Brainwashed by extracellular vesicles: the role of extracellular vesicles in primary and metastatic brain tumour microenvironment

References

• Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med. 2013;19(11):1423–11.
   PubMed Web of Science ®Google Scholar
• Whiteside TL. The tumor microenvironment and its role in promoting tumor growth. Oncogene. 2008;27(45):5904–5912.
   PubMed Web of Science ®Google Scholar
• Quail DF, Joyce JA. The microenvironmental landscape of brain tumors. Cancer Cell. 2017;31(3):326–341.
   PubMed Web of Science ®Google Scholar
• Broekman ML, Maas SLN, Abels ER, et al. Multidimensional communication in the microenvirons of glioblastoma. Nat Rev Neurol. 2018;14(8):482–495.
   PubMed Web of Science ®Google Scholar
• D’Asti E, Chennakrishnaiah S, Lee TH, et al. Extracellular vesicles in brain tumor progression. Cell Mol Neurobiol. 2016;36(3):383–407.
   PubMed Web of Science ®Google Scholar
• Abels ER, Breakefield XO. Introduction to extracellular vesicles: biogenesis, RNA cargo selection, content, release, and uptake. Cell Mol Neurobiol. 2016;36(3):301–312.
   PubMed Web of Science ®Google Scholar
• Kucharzewska P, Christianson HC, Welch JE, et al. Exosomes reflect the hypoxic status of glioma cells and mediate hypoxia-dependent activation of vascular cells during tumor development. Proc Natl Acad Sci U S A. 2013;110(18):7312–7317.
   PubMed Web of Science ®Google Scholar
• Svensson KJ, Kucharzewska P, Christianson HC, et al. 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.
   PubMed Web of Science ®Google Scholar
• de Vrij J, Maas SL, Kwappenberg KM, et al. Glioblastoma-derived extracellular vesicles modify the phenotype of monocytic cells. Int J Cancer. 2015;137(7):1630–1642.
   PubMed Web of Science ®Google Scholar
• van der Vos KE, Abels ER, Zhang X, et al. Directly visualized glioblastoma-derived extracellular vesicles transfer RNA to microglia/macrophages in the brain. Neuro Oncol. 2016;18(1):58–69.
   PubMed Web of Science ®Google Scholar
• Bronisz A, Wang Y, Nowicki MO, et al. Extracellular vesicles modulate the glioblastoma microenvironment via a tumor suppression signaling network directed by miR-1. Cancer Res. 2014;74(3):738–750.
   PubMed Web of Science ®Google Scholar
• Fong MY, Zhou W, Liu L, et al. Breast-cancer-secreted miR-122 reprograms glucose metabolism in premetastatic niche to promote metastasis. Nat Cell Biol. 2015;17(2):183–194.
   PubMed Web of Science ®Google Scholar
• Zhang L, Zhang S, Yao J, et al. Microenvironment-induced PTEN loss by exosomal microRNA primes brain metastasis outgrowth. Nature. 2015;527(7576):100–104.
   PubMed Web of Science ®Google Scholar
• Tominaga N, Kosaka N, Ono M, et al. Brain metastatic cancer cells release microRNA-181c-containing extracellular vesicles capable of destructing blood-brain barrier. Nat Commun. 2015;6:6716.
   PubMed Web of Science ®Google Scholar
• Zhou W, Fong MY, Min Y, et al. Cancer-secreted miR-105 destroys vascular endothelial barriers to promote metastasis. Cancer Cell. 2014;25(4):501–515.
   PubMed Web of Science ®Google Scholar
• Zhu G, Sun C, Liu W. Effects of neurotrophin-3 on the differentiation of neural stem cells into neurons and oligodendrocytes. Neural Regen Res. 2012;7(19):1483–1487.
   Web of Science ®Google Scholar
• Lawn S, Krishna N, Pisklakova A, et al. Neurotrophin signaling via TrkB and TrkC receptors promotes the growth of brain tumor-initiating cells. J Biol Chem. 2015;290(6):3814–3824.
   Web of Science ®Google Scholar
• Louie E, Chen XF, Coomes A, et al. Neurotrophin-3 modulates breast cancer cells and the microenvironment to promote the growth of breast cancer brain metastasis. Oncogene. 2013;32(35):4064–4077.
   PubMed Web of Science ®Google Scholar
• Harper J, Moses MA. Molecular regulation of tumor angiogenesis: mechanisms and therapeutic implications. Exs. 2006;96:223–268.
   PubMedGoogle Scholar
• Liu Y, Carson-Walter EB, Cooper A, et al. Vascular gene expression patterns are conserved in primary and metastatic brain tumors. J Neurooncol. 2010;99(1):13–24.
