Molecular subtypes and differentiation programmes of glioma stem cells as determinants of extracellular vesicle profiles and endothelial cell-stimulating activities

References

• Wen PY, Kesari S. Malignant gliomas in adults. N Engl J Med. 2008;359(5):1–16.
   Web of Science ®Google Scholar
• Weller M, Wick W, Aldape K, et al. Glioma. Nat Rev Dis Primers. 2015 Jul 16;1:15017.
   PubMed Web of Science ®Google Scholar
• Sturm D, Bender S, Jones DT, et al. Paediatric and adult glioblastoma: multiform (epi)genomic culprits emerge. Nat Rev Cancer. 2014;14(2):92–107.
   PubMed Web of Science ®Google Scholar
• Ceccarelli M, Barthel FP, Malta TM, et al. Molecular profiling reveals biologically discrete subsets and pathways of progression in diffuse glioma. Cell. 2016 Jan 28;164(3):550–563.
   PubMed Web of Science ®Google Scholar
• Verhaak RG, Hoadley KA, Purdom E, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010 Jan 19;17(1):98–110.
   PubMed Web of Science ®Google Scholar
• Patel AP, Tirosh I, Trombetta JJ, et al. Single-cell RNA-seq highlights intratumoral heterogeneity in primary glioblastoma. Science (New York, NY). 2014 Jun 20;344(6190):1396–1401.
   Google Scholar
• Sottoriva A, Spiteri I, Piccirillo SG, et al. Intratumor heterogeneity in human glioblastoma reflects cancer evolutionary dynamics. Proc Natl Acad Sci U S A. 2013 May 3;110(10):4009–4014.
   PubMed Web of Science ®Google Scholar
• Phillips HS, Kharbanda S, Chen R, et al. Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell. 2006 Mar;9(3):157–173.
   PubMed Web of Science ®Google Scholar
• Singh SK, Hawkins C, Clarke ID, et al. Identification of human brain tumour initiating cells. Nature. 2004 Nov 18;432(7015):396–401.
   PubMed Web of Science ®Google Scholar
• Lathia JD, Mack SC, Mulkearns-Hubert EE, et al. Cancer stem cells in glioblastoma. Genes Dev. 2015 Jun 15;29(12):1203–1217.
   PubMed Web of Science ®Google Scholar
• Lan X, Jorg DJ, Cavalli FMG, et al. Fate mapping of human glioblastoma reveals an invariant stem cell hierarchy. Nature. 2017 Sep 14;549(7671):227–232.
   PubMed Web of Science ®Google Scholar
• Vescovi AL, Galli R, Reynolds BA. Brain tumour stem cells. Nat Rev Cancer. 2006 Jun;6(6):425–436.
   PubMed Web of Science ®Google Scholar
• Calabrese C, Poppleton H, Kocak M, et al. A perivascular niche for brain tumor stem cells. Cancer Cell. 2007 Jan;11(1):69–82.
   PubMed Web of Science ®Google Scholar
• Bao S, Wu Q, Sathornsumetee S, et al. Stem cell-like glioma cells promote tumor angiogenesis through vascular endothelial growth factor. Cancer Res. 2006 Aug 15;66(16):7843–7848.
   PubMed Web of Science ®Google Scholar
• Jain RK, Di TE, Duda DG, et al. Angiogenesis in brain tumours. Nat Rev Neurosci. 2007 Aug;8(8):610–622.
   PubMed Web of Science ®Google Scholar
• Mao P, Joshi K, Li J, et al. Mesenchymal glioma stem cells are maintained by activated glycolytic metabolism involving aldehyde dehydrogenase 1A3. Proc Natl Acad Sci U S A. 2013 May 21;110(21):8644–8649.
   PubMed Web of Science ®Google Scholar
• Nakano I, Garnier D, Minata M, et al. Extracellular vesicles in the biology of brain tumour stem cells - implications for inter-cellular communication, therapy and biomarker development. Semin Cell Dev Biol. 2015;40(15):17–26.
   Google Scholar
• Al-Nedawi K, Meehan B, Micallef J, et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol. 2008 May;10(5):619–624.
