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Peripheral Blood Cell Interactions of Cancer-Derived Exosomes Affect Immune Function

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Cancer Microenvironment

Abstract

Cancer-derived exosomes are constitutively produced and secreted into the blood and biofluids of their host patients providing a liquid biopsy for early detection and diagnosis. Given their ubiquitous nature, cancer exosomes influence biological mechanisms that are beneficial to the tumor cells where they are produced and the microenvironment in which these tumors exist. Accumulating evidence suggests that exosomes transport proteins, lipids, DNA, mRNA, miRNA and long non coding RNA (lncRNA) for the purpose of cell-cell and cell-extracellular communication. These exosomes consistently reflect the status as well as identity of their cell of origin and as such may conceivably be affecting the ability of a functional immune system to recognize and eliminate cancer cells. Recognizing and mapping the pathways in which immune suppression is garnered through these tumor derived exosome (TEX) may lead to treatment strategies in which specific cell membrane proteins or receptors may be targeted, allowing for immune surveillance to once again help with the treatment of cancer. This Review focuses on how cancer exosomes interact with immune cells in the blood.

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Fig. 1: Tumor derived exosomes (TEX) function in favor of metastasis, support angiogenesis, confer chemoresistance and promote immune-suppression and cellular proliferation
Fig. 2: Cancer cells release exosomes which are taken up by other cancer cells, endothelial cells, epithelial cells, fibroblasts, bone marrow myeloid precursor cells, and mesenchymal stem cells

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References

  1. Thery C, Zitvogel L, Amigorena S (2002) Exosomes: composition, biogenesis and function. Nat Rev Immunol 2(8):569–579

    Article  CAS  PubMed  Google Scholar 

  2. Ratajczak J, Miekus K, Kucia M et al (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20(5):847–856

    Article  CAS  PubMed  Google Scholar 

  3. Iero M, Valenti R, Huber V et al (2008) Tumour-released exosomes and their implications in cancer immunity. Cell Death Differ 15(1):80–88

    Article  CAS  PubMed  Google Scholar 

  4. Bobrie A, Krumeich S, Reyal F et al (2012) Rab27a supports exosome-dependent and -independent mechanisms that modify the tumor microenvironment and can promote tumor progression. Cancer Res 72(19):4920–4930

    Article  CAS  PubMed  Google Scholar 

  5. Kalluri R (2016) The biology and function of exosomes in cancer. J Clin Invest 126(4):1208–1215

    Article  PubMed  PubMed Central  Google Scholar 

  6. Feng D, Zhao W-L, Ye Y-Y et al (2010) Cellular internalization of exosomes occurs through phagocytosis. Traffic 11(5):675–687

    Article  CAS  PubMed  Google Scholar 

  7. Thery C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9(8):581–593

    Article  CAS  PubMed  Google Scholar 

  8. Zhang HG, Grizzle WE (2011) Exosomes and cancer: a newly described pathway of immune suppression. Clin Cancer Res 17(5):959–964

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Wolfers J, Lozier A, Raposo G et al (2001) Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7(3):297–303

    Article  CAS  PubMed  Google Scholar 

  10. Mallegol J, van Niel G, Heyman M (2005) Phenotypic and functional characterization of intestinal epithelial exosomes. Blood Cell Mol Dis 35(1):11–16

    Article  CAS  Google Scholar 

  11. Hao S, Bai O, Li F, Yuan J, Laferte S, Xiang J (2007) Mature dendritic cells pulsed with exosomes stimulate efficient cytotoxic T-lymphocyte responses and antitumour immunity. Immunology 120(1):90–102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Zeelenberg IS, Ostrowski M, Krumeich S et al (2008) Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res 68(4):1228–1235

    Article  CAS  PubMed  Google Scholar 

  13. Zeelenberg IS, van Maren WWC, Boissonnas A et al (2011) Antigen localization controls T cell-mediated tumor immunity. J Immunol 187(3):1281–1288

    Article  CAS  PubMed  Google Scholar 

  14. Safaei R, Larson BJ, Cheng TC et al (2005) Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol Cancer Ther 4(10):1595–1604

    Article  CAS  PubMed  Google Scholar 

  15. Shedden K, Xie XT, Chandaroy P, Chang YT, Rosania GR (2003) Expulsion of small molecules in vesicles shed by Cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res 63(15):4331–4337

