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Brain Tumor Microvesicles: Insights into Intercellular Communication in the Nervous System

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Abstract

Brain tumors are heterogeneous tumors composed of differentiated tumor cells that resemble various neural cells and a small number of multipotent cancer stem cells. These tumors modify normal cells in their environment to promote tumor growth, invasion and metastases by various ways. Recent publications show that glioblastoma cells release microvesicles that contain a select subset of cellular proteins and RNAs. These microvesicles are avidly taken up by normal cells in cell culture and can change the translational profile of these cells through delivery of tumor-derived mRNAs, which are translated into functional proteins. In addition to mRNA and proteins, microvesicles have been shown to contain microRNAs, non-coding RNAs and DNA. This commentary explores the recent advances in this novel intercellular communication route and discusses the potential physiological role of microvesicles in brain tumorigenesis.

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References

  • Aguzzi A, Rajendran L (2009) The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64:783–790

    Article  PubMed  CAS  Google Scholar 

  • Aitken CE, Petrov A, Puglisi JD (2010) Single ribosome dynamics and the mechanism of translation. Annu Rev Biophys 39:491–513

    Article  PubMed  CAS  Google Scholar 

  • Alais S, Simoes S, Baas D, Lehmann S, Raposo G, Darlix JL, Leblanc P (2008) Mouse neuroblastoma cells release prion infectivity associated with exosomal vesicles. Biol Cell 100:603–615

    Article  PubMed  CAS  Google Scholar 

  • Al-Nedawi K, Meehan B, Micallef J, Lhotak V, May L, Guha A, Rak J (2008) Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10:619–624

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Erviti L, Seow Y, Yin H, Betts C, Lakhal S, Wood MJ (2011) Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat Biotechnol. doi:10.1038/nbt.1807 (Epub ahead of print)

  • Bakhti M, Winter C, Simons M (2011) Inhibition of myelin membrane sheath formation by oligodendrocyte-derived exosome-like vesicles. J Biol Chem 286:787–796

    Article  PubMed  CAS  Google Scholar 

  • Balaj L, Lessard R, Dai L, Cho Y-J, Pomeroy SL, Breakefield XO, Skog J (2011) Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2:180

    Article  PubMed  Google Scholar 

  • Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215–233

    Article  PubMed  CAS  Google Scholar 

  • Bergsmedh A, Szeles A, Henriksson M, Bratt A, Folkman MJ, Spetz AL, Holmgren L (2001) Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA 98:6407–6411

    Article  PubMed  CAS  Google Scholar 

  • Bianco F, Perrotta C, Novellino L, Francolini M, Riganti L, Menna E, Saglietti L, Schuchman EH, Furlan R, Clementi E, Matteoli M, Verderio C (2009) Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 28:1043–1054

    Article  PubMed  CAS  Google Scholar 

  • Bruno S, Grange C, Deregibus MC, Calogero RA, Saviozzi S, Collino F, Morando L, Busca A, Falda M, Bussolati B, Tetta C, Camussi G (2009) Mesenchymal stem cell-derived microvesicles protect against acute tubular injury. J Am Soc Nephrol 20:1053–1067

    Article  PubMed  CAS  Google Scholar 

  • Cocucci E, Racchetti G, Meldolesi J (2009) Shedding microvesicles: artefacts no more. Trends Cell Biol 19:43–51

    Article  PubMed  CAS  Google Scholar 

  • Cordaux R, Batzer MA (2009) The impact of retrotransposons on human genome evolution. Nat Rev Genet 10:691–703

    Article  PubMed  CAS  Google Scholar 

  • Court FA, Hendriks WT, MacGillavry HD, Alvarez J, van Minnen J (2008) Schwann cell to axon transfer of ribosomes: toward a novel understanding of the role of glia in the nervous system. J Neurosci 28:11024–11029

    Article  PubMed  CAS  Google Scholar 

  • Croce CM (2009) Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 10:704–714

    Article  PubMed  CAS  Google Scholar 

  • Day JR, Jost M, Reynolds MA, Groskopf J, Rittenhouse H (2011) PCA3: from basic molecular science to the clinical lab. Cancer Lett 301:1–6

    Article  PubMed  CAS  Google Scholar 

  • Deregibus MC, Cantaluppi V, Calogero R, Lo Iacono M, Tetta C, Biancone L, Bruno S, Bussolati B, Camussi G (2007) Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 110:2440–2448

    Article  PubMed  CAS  Google Scholar 

  • Di Vizio D, Kim J, Hager MH, Morello M, Yang W, Lafargue CJ, True LD, Rubin MA, Adam RM, Beroukhim R, Demichelis F, Freeman MR (2009) Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 69:5601–5609

    Article  PubMed  CAS  Google Scholar 

  • Dinger ME, Pang KC, Mercer TR, Mattick JS (2008) Differentiating protein-coding and noncoding RNA: challenges and ambiguities. PLoS Comput Biol 4:e1000176

    Article  PubMed  Google Scholar 

  • Elbashir SM, Lendeckel W, Tuschl T (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15:188–200

    Article  PubMed  CAS  Google Scholar 

  • Emmanouilidou E, Melachroinou K, Roumeliotis T, Garbis SD, Ntzouni M, Margaritis LH, Stefanis L, Vekrellis K (2010) Cell-produced alpha-synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. J Neurosci 30:6838–6851

    Article  PubMed  CAS  Google Scholar 

  • Ender C, Krek A, Friedländer MR, Beitzinger M, Weinmann L, Chen W, Pfeffer S, Rajewsky N, Meister G (2008) A human snoRNA with microRNA-like functions. Mol Cell 32:519–528

    Article  PubMed  CAS  Google Scholar 

  • Fauré J, Lachenal G, Court M, Hirrlinger J, Chatellard-Causse C, Blot B, Grange J, Schoehn G, Goldberg Y, Boyer V, Kirchhoff F, Raposo G, Garin J, Sadoul R (2006) Exosomes are released by cultured cortical neurones. Mol Cell Neurosci 31:642–648

    Article  PubMed  Google Scholar 

  • Feng J, Funk WD, Wang SS, Weinrich SL, Avilion AA, Chiu CP, Adams RR, Chang E, Allsopp RC, Yu J (1995) The RNA component of human telomerase. Science 269:1236–1241

    Article  PubMed  CAS  Google Scholar 

  • Fu X, Ravindranath L, Tran N, Petrovics G, Srivastava S (2006) Regulation of apoptosis by a prostate-specific and prostate cancer-associated noncoding gene, PCGEM1. DNA Cell Biol 25:135–141

    Article  PubMed  Google Scholar 

  • Galli R, Binda E, Orfanelli U, Cipelletti B, Gritti A, De Vitis S, Fiocco R, Foroni C, Dimeco F, Vescovi A (2004) Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res 64:7011–7021

    Article  PubMed  CAS  Google Scholar 

  • Germano I, Swiss V, Casaccia P (2010) Primary brain tumors, neural stem cell, and brain tumor cancer cells: where is the link? Neuropharmacology 58:903–910

    Article  PubMed  CAS  Google Scholar 

  • Gribaldo S, Brochier-Armanet C (2006) The origin and evolution of Archaea: a state of the art. Philos Trans R Soc Lond B Biol Sci 361:1007–1022

    Article  PubMed  CAS  Google Scholar 

  • Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S (1983) The RNA moiety of ribonuclease P is the catalytic subunit of the enzyme. Cell 35:849–857

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Gupta RA, Shah N, Wang KC, Kim J, Horlings HM, Wong DJ, Tsai MC, Hung T, Argani P, Rinn JL, Wang Y, Brzoska P, Kong B, Li R, West RB, van de Vijver MJ, Sukumar S (2010) Long non-coding RNA HOTAIR reprograms chromatin state to promote cancer metastasis. Nature 464:1071–1076

    Article  PubMed  CAS  Google Scholar 

  • Harris TJ, McCormick F (2010) The molecular pathology of cancer. Nat Rev Clin Oncol 7:251–265

    Article  PubMed  CAS  Google Scholar 

  • Holmgren L, Szeles A, Rajnavölgyi E, Folkman J, Klein G, Ernberg I, Falk KI (1999) Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood 93:3956–3963

    PubMed  CAS  Google Scholar 

  • Hong BS, Cho JH, Kim H, Choi EJ, Rho S, Kim J, Kim JH, Choi DS, Kim YK, Hwang D, Gho YS (2009) Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells. BMC Genomics 10:556

    Article  PubMed  Google Scholar 

  • Hunter MP, Ismail N, Zhang X, Aguda BD, Lee EJ, Yu L, Xiao T, Schafer J, Lee ML, Schmittgen TD, Nana-Sinkam SP, Jarjoura D, Marsh CB (2008) Detection of microRNA expression in human peripheral blood microvesicles. PLoS One 3:e3694

    Article  PubMed  Google Scholar 

  • Iero M, Valenti R, Huber V, Filipazzi P, Parmiani G, Fais S, Rivoltini L (2008) Tumour-released exosomes and their implications in cancer immunity. Cell Death Diff 15:80–88

    Article  CAS  Google Scholar 

  • Jain R, Rivera MC, Moore JE, Lake JA (2002) Horizontal gene transfer in microbial genome evolution. Theor Popul Biol 61:489–495

    Article  PubMed  Google Scholar 

  • Jarrous N, Reiner R (2007) Human RNase P: a tRNA-processing enzyme and transcription factor. Nucleic Acids Res 35:3519–3524

    Article  PubMed  CAS  Google Scholar 

  • Ji P, Diederichs S, Wang W, Böing S, Metzger R, Schneider PM, Tidow N, Brandt B, Buerger H, Bulk E, Thomas M, Berdel WE, Serve H, Müller-Tidow C (2003) MALAT-1, a novel noncoding RNA, and thymosin beta4 predict metastasis and survival in early-stage non-small cell lung cancer. Oncogene 22:8031–8041

    Article  PubMed  Google Scholar 

  • Kapranov P, Cheng J, Dike S, Nix DA, Duttagupta R, Willingham AT, Stadler PF, Hertel J, Hackermüller J, Hofacker IL, Bell I, Cheung E, Drenkow J, Dumais E, Patel S, Helt G, Ganesