Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

ACC 2024 Congress

Catch up on all the top stories and latest evidence in cardiology research with our ACC 2024 Congress hub page.
ADVANCED SEARCH
Log in
Top
Journal of Hematology & Oncology
Published in: Journal of Hematology & Oncology 1/2019

Open Access 01-12-2019 | Review

Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment

Authors: Xinyu Tian, Han Shen, Zhiyang Li, Tingting Wang, Shengjun Wang

Published in: Journal of Hematology & Oncology | Issue 1/2019

Login to get access

Abstract

Plenty of immune cells infiltrate into the tumor microenvironment (TME) during tumor progression, in which myeloid-derived suppressor cells (MDSCs) represent a heterogeneous population of immature myeloid cells with immunosuppressive activity. Tumor cells and stromal cells facilitate the activation and expansion of MDSCs in TME via intercellular communication, and expanded MDSCs suppress anti-tumor immune responses through direct and indirect mechanisms. Currently, exosomes, which are a kind of extracellular vesicles (EVs) that can convey functional components, are demonstrated to participate in the local and distal intercellular communication between cells. Numerous studies have supposed that tumor-derived exosomes (TEXs), whose assembly and release can be modulated by TME, are capable of modulating the cell biology of MDSCs, including facilitating their activation, promoting the expansion, and enhancing the immunosuppressive function. Therefore, in this review, we mainly focus on the role of TEXs in the cell-cell communication between tumor cells and MDSCs, and discuss their clinical applications.
Literature
1.
Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell. 2016;30(6):836–48.PubMedPubMedCentralCrossRef
2.
Choo YW, Kang M, Kim HY, Han J, Kang S, Lee JR, et al. M1 Macrophage-derived nanovesicles potentiate the anticancer efficacy of immune checkpoint inhibitors. ACS Nano. 2018;12(9):8977–93.PubMedCrossRef
3.
Wang Y, Tian J, Tang X, Rui K, Tian X, Ma J, et al. Exosomes released by granulocytic myeloid-derived suppressor cells attenuate DSS-induced colitis in mice. Oncotarget. 2016;7(13):15356–68.PubMedPubMedCentral
4.
5.
Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, et al. Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res. 2006;66(18):9290–8.PubMedCrossRef
6.
Chen W, Jiang J, Xia W, Huang J. Tumor-related exosomes contribute to tumor-promoting microenvironment: an immunological perspective. J Immunol Res. 2017;2017:1073947.PubMedPubMedCentral
7.
8.
Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, et al. The terminology issue for myeloid-derived suppressor cells. Cancer Res. 2007;67(1):425.PubMedPubMedCentralCrossRef
9.
Tian J, Rui K, Hong Y, Wang X, Xiao F, Lin X, et al. Increased GITRL Impairs the function of myeloid-derived suppressor cells and exacerbates primary Sjogren syndrome. J Immunol. 2019;202(6):1693–703.PubMedCrossRef
10.
11.
12.
Dumitru CA, Moses K, Trellakis S, Lang S, Brandau S. Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol Immunother. 2012;61(8):1155–67.PubMedCrossRef
13.
Solito S, Marigo I, Pinton L, Damuzzo V, Mandruzzato S, Bronte V. Myeloid-derived suppressor cell heterogeneity in human cancers. Ann N Y Acad Sci. 2014;1319:47–65.PubMedCrossRef
14.
Zheng Y, Tian X, Wang T, Xia X, Cao F, Tian J, et al. Long noncoding RNA Pvt1 regulates the immunosuppression activity of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. Mol Cancer. 2019;18(1):61.PubMedPubMedCentralCrossRef
15.
Betsch A, Rutgeerts O, Fevery S, Sprangers B, Verhoef G, Dierickx D, et al. Myeloid-derived suppressor cells in lymphoma: the good, the bad and the ugly. Blood Rev. 2018;32(6):490–8.PubMedCrossRef
16.
Li L, Wang L, Li J, Fan Z, Yang L, Zhang Z, et al. Metformin-induced reduction of CD39 and CD73 blocks myeloid-derived suppressor cell activity in patients with ovarian cancer. Cancer Res. 2018;78(7):1779–91.PubMedPubMedCentralCrossRef
17.
18.
EL Andaloussi S, Mager I, Breakefield XO, Wood MJ. Extracellular vesicles: biology and emerging therapeutic opportunities. Nat Rev Drug Disc. 2013;12(5):347–57.CrossRef
19.
20.
Bebelman MP, Smit MJ, Pegtel DM, Baglio SR. Biogenesis and function of extracellular vesicles in cancer. Pharmacol Ther. 2018;188:1–11.PubMedCrossRef
21.
Villarroya-Beltri C, Baixauli F, Gutierrez-Vazquez C, Sanchez-Madrid F, Mittelbrunn M. Sorting it out: regulation of exosome loading. Semin Cancer Biol. 2014;28:3–13.PubMedPubMedCentralCrossRef
22.
Yanez-Mo M, Siljander PR, Andreu Z, Zavec AB, Borras FE, Buzas EI, et al. Biological properties of extracellular vesicles and their physiological functions. J Extracell Vesicles. 2015;4:27066.PubMedCrossRef
23.
Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM. 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):17713–24.PubMedPubMedCentralCrossRef
24.
Colombo M, Moita C, van Niel G, Kowal J, Vigneron J, Benaroch P, et al. Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci. 2013;126(Pt 24):5553–65.PubMedCrossRef
25.
26.
Kosaka N, Iguchi H, Hagiwara K, Yoshioka Y, Takeshita F, Ochiya T. Neutral sphingomyelinase 2 (nSMase2)-dependent exosomal transfer of angiogenic microRNAs regulate cancer cell metastasis. J Biol Chem. 2013;288(15):10849–59.PubMedPubMedCentralCrossRef
27.
Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T. Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem. 2010;285(23):17442–52.PubMedPubMedCentralCrossRef
28.
Wu B, Su S, Patil DP, Liu H, Gan J, Jaffrey SR, et al. Molecular basis for the specific and multivariant recognitions of RNA substrates by human hnRNP A2/B1. Nat Commun. 2018;9(1):420.PubMedPubMedCentralCrossRef
29.
Villarroya-Beltri C, Gutierrez-Vazquez C, Sanchez-Cabo F, Perez-Hernandez D, Vazquez J, Martin-Cofreces N, et al. Sumoylated hnRNPA2B1 controls the sorting of miRNAs into exosomes through binding to specific motifs. Nat Commun. 2013;4:2980.PubMedCrossRef
30.
Koppers-Lalic D, Hackenberg M, Bijnsdorp IV, van Eijndhoven MAJ, Sadek P, Sie D, et al. Nontemplated nucleotide additions distinguish the small RNA composition in cells from exosomes. Cell Rep. 2014;8(6):1649–58.CrossRefPubMed
31.
Guduric-Fuchs J, O'Connor A, Camp B, O'Neill CL, Medina RJ, Simpson DA. Selective extracellular vesicle-mediated export of an overlapping set of microRNAs from multiple cell types. BMC Genomics. 2012;13:357.PubMedPubMedCentralCrossRef
32.
Gibbings DJ, Ciaudo C, Erhardt M, Voinnet O. Multivesicular bodies associate with components of miRNA effector complexes and modulate miRNA activity. Nat Cell Biol. 2009;11(9):1143–9.PubMedCrossRef
33.
Sun Z, Yang S, Zhou Q, Wang G, Song J, Li Z, et al. Emerging role of exosome-derived long non-coding RNAs in tumor microenvironment. Mol Cancer. 2018;17(1):82.PubMedPubMedCentralCrossRef
34.
