nach oben

Tumor Biology

Erschienen in:

01.09.2014 | Review

Extracellular vesicles shed by glioma cells: pathogenic role and clinical value

verfasst von: Dimitry A. Chistiakov, Vladimir P. Chekhonin

Erschienen in: Tumor Biology | Ausgabe 9/2014

Einloggen, um Zugang zu erhalten

Abstract

Extracellular vesicles (EVs) are commonly used by normal and tumor cells for communication at long distances to exchange by complex molecular messages and deliver a variety of essential biomolecules. EVs (exosomes and microvesicles) released in large numbers by glioma cells represent a key mechanism of intercellular signaling. Tumor-derived EVs are produced to regulate all vital functions of tumor cells including growth, proliferation, migration, survival, malignancy, invasion, and resistance to host anti-tumor immunity and anti-cancer drugs. Glioma EVs were shown to carry a variety of biomolecules such as oncogenic growth factors, receptors, enzymes, transcription factors, signaling and immunomodulatory molecules, DNA of mutated and nonmutated oncogenes, RNA transcripts, and noncoding RNA including retrotransposons, vault RNA, and microRNAs. Glioma-derived EVs can be useful as a source of potential tumor-associated biomarkers essential for development and validation of new diagnostic and prognostic tools for glioma and glioblastoma. Tumor EVs are enriched with glioma antigens that could be helpful, for example, for development of new advanced anti-tumor immune vaccines based on autologous dendritic cells stimulated by tumor-specific antigens.

Hanson PI, Cashikar A. Multivesicular body morphogenesis. Annu Rev Cell Dev Biol. 2012;28:337–62. PMID: 22831642.PubMed

Morita E. Differential requirements of mammalian ESCRTs in multivesicular body formation, virus budding and cell division. FEBS J. 2012;279(8):1399–406. PMID: 22340600.PubMed

Chen BJ, Lamb RA. Mechanisms for enveloped virus budding: can some viruses do without an ESCRT? Virology. 2008;372(2):221–32. PMID: 18063004.PubMedCentralPubMed

Von Bartheld CS, Altick AL. Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog Neurobiol. 2011;93(3):313–40. PMID: 21216273.

Théry C, Boussac M, Veron P, Ricciardi-Castagnoli P, Raposo G, Garin J, et al. Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J Immunol. 2001;166(12):7309–18. PMID: 11390481.PubMed

Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science. 2008;319(5867):1244–7. PMID: 18309083.PubMed

Muntasell A, Berger AC, Roche PA. T cell-induced secretion of MHC class II-peptide complexes on B cell exosomes. EMBO J. 2007;26(19):4263–72. PMID: 17805347.PubMedCentralPubMed

Feng D, Zhao WL, Ye YY, Bai XC, Liu RQ, Chang LF, et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic. 2010;11(5):675–87. PMID: 20136776.PubMed

Doeuvre L, Plawinski L, Toti F, Anglés-Cano E. Cell-derived microparticles: a new challenge in neuroscience. J Neurochem. 2009;110(2):457–68. PMID: 19457085.PubMed

10.

Al-Nedawi K, Meehan B, Rak J. Microvesicles: messengers and mediators of tumor progression. Cell Cycle. 2009;8(13):2014–8. PMID: 19535896.PubMed

11.

Turola E, Furlan R, Bianco F, Matteoli M, Verderio C. Microglial microvesicle secretion and intercellular signaling. Front Physiol. 2012;3:149. PMID: 22661954.PubMedCentralPubMed

12.

Guescini M, Genedani S, Stocchi V, Agnati LF. Astrocytes and glioblastoma cells release exosomes carrying mtDNA. J Neural Transm. 2010;117(1):1–4. PMID: 19680595.PubMed

13.

Castejón OJ, Arismendi GJ. Nerve cell death types in the edematous human cerebral cortex. J Submicrosc Cytol Pathol. 2006;38(1):21–36. PMID: 17283964.PubMed

14.

Bovellan M, Fritzsche M, Stevens C, Charras G. Death-associated protein kinase (DAPK) and signal transduction: blebbing in programmed cell death. FEBS J. 2010;277(1):58–65. PMID: 19878312.PubMed

15.

Théry 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. PMID: 18228490.

16.

Booth AM, Fang Y, Fallon JK, Yang JM, Hildreth JE, Gould SJ. Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J Cell Biol. 2006;172(6):923–35. PMID: 16533950.PubMedCentralPubMed

17.

Bourkoula E, Mangoni D, Ius T, Pucer A, Isola M, Musiello D, et al. Glioma-associated stem cells: a novel class of tumor-supporting cells able to predict prognosis of human low-grade gliomas. Stem Cells. 2014;32:1239–53. PMID: 24375787.PubMed

18.

Lo Cicero A, Schiera G, Proia P, Saladino P, Savettieri G, Di Liegro CM, 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):1353–7. PMID: 21842121.PubMed

19.