   PubMed Web of Science ®Google Scholar
• Smith ER, Zurakowski D, Saad A, et al. Urinary biomarkers predict brain tumor presence and response to therapy. Clin Cancer Res. 2008;14(8):2378–2386.
   PubMed Web of Science ®Google Scholar
• Soda Y, Marumoto T, Friedmann-Morvinski D, et al. Transdifferentiation of glioblastoma cells into vascular endothelial cells. Proc Natl Acad Sci U S A. 2011;108(11):4274–4280.
   PubMed Web of Science ®Google Scholar
• Dey N, Barwick BG, Moreno CS, et al. Wnt signaling in triple negative breast cancer is associated with metastasis. BMC Cancer. 2013;13:537.
   PubMed Web of Science ®Google Scholar
• Fang J, Shing Y, Wiederschain D, et al. Matrix metalloproteinase-2 is required for the switch to the angiogenic phenotype in a tumor model. Proc Natl Acad Sci U S A. 2000;97(8):3884–3889.
   Web of Science ®Google Scholar
• Yang J, McNeish B, Butterfield C, et al. Lipocalin 2 is a novel regulator of angiogenesis in human breast cancer. Faseb J. 2013;27(1):45–50.
   Web of Science ®Google Scholar
• Kholia S, Ranghino A, Garnieri P, et al. Extracellular vesicles as new players in angiogenesis. Vascul Pharmacol. 2016;86:64–70.
   Web of Science ®Google Scholar
• Skog J, Wurdinger T, van Rijn S, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470–1476.
   PubMed Web of Science ®Google Scholar
• Giusti I, Delle Monache S, Di Francesco M, et al. From glioblastoma to endothelial cells through extracellular vesicles: messages for angiogenesis. Tumour Biol. 2016;37(9):12743–12753.
   Google Scholar
• Liu S, Sun J, Lan Q. Glioblastoma microvesicles promote endothelial cell proliferation through Akt/beta-catenin pathway. Int J Clin Exp Pathol. 2014;7(8):4857–4866.
   Web of Science ®Google Scholar
• Maji S, Chaudhary P, Akopova I, et al. Exosomal annexin II promotes angiogenesis and breast cancer metastasis. Mol Cancer Res. 2017;15(1):93–105.
   PubMed Web of Science ®Google Scholar
• Sun X, Ma X, Wang J, et al. Glioma stem cells-derived exosomes promote the angiogenic ability of endothelial cells through miR-21/VEGF signal. Oncotarget. 2017;8(22):36137–36148.
   PubMedGoogle Scholar
• Li CC, Eaton SA, Young PE, et al. Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol. 2013;10(8):1333–1344.
   PubMed Web of Science ®Google Scholar
• Lang HL, Hu GW, Chen Y, et al. Glioma cells promote angiogenesis through the release of exosomes containing long non-coding RNA POU3F3. Eur Rev Med Pharmacol Sci. 2017;21(5):959–972.
   PubMed Web of Science ®Google Scholar
• Camacho L, Guerrero P, Marchetti D. MicroRNA and protein profiling of brain metastasis competent cell-derived exosomes. PLoS One. 2013;8(9):e73790.
   PubMed Web of Science ®Google Scholar
• Zeng L, He X, Wang Y, et al. MicroRNA-210 overexpression induces angiogenesis and neurogenesis in the normal adult mouse brain. Gene Ther. 2014;21(1):37–43.
   PubMed Web of Science ®Google Scholar
• Zhu C, Kros JM, Cheng C, et al. The contribution of tumor-associated macrophages in glioma neo-angiogenesis and implications for anti-angiogenic strategies. Neuro Oncol. 2017;19:1435–1446.
   Web of Science ®Google Scholar
• Taraboletti G, D’Ascenzo S, Borsotti P, et al. Shedding of the matrix metalloproteinases MMP-2, MMP-9, and MT1-MMP as membrane vesicle-associated components by endothelial cells. Am J Pathol. 2002;160(2):673–680.
   PubMed Web of Science ®Google Scholar
• Fridman WH, Zitvogel L, Sautes-Fridman C, et al. The immune contexture in cancer prognosis and treatment. Nat Rev Clin Oncol. 2017;14(12):717–734.
   PubMed Web of Science ®Google Scholar
• Hamilton A, Sibson NR. Role of the systemic immune system in brain metastasis. Mol Cell Neurosci. 2013;53:42–51.
   Web of Science ®Google Scholar
• Hambardzumyan D, Gutmann DH, Kettenmann H. The role of microglia and macrophages in glioma maintenance and progression. Nat Neurosci. 2016;19(1):20–27.
   PubMed Web of Science ®Google Scholar
• Coniglio SJ, Eugenin E, Dobrenis K, et al. Microglial stimulation of glioblastoma invasion involves epidermal growth factor receptor (EGFR) and colony stimulating factor 1 receptor (CSF-1R) signaling. Mol Med. 2012;18:519–527.
   PubMed Web of Science ®Google Scholar
• Andreou KE, Soto MS, Allen D, et al. Anti-inflammatory microglia/macrophages as a potential therapeutic target in brain metastasis. Front Oncol. 2017;7:251.
   Web of Science ®Google Scholar
• Fossati G, Ricevuti G, Edwards SW, et al. Neutrophil infiltration into human gliomas. Acta Neuropathol. 1999;98(4):349–354.
   PubMed Web of Science ®Google Scholar
• Liang J, Piao Y, Holmes L, et al. Neutrophils promote the malignant glioma phenotype through S100A4. Clin Cancer Res. 2014;20(1):187–198.
   PubMed Web of Science ®Google Scholar
• Iwatsuki K, Kumara E, Yoshimine T, et al. Elastase expression by infiltrating neutrophils in gliomas. Neurol Res. 2000;22(5):465–468.
   Web of Science ®Google Scholar
• Jacobs JF, Idema AJ, Bol KF, et al. Regulatory T cells and the PD-L1/PD-1 pathway mediate immune suppression in malignant human brain tumors. Neuro Oncol. 2009;11(4):394–402.
   PubMed Web of Science ®Google Scholar
• Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996;183(3):1161–1172.
   PubMed Web of Science ®Google Scholar
• Denzer K, van Eijk M, Kleijmeer MJ, et al. Follicular dendritic cells carry MHC class II-expressing microvesicles at their surface. J Immunol. 2000;165(3):1259–1265.
   PubMed Web of Science ®Google Scholar
• Thery C, Regnault A, Garin J, et al. Molecular characterization of dendritic cell-derived exosomes. Selective accumulation of the heat shock protein hsc73. J Cell Biol. 1999;147(3):599–610.
   PubMed Web of Science ®Google Scholar
• Clayton A, Mitchell JP, Court J, et al. Human tumor-derived exosomes down-modulate NKG2D expression. J Immunol. 2008;180(11):7249–7258.
   PubMed Web of Science ®Google Scholar
• Chalmin F, Ladoire S, Mignot G, 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
• Ridder K, Sevko A, Heide J, et al. Extracellular vesicle-mediated transfer of functional RNA in the tumor microenvironment. Oncoimmunology. 2015;4(6):e1008371.
   PubMed Web of Science ®Google Scholar
• Hellwinkel JE, Redzic JS, Harland TA, et al. Glioma-derived extracellular vesicles selectively suppress immune responses. Neuro Oncol. 2016;18(4):497–506.
   PubMed Web of Science ®Google Scholar
• Domenis R, Cesselli D, Toffoletto B, 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.
   PubMed Web of Science ®Google Scholar
• Ricklefs FL, Alayo Q, Krenzlin H, et al. Immune evasion mediated by PD-L1 on glioblastoma-derived extracellular vesicles. Sci Adv. 2018;4(3):eaar2766.
   PubMed Web of Science ®Google Scholar
• Chow A, Zhou W, Liu L, et al. Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-kappaB. Sci Rep. 2014;4:5750.
   PubMed Web of Science ®Google Scholar
• Jaiswal R, Johnson MS, Pokharel D, et al. Microparticles shed from multidrug resistant breast cancer cells provide a parallel survival pathway through immune evasion. BMC Cancer. 2017;17(1):104.
   PubMed Web of Science ®Google Scholar
• Wasilewski D, Priego N, Fustero-Torre C, et al. Reactive astrocytes in brain metastasis. Front Oncol. 2017;7:298.
   Web of Science ®Google Scholar
• Obenauf AC, Massague J. Surviving at a distance: organ specific metastasis. Trends Cancer. 2015;1(1):76–91.
   PubMed Web of Science ®Google Scholar
• Kore RA, Abraham EC. Inflammatory cytokines, interleukin-1 beta and tumor necrosis factor-alpha, upregulated in glioblastoma multiforme, raise the levels of CRYAB in exosomes secreted by U373 glioma cells. Biochem Biophys Res Commun. 2014;453(3):326–331.
   PubMed Web of Science ®Google Scholar
• Guescini M, Genedani S, Stocchi V, et al. Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J Neural Transm (Vienna). 2010;117(1):1–4.
   PubMed Web of Science ®Google Scholar
• Sansone P, Savini C, Kurelac I, et al. Packaging and transfer of mitochondrial DNA via exosomes regulate escape from dormancy in hormonal therapy-resistant breast cancer. Proc Natl Acad Sci U S A. 2017;114(43):E9066–E75.
   PubMed Web of Science ®Google Scholar
• Lo Cicero A, Schiera G, Proia P, et al. Oligodendroglioma cells shed microvesicles which contain TRAIL as well as molecular chaperones and induce cell death in astrocytes. Int J Oncol. 2011;39(6):1353–1357.
   PubMed Web of Science ®Google Scholar
• Pickup MW, Mouw JK, Weaver VM. The extracellular matrix modulates the hallmarks of cancer. EMBO Rep. 2014;15(12):1243–1253.
   PubMed Web of Science ®Google Scholar
• Lau LW, Cua R, Keough MB, et al. Pathophysiology of the brain extracellular matrix: a new target for remyelination. Nat Rev Neurosci. 2013;14(10):722–729.
   PubMed Web of Science ®Google Scholar
• Varga I, Hutoczki G, Szemcsak CD, et al. Brevican, neurocan, tenascin-C and versican are mainly responsible for the invasiveness of low-grade astrocytoma. Pathol Oncol Res. 2012;18(2):413–420.
   PubMed Web of Science ®Google Scholar
• Novak U, Kaye AH. Extracellular matrix and the brain: components and function. J Clin Neurosci. 2000;7(4):280–290.
   Web of Science ®Google Scholar
• Virga J, Szemcsak CD, Remenyi-Puskar J, et al. Differences in extracellular matrix composition and its role in invasion in primary and secondary intracerebral malignancies. Anticancer Res. 2017;37(8):4119–4126.
   Web of Science ®Google Scholar
• Sanderson RD, Bandari SK, Vlodavsky I. Proteases and glycosidases on the surface of exosomes: newly discovered mechanisms for extracellular remodeling. Matrix Biol. 2019 Jan;75–76:160–169.
   Google Scholar
• Mu W, Rana S, Zoller M. Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia. 2013;15(8):875–887.
   PubMed Web of Science ®Google Scholar
• Evans SM, Putt M, Yang XY, et al. Initial evidence that blood-borne microvesicles are biomarkers for recurrence and survival in newly diagnosed glioblastoma patients. J Neurooncol. 2016;127(2):391–400.
   Web of Science ®Google Scholar
• Manterola L, Guruceaga E, Gallego Perez-Larraya J, et al. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro Oncol. 2014;16(4):520–527.
   PubMed Web of Science ®Google Scholar
• Shao H, Chung J, Lee K, et al. Chip-based analysis of exosomal mRNA mediating drug resistance in glioblastoma. Nat Commun. 2015;6:6999.
   PubMed Web of Science ®Google Scholar
• Fraser K, Jo A, Giedt J, et al. Characterization of single microvesicles in plasma from glioblastoma patients. Neuro Oncol. 2019 May;21(5):606–615.
   Google Scholar
• Lee K, Fraser K, Ghaddar B, et al. Multiplexed profiling of single extracellular vesicles. ACS Nano. 2018;12(1):494–503.
   PubMed Web of Science ®Google Scholar
• Shao H, Chung J, Balaj L, et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med. 2012;18(12):1835–1840.
   PubMed Web of Science ®Google Scholar
• Erkan EP, Senfter D, Madlener S, et al. Extracellular vesicle-mediated suicide mRNA/protein delivery inhibits glioblastoma tumor growth in vivo. Cancer Gene Ther. 2017;24(1):38–44.
   PubMed Web of Science ®Google Scholar
• Munoz JL, Bliss SA, Greco SJ, et al. Delivery of functional anti-miR-9 by mesenchymal stem cell-derived exosomes to glioblastoma multiforme cells conferred chemosensitivity. Mol Ther Nucleic Acids. 2013;2:e126.
   PubMedGoogle Scholar
• Yang T, Fogarty B, LaForge B, et al. Delivery of small interfering RNA to inhibit vascular endothelial growth factor in zebrafish using natural brain endothelia cell-secreted exosome nanovesicles for the treatment of brain cancer. Aaps J. 2017;19(2):475–486.
   PubMed Web of Science ®Google Scholar
• Katakowski M, Buller B, Zheng X, et al. Exosomes from marrow stromal cells expressing miR-146b inhibit glioma growth. Cancer Lett. 2013;335(1):201–204.
   PubMed Web of Science ®Google Scholar
• Bhaskaran V, Nowicki MO, Idriss M, et al. The functional synergism of microRNA clustering provides therapeutically relevant epigenetic interference in glioblastoma. Nat Commun. 2019;10(1):442.
   Web of Science ®Google Scholar
• Bu N, Wu H, Sun B, et al. Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma. J Neurooncol. 2011;104(3):659–667.
   PubMed Web of Science ®Google Scholar