    CAS  PubMed  Google Scholar 

  16. Khan S, Aspe JR, Asumen MG et al (2009) Extracellular, cell-permeable survivin inhibits apoptosis while promoting proliferative and metastatic potential. Br J Cancer 100(7):1073–1086

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Wang J, Hendrix A, Hernot S et al (2014) Bone marrow stromal cell–derived exosomes as communicators in drug resistance in multiple myeloma cells. Blood 124(4):555–566

    Article  CAS  PubMed  Google Scholar 

  18. D-d Y, Wu Y, Zhang X-h et al (2016) Exosomes from adriamycin-resistant breast cancer cells transmit drug resistance partly by delivering miR-222. Tumor Biol 37(3):3227–3235

    Article  CAS  Google Scholar 

  19. Mitchell P, Welton J, Staffurth J et al (2009) Can urinary exosomes act as treatment response markers in prostate cancer? J Transl Med 7(1):4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Taylor DD, Gercel-Taylor C (2008) MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110(1):13–21

    Article  CAS  PubMed  Google Scholar 

  21. Skog J, Wurdinger T, van Rijn S et al (2008) Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10(12):1470–1476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Welton JL, Khanna S, Giles PJ et al (2010) Proteomics analysis of bladder cancer exosomes. Mol Cell Proteomics 9(6):1324–1338

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Keller S, Ridinger J, Rupp A-K, Janssen J, Altevogt P (2011) Body fluid derived exosomes as a novel template for clinical diagnostics. J Transl Med 9(1):86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Hong C-S, Miller L, Whiteside TL, Boyiadzis M (2014) Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia. Front Immunol 5:160

  25. Turay D, Khan S, Osterman CJD et al (2016) Proteomic profiling of serum-derived exosomes from ethnically diverse prostate Cancer patients. Cancer Investig 34(1):1–11

    Article  CAS  Google Scholar 

  26. Deregibus MC, Cantaluppi V, Calogero R et al (2007) Endothelial progenitor cell–derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110(7):2440–2448

    Article  CAS  PubMed  Google Scholar 

  27. Kawamoto T, Ohga N, Akiyama K et al (2012) Tumor-derived microvesicles induce proangiogenic phenotype in endothelial cells via endocytosis. PLoS One 7(3):e34045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T (2013) Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic MicroRNAs regulate cancer cell metastasis. J Biol Chem 288(15):10849–10859

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Graves LE, Ariztia EV, Navari JR, Matzel HJ, Stack MS, Fishman DA (2004) Proinvasive properties of ovarian cancer ascites-derived membrane vesicles. Cancer Res 64(19):7045–7049

    Article  CAS  PubMed  Google Scholar 

  30. Hood JL, San RS, Wickline SA (2011) Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71(11):3792–3801

    Article  CAS  PubMed  Google Scholar 

  31. Luga V, Zhang L, Viloria-Petit Alicia M et al (2012) Exosomes mediate stromal mobilization of autocrine Wnt-PCP signaling in breast cancer cell migration. Cell 151(7):1542–1556

    Article  CAS  PubMed  Google Scholar 

  32. Peinado H, Aleckovic M, Lavotshkin S et al (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat Med 18(6):883–891

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Suetsugu A, Honma K, Saji S, Moriwaki H, Ochiya T, Hoffman RM (2013) Imaging exosome transfer from breast cancer cells to stroma at metastatic sites in orthotopic nude-mouse models. Adv Drug Deliv Rev 65(3):383–390

    Article  CAS  PubMed  Google Scholar 

  34. Mulcahy LA, Pink RC, Carter DRF (2014) Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles 3. https://doi.org/10.3402/jev.v3403.24641

  35. Nazarenko I, Rana S, Baumann A et al (2010) Cell surface Tetraspanin Tspan8 contributes to molecular pathways of exosome-induced endothelial cell activation. Cancer Res 70(4):1668–1678

    Article  CAS  PubMed  Google Scholar 

  36. Rana S, Yue S, Stadel D, Zöller M (2012) Toward tailored exosomes: the exosomal tetraspanin web contributes to target cell selection. Int J Biochem Cell Biol 44(9):1574–1584

    Article  CAS  PubMed  Google Scholar 

  37. Paggetti J, Haderk F, Seiffert M et al (2015) Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts. Blood 126(9):1106–1117

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Obregon C, Rothen-Rutishauser B, Gerber P, Gehr P, Nicod LP (2009) Active uptake of dendritic cell-derived exovesicles by epithelial cells induces the release of inflammatory mediators through a TNF-α-mediated pathway. Am J Pathol 175(2):696–705