Shao H, Chung J, Balaj L, Charest A, Bigner DD, Carter BS, et al. Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. Nat Med. 2012;18(12):1835–40. PMID: 23142818.PubMedCentralPubMed

20.

Neckers L, Ivy SP. Heat shock protein 90. Curr Opin Oncol. 2003;15(6):419–24. PMID: 14624223.PubMed

21.

Phuyal S, Hessvik NP, Skotland T, Sandvig K, Llorente A. Regulation of exosome release by glycosphingolipids and flotillins. FEBS J. 2014;281(9):2214–27. PMID: 24605801.PubMed

22.

Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci. 2002;114(Pt 23):4143–51. PMID: 11739647.

23.

Katzmann DJ, Odorizzi G, Emr SD. Receptor downregulation and multivesicular-body sorting. Nat Rev Mol Cell Biol. 2002;3(12):893–905. PMID: 12461556.PubMed

24.

Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, et al. Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol. 2012;14(7):677–85. PMID: 22660413.PubMed

25.

Graner MW, Alzate O, Dechkovskaia AM, Keene JD, Sampson JH, Mitchell DA, et al. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009;23(5):1541–57. PMID: 19109410.PubMedCentralPubMed

26.

Epple LM, Griffiths SG, Dechkovskaia AM, Dusto NL, White J, Ouellette RJ, et al. Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS ONE. 2012;7(7):e42064. PMID: 22848702.PubMedCentralPubMed

27.

Redzic JS, Ung TH, Graner MW. Glioblastoma extracellular vesicles: reservoirs of potential biomarkers. Pharmgenomics Pers Med. 2014;7:65–77. PMID: 24634586.PubMedCentralPubMed

28.

Gan HK, Cvrljevic AN, Johns TG. The epidermal growth factor receptor variant III (EGFRvIII): where wild things are altered. FEBS J. 2013;280(21):5350–70. PMID: 23777544.PubMed

29.

Heimberger AB, Suki D, Yang D, Shi W, Aldape K. The natural history of EGFR and EGFRvIII in glioblastoma patients. J Transl Med. 2005;3:38. PMID: 16236164.PubMedCentralPubMed

30.

Kucharzewska P, Christianson HC, Welch JE, Svensson KJ, Fredlund E, Ringnér M, 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 USA. 2013;110:7312–7. PMID: 23589885.PubMedCentralPubMed

31.

Balaj L, Lessard R, Dai L, Pomeroy SL, Breakefield XO, Skog J. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun. 2011;2:180. PMID: 21285958.PubMedCentralPubMed

32.

Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol. 2008;10(12):1470–6. PMID: 19011622.PubMedCentralPubMed

33.

Noerholm M, Balaj L, Limperg T, Salehi A, Zhu LD, Hochberg FH, et al. RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer. 2012;12:22. PMID: 22251860.PubMedCentralPubMed

34.

Nilsson RJ, Balaj L, Hulleman E, van Rijn S, Pegtel DM, Walraven M, et al. Blood platelets contain tumor-derived RNA biomarkers. Blood. 2009;118(13):3680–3. PMID: 21832279.

35.

Li CC, Eaton SA, Young PE, Lee M, Shuttleworth R, Humphreys DT, et al. Glioma microvesicles carry selectively packaged coding and non-coding RNAs which alter gene expression in recipient cells. RNA Biol. 2013;10(8):1333–44. PMID: 23807490.PubMedCentralPubMed

36.

Pal A, Srivastava T, Sharma MK, Mehndiratta M, Das P, Sinha S, et al. Aberrant methylation and associated transcriptional mobilization of Alu elements contributes to genomic instability in hypoxia. J Cell Mol Med. 2010;14(11):2646–54. PMID: 19508390.PubMedCentralPubMed

37.

Godlewski J, Nowicki MO, Bronisz A, Nuovo G, Palatini J, De Lay M, et al. MicroRNA-451 regulates LKB1/AMPK signaling and allows adaptation to metabolic stress in glioma cells. Mol Cell. 2010;37:620–32. PMID: 20227367.PubMedCentralPubMed

38.

Krichevsky AM, Gabriely G. miR-21: a small multi-faceted RNA. J Cell Mol Med. 2009;13(1):39–53. PMID: 19175699.PubMedCentralPubMed

39.

Akers JC, Ramakrishnan V, Kim R, Skog J, Nakano I, Pingle S, et al. MiR-21 in the extracellular vesicles (EVs) of cerebrospinal fluid (CSF): a platform for glioblastoma biomarker development. PLoS ONE. 2013;8(10):e78115. PMID: 24205116.PubMedCentralPubMed

40.

Lu C, Shervington A. Chemoresistance in gliomas. Mol Cell Biochem. 2008;312(1–2):71–80. PMID: 18259841.PubMed

41.

Persson H, Kvist A, Vallon-Christersson J, Medstrand P, Borg A, Rovira C. The non-coding RNA of the multidrug resistance-linked vault particle encodes multiple regulatory small RNAs. Nat Cell Biol. 2009;11(10):1268–71. PMID: 19749744.PubMed

42.

Christianson HC, Svensson KJ, van Kuppevelt TH, Li JP, Belting M. Cancer cell exosomes depend on cell-surface heparan sulfate proteoglycans for their internalization and functional activity. Proc Natl Acad Sci USA. 2013;110(43):17380–5. PMID: 24101524.PubMedCentralPubMed

43.

Wade A, Robinson AE, Engler JR, Petritsch C, James CD, Phillips JJ. Proteoglycans and their roles in brain cancer. FEBS J. 2013;280(10):2399–417. PMID: 23281850.PubMedCentralPubMed

44.

Svensson KJ, Christianson HC, Wittrup A, Bourseau-Guilmain E, Lindqvist E, Svensson LM, et al. 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. PMID: 23653359.PubMedCentralPubMed

45.

Atai NA, Balaj L, van Veen H, Breakefield XO, Jarzyna PA, Van Noorden CJ, et al. Heparin blocks transfer of extracellular vesicles between donor and recipient cells. J Neurooncol. 2013;115(3):343–51. PMID: 24002181.PubMed

46.

Thayanithy V, Babatunde V, Dickson EL, Wong P, Oh S, Ke X, et al. Tumor exosomes induce tunneling nanotubes in lipid raft-enriched regions of human mesothelioma cells. Exp Cell Res. 2014;323(1):1781–8. PMID: 24468420.

47.

Davis DM, Sowinski S. Membrane nanotubes: dynamic long-distance connections between animal cells. Nat Rev Mol Cell Biol. 2008;9(6):431–6. PMID: 18431401.PubMed

48.

Fang Y, Wu N, Gan X, Yan W, Morrell JC, Gould SJ. Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biol. 2007;5(6):e158. PMID: 17550307.PubMedCentralPubMed

49.

Jia S, Zocco D, Samuels ML, Chou MF, Chammas R, Skog J, et al. Emerging technologies in extracellular vesicle-based molecular diagnostics. Expert Rev Mol Diagn. 2014;14(3):307–21. PMID: 24575799.PubMed

50.

Ohgaki H, Kleihues P. Genetic pathways to primary and secondary glioblastoma. Am J Pathol. 2007;170(5):1445–53. PMID: 17456751.PubMedCentralPubMed

51.

Paul I, Bhattacharya S, Chatterjee A, Ghosh MK. Current understanding on EGFR and Wnt/β-catenin signaling in glioma and their possible crosstalk. Genes Cancer. 2013;4(11–12):427–46. PMID: 24386505.PubMedCentralPubMed

52.

Frederick L, Wang XY, Eley G, James CD. Diversity and frequency of epidermal growth factor receptor mutations in human glioblastomas. Cancer Res. 2000;60(5):1383–7. PMID: 10728703.PubMed

53.

Hermanson M, Funa K, Hartman M, Claesson-Welsh L, Heldin CH, Westermark B, et al. Platelet-derived growth factor and its receptors in human glioma tissue: expression of messenger RNA and protein suggests the presence of autocrine and paracrine loops. Cancer Res. 1992;52(11):3213–9. PMID: 1317261.PubMed

54.

Nazarenko I, Hede SM, He X, Hedrén A, Thompson J, Lindström MS, et al. PDGF and PDGF receptors in glioma. Ups J Med Sci. 2012;117(2):99–112. PMID: 22509804.PubMedCentralPubMed

55.

Shih AH, Holland EC. Platelet-derived growth factor (PDGF) and glial tumorigenesis. Cancer Lett. 2006;232(2):139–47. PMID: 16139423.PubMed

56.

Hsieh AC, Moasser MM. Targeting HER proteins in cancer therapy and the role of the non-target HER3. Br J Cancer. 2007;97(4):453–7. PMID: 17667926.PubMedCentralPubMed

57.

Moasser MM. The oncogene HER2: its signaling and transforming functions and its role in human cancer pathogenesis. Oncogene. 2007;26(45):6469–87. PMID: 17471238.PubMedCentralPubMed

58.

Chan JA, Krichevsky AM, Kosik KS. MicroRNA-21 is an antiapoptotic factor in human glioblastoma cells. Cancer Res. 2005;65(14):6029–33. PMID: 16024602.PubMed

59.

Chen Y, Liu W, Chao T, Zhang Y, Yan X, Gong Y, et al. MicroRNA-21 down-regulates the expression of tumor suppressor PDCD4 in human glioblastoma cell T98G. Cancer Lett. 2008;272:197–205. PMID: 19013014.PubMed

60.

Papagiannakopoulos T, Shapiro A, Kosik KS. MicroRNA-21 targets a network of key tumor-suppressive pathways in glioblastoma cells. Cancer Res. 2008;68(19):8164–72. PMID: 18829576.PubMed

61.

Buscaglia LE, Li Y. Apoptosis and the target genes of microRNA-21. Chin J Cancer. 2011;30(6):371–80. PMID: 21627859.PubMedCentralPubMed

62.

Mongiardi MP. Angiogenesis and hypoxia in glioblastoma: a focus on cancer stem cells. CNS Neurol Disord Drug Targets. 2012;11(7):878–83. PMID: 23131159.PubMed

63.

Verginelli F, Perin A, Dali R, Fung KH, Lo R, Longatti P, et al. Transcription factors FOXG1 and Groucho/TLE promote glioblastoma growth. Nat Commun. 2013;4:2956. PMID: 24356439.PubMedCentralPubMed

64.

Mossink MH, van Zon A, Scheper RJ, Sonneveld P, Wiemer EA. Vaults: a ribonucleoprotein particle involved in drug resistance? Oncogene. 2003;22(47):7458–67. PMID: 14576851.PubMed

65.

Nie L, Zhao Y, Wu W, Yang YZ, Wang HC, Sun XH, et al. Notch-induced Asb2 expression promotes protein ubiquitination by forming non-canonical E3 ligase complexes. Cell Res. 2011;21(5):754–69. PMID: 21119685.PubMedCentralPubMed

66.

Saidi A, Hagedorn M, Allain N, Verpelli C, Sala C, Bello L, et al. Combined targeting of interleukin-6 and vascular endothelial growth factor potently inhibits glioma growth and invasiveness. Int J Cancer. 2009;125(5):1054–64. PMID: 19431143.PubMed

67.

Samaras V, Piperi C, Levidou G, Zisakis A, Kavantzas N, Themistocleous MS, et al. Analysis of interleukin (IL)-8 expression in human astrocytomas: associations with IL-6, cyclooxygenase-2, vascular endothelial growth factor, and microvessel morphometry. Hum Immunol. 2009;70(6):391–7. PMID: 19332096.PubMed

68.

Cuevas P, Carceller F, Angulo J, González-Corrochano R, Cuevas-Bourdier A, Giménez-Gallego G, et al. Antiglioma effects of a new, low molecular mass, inhibitor of fibroblast growth factor. Neurosci Lett. 2011;491(1):1–7. PMID: 21193016.PubMed

69.

Jiang L, Lin C, Song L, Wu J, Chen B, Ying Z, et al. MicroRNA-30e* promotes human glioma cell invasiveness in an orthotopic xenotransplantation model by disrupting the NF-κB/IκBα negative feedback loop. J Clin Invest. 2012;122(1):33–47. PMID: 22156201.PubMedCentralPubMed

70.

Wang J, Wang Y, Wang Y, Ma Y, Lan Y, Yang X, et al. Transforming growth factor β-regulated microRNA-29a promotes angiogenesis through targeting the phosphatase and tensin homolog in endothelium. J Biol Chem. 2012;288(15):10418–26. PMID: 23426367.

71.

Yang C, Wang C, Chen X, Chen S, Zhang Y, Zhi F, et al. Identification of seven serum microRNAs from a genome-wide serum microRNA expression profile as potential noninvasive biomarkers for malignant astrocytomas. Int J Cancer. 2013;132(1):116–27. PMID: 22674182.PubMed

72.

Günther W, Skaftnesmo KO, Arnold H, Terzis AJ. Molecular approaches to brain tumour invasion. Acta Neurochir (Wien). 2003;145(12):1029–36. PMID: 14663559.

73.

Arscott WT, Tandle AT, Zhao S, Shabason JE, Gordon IK, Schlaff CD, et al. Ionizing radiation and glioblastoma exosomes: implications in tumor biology and cell migration. Transl Oncol. 2013;6(6):638–48. PMID: 24466366.PubMedCentralPubMed

74.

Kiefel H, Bondong S, Hazin J, Ridinger J, Schirmer U, Riedle S, et al. L1CAM: a major driver for tumor cell invasion and motility. Cell Adh Migr. 2012;6(4):374–84. PMID: 22796939.PubMedCentralPubMed

75.

Yang M, Adla S, Temburni MK, Patel VP, Lagow EL, Brady OA, et al. Stimulation of glioma cell motility by expression, proteolysis, and release of the L1 neural cell recognition molecule. Cancer Cell Int. 2009;9:27. PMID: 19874583.PubMedCentralPubMed

76.

Yang M, Li Y, Chilukuri K, Brady OA, Boulos MI, Kappes JC, et al. L1 stimulation of human glioma cell motility correlates with FAK activation. J Neurooncol. 2011;105(1):27–44. PMID: 21373966.PubMedCentralPubMed

77.

Gast D, Riedle S, Kiefel H, Müerköster SS, Schäfer H, Schäfer MK, et al. The RGD integrin binding site in human L1-CAM is important for nuclear signaling. Exp Cell Res. 2008;314(13):2411–8. PMID: 18555990.PubMed

78.

Mohanan V, Temburni MK, Kappes JC, Galileo DS. L1CAM stimulates glioma cell motility and proliferation through the fibroblast growth factor receptor. Clin Exp Metastasis. 2013;30(4):507–20. PMID: 23212305.PubMed

79.

Kiefel H, Bondong S, Pfeifer M, Schirmer U, Erbe-Hoffmann N, Schäfer H, et al. EMT-associated up-regulation of L1CAM provides insights into L1CAM-mediated integrin signalling and NF-κB activation. Carcinogenesis. 2012;33(10):1919–29. PMID: 22764136.PubMed

80.

Svensson KJ, Kucharzewska P, Christianson HC, Sköld S, Löfstedt T, Johansson MC, 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 USA. 2011;108(32):13147–52. PMID: 21788507.PubMedCentralPubMed

81.

Wang H, Shen W, Huang H, Huang H, Hu L, Ramdas L, et al. Insulin-like growth factor binding protein 2 enhances glioblastoma invasion by activating invasion-enhancing genes. Cancer Res. 2003;63(15):4315–21. PMID: 12907597.PubMed

82.

Hsieh D, Hsieh A, Stea B, Ellsworth R. IGFBP2 promotes glioma tumor stem cell expansion and survival. Biochem Biophys Res Commun. 2010;397(2):367–72. PMID: 20515648.PubMed

83.

Chen CC, Lau LF. Functions and mechanisms of action of CCN matricellular proteins. Int J Biochem Cell Biol. 2009;41(4):771–83. PMID: 18775791.PubMedCentralPubMed

84.

Edwards LA, Woolard K, Son MJ, Li A, Lee J, Ene C, et al. Effect of brain- and tumor-derived connective tissue growth factor on glioma invasion. J Natl Cancer Inst. 2011;103(15):1162–78. PMID: 21771732.PubMedCentralPubMed

85.

Wooten MW, Vandenplas ML, Seibenhener ML, Geetha T, Diaz-Meco MT. Nerve growth factor stimulates multisite tyrosine phosphorylation and activation of the atypical protein kinase C’s via a src kinase pathway. Mol Cell Biol. 2001;21(24):8414–27. PMID: 11713277.PubMedCentralPubMed

86.

Renshaw MW, Price LS, Schwartz MA. Focal adhesion kinase mediates the integrin signaling requirement for growth factor activation of MAP kinase. J Cell Biol. 2001;147(3):611–8. PMID: 10545504.

87.

Wang M, Wang T, Liu S, Yoshida D, Teramoto A. The expression of matrix metalloproteinase-2 and -9 in human gliomas of different pathological grades. Brain Tumor Pathol. 2003;20(2):65–72. PMID: 14756443.PubMed

88.

Nakada M, Okada Y, Yamashita J. The role of matrix metalloproteinases in glioma invasion. Front Biosci. 2003;8:e261–9. PMID: 12456313.PubMed

89.

Tamura M, Gu J, Matsumoto K, Aota S, Parsons R, Yamada KM, et al. Inhibition of cell migration, spreading, and focal adhesions by tumor suppressor PTEN. Science. 1998;280(5369):1614–7. PMID: 9616126.PubMed

90.

Endersby R, Baker SJ. PTEN signaling in brain: neuropathology and tumorigenesis. Oncogene. 2008;27(41):5416–30. PMID: 18794877.PubMed

91.

Koul D. PTEN signaling pathways in glioblastoma. Cancer Biol Ther. 2008;7(9):1321–5. PMID: 18836294.PubMed

92.

D’Agostino S, Salamone M, Di Liegro I, Vittorelli ML. Membrane vesicles shed by oligodendroglioma cells induce neuronal apoptosis. Int J Oncol. 2006;29(5):1075–85. PMID: 17016637.PubMed

93.

Declèves X, Amiel A, Delattre JY, Scherrmann JM. Role of ABC transporters in the chemoresistance of human gliomas. Curr Cancer Drug Targets. 2006;6(5):433–45. PMID: 16918310.PubMed

94.

Aronica E, Gorter JA, van Vliet EA, Spliet WG, van Veelen CW, van Rijen PC, et al. Overexpression of the human major vault protein in gangliogliomas. Epilepsia. 2003;44(9):1166–75. PMID: 12919388.PubMed

95.

Soichi O, Masanori N, Hideo T, Kazunori A, Nobuya I, Jun-ichi K, et al. Clinical significance of ABCA2 a possible molecular marker for oligodendrogliomas. Neurosurgery. 2007;60(4):707–14. PMID: 17415208.PubMed

96.

Tanaka H, Tsukihara T. Structural studies of large nucleoprotein particles, vaults. Proc Jpn Acad Ser B Phys Biol Sci. 2012;88(8):416–33. PMID: 23060231.PubMedCentralPubMed

97.

Berger W, Steiner E, Grusch M, Elbling L, Micksche M. Vaults and the major vault protein: novel roles in signal pathway regulation and immunity. Cell Mol Life Sci. 2009;66(1):43–61. PMID: 18759128.PubMed

98.

Chistiakov DA, Chekhonin VP. Contribution of microRNAs to radio- and chemoresistance of brain tumors and their therapeutic potential. Eur J Pharmacol. 2012;684(1–3):8–18. PMID: 22484336.PubMed

99.

Steiner E, Holzmann K, Elbling L, Micksche M, Berger W. Cellular functions of vaults and their involvement in multidrug resistance. Curr Drug Targets. 2006;7(8):923–34. PMID: 16918321.PubMed

100.

Huang FF, Zhang L, Wu DS, Yuan XY1, Chen FP1, Zeng H, et al. PTEN regulates BCRP/ABCG2 and the side population through the PI3K/Akt pathway in chronic myeloid leukemia. PLoS ONE. 2014;9(3):e88298. PMID: 24603487.PubMedCentralPubMed

101.

Zhu H, Wu H, Liu X, Evans BR, Medina DJ, Liu CG, et al. Role of MicroRNA miR-27a and miR-451 in the regulation of MDR1/P-glycoprotein expression in human cancer cells. Biochem Pharmacol. 2008;76(5):582–8. PMID: 18619946.PubMedCentralPubMed

102.

Li Z, Hu S, Wang J, Cai J, Xiao L, Yu L, et al. MiR-27a modulates MDR1/P-glycoprotein expression by targeting HIPK2 in human ovarian cancer cells. Gynecol Oncol. 2010;119(1):125–30. PMID: 20624637.PubMed

103.

Qiu B, Zhang D, Wang C, Tao J, Tie X, Qiao Y, et al. IL-10 and TGF-β2 are overexpressed in tumor spheres cultured from human gliomas. Mol Biol Rep. 2011;38(5):3585–91. PMID: 21088899.PubMed

104.

Wainwright DA, Balyasnikova IV, Chang AL, Ahmed AU, Moon KS, Auffinger B, et al. IDO expression in brain tumors increases the recruitment of regulatory T cells and negatively impacts survival. Clin Cancer Res. 2012;18(22):6110–21. PMID: 22932670.PubMedCentralPubMed

105.

Jordan JT, Sun W, Hussain SF, DeAngulo G, Prabhu SS, Heimberger AB, et al. Preferential migration of regulatory T cells mediated by glioma-secreted chemokines can be blocked with chemotherapy. Cancer Immunol Immunother. 2008;57(1):123–31. PMID: 17522861.PubMed

106.

Ooi YC, Tran P, Ung N, Thill K, Trang A, Fong BM, et al. The role of regulatory T-cells in glioma immunology. Clin Neurol Neurosurg. 2014;119C:125–32. PMID: 24582432.

107.

Rolle CE, Sengupta S, Lesniak MS. Mechanisms of immune evasion by gliomas. Adv Exp Med Biol. 2012;746:53–76. PMID: 22639159.PubMed

108.

Zagzag D, Salnikow K, Chiriboga L, Yee H, Lan L, Ali MA, et al. Downregulation of major histocompatibility complex antigens in invading glioma cells: stealth invasion of the brain. Lab Invest. 2005;85(3):328–41. PMID: 15716863.PubMed

109.

Liu ZM, Wang YB, Yuan XH. Exosomes from murine-derived GL26 cells promote glioblastoma tumor growth by reducing number and function of CD8 + T cells. Asian Pac J Cancer Prev. 2013;14(1):309–14. PMID: 23534743.PubMed

110.

Krejsgaard T, Vetter-Kauczok CS, Woetmann A, Kneitz H, Eriksen KW, Lovato P, et al. Ectopic expression of B-lymphoid kinase in cutaneous T-cell lymphoma. Blood. 2009;113(23):5896–904. PMID: 19351960.PubMedCentralPubMed

111.

Malek SN, Dordai DI, Reim J, Dintzis H, Desiderio S. Malignant transformation of early lymphoid progenitors in mice expressing an activated Blk tyrosine kinase. Proc Natl Acad Sci USA. 1998;95(13):7351–6. PMID: 9636152.PubMedCentralPubMed

112.

Saharinen J, Keski-Oja J. Specific sequence motif of 8-Cys repeats of TGF-beta binding proteins, LTBPs, creates a hydrophobic interaction surface for binding of small latent TGF-beta. Mol Biol Cell. 2000;11(8):2691–704. PMID: 10930463.PubMedCentralPubMed

113.

Kantola AK, Keski-Oja J, Koli K. Fibronectin and heparin binding domains of latent TGF-beta binding protein (LTBP)-4 mediate matrix targeting and cell adhesion. Exp Cell Res. 2008;314(13):2488–500. PMID: 18585707.PubMed

114.

Koli K, Wempe F, Sterner-Kock A, Kantola A, Komor M, Hofmann WK, et al. Disruption of LTBP-4 function reduces TGF-beta activation and enhances BMP-4 signaling in the lung. J Cell Biol. 2004;167(1):123–33. PMID: 15466481.PubMedCentralPubMed

115.

Kretschmer C, Conradi A, Kemmner W, Sterner-Kock A. Latent transforming growth factor binding protein 4 (LTBP4) is downregulated in mouse and human DCIS and mammary carcinomas. Cell Oncol (Dordr). 2011;34(5):419–34. PMID: 21468687.

116.

Bultmann I, Conradi A, Kretschmer C, Sterner-Kock A. Latent transforming growth factor β-binding protein 4 is downregulated in esophageal cancer via promoter methylation. PLoS ONE. 2013;8(5):e65614. PMID: 23741501.PubMedCentralPubMed

117.

Taylor DD, Zacharias W, Gercel-Taylor C. Exosome isolation for proteomic analyses and RNA profiling. Methods Mol Biol. 2011;728:235–46. PMID: 21468952.PubMed

118.

Alvarez ML, Khosroheidari M, Kanchi Ravi R, DiStefano JK. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int. 2012;82(9):1024–32. PMID: 22785172.PubMed

119.

Momen-Heravi F, Balaj L, Alian S, Trachtenberg AJ, Hochberg FH, Skog J, et al. Impact of biofluid viscosity on size and sedimentation efficiency of the isolated microvesicles. Front Physiol. 2012;3:162. PMID: 22661955.PubMedCentralPubMed

120.

Lopez-Gines C, Cerda-Nicolas M, Gil-Benso R, Pellin A, Lopez-Guerrero JA, Callaghan R, et al. Association of chromosome 7, chromosome 10 and EGFR gene amplification in glioblastoma multiforme. Clin Neuropathol. 2005;24:209–18. PMID: 16167544.PubMed

121.

Bieńkowski M, Piaskowski S, Stoczyńska-Fidelus E, Szybka M, Banaszczyk M, Witusik-Perkowska M, et al. Screening for EGFR amplifications with a novel method and their significance for the outcome of glioblastoma patients. PLoS ONE. 2013;8(6):e65444. PMID: 23762372.PubMedCentralPubMed

122.

Sauter G, Maeda T, Waldman FM, Davis RL, Feuerstein BG. Patterns of epidermal growth factor receptor amplification in malignant gliomas. Am J Pathol. 1996;148(4):1047–53. PMID: 8644846.PubMedCentralPubMed

123.

Wang G, Sai K, Gong F, Yang Q, Chen F, Lin J. Mutation of isocitrate dehydrogenase 1 induces glioma cell proliferation via nuclear factor-κB activation in a hypoxia-inducible factor 1α-dependent manner. Mol Med Rep. 2014;9:1799–805. PMID: 24626950.PubMed

124.

Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 2009;462(7274):739–44. PMID: 19935646.PubMedCentralPubMed

125.

Duncan CG, Barwick BG, Jin G, Rago C, Kapoor-Vazirani P, Powell DR, et al. A heterozygous IDH1R132H/WT mutation induces genome-wide alterations in DNA methylation. Genome Res. 2012;22(12):2339–55. PMID: 22899282.PubMedCentralPubMed

126.

Ichimura K. Molecular pathogenesis of IDH mutations in gliomas. Brain Tumor Pathol. 2012;29(3):131–9. PMID: 22399191.PubMed

127.

Verhaak RG, Hoadley KA, Purdom E, Wang V, Qi Y, Wilkerson MD, et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell. 2010;17(1):98–110. PMID: 20129251.PubMedCentralPubMed

128.

Chen WW, Balaj L, Liau LM, Samuels ML, Kotsopoulos SK, Maguire CA, et al. BEAMing and droplet digital PCR analysis of mutant IDH1 mRNA in glioma patient serum and cerebrospinal fluid extracellular vesicles. Mol Ther Nucleic Acids. 2013;2:e109. PMID: 23881452.PubMedCentralPubMed

129.

Forseen SE, Potti A, Koka V, Koch M, Fraiman G, Levitt R. Identification and relationship of HER-2/neu overexpression to short-term mortality in primary malignant brain tumors. Anticancer Res. 2002;22:1599–602. PMID: 12168843.PubMed

130.

Belgrader P, Tanner SC, Regan JF, Koehler R, Hindson BJ, Brown AS. Droplet digital PCR measurement of HER2 copy number alteration in formalin-fixed paraffin-embedded breast carcinoma tissue. Clin Chem. 2013;59(6):991–4. PMID: 23358413.PubMed

131.

Wang J, Yi X, Tang H, Han H, Wu M, Zhou F. Direct quantification of microRNA at low picomolar level in sera of glioma patients using a competitive hybridization followed by amplified voltammetric detection. Anal Chem. 2012;84(15):6400–6. PMID: 22788545.PubMedCentralPubMed

132.

