Glioblastoma stem cell-derived exosomes induce M2 macrophages and PD-L1 expression on human monocytes

References

• Simons M, Raposo G. Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21(4):575–581. doi:10.1016/j.ceb.2009.03.007
   PubMed Web of Science ®Google Scholar
• Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014;3:1–14. doi:10.3402/jev.v3.24641.
   Google Scholar
• Tian T, Zhu YL, Hu FH, Wang YY, Huang NP, Xiao ZD. Dynamics of exosome internalization and trafficking. J Cell Physiol. 2013;228(7):1487–1495. doi:10.1002/jcp.24304
   PubMed Web of Science ®Google Scholar
• Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, Morgelin M, Belting M. Exosome uptake depends on ERK1/2-heat shock protein 27 signaling and lipid raft-mediated endocytosis negatively regulated by caveolin-1. J Biol Chem. 2013;288(24):17713–17724. doi:10.1074/jbc.M112.445403
   PubMed Web of Science ®Google Scholar
• Manda SV, Kataria Y, Tatireddy BR, Ramakrishnan B, Ratnam BG, Lath R, Ranjan A, Ray A. Exosomes as a biomarker platform for detecting epidermal growth factor receptor-positive high-grade gliomas. J Neurosurg. 2017:1–11. doi:10.3171/2016.11.JNS161187
   PubMed Web of Science ®Google Scholar
• Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, Rak J. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci U S A. 2009;106(10):3794–3799. doi:10.1073/pnas.0804543106
   PubMed Web of Science ®Google Scholar
• Skog J, Wurdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Jr., Carter BS, Krichevsky AM, Breakefield XO. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470–1476. doi:10.1038/ncb1800
   PubMed Web of Science ®Google Scholar
• Svensson KJ, Kucharzewska P, Christianson HC, Skold S, Lofstedt T, Johansson MC, Morgelin M, Bengzon J, Ruf W, Belting M. Hypoxia triggers a proangiogenic pathway involving cancer cell microvesicles and PAR-2-mediated heparin-binding EGF signaling in endothelial cells. Proc Natl Acad Sci U S A. 2011;108(32):13147–13152. doi:10.1073/pnas.1104261108
   PubMed Web of Science ®Google Scholar
• Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA, Bigner DD. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009;23(5):1541–1557. doi:10.1096/fj.08-122184
   PubMed Web of Science ®Google Scholar
• Bu N, Wu H, Sun B, Zhang G, Zhan S, Zhang R, Zhou L. Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma. J Neurooncol. 2011;104(3):659–667. doi:10.1007/s11060-011-0537-1
   PubMed Web of Science ®Google Scholar
• Zhang HG, Kim H, Liu C, Yu S, Wang J, Grizzle WE, Kimberly RP, Barnes S. Curcumin reverses breast tumor exosomes mediated immune suppression of NK cell tumor cytotoxicity. Biochim Biophys Acta. 2007;1773(7):1116–1123. doi:10.1016/j.bbamcr.2007.04.015
   PubMed Web of Science ®Google Scholar
• Yu S, Liu C, Su K, Wang J, Liu Y, Zhang L, Li C, Cong Y, Kimberly R, Grizzle WE, et al. Tumor exosomes inhibit differentiation of bone marrow dendritic cells. J Immunol. 2007;178(11):6867–6875. doi:10.4049/jimmunol.178.11.6867
   PubMed Web of Science ®Google Scholar
• Abusamra AJ, Zhong Z, Zheng X, Li M, Ichim TE, Chin JL, Min WP. Tumor exosomes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol Dis. 2005;35(2):169–173. doi:10.1016/j.bcmd.2005.07.001
   PubMed Web of Science ®Google Scholar
• Clayton A, Mitchell JP, Court J, Mason MD, Tabi Z. Human tumor-derived exosomes selectively impair lymphocyte responses to interleukin-2. Cancer Res. 2007;67(15):7458–7466. doi:10.1158/0008-5472.CAN-06-3456
   PubMed Web of Science ®Google Scholar
• Szajnik M, Czystowska M, Szczepanski MJ, Mandapathil M, Whiteside TL. Tumor-derived microvesicles induce, expand and up-regulate biological activities of human regulatory T cells (Treg). PLoS One. 2010;5(7):e11469. doi:10.1371/journal.pone.0011469
   PubMed Web of Science ®Google Scholar
• Gabrusiewicz K, Rodriguez B, Wei J, Hashimoto Y, Healy LM, Maiti SN, Thomas G, Zhou S, Wang Q, Elakkad A, et al. Glioblastoma-infiltrated innate immune cells resemble M0 macrophage phenotype. JCI insight. 2016;1(2):1–19. doi:10.1172/jci.insight.85841.
   Web of Science ®Google Scholar
• Wynn TA, Chawla A, Pollard JW. Macrophage biology in development, homeostasis and disease. Nature. 2013;496(7446):445–455. doi:10.1038/nature12034
   PubMed Web of Science ®Google Scholar
• Sica A, Mantovani A. Macrophage plasticity and polarization: in vivo veritas. J Clin Invest. 2012;122(3):787–795. doi:10.1172/JCI59643
   PubMed Web of Science ®Google Scholar
• Wu A, Wei J, Kong LY, Wang Y, Priebe W, Qiao W, Sawaya R, Heimberger AB. Glioma cancer stem cells induce immunosuppressive macrophages/microglia. Neuro Oncol. 2010;12(11):1113–1125. doi:10.1093/neuonc/noq082
   PubMed Web of Science ®Google Scholar
• Yu H, Kortylewski M, Pardoll D. Crosstalk between cancer and immune cells: role of STAT3 in the tumour microenvironment. Nat Rev Immunol. 2007;7(1):41–51. doi:10.1038/nri1995
   PubMed Web of Science ®Google Scholar
• Wei J, Barr J, Kong LY, Wang Y, Wu A, Sharma AK, Gumin J, Henry V, Colman H, Priebe W, et al. Glioblastoma cancer-initiating cells inhibit T-cell proliferation and effector responses by the signal transducers and activators of transcription 3 pathway. Mol Cancer Ther. 2010;9(1):67–78. doi:10.1158/1535-7163.MCT-09-0734
   PubMed Web of Science ®Google Scholar
• Thery C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr Protoc Cell Biol. 2006;Chapter 3:Unit 3 22.
   PubMedGoogle Scholar
• Logozzi M, De Milito A, Lugini L, Borghi M, Calabro L, Spada M, Perdicchio M, Marino ML, Federici C, Iessi E, et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One. 2009;4(4):e5219. doi:10.1371/journal.pone.0005219
   PubMed Web of Science ®Google Scholar
• Schenkel AR, Mamdouh Z, Muller WA. Locomotion of monocytes on endothelium is a critical step during extravasation. Nat Immunol. 2004;5(4):393–400. doi:10.1038/ni1051
   PubMed Web of Science ®Google Scholar
• Cogswell J, Inzunza HD, Wu Q, Feder JN, Mintier G, Novotny J, Cardona DM. An Analytical Comparison of Dako 28-8 PharmDx Assay and an E1L3N Laboratory-Developed Test in the Immunohistochemical Detection of Programmed Death-Ligand 1. Mol Diagn Ther. 2017;21(1):85–93. doi:10.1007/s40291-016-0237-9
   PubMed Web of Science ®Google Scholar
• Vries MH, Wagenaar A, Verbruggen SE, Molin DG, Dijkgraaf I, Hackeng TH, Post MJ. CXCL1 promotes arteriogenesis through enhanced monocyte recruitment into the peri-collateral space. Angiogenesis. 2015;18(2):163–171. doi:10.1007/s10456-014-9454-1
   PubMed Web of Science ®Google Scholar
• Fang L, Hodge J, Saaoud F, Wang J, Iwanowycz S, Wang Y, Hui Y, Evans TD, Razani B, Fan D. Transcriptional factor EB regulates macrophage polarization in the tumor microenvironment. Oncoimmunology. 2017;6(5):e1312042. doi:10.1080/2162402X.2017.1312042
   PubMed Web of Science ®Google Scholar
• Rocher C, Singla DK. SMAD-PI3K-Akt-mTOR pathway mediates BMP-7 polarization of monocytes into M2 macrophages. PLoS One. 2013;8(12):e84009. doi:10.1371/journal.pone.0084009
   PubMed Web of Science ®Google Scholar
• Zhou J, Qu Z, Sun F, Han L, Li L, Yan S, Stabile LP, Chen LF, Siegfried JM, Xiao G. Myeloid STAT3 Promotes Lung Tumorigenesis by Transforming Tumor Immunosurveillance into Tumor-Promoting Inflammation. Cancer Immunol Res. 2017;5(3):257–268. doi:10.1158/2326-6066.CIR-16-0073
   PubMed Web of Science ®Google Scholar
• Gkouveris I, Nikitakis N, Karanikou M, Rassidakis G, Sklavounou A. JNK1/2 expression and modulation of STAT3 signaling in oral cancer. Oncology letters. 2016;12(1):699–706.
   PubMed Web of Science ®Google Scholar
• Andre F, Schartz NE, Movassagh M, Flament C, Pautier P, Morice P, Pomel C, Lhomme C, Escudier B, Le Chevalier T, et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet. 2002;360(9329):295–305. doi:10.1016/S0140-6736(02)09552-1
   PubMed Web of Science ®Google Scholar
• Hellwinkel JE, Redzic JS, Harland TA, Gunaydin D, Anchordoquy TJ, Graner MW. Glioma-derived extracellular vesicles selectively suppress immune responses. Neuro Oncol. 2016;18(4):497–506. doi:10.1093/neuonc/nov170
   PubMed Web of Science ®Google Scholar
• Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med. 2001;7(3):297–303. doi:10.1038/85438
   PubMed Web of Science ®Google Scholar
• Xiang X, Poliakov A, Liu C, Liu Y, Deng ZB, Wang J, Cheng Z, Shah SV, Wang GJ, Zhang L, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer. 2009;124(11):2621–2633. doi:10.1002/ijc.24249
   PubMed Web of Science ®Google Scholar
• Andreola G, Rivoltini L, Castelli C, Huber V, Perego P, Deho P, Squarcina P, Accornero P, Lozupone F, Lugini L, et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med. 2002;195(10):1303–1316. doi:10.1084/jem.20011624
   PubMed Web of Science ®Google Scholar
• Klibi J, Niki T, Riedel A, Pioche-Durieu C, Souquere S, Rubinstein E, Le Moulec S, Guigay J, Hirashima M, Guemira F, et al. Blood diffusion and Th1-suppressive effects of galectin-9-containing exosomes released by Epstein-Barr virus-infected nasopharyngeal carcinoma cells. Blood. 2009;113(9):1957–1966. doi:10.1182/blood-2008-02-142596
   PubMed Web of Science ®Google Scholar
• Taylor DD, Gercel-Taylor C, Lyons KS, Stanson J, Whiteside TL. T-cell apoptosis and suppression of T-cell receptor/CD3-zeta by Fas ligand-containing membrane vesicles shed from ovarian tumors. Clin Cancer Res. 2003;9(14):5113–5119.
   PubMed Web of Science ®Google Scholar
• Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, Boireau W, Rouleau A, Simon B, Lanneau D, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120(2):457–471.
   PubMed Web of Science ®Google Scholar
• Xiang X, Liu Y, Zhuang X, Zhang S, Michalek S, Taylor DD, Grizzle W, Zhang HG. TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. Am J Pathol. 2010;177(4):1606–1610. doi:10.2353/ajpath.2010.100245
   PubMed Web of Science ®Google Scholar
• Domenis R, Cesselli D, Toffoletto B, Bourkoula E, Caponnetto F, Manini I, Beltrami AP, Ius T, Skrap M, Di Loreto C, et al. Systemic T Cells Immunosuppression of Glioma Stem Cell-Derived Exosomes Is Mediated by Monocytic Myeloid-Derived Suppressor Cells. PLoS One. 2017;12(1):e0169932. doi:10.1371/journal.pone.0169932
   PubMed Web of Science ®Google Scholar
• Okada M, Saio M, Kito Y, Ohe N, Yano H, Yoshimura S, Iwama T, Takami T. Tumor-associated macrophage/microglia infiltration in human gliomas is correlated with MCP-3, but not MCP-1. Int J Oncol. 2009;34(6):1621–1627.