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Clayton A, Turkes A, Dewitt S, Steadman R, Mason MD, Hallett MB (2004) Adhesion and signaling by B cell-derived exosomes: the role of integrins. FASEB J 18:977–979

    Article  CAS  PubMed  Google Scholar 

  40. Franzen CA, Simms PE, Van Huis AF, Foreman KE, Kuo PC, Gupta GN (2014) Characterization of uptake and internalization of exosomes by bladder cancer cells. Biomed Res Int 2014:619829

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Parolini I, Federici C, Raggi C et al (2009) Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem 284(49):34211–34222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Smyth TJ, Redzic JS, Graner MW, Anchordoquy TJ (2014) Examination of the specificity of tumor cell derived exosomes with tumor cells in vitro. Biochim Biophys Acta Biomembr 1838(11):2954–2965

    Article  CAS  Google Scholar 

  43. Escrevente C, Keller S, Altevogt P, Costa J (2011) Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 11(1):1–10

    Article  CAS  Google Scholar 

  44. Svensson KJ, Christianson HC, Wittrup A et al (2013) Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid raft-mediated endocytosis negatively regulated by Caveolin-1. J Biol Chem 288(24):17713–17724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Christianson HC, Svensson KJ, van Kuppevelt TH, Li J-P, Belting M (2013) Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci 110(43):17380–17385

    Article  PubMed  PubMed Central  Google Scholar 

  46. Chiba M, Kimura M, Asari S (2012) Exosomes secreted from human colorectal cancer cell lines contain mRNAs, microRNAs and natural antisense RNAs, that can transfer into the human hepatoma HepG2 and lung cancer A549 cell lines. Oncol Rep 28(5):1551–1558

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. O’Brien K, Rani S, Corcoran C et al (2013) Exosomes from triple-negative breast cancer cells can transfer phenotypic traits representing their cells of origin to secondary cells. Eur J Cancer 49(8):1845–1859

    Article  CAS  PubMed  Google Scholar 

  48. Riches A, Campbell E, Borger E, Powis S (2014) Regulation of exosome release from mammary epithelial and breast cancer cells – a new regulatory pathway. Eur J Cancer 50(5):1025–1034

    Article  CAS  PubMed  Google Scholar 

  49. Bennit HF, Gonda A, Oppegard L, Chi D, Khan S, Wall NR (2017) Uptake of lymphoma-derived exosomes by peripheral blood leukocytes. Blood and Lymphatic Cancer: Targets and Therapy 7:9–23

  50. Lässer C, Seyed Alikhani V, Ekström K et al (2011) Human saliva, plasma and breast milk exosomes contain RNA: uptake by macrophages. J Transl Med 9(1):1–8

    Article  CAS  Google Scholar 

  51. Chow A, Zhou W, Liu L et al (2014) Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-κB. Sci Rep 4:5750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Saunderson SC, Dunn AC, Crocker PR, McLellan AD (2014) CD169 mediates the capture of exosomes in spleen and lymph node. Blood 123(2):208–216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Barrès C, Blanc L, Bette-Bobillo P et al (2010) Galectin-5 is bound onto the surface of rat reticulocyte exosomes and modulates vesicle uptake by macrophages. Blood 115(3):696–705

    Article  CAS  PubMed  Google Scholar 

  54. Danesh A, Inglis HC, Jackman RP et al (2014) Exosomes from red blood cell units bind to monocytes and induce proinflammatory cytokines, boosting T-cell responses in vitro. Blood 123(5):687–696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Cai J, Han Y, Ren H et al (2013) Extracellular vesicle-mediated transfer of donor genomic DNA to recipient cells is a novel mechanism for genetic influence between cells. J Mol Cell Biol 5(4):227–238

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Cai J, Wu G, Tan X et al (2014) Transferred BCR/ABL DNA from K562 extracellular vesicles causes chronic myeloid leukemia in immunodeficient mice. PLoS One 9(8):e105200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Morelli AE, Larregina AT, Shufesky WJ et al (2004) Endocytosis, intracellular sorting, and processing of exosomes by dendritic cells. Blood 104(10):3257–3266

    Article  CAS  PubMed  Google Scholar 

  58. Wubbolts R, Leckie RS, Veenhuizen PT et al (2003) Proteomic and biochemical analyses of human B cell-derived exosomes. Potential implications for their function and multivesicular body formation. J Biol Chem 278(13):10963–10972

    Article  CAS  PubMed  Google Scholar 

  59. Segura E, Guerin C, Hogg N, Amigorena S, Thery C (2007) CD8+ dendritic cells use LFA-1 to capture MHC-peptide complexes from exosomes in vivo. J Immunol 179(3):1489–1496

    Article  CAS  PubMed  Google Scholar 

  60. Xie J, Zhu H, Guo L et al (2010) Lectin-like oxidized low-density lipoprotein receptor-1 delivers heat shock protein 60-fused antigen into the MHC class I presentation pathway. J Immunol 185(4):2306–2313

    Article  CAS  PubMed  Google Scholar 

  61. Bastos-Amador P, Perez-Cabezas B, Izquierdo-Useros N et al (2012) Capture of cell-derived microvesicles (exosomes and apoptotic bodies) by human plasmacytoid dendritic cells. J Leukoc Biol 91(5):751–758

    Article  CAS  PubMed  Google Scholar 

  62. Czernek L, Chworos A, Duechler M (2015) The uptake of extracellular vesicles is affected by the differentiation status of myeloid cells. Scand J Immunol 82(6):506–514

    Article  CAS  PubMed  Google Scholar 

  63. Sheng H, Hassanali S, Nugent C et al (2011) Insulinoma-released exosomes or microparticles are immunostimulatory and can activate autoreactive T cells spontaneously developed in nonobese diabetic mice. J Immunol 187(4):1591–1600

    Article  CAS  PubMed  Google Scholar 

  64. Skokos D, Botros HG, Demeure C et al (2003) Mast cell-derived exosomes induce phenotypic and functional maturation of dendritic cells and elicit specific immune responses in vivo. J Immunol 170(6):3037–3045

    Article  CAS  PubMed  Google Scholar 

  65. Yu S, Liu C, Su K et al (2007) Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol 178(11):6867–6875

    Article  CAS  PubMed  Google Scholar 

  66. Xiang X, Poliakov A, Liu C et al (2009) Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer 124(11):2621–2633

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Segura E, Amigorena S, Thery C (2005) Mature dendritic cells secrete exosomes with strong ability to induce antigen-specific effector immune responses. Blood Cells Mol Dis 35(2):89–93

    Article  CAS  PubMed  Google Scholar 

  68. Segura E, Nicco C, Lombard B et al (2005) ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 106(1):216–223

    Article  CAS  PubMed  Google Scholar 

  69. Kopper L, Sebestyen A, Gallai M, Kovalszky I (1997) Syndecan-1 - a new piece in B-cell puzzle. Pathol Oncol Res 3(3):183–191

    Article  CAS  PubMed  Google Scholar 

  70. Sanderson RD, Lalor P, Bernfield M (1989) B lymphocytes express and lose syndecan at specific stages of differentiation. Cell Regul 1(1):27–35

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Vallhov H, Gutzeit C, Johansson SM et al (2011) Exosomes containing glycoprotein 350 released by EBV-transformed B cells selectively target B cells through CD21 and block EBV infection in vitro. J Immunol 186(1):73–82

    Article  CAS  PubMed  Google Scholar 

  72. Hazan-Halevy I, Rosenblum D, Weinstein S, Bairey O, Raanani P, Peer D (2015) Cell-specific uptake of mantle cell lymphoma-derived exosomes by malignant and non-malignant B-lymphocytes. Cancer Lett 364(1):59–69

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Raposo G, Nijman HW, Stoorvogel W et al (1996) B lymphocytes secrete antigen-presenting vesicles. J Exp Med 183(3):1161–1172

    Article  CAS  PubMed  Google Scholar 

  74. Escola JM, Kleijmeer MJ, Stoorvogel W, Griffith JM, Yoshie O, Geuze HJ (1998) Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J Biol Chem 273(32):20121–20127

    Article  CAS  PubMed  Google Scholar 

  75. Dolcetti R (2015) Cross-talk between Epstein-Barr virus and microenvironment in the pathogenesis of lymphomas. Semin Cancer Biol 34:58–69

    Article  CAS  PubMed  Google Scholar 

  76. Nanbo A, Kawanishi E, Yoshida R, Yoshiyama H (2013) Exosomes derived from Epstein-Barr virus-infected cells are internalized via caveola-dependent endocytosis and promote phenotypic modulation in target cells. J Virol 87(18):10334–10347

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Gutzeit C, Nagy N, Gentile M et al (2014) Exosomes derived from Burkitt's lymphoma cell lines induce proliferation, differentiation, and class-switch recombination in B cells. J Immunol 192(12):5852–5862

    Article  CAS  PubMed  Google Scholar 

  78. Dukers DF, Meij P, Vervoort MB et al (2000) Direct immunosuppressive effects of EBV-encoded latent membrane protein 1. J Immunol 165(2):663–670

    Article  CAS  PubMed  Google Scholar 

  79. Vincent-Schneider H, Stumptner-Cuvelette P, Lankar D et al (2002) Exosomes bearing HLA-DR1 molecules need dendritic cells to efficiently stimulate specific T cells. Int Immunol 14(7):713–722

    Article  CAS  PubMed  Google Scholar 

  80. Thery C, Duban L, Segura E, Veron P, Lantz O, Amigorena S (2002) Indirect activation of naive CD4+ T cells by dendritic cell-derived exosomes. Nat Immunol 3(12):1156–1162

    Article  CAS  PubMed  Google Scholar 

  81. Sprent J (2005) Direct stimulation of naive T cells by antigen-presenting cell vesicles. Blood Cells Mol Dis 35(1):17–20

    Article  CAS  PubMed  Google Scholar 

  82. Zech D, Rana S, Buchler MW, Zoller M (2012) Tumor-exosomes and leukocyte activation: an ambivalent crosstalk. Cell Commun Signal 10(1):37

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Arnold PY, Mannie MD (1999) Vesicles bearing MHC class II molecules mediate transfer of antigen from antigen-presenting cells to CD4+ T cells. Eur J Immunol 29(4):1363–1373

    Article  CAS  PubMed  Google Scholar 

  84. Hwang I, Ki D (2011) Receptor-mediated T cell absorption of antigen presenting cell-derived molecules. Front Biosci (Landmark Ed) 16:411–421

    Article  CAS  Google Scholar 

  85. Nolte-'t Hoen EN, Buschow SI, Anderton SM, Stoorvogel W, Wauben MH (2009) Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 113(9):1977–1981

    Article  CAS  PubMed  Google Scholar 

  86. Stenqvist AC, Nagaeva O, Baranov V, Mincheva-Nilsson L (2013) Exosomes secreted by human placenta carry functional Fas ligand and TRAIL molecules and convey apoptosis in activated immune cells, suggesting exosome-mediated immune privilege of the fetus. J Immunol 191(11):5515–5523

    Article  CAS  PubMed  Google Scholar 

  87. Wang R, Xu A, Zhang X, Wu J et al (2017) Novel exosome-targeted T-cell-based vaccine counteracts T-cell anergy and converts CTL exhaustion in chronic infection via CD40L signaling through the mTORC1 pathway. Cell Mol Immunol 14(6):529–545

  88. Clayton A, Mitchell JP, Court J, Linnane S, Mason MD, Tabi Z (2008) Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol 180(11):7249–7258

    Article  CAS  PubMed  Google Scholar 

  89. Clayton A, Tabi Z (2005) Exosomes and the MICA-NKG2D system in cancer. Blood Cells Mol Dis 34(3):206–213

    Article  CAS  PubMed  Google Scholar 

  90. Ashiru O, Boutet P, Fernandez-Messina L et al (2010) 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 70(2):481–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Hong CS, Muller L, Whiteside TL, Boyiadzis M (2014) Plasma exosomes as markers of therapeutic response in patients with acute myeloid leukemia. Front Immunol 5:160

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Viaud S, Terme M, Flament C et al (2009) Dendritic cell-derived exosomes promote natural killer cell activation and proliferation: a role for NKG2D ligands and IL-15Ralpha. PLoS One 4(3):e4942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Keller S, Konig AK, Marme F et al (2009) Systemic presence and tumor-growth promoting effect of ovarian carcinoma released exosomes. Cancer Lett 278(1):73–81

    Article  CAS  PubMed  Google Scholar 

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Research reported in this publication was supported by NIH awards P20MD006988.

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Correspondence to Nathan R. Wall.

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Ferguson Bennit, H.R., Gonda, A., McMullen, J.R.W. et al. Peripheral Blood Cell Interactions of Cancer-Derived Exosomes Affect Immune Function. Cancer Microenvironment 12, 29–35 (2019). https://doi.org/10.1007/s12307-018-0209-1

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