Wang Q, Li P, Li A, Jiang W, Wang H, Wang J, et al. Plasma specific miRNAs as predictive biomarkers for diagnosis and prognosis of glioma. J Exp Clin Cancer Res. 2013;31:97. PMID: 23174013.

133.

Teplyuk NM, Mollenhauer B, Gabriely G, Giese A, Kim E, Smolsky M, et al. MicroRNAs in cerebrospinal fluid identify glioblastoma and metastatic brain cancers and reflect disease activity. Neuro Oncol. 2012;14:689–700. PMID: 22492962.PubMedCentralPubMed

134.

Koshkin PA, Chistiakov DA, Nikitin AG, Konovalov AN, Potapov AA, Usachev DY, et al. Analysis of expression of microRNAs and genes involved in the control of key signaling mechanisms that support or inhibit development of brain tumors of different grades. Clin Chim Acta. 2014;430:55–62. PMID: 24412320.PubMed

135.

Manterola L, Guruceaga E, Gállego Pérez-Larraya J, González-Huarriz M, Jauregui P, Tejada S, et al. A small noncoding RNA signature found in exosomes of GBM patient serum as a diagnostic tool. Neuro Oncol. 2014;16:520–7. PMID: 24435880.PubMedCentralPubMed

136.

Bronisz A, Godlewski J, Wallace JA, Merchant AS, Nowicki MO, Mathsyaraja H, et al. Reprogramming of the tumour microenvironment by stromal PTEN-regulated miR-320. Nat Cell Biol. 2011;14(2):159–67. PMID: 22179046.PubMedCentralPubMed

137.

Yang L, Carbone DP. Tumor-host immune interactions and dendritic cell dysfunction. Adv Cancer Res. 2004;92:13–27. PMID: 15530555.PubMed

138.

Kim W, Liau LM. Dendritic cell vaccines for brain tumors. Neurosurg Clin N Am. 2010;21(1):139–57. PMID: 19944973.PubMedCentralPubMed

139.

Bu N, Wu H, Sun B, Zhang G, Zhan S, Zhang R, et al. Exosome-loaded dendritic cells elicit tumor-specific CD8+ cytotoxic T cells in patients with glioma. J Neurooncol. 2011;104(3):659–67. PMID: 21336773.PubMed

140.

André F, Chaput N, Schartz NE, Flament C, Aubert N, Bernard J, et al. Exosomes as potent cell-free peptide-based vaccine I. Dendritic cell-derived exosomes transfer functional MHC class I/peptide complexes to dendritic cells. J Immunol. 2004;172(4):2126–36. PMID: 14764678.PubMed

141.

Hu YL, Fu YH, Tabata Y, Gao JQ. Mesenchymal stem cells: a promising targeted-delivery vehicle in cancer gene therapy. J Control Release. 2010;147(2):154–62. PMID: 20493219.PubMed

142.

Munoz JL, Bliss SA, Greco SJ, Ramkissoon SH, Ligon KL, Rameshwar P, 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. PMID: 24084846.PubMedCentralPubMed

143.

Nduom EK, Yang C, Merrill MJ, Zhuang Z, Lonser RR. Characterization of the blood–brain barrier of metastatic and primary malignant neoplasms. J Neurosurg. 2013;119(2):427–33. PMID: 23621605.PubMed

Titel: Extracellular vesicles shed by glioma cells: pathogenic role and clinical value
verfasst von: Dimitry A. Chistiakov
Vladimir P. Chekhonin
Publikationsdatum: 01.09.2014
Verlag: Springer Netherlands
Erschienen in: Tumor Biology / Ausgabe 9/2014
Print ISSN: 1010-4283
Elektronische ISSN: 1423-0380
DOI: https://doi.org/10.1007/s13277-014-2262-9

Springer Medizin

Extracellular vesicles shed by glioma cells: pathogenic role and clinical value

Abstract

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie

Springer Medizin

Abstract

Bitte loggen Sie sich ein, um Zugang zu diesem Inhalt zu erhalten

Weitere Artikel der Ausgabe 9/2014

MiR-186 targets ROCK1 to suppress the growth and metastasis of NSCLC cells

Regulation of metastasis of pediatric multiple myeloma by MMP13

SMAD7: a timer of tumor progression targeting TGF-β signaling

Correlation between fertility drugs use and malignant melanoma incidence: the state of the art

Transarterial embolization with or without chemotherapy for advanced hepatocellular carcinoma: a systematic review

PLGF inhibition impairs metastasis of larynx carcinoma through MMP3 downregulation

Neu im Fachgebiet Onkologie

Adjuvante Immuntherapie verlängert Leben bei RCC

Alectinib verbessert krankheitsfreies Überleben bei ALK-positivem NSCLC

Bei Senioren mit Prostatakarzinom auf Anämie achten!

ICI-Therapie in der Schwangerschaft wird gut toleriert

Update Onkologie