   PubMed Web of Science ®Google Scholar
• Wang D, Sun H, Wei J, Cen B, DuBois RN. CXCL1 is critical for pre-metastatic niche formation and metastasis in colorectal cancer. Cancer Res. 2017;77(13):3655–3665. doi:10.1158/0008-5472.CAN-16-3199.
   Google Scholar
• Haderk F, Schulz R, Iskar M, Cid LL, Worst T, Willmund KV, Schulz A, Warnken U, Seiler J, Benner A, et al. Tumor-derived exosomes modulate PD-L1 expression in monocytes. Sci Immunol. 2017;2(13). doi:10.1126/sciimmunol.aah5509
   PubMed Web of Science ®Google Scholar
• van der Vos KE, Abels ER, Zhang X, Lai C, Carrizosa E, Oakley D, Prabhakar S, Mardini O, Crommentuijn MH, Skog J, et al. Directly visualized glioblastoma-derived extracellular vesicles transfer RNA to microglia/macrophages in the brain. Neuro Oncol. 2016;18(1):58–69. doi:10.1093/neuonc/nov244
   PubMed Web of Science ®Google Scholar
• Yu H, Pardoll D, Jove R. STATs in cancer inflammation and immunity: a leading role for STAT3. Nat Rev Cancer. 2009;9(11):798–809. doi:10.1038/nrc2734
   PubMed Web of Science ®Google Scholar
• Niemand C, Nimmesgern A, Haan S, Fischer P, Schaper F, Rossaint R, Heinrich PC, Muller-Newen G. Activation of STAT3 by IL-6 and IL-10 in primary human macrophages is differentially modulated by suppressor of cytokine signaling 3. J Immunol. 2003;170(6):3263–3272. doi:10.4049/jimmunol.170.6.3263
   PubMed Web of Science ®Google Scholar
• Marzec M, Zhang Q, Goradia A, Raghunath PN, Liu X, Paessler M, Wang HY, Wysocka M, Cheng M, Ruggeri BA, et al. Oncogenic kinase NPM/ALK induces through STAT3 expression of immunosuppressive protein CD274 (PD-L1, B7-H1). Proc Natl Acad Sci U S A. 2008;105(52):20852–20857. doi:10.1073/pnas.0810958105
   PubMed Web of Science ®Google Scholar
• Horlad H, Ma C, Yano H, Pan C, Ohnishi K, Fujiwara Y, Endo S, Kikukawa Y, Okuno Y, Matsuoka M, et al. An IL-27/Stat3 axis induces expression of programmed cell death 1 ligands (PD-L1/2) on infiltrating macrophages in lymphoma. Cancer Sci. 2016;107(11):1696–1704. doi:10.1111/cas.13065
   PubMed Web of Science ®Google Scholar
• Chen W, Ma T, Shen XN, Xia XF, Xu GD, Bai XL, Liang TB. Macrophage-induced tumor angiogenesis is regulated by the TSC2-mTOR pathway. Cancer Res. 2012;72(6):1363–1372. doi:10.1158/0008-5472.CAN-11-2684
   PubMed Web of Science ®Google Scholar
• Bloch O, Crane CA, Kaur R, Safaee M, Rutkowski MJ, Parsa AT. Gliomas promote immunosuppression through induction of B7-H1 expression in tumor-associated macrophages. Clin Cancer Res. 2013;19(12):3165–3175. doi:10.1158/1078-0432.CCR-12-3314
   PubMed Web of Science ®Google Scholar