tumor nanoparticles induce apoptosis of pancreatic cancer cells FASEB J 22 2008 3358 3369
111. E. Ristorcelli, E. Beraud, S. Mathieu, D. Lombardo, and A. Verine Essential role of Notch signaling in apoptosis of human pancreatic tumoral cells mediated by exosomal nanoparticles 125 2009 1016 1026
112. J.L. Qu, X.J. Qu, M.F. Zhao, J.E. GTeng, Y. Zhang, K.Z. Hou, Y.H. Jiang, X.H. Yang, and Y.P. Liu Gastric cancer exosomes promote tumour cell proliferation through PI3K/Akt and MAPK/ERK activation Dig Liver Dis 41 2009 875 880
113. S. Khan, J.M.S. Jutzy, J.R. Aspe, D.W. McGregor, J.W. Neidigh, and N.R. Wall Survivin is released from cancer cells via exosomes Apoptosis 16 2011 1 12
114. M.A. Antonyak, B. Li, L.K. Boroughs, J.L. Johnson, J.E. Druso, K.L. Bryant, D.A. Holowks, and R.A. Cerione Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells Proc Natl Acad Sci U S A 12 2011 4852 4857
115. Z. Deng, Z. Cheng, X. Xiang, J. Yan, X. Zhuang, C. Lkiu, 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
116. L.R. McNally, D.R. Welch, B.H. Beck, L.J. Stafford, J.W. Long, J.C. Sellers, Z.Q. Huang, W.E. Grizzle, C.R. Stockard, K.T. Nash, and D.J. Buchsbaum KISS1 over-expression suppresses metastasis of pancreatic adenocarcinoma in a xenograft mouse model Clin Exp Metastasis 27 2010 591 600
117. Y.Y. Chen, M.M. Posada, L.L. Blazer, T. Zhao, and G.R. Rosania The role of the VPS4A-exosome pathway in the intrinsic egress route of a DNA-binding anticancer drug Pharm Res 23 2006 1687 1695
118. J. Li, C.A. Sherman-Baust, M. Tsai-Turton, R.E. Bristow, R.B. Roden, and P. Morin Claudin-containing exosomes in the peripheral circulation of women with ovarian cancer BMC Cancer 9 2009 244
119. J. Nilsson, J. Skog, A. Nordstrand, V. Baranov, L. Mincheva-Nilsson, X.O. Breakefield, and A. Widmark Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer Br J Cancer 100 2009 1603 1607
120. 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
121. E. Iessi, M.L. Marino, F. Lozupone, S. Fais, and A. de Milito Tumor acidity and malignancy: novel aspects in the design of anti-tumor therapy Cancer Ther 6 2008 55 66
122. 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
123. N.K. Narayanan, D. Nargi, C. Randolph, and B.A. Narayanan Liposome encapsulation of curcumin and resveratrol in combination reduces prostate cancer incidence in PTEN knockout mice Int J Cancer 125 2009 1 8
124. D. Sun, X. Zhuang, X. Xiang, Y. Liu, S. Zhang, C. Liu, S. Barnes, W. Grizzle, D. Miller, and H.G. Zhang A novel nanoparticle drug delivery system: the anti-inflammatory activity of curcumin is enhanced when encapsulated in exosomes Mol Ther 18 2010 1606 1614
125. D. Sun, X. Zhuang, S. Zhang, Z.B. Deng, W. Grizzle, D. Miller, and H.G. Zhang Exosomes are endogenous nanoparticles that can deliver biological information between cells Adv Drug Deliv Rev 65 2013 342 347
126. S.-I. Ohno, M. Takanashi, K. Sudo, S. Ueda, A. Ishikawa, N. Matsuyama, K. Fujita, T. Mizutani, T. Ohgi, T. Ochiya, N. Gotoh, and M. Kuroda Systemically injected exosomes targeted to EGFR deliver antitumor microRNA to breast cancer cells Mol Ther 21 2013 185 191