Tumor-Derived EV-Encapsulated miR-181b-5p Induces Angiogenesis to Foster Tumorigenesis and Metastasis of ESCC

Rustgi, 2014, Esophageal carcinoma, N. Engl. J. Med., 371, 2499, 10.1056/NEJMra1314530 Murphy, 2017, International cancer seminars: a focus on esophageal squamous cell carcinoma, Ann. Oncol., 28, 2086, 10.1093/annonc/mdx279 Taylor, 2013, Squamous dysplasia—the precursor lesion for esophageal squamous cell carcinoma, Cancer Epidemiol. Biomarkers Prev., 22, 540, 10.1158/1055-9965.EPI-12-1347 Arnold, 2015, Global incidence of oesophageal cancer by histological subtype in 2012, Gut, 64, 381, 10.1136/gutjnl-2014-308124 Dotto, 2016, Squamous cell cancers: a unified perspective on biology and genetics, Cancer Cell, 29, 622, 10.1016/j.ccell.2016.04.004 Weis, 2011, Tumor angiogenesis: molecular pathways and therapeutic targets, Nat. Med., 17, 1359, 10.1038/nm.2537 Dimova, 2014, Angiogenesis in cancer - general pathways and their therapeutic implications, J. BUON, 19, 15 Chen, 2019, Epigenetically upregulated oncoprotein PLCE1 drives esophageal carcinoma angiogenesis and proliferation via activating the PI-PLCε-NF-κB signaling pathway and VEGF-C/ Bcl-2 expression, Mol. Cancer, 18, 1, 10.1186/s12943-018-0930-x Small, 2014, Hypertension due to antiangiogenic cancer therapy with vascular endothelial growth factor inhibitors: understanding and managing a new syndrome, Can. J. Cardiol., 30, 534, 10.1016/j.cjca.2014.02.011 Cocucci, 2015, Ectosomes and exosomes: shedding the confusion between extracellular vesicles, Trends Cell Biol., 25, 364, 10.1016/j.tcb.2015.01.004 Milane, 2015, Exosome mediated communication within the tumor microenvironment, J. Control. Release, 219, 278, 10.1016/j.jconrel.2015.06.029 Zeng, 2018, Cancer-derived exosomal miR-25-3p promotes pre-metastatic niche formation by inducing vascular permeability and angiogenesis, Nat. Commun., 9, 5395, 10.1038/s41467-018-07810-w Lin, 2018, Hepatocellular carcinoma cell-secreted Exosomal MicroRNA-210 promotes angiogenesis in vitro and in vivo, Mol. Ther. Nucleic Acids, 11, 243, 10.1016/j.omtn.2018.02.014 Kourembanas, 2015, Exosomes: vehicles of intercellular signaling, biomarkers, and vectors of cell therapy, Annu. Rev. Physiol., 77, 13, 10.1146/annurev-physiol-021014-071641 Hayes, 2014, MicroRNAs in cancer: biomarkers, functions and therapy, Trends Mol. Med., 20, 460, 10.1016/j.molmed.2014.06.005 Stark, 2005, Animal MicroRNAs confer robustness to gene expression and have a significant impact on 3'UTR evolution, Cell, 123, 1133, 10.1016/j.cell.2005.11.023 Ambros, 2004, The functions of animal microRNAs, Nature, 431, 350, 10.1038/nature02871 Bartel, 2004, MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 116, 281, 10.1016/S0092-8674(04)00045-5 Fiedler, 2016, New Insights Into miR-17-92 Cluster Regulation and Angiogenesis, Circ. Res., 118, 9, 10.1161/CIRCRESAHA.115.307935 Mao, 2015, Tumor-derived microRNA-494 promotes angiogenesis in non-small cell lung cancer, Angiogenesis, 18, 373, 10.1007/s10456-015-9474-5 Sasahira, 2012, Downregulation of miR-126 induces angiogenesis and lymphangiogenesis by activation of VEGF-A in oral cancer, Br. J. Cancer, 107, 700, 10.1038/bjc.2012.330 Geng, 2014, MicroRNA-192 suppresses liver metastasis of colon cancer, Oncogene, 33, 5332, 10.1038/onc.2013.478 Wang, 2013, MicroRNA-195 suppresses angiogenesis and metastasis of hepatocellular carcinoma by inhibiting the expression of VEGF, VAV2, and CDC42, Hepatology, 58, 642, 10.1002/hep.26373 Chou, 2013, GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression, Nat. Cell Biol., 15, 201, 10.1038/ncb2672 Park, 2017, miR-184 exhibits