   PubMed Web of Science ®Google Scholar
• Osswald M, Jung E, Sahm F, et al. Brain tumour cells interconnect to a functional and resistant network. Nature. 2015 Mar 12;528(7580):93–98.
   PubMed Web of Science ®Google Scholar
• Hardee ME, Zagzag D. Mechanisms of glioma-associated neovascularization. Am J Pathol. 2012 Oct;181(4):1126–1141.
   PubMed Web of Science ®Google Scholar
• Godlewski J, Krichevsky AM, Johnson MD, et al. Belonging to a network–microRNAs, extracellular vesicles, and the glioblastoma microenvironment. Neuro Oncol. 2015 May;17(5):652–662.
   PubMed Web of Science ®Google Scholar
• Skog J, Wurdinger T, Van RS, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008 Nov 16;10(12):1470–1476.
   PubMed Web of Science ®Google Scholar
• Colombo M, Raposo G, Thery C. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol. 2014;30:255–289.
   PubMed Web of Science ®Google Scholar
• Raposo G, Nijman HW, Stoorvogel W, et al. B lymphocytes secrete antigen-presenting vesicles. J Exp Med. 1996 Jan 3;183(3):1161–1172.
   PubMed Web of Science ®Google Scholar
• Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016 Feb 23;113(8):E968–E977.
   PubMed Web of Science ®Google Scholar
• Zappulli V, Friis KP, Fitzpatrick Z, et al. Extracellular vesicles and intercellular communication within the nervous system. J Clin Invest. 2016;126(4):1198–1207.
   PubMed Web of Science ®Google Scholar
• Rak J. Extracellular vesicles - biomarkers and effectors of the cellular interactome in cancer. Front Pharmacol. 2013;4:21.
   Web of Science ®Google Scholar
• Ricklefs F, Mineo M, Rooj AK, et al. Extracellular vesicles from high-grade glioma exchange diverse pro-oncogenic signals that maintain intratumoral heterogeneity. Cancer Res. 2016 May 15;76(10):2876–2881.
   Web of Science ®Google Scholar
• Treps L, Perret R, Edmond S, et al. Glioblastoma stem-like cells secrete the pro-angiogenic VEGF-A factor in extracellular vesicles. J Extracell Vesicles. 2017;6(1):1359479.
   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
• Montermini L, Meehan B, Garnier D, et al. Inhibition of oncogenic epidermal growth factor receptor kinase triggers release of exosome-like extracellular vesicles and impacts their phosphoprotein and DNA content. J Biol Chem. 2015;290(40):24534–24546.
   PubMed Web of Science ®Google Scholar
• Shevchenko A, Tomas H, Havlis J, et al. In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc. 2006;1(6):2856–2860.
   PubMed Web of Science ®Google Scholar
• Yu J, May L, Milsom C, et al. Contribution of host-derived tissue factor to tumor neovascularization. Arterioscler Thromb Vasc Biol. 2008 Nov;28(11):1975–1981.
   Web of Science ®Google Scholar
• Lee TH, Chennakrishnaiah S, Meehan B, et al. Barriers to horizontal cell transformation by extracellular vesicles containing oncogenic H-ras. Oncotarget. 2016;7(32):51991–52002.
   Google Scholar
• Arraud N, Linares R, Tan S, et al. Extracellular vesicles from blood plasma: determination of their morphology, size, phenotype and concentration. J Thromb Haemost. 2014;12(5):614–627.
   PubMed Web of Science ®Google Scholar
• Choi D, Lee TH, Spinelli C, et al. Extracellular vesicle communication pathways as regulatory targets of oncogenic transformation. Semin Cell Dev Biol. 2017;67:11–22.
   PubMed Web of Science ®Google Scholar
• Ouchi R, Okabe S, Migita T, et al. Senescence from glioma stem cell differentiation promotes tumor growth. Biochem Biophys Res Commun. 2016 May;470(2):275–281.
   Web of Science ®Google Scholar
• Pollard SM, Yoshikawa K, Clarke ID, et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell. 2009;4(6):568–580.
   PubMed Web of Science ®Google Scholar
• Garnier D, Magnus N, Meehan B, et al. Qualitative changes in the proteome of extracellular vesicles accompanying cancer cell transition to mesenchymal state. Exp Cell Res. 2013;319(17):2747–2757.
   PubMed Web of Science ®Google Scholar
• Singh SK, Clarke ID, Terasaki M, et al. Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003;63(18):5821–5828.
   PubMed Web of Science ®Google Scholar
• Fang Y, Garnier D, Lee TH, et al. PML-RARa modulates the vascular signature of extracellular vesicles released by acute promyelocytic leukemia cells. Angiogenesis. 2016;19(1):25–38.
   Web of Science ®Google Scholar
• Warde-Farley D, Donaldson SL, Comes O, et al. The GeneMANIA prediction server: biological network integration for gene prioritization and predicting gene function. Nucleic Acids Res. 2010 Jul;38(Web Server issue):W214–W220.
   PubMed Web of Science ®Google Scholar
• Mulcahy LA, Pink RC, Carter DR. Routes and mechanisms of extracellular vesicle uptake. J Extracell Vesicles. 2014 Apr 8;3. DOI:10.3402/jev.v3.24641.eCollection;%2014.:10.
   Google Scholar
• Al-Nedawi K, Meehan B, Kerbel RS, et al. 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.
   PubMed Web of Science ®Google Scholar
• Chinot OL, Reardon DA. The future of antiangiogenic treatment in glioblastoma. Curr Opin Neurol. 2014;27(6):675–682.
   Web of Science ®Google Scholar
• Kim CW, Lee HM, Lee TH, et al. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res. 2002;62(21):6312–6317.
   PubMed Web of Science ®Google Scholar
• Garnier D, Magnus N, Lee TH, et al. Cancer cells induced to express mesenchymal phenotype release exosome-like extracellular vesicles carrying tissue factor. J Biol Chem. 2012;287(52):43565–43572.
   PubMed Web of Science ®Google Scholar
• Deregibus MC, Cantaluppi V, Calogero R, et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood. 2007;110(7):2440–2448.
   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
• Treps L, Edmond S, Harford-Wright E, et al. Extracellular vesicle-transported Semaphorin3A promotes vascular permeability in glioblastoma. Oncogene. 2016 19;35(20):2615–2623.
   PubMed Web of Science ®Google Scholar
• Webber J, Yeung V, Clayton A. Extracellular vesicles as modulators of the cancer microenvironment. Semin Cell Dev Biol. 2015;40:27–34.
   PubMed Web of Science ®Google Scholar
• Chiao MT, Yang YC, Cheng WY, et al. CD133+ glioblastoma stem-like cells induce vascular mimicry in vivo. Curr Neurovasc Res. 2011;8(3):210–219.
   PubMed Web of Science ®Google Scholar
• Figueroa J, Phillips LM, Shahar T, et al. Exosomes from glioma-associated mesenchymal stem cells increase the tumorigenicity of glioma stem-like cells via transfer of miR-1587. Cancer Res. 2017 Nov 1;77(21):5808–5819.
   PubMed Web of Science ®Google Scholar
• Hu B, Wang Q, Wang YA, et al. Epigenetic activation of WNT5A drives glioblastoma stem cell differentiation and invasive growth. Cell. 2016;167(5):1281–1295.
   PubMed Web of Science ®Google Scholar
• Wang J, Cazzato E, Ladewig E, et al. Clonal evolution of glioblastoma under therapy. Nat Genet. 2016;48(7):768–776.
   PubMed Web of Science ®Google Scholar
• Garnier D, Jabado N, Rak J. Extracellular vesicles as prospective carriers of oncogenic protein signatures in adult and paediatric brain tumours. Proteomics. 2013;13(10–11):1595–1607.
   Web of Science ®Google Scholar
• Tauro BJ, Mathias RA, Greening DW, et al. Oncogenic H-Ras reprograms Madin-Darby canine kidney (MDCK) cell-derived exosomal proteins following epithelial-mesenchymal transition. Mol Cell Proteomics. 2013;12(8):2148–2159.
   PubMed Web of Science ®Google Scholar