Fan Q, Yang L, Zhang X, Peng X, Wei S, Su D, et al. The emerging role of exosome-derived non-coding RNAs in cancer biology. Cancer Lett. 2018;414:107–15.PubMedCrossRef
35.
Ito I, Asai A, Suzuki S, Kobayashi M, Suzuki F. M2b macrophage polarization accompanied with reduction of long noncoding RNA GAS5. Biochem Biophys Res Commun. 2017;493(1):170–5.PubMedCrossRef
36.
Chen L, Yang W, Guo Y, Chen W, Zheng P, Zeng J, et al. Exosomal lncRNA GAS5 regulates the apoptosis of macrophages and vascular endothelial cells in atherosclerosis. PloS One. 2017;12(9):e0185406.PubMedPubMedCentralCrossRef
37.
Li Y, Zheng Q, Bao C, Li S, Guo W, Zhao J, et al. Circular RNA is enriched and stable in exosomes: a promising biomarker for cancer diagnosis. Cell Res. 2015;25(8):981–4.PubMedPubMedCentralCrossRef
38.
39.
Bolukbasi MF, Mizrak A, Ozdener GB, Madlener S, Strobel T, Erkan EP, et al. miR-1289 and “Zipcode”-like sequence enrich mRNAs in microvesicles. Mol Ther Nucleic Acids. 2012;1:e10.PubMedPubMedCentralCrossRef
40.
Ludwig S, Floros T, Theodoraki MN, Hong CS, Jackson EK, Lang S, et al. Suppression of lymphocyte functions by plasma exosomes correlates with disease activity in patients with head and neck cancer. Clin Cancer Res. 2017;23(16):4843–54.PubMedPubMedCentralCrossRef
41.
Szczepanski MJ, Szajnik M, Welsh A, Whiteside TL, Boyiadzis M. Blast-derived microvesicles in sera from patients with acute myeloid leukemia suppress natural killer cell function via membrane-associated transforming growth factor-beta1. Haematologica. 2011;96(9):1302–9.PubMedPubMedCentralCrossRef
42.
43.
44.
Whiteside TL. Exosome and mesenchymal stem cell cross-talk in the tumor microenvironment. Semin Immunol. 2018;35:69–79.PubMedCrossRef
45.
46.
Tian J, Rui K, Tang X, Ma J, Wang Y, Tian X, et al. MicroRNA-9 Regulates the differentiation and function of myeloid-derived suppressor cells via targeting Runx1. J Immunol. 2015;195(3):1301–11.PubMedCrossRef
47.
Umansky V, Sevko A. Tumor microenvironment and myeloid-derived suppressor cells. Cancer Microenviron. 2013;6(2):169–77.PubMedCrossRef
48.
Yan D, Yang Q, Shi M, Zhong L, Wu C, Meng T, et al. Polyunsaturated fatty acids promote the expansion of myeloid-derived suppressor cells by activating the JAK/STAT3 pathway. Eur J Immunol. 2013;43(11):2943–55.PubMedCrossRef
49.
50.
Condamine T, Kumar V, Ramachandran IR, Youn JI, Celis E, Finnberg N, et al. ER stress regulates myeloid-derived suppressor cell fate through TRAIL-R-mediated apoptosis. J Clin Invest. 2014;124(6):2626–39.PubMedPubMedCentralCrossRef
51.
Nan J, Xing YF, Hu B, Tang JX, Dong HM, He YM, et al. Endoplasmic reticulum stress induced LOX-1(+ ) CD15(+) polymorphonuclear myeloid-derived suppressor cells in hepatocellular carcinoma. Immunology. 2018;154(1):144–55.PubMedCrossRef
52.
Bronte V, Brandau S, Chen SH, Colombo MP, Frey AB, Greten TF, et al. Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun. 2016;7:12150.PubMedPubMedCentralCrossRef
53.
Damuzzo V, Pinton L, Desantis G, Solito S, Marigo I, Bronte V, et al. Complexity and challenges in defining myeloid-derived suppressor cells. Cytometry B Clin Cytom. 2015;88(2):77–91.PubMedCrossRef
54.
Condamine T, Dominguez GA, Youn JI, Kossenkov AV, Mony S, Alicea-Torres K, et al. Lectin-type oxidized LDL receptor-1 distinguishes population of human polymorphonuclear myeloid-derived suppressor cells in cancer patients. Sci Immunol. 2016;1(2):aaf8943.PubMedPubMedCentralCrossRef
55.
Mandruzzato S, Brandau S, Britten CM, Bronte V, Damuzzo V, Gouttefangeas C, et al. Toward harmonized phenotyping of human myeloid-derived suppressor cells by flow cytometry: results from an interim study. Cancer Immunol Immunother. 2016;65(2):161–9.PubMedPubMedCentralCrossRef
56.
Youn JI, Collazo M, Shalova IN, Biswas SK, Gabrilovich DI. Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J Leukoc Biol. 2012;91(1):167–81.PubMedPubMedCentralCrossRef
57.
Gato M, Blanco-Luquin I, Zudaire M, de Morentin XM, Perez-Valderrama E, Zabaleta A, et al. Drafting the proteome landscape of myeloid-derived suppressor cells. Proteomics. 2016;16(2):367–78.PubMedCrossRef
58.
Gato-Canas M, Martinez de Morentin X, Blanco-Luquin I, Fernandez-Irigoyen J, Zudaire I, Liechtenstein T, et al. A core of kinase-regulated interactomes defines the neoplastic MDSC lineage. Oncotarget. 2015;6(29):27160–75.PubMedPubMedCentralCrossRef
59.
He YM, Li X, Perego M, Nefedova Y, Kossenkov AV, Jensen EA, et al. Transitory presence of myeloid-derived suppressor cells in neonates is critical for control of inflammation. Nat Med. 2018;24(2):224–31.PubMedPubMedCentralCrossRef
60.
Condamine T, Ramachandran I, Youn JI, Gabrilovich DI. Regulation of tumor metastasis by myeloid-derived suppressor cells. Annu Rev Med. 2015;66:97–110.PubMedCrossRef
61.
Kusmartsev S, Nefedova Y, Yoder D, Gabrilovich DI. Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol. 2004;172(2):989–99.PubMedCrossRef
62.
Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, et al. Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 2006;66(2):1123–31.PubMedCrossRef
63.
Weber R, Fleming V, Hu X, Nagibin V, Groth C, Altevogt P, et al. Myeloid-derived suppressor cells hinder the anti-cancer activity of immune checkpoint inhibitors. Front Immunol. 2018;9:1310.PubMedPubMedCentralCrossRef
64.
Deng Z, Rong Y, Teng Y, Zhuang X, Samykutty A, Mu J, et al. Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene. 2017;36(5):639–51.PubMedCrossRef
65.
Chen F, Zhuang X, Lin L, Yu P, Wang Y, Shi Y, et al. New horizons in tumor microenvironment biology: challenges and opportunities. BMC Med. 2015;13:45.PubMedPubMedCentralCrossRef
66.
Joyce JA, Pollard JW. Microenvironmental regulation of metastasis. Nat Rev Cancer. 2009;9(4):239–52.PubMedCrossRef
67.
Hanahan D, Coussens LM. Accessories to the crime: functions of cells recruited to the tumor microenvironment. Cancer Cell. 2012;21(3):309–22.PubMedCrossRef
68.
Bissell MJ, Hines WC. Why don’t we get more cancer? A proposed role of the microenvironment in restraining cancer progression. Nat Med. 2011;17(3):320–9.PubMedPubMedCentralCrossRef
69.
70.
Tesi RJ. MDSC; the most important cell you have never heard of. Trends Pharmacol Sci. 2019;40(1):4–7.PubMedCrossRef
71.
72.
Chen D, Xie J, Fiskesund R, Dong W, Liang X, Lv J, et al. Chloroquine modulates antitumor immune response by resetting tumor-associated macrophages toward M1 phenotype. Nat Commun. 2018;9(1):873.PubMedPubMedCentralCrossRef
73.
Taylor NA, Vick SC, Iglesia MD, Brickey WJ, Midkiff BR, McKinnon KP, et al. Treg depletion potentiates checkpoint inhibition in claudin-low breast cancer. J Clin Invest. 2017;127(9):3472–83.PubMedPubMedCentralCrossRef
74.
Sun Q, Zhang B, Hu Q, Qin Y, Xu W, Liu W, et al. The impact of cancer-associated fibroblasts on major hallmarks of pancreatic cancer. Theranostics. 2018;8(18):5072–87.PubMedPubMedCentralCrossRef
75.
Barbazan J, Matic VD. Cancer associated fibroblasts: is the force the path to the dark side? Curr Opin Cell Biol. 2019;56:71–9.PubMedCrossRef
76.
Du YE, Tu G, Yang G, Li G, Yang D, Lang L, et al. MiR-205/YAP1 in Activated Fibroblasts of Breast Tumor Promotes VEGF-independent Angiogenesis through STAT3 Signaling. Theranostics. 2017;7(16):3972–88.PubMedPubMedCentralCrossRef
77.
Kumar S, Wilkes DW, Samuel N, Blanco MA, Nayak A, Alicea-Torres K, et al. DeltaNp63-driven recruitment of myeloid-derived suppressor cells promotes metastasis in triple-negative breast cancer. J Clin Invest. 2018;128(11):5095–109.PubMedPubMedCentralCrossRef
78.
Tesfamariam B. Involvement of platelets in tumor cell metastasis. Pharmacol Ther. 2016;157:112–9.PubMedCrossRef
79.
Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124(2):263–6.PubMedCrossRef
80.
Wyckoff JB, Wang Y, Lin EY, Li JF, Goswami S, Stanley ER, et al. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors. Cancer Res. 2007;67(6):2649–56.PubMedCrossRef
81.
82.
Palumbo JS, Talmage KE, Massari JV, La Jeunesse CM, Flick MJ, Kombrinck KW, et al. Platelets and fibrin(ogen) increase metastatic potential by impeding natural killer cell-mediated elimination of tumor cells. Blood. 2005;105(1):178–85.PubMedCrossRef
83.
Garcia-Romero N, Esteban-Rubio S, Rackov G, Carrion-Navarro J, Belda-Iniesta C, Ayuso-Sacido A. Extracellular vesicles compartment in liquid biopsies: Clinical application. Mol Aspects Med. 2018;60:27–37.PubMedCrossRef
84.
Liu RT, Huang CC, You HL, Chou FF, Hu CC, Chao FP, et al. Overexpression of tumor susceptibility gene TSG101 in human papillary thyroid carcinomas. Oncogene. 2002;21(31):4830–7.PubMedCrossRef
85.
Oh KB, Stanton MJ, West WW, Todd GL, Wagner KU. Tsg101 is upregulated in a subset of invasive human breast cancers and its targeted overexpression in transgenic mice reveals weak oncogenic properties for mammary cancer initiation. Oncogene. 2007;26(40):5950–9.PubMedCrossRef
86.
87.
Li L, Li C, Wang S, Wang Z, Jiang J, Wang W, et al. Exosomes derived from hypoxic oral squamous cell carcinoma cells deliver miR-21 to normoxic cells to elicit a prometastatic phenotype. Cancer Res. 2016;76(7):1770–80.PubMedCrossRef
88.
Parolini I, Federici C, Raggi C, Lugini L, Palleschi S, De Milito A, et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J Biol Chem. 2009;284(49):34211–22.PubMedPubMedCentralCrossRef
89.
Logozzi M, Angelini DF, Iessi E, Mizzoni D, Di Raimo R, Federici C, et al. Increased PSA expression on prostate cancer exosomes in in vitro condition and in cancer patients. Cancer Lett. 2017;403:318–29.PubMedCrossRef
90.
Hsu YL, Hung JY, Chang WA, Lin YS, Pan YC, Tsai PH, et al. Hypoxic lung cancer-secreted exosomal miR-23a increased angiogenesis and vascular permeability by targeting prolyl hydroxylase and tight junction protein ZO-1. Oncogene. 2017;36(34):4929–42.PubMedCrossRef
91.
Dorayappan KDP, Wanner R, Wallbillich JJ, Saini U, Zingarelli R, Suarez AA, et al. Hypoxia-induced exosomes contribute to a more aggressive and chemoresistant ovarian cancer phenotype: a novel mechanism linking STAT3/Rab proteins. Oncogene. 2018;37(28):3806–21.PubMedPubMedCentralCrossRef
92.
Xue M, Chen W, Xiang A, Wang R, Chen H, Pan J, et al. Hypoxic exosomes facilitate bladder tumor growth and development through transferring long non-coding RNA-UCA1. Mol Cancer. 2017;16(1):143.PubMedPubMedCentralCrossRef
93.
Vulpis E, Cecere F, Molfetta R, Soriani A, Fionda C, Peruzzi G, et al. Genotoxic stress modulates the release of exosomes from multiple myeloma cells capable of activating NK cell cytokine production: Role of HSP70/TLR2/NF-kB axis. Oncoimmunology. 2017;6(3):e1279372.PubMedPubMedCentralCrossRef
94.
Wei Y, Wang D, Jin F, Bian Z, Li L, Liang H, et al. Pyruvate kinase type M2 promotes tumour cell exosome release via phosphorylating synaptosome-associated protein 23. Nat Commun. 2017;8:14041.PubMedPubMedCentralCrossRef
95.
96.
Fukuda M. Versatile role of Rab27 in membrane trafficking: focus on the Rab27 effector families. J Biochem. 2005;137(1):9–16.PubMedCrossRef
97.
98.
Yu X, Harris SL, Levine AJ. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006;66(9):4795–801.PubMedCrossRef
99.
Sun Y, Zheng W, Guo Z, Ju Q, Zhu L, Gao J, et al. A novel TP53 pathway influences the HGS-mediated exosome formation in colorectal cancer. Sci Rep. 2016;6:28083.PubMedPubMedCentralCrossRef
100.
Mao J, Liang Z, Zhang B, Yang H, Li X, Fu H, et al. UBR2 enriched in p53 deficient mouse bone marrow mesenchymal stem cell-exosome promoted gastric cancer progression via Wnt/beta-catenin pathway. Stem Cells. 2017;35(11):2267–79.PubMedCrossRef
101.
Choi D, Montermini L, Kim DK, Meehan B, Roth FP, Rak J. The impact of oncogenic EGFRvIII on the proteome of extracellular vesicles released from glioblastoma cells. Mol Cell Proteomics. 2018;17(10):1948–64.PubMedCrossRefPubMedCentral
102.
Thompson CA, Purushothaman A, Ramani VC, Vlodavsky I, Sanderson RD. Heparanase regulates secretion, composition, and function of tumor cell-derived exosomes. J Biol Chem. 2013;288(14):10093–9.PubMedPubMedCentralCrossRef
103.
104.
Vlodavsky I, Gross-Cohen M, Weissmann M, Ilan N, Sanderson RD. Opposing functions of heparanase-1 and heparanase-2 in cancer progression. Trends Biochem Sci. 2018;43(1):18–31.PubMedCrossRef
105.
Overmiller AM, Pierluissi JA, Wermuth PJ, Sauma S, Martinez-Outschoorn U, Tuluc M, et al. Desmoglein 2 modulates extracellular vesicle release from squamous cell carcinoma keratinocytes. FASEB J. 2017;31(8):3412–24.PubMedPubMedCentralCrossRef
106.
Ramteke A, Ting H, Agarwal C, Mateen S, Somasagara R, Hussain A, et al. Exosomes secreted under hypoxia enhance invasiveness and stemness of prostate cancer cells by targeting adherens junction molecules. Mol Carcinog. 2015;54(7):554–65.PubMedCrossRef
107.
Hendrix A, De Wever O. Rab27 GTPases distribute extracellular nanomaps for invasive growth and metastasis: implications for prognosis and treatment. Int J Mol Sci. 2013;14(5):9883–92.PubMedPubMedCentralCrossRef
108.
Grosshans BL, Ortiz D, Novick P. Rabs and their effectors: achieving specificity in membrane traffic. Proc Natl Acad Sci U S A. 2006;103(32):11821–7.PubMedPubMedCentralCrossRef
109.
Pereira-Leal JB, Seabra MC. Evolution of the Rab family of small GTP-binding proteins. J Mol Biol. 2001;313(4):889–901.PubMedCrossRef
110.
Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008;10(5):619–24.PubMedCrossRef
111.
Tian X, Ma J, Wang T, Tian J, Zhang Y, Mao L, et al. Long non-coding RNA HOXA transcript antisense RNA myeloid-specific 1-HOXA1 axis downregulates the immunosuppressive activity of myeloid-derived suppressor cells in lung cancer. Front Immunol. 2018;9:473.PubMedPubMedCentralCrossRef
112.
Tian X, Ma J, Wang T, Tian J, Zheng Y, Peng R, et al. Long non-coding RNA RUNXOR accelerates MDSC-mediated immunosuppression in lung cancer. BMC Cancer. 2018;18(1):660.PubMedPubMedCentralCrossRef
113.
Wang J, De Veirman K, De Beule N, Maes K, De Bruyne E, Van Valckenborgh E, et al. The bone marrow microenvironment enhances multiple myeloma progression by exosome-mediated activation of myeloid-derived suppressor cells. Oncotarget. 2015;6(41):43992–4004.PubMedPubMedCentral
114.
Xiang X, Poliakov A, Liu C, Liu Y, Deng ZB, Wang J, et al. Induction of myeloid-derived suppressor cells by tumor exosomes. Int J Cancer. 2009;124(11):2621–33.PubMedPubMedCentralCrossRef
115.
Liu Y, Xiang X, Zhuang X, Zhang S, Liu C, Cheng Z, et al. Contribution of MyD88 to the tumor exosome-mediated induction of myeloid derived suppressor cells. Am J Pathol. 2010;176(5):2490–9.PubMedPubMedCentralCrossRef
116.
Chalmin F, Ladoire S, Mignot G, Vincent J, Bruchard M, Remy-Martin JP, et al. Membrane-associated Hsp72 from tumor-derived exosomes mediates STAT3-dependent immunosuppressive function of mouse and human myeloid-derived suppressor cells. J Clin Invest. 2010;120(2):457–71.PubMedPubMedCentral
117.
Wang J, De Veirman K, Faict S, Frassanito MA, Ribatti D, Vacca A, et al. Multiple myeloma exosomes establish a favourable bone marrow microenvironment with enhanced angiogenesis and immunosuppression. J Pathol. 2016;239(2):162–73.PubMedCrossRef
118.
Guo X, Qiu W, Liu Q, Qian M, Wang S, Zhang Z, et al. Immunosuppressive effects of hypoxia-induced glioma exosomes through myeloid-derived suppressor cells via the miR-10a/Rora and miR-21/Pten Pathways. Oncogene. 2018;37(31):4239–59.PubMedCrossRef
119.
Li L, Cao B, Liang X, Lu S, Luo H, Wang Z, et al. Microenvironmental oxygen pressure orchestrates an anti- and pro-tumoral γδ T cell equilibrium via tumor-derived exosomes. Oncogene. 2019;38(15):2830–43.PubMedCrossRef
120.
Basso D, Gnatta E, Padoan A, Fogar P, Furlanello S, Aita A, et al. PDAC-derived exosomes enrich the microenvironment in MDSCs in a SMAD4-dependent manner through a new calcium related axis. Oncotarget. 2017;8(49):84928–44.PubMedPubMedCentralCrossRef
121.
Bruns H, Bottcher M, Qorraj M, Fabri M, Jitschin S, Dindorf J, et al. CLL-cell-mediated MDSC induction by exosomal miR-155 transfer is disrupted by vitamin D. Leukemia. 2017;31(4):985–8.PubMedCrossRef
122.
Ridder K, Sevko A, Heide J, Dams M, Rupp AK, Macas J, et al. Extracellular vesicle-mediated transfer of functional RNA in the tumor microenvironment. Oncoimmunology. 2015;4(6):e1008371.PubMedPubMedCentralCrossRef
123.
Guo X, Qiu W, Wang J, Liu Q, Qian M, Wang S. Glioma exosomes mediate the expansion and function of myeloid-derived suppressor cells through microRNA-29a/Hbp1 and microRNA-92a/Prkar1a pathways. Int J Cancer. 2019;144(12):3111–26.PubMedCrossRef
124.
Xiang X, Liu Y, Zhuang X, Zhang S, Michalek S, Taylor DD, et al. TLR2-mediated expansion of MDSCs is dependent on the source of tumor exosomes. Am J Pathol. 2010;177(4):1606–10.PubMedPubMedCentralCrossRef
125.
126.
127.
Barile L, Vassalli G. Exosomes: therapy delivery tools and biomarkers of diseases. Pharmacol Ther. 2017;174:63–78.PubMedCrossRef
128.
Kai K, Dittmar RL, Sen S. Secretory microRNAs as biomarkers of cancer. Sem Cell Develop Biol. 2018;78:22–36.CrossRef
129.
130.
Melo SA, Luecke LB, Kahlert C, Fernandez AF, Gammon ST, Kaye J, et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature. 2015;523(7559):177–82.PubMedPubMedCentralCrossRef
131.
Lai X, Wang M, McElyea SD, Sherman S, House M, Korc M. A microRNA signature in circulating exosomes is superior to exosomal glypican-1 levels for diagnosing pancreatic cancer. Cancer Lett. 2017;393:86–93.PubMedPubMedCentralCrossRef
132.
133.
Eichelser C, Stuckrath I, Muller V, Milde-Langosch K, Wikman H, Pantel K, et al. Increased serum levels of circulating exosomal microRNA-373 in receptor-negative breast cancer patients. Oncotarget. 2014;5(20):9650–63.PubMedPubMedCentralCrossRef
134.
135.
Hornick NI, Huan J, Doron B, Goloviznina NA, Lapidus J, Chang BH, et al. Serum exosome microrna as a minimally-invasive early biomarker of AML. Sci Rep. 2015;5:11295.PubMedPubMedCentralCrossRef
136.
Li Z, Ma YY, Wang J, Zeng XF, Li R, Kang W, et al. Exosomal microRNA-141 is upregulated in the serum of prostate cancer patients. Onco Targets Ther. 2016;9:139–48.PubMed
137.
Yu B, Du Q, Li H, Liu HY, Ye X, Zhu B, et al. Diagnostic potential of serum exosomal colorectal neoplasia differentially expressed long non-coding RNA (CRNDE-p) and microRNA-217 expression in colorectal carcinoma. Oncotarget. 2017;8(48):83745–53.PubMedPubMedCentral
138.
Zhang J, Liu SC, Luo XH, Tao GX, Guan M, Yuan H, et al. Exosomal long noncoding RNAs are differentially expressed in the cervicovaginal lavage samples of cervical cancer patients. J Clin Lab Anal. 2016;30(6):1116–21.PubMedCrossRefPubMedCentral
139.
Wang J, Zhou Y, Lu J, Sun Y, Xiao H, Liu M, et al. Combined detection of serum exosomal miR-21 and HOTAIR as diagnostic and prognostic biomarkers for laryngeal squamous cell carcinoma. Med Oncol. 2014;31(9):148.PubMedCrossRef
140.
Pan L, Liang W, Fu M, Huang ZH, Li X, Zhang W, et al. Exosomes-mediated transfer of long noncoding RNA ZFAS1 promotes gastric cancer progression. J Cancer Res Clin Oncol. 2017;143(6):991–1004.PubMedCrossRef
141.
142.
Huang R, He L, Xia Y, Xu H, Liu C, Xie H, et al. A sensitive aptasensor based on a hemin/G-quadruplex-assisted signal amplification strategy for electrochemical detection of gastric cancer exosomes. Small. 2019;15(19):e1900735.PubMedCrossRef
143.
Li Z, Hu C, Jia J, Xia Y, Xie H, Shen M, et al. Establishment and evaluation of a simple size-selective method for exosome enrichment and purification. J Biomed Nanotechnol. 2019;15(5):1090–6.PubMedCrossRef
144.
145.
Metadata
Title
Tumor-derived exosomes, myeloid-derived suppressor cells, and tumor microenvironment
Authors
Xinyu Tian
Han Shen
Zhiyang Li
Tingting Wang
Shengjun Wang
Publication date
01-12-2019
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2019
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-019-0772-z

Other articles of this Issue 1/2019

Journal of Hematology & Oncology 1/2019 Go to the issue

Correction

Correction to: Oroxylin A promotes PTEN-mediated negative regulation of MDM2 transcription via SIRT3-mediated deacetylation to stabilize p53 and inhibit glycolysis in wt-p53 cancer cells

Research

Nuclear factor of activated T-cells, NFATC1, governs FLT3ITD-driven hematopoietic stem cell transformation and a poor prognosis in AML

Research

Burden of lymphoma in China, 2006–2016: an analysis of the Global Burden of Disease Study 2016

Research

Allogeneic hematopoietic cell transplantation provides effective salvage despite refractory disease or failed prior autologous transplant in angioimmunoblastic T-cell lymphoma: a CIBMTR analysis

Review

Platelet integrin αIIbβ3: signal transduction, regulation, and its therapeutic targeting

Review

TCR-like antibodies in cancer immunotherapy
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Watch now

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine
Image Credits