angiostatic properties via regulation of Akt and VEGF signaling pathways, FASEB J., 31, 256, 10.1096/fj.201600746r Fang, 2018, Hepatoma cell-secreted exosomal microRNA-103 increases vascular permeability and promotes metastasis by targeting junction proteins, Hepatology, 68, 1459, 10.1002/hep.29920 Zhou, 2014, Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis, Cancer Cell, 25, 501, 10.1016/j.ccr.2014.03.007 Park, 2006, Human umbilical vein endothelial cells and human dermal microvascular endothelial cells offer new insights into the relationship between lipid metabolism and angiogenesis, Stem Cell Rev., 2, 93, 10.1007/s12015-006-0015-x Valadi, 2007, Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells, Nat. Cell Biol., 9, 654, 10.1038/ncb1596 Li, 2013, Exosomes mediate the cell-to-cell transmission of IFN-α-induced antiviral activity, Nat. Immunol., 14, 793, 10.1038/ni.2647 Leonardi, 2012, The tumor microenvironment in hepatocellular carcinoma (review), Int. J. Oncol., 40, 1733 Li, 2019, Exosomal FMR1-AS1 facilitates maintaining cancer stem-like cell dynamic equilibrium via TLR7/NFκB/c-Myc signaling in female esophageal carcinoma, Mol. Cancer, 18, 22, 10.1186/s12943-019-0949-7 Min, 2018, Exosomes derived from irradiated esophageal carcinoma-infiltrating T cells promote metastasis by inducing the epithelial-mesenchymal transition in esophageal cancer cells, Pathol. Oncol. Res., 24, 11, 10.1007/s12253-016-0185-z Li, 2019, Tumor-derived exosomal HMGB1 promotes esophageal squamous cell carcinoma progression through inducing PD1+ TAM expansion, Oncogenesis, 8, 17, 10.1038/s41389-019-0126-2 Wu, 2019, MicroRNA-181b blocks gensenoside Rg3-mediated tumor suppression of gallbladder carcinoma by promoting autophagy flux via CREBRF/CREB3 pathway, Am. J. Transl. Res., 11, 5776 Graham, 2017, miR-181b-5p modulates cell migratory proteins, tissue inhibitor of metalloproteinase 3, and annexin A2 during in vitro decidualization in a human endometrial stromal cell line, Reprod. Sci., 24, 1264, 10.1177/1933719116682877 Zhi, 2015, Identification of 9 serum microRNAs as potential noninvasive biomarkers of human astrocytoma, Neuro-oncol., 17, 383, 10.1093/neuonc/nou169 Zhi, 2013, Identification of circulating microRNAs as potential biomarkers for detecting acute myeloid leukemia, PLoS ONE, 8, e56718, 10.1371/journal.pone.0056718 Zhi, 2014, MiR-181b-5p downregulates NOVA1 to suppress proliferation, migration and invasion and promote apoptosis in astrocytoma, PLoS ONE, 9, e109124, 10.1371/journal.pone.0109124 Chu, 2004, PTEN regulatory functions in tumor suppression and cell biology, Med. Sci. Monit., 10, RA235 Brognard, 2008, PHLiPPing the switch on Akt and protein kinase C signaling, Trends Endocrinol. Metab., 19, 223, 10.1016/j.tem.2008.04.001 Harfouche, 2002, Mechanisms which mediate the antiapoptotic effects of angiopoietin-1 on endothelial cells, Microvasc. Res., 64, 135, 10.1006/mvre.2002.2421 Maisonpierre, 1997, Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis, Science, 277, 55, 10.1126/science.277.5322.55 Tsigkos, 2006, Regulation of Ang2 release by PTEN/PI3-kinase/Akt in lung microvascular endothelial cells, J. Cell. Physiol., 207, 506, 10.1002/jcp.20592 Cheng, 2013, Potential mechanism for endothelial progenitor cell therapy in acute myocardial infarction: Activation of VEGF- PI3K/Akte-NOS pathway, Ann. Clin. Lab. Sci., 43, 395 Ju, 2014, Angiopoietin-2 secretion by endothelial cell exosomes: regulation by the phosphatidylinositol 3-kinase (PI3K)/Akt/endothelial nitric oxide synthase (eNOS) and syndecan-4/syntenin pathways, J. Biol. Chem., 289, 510, 10.1074/jbc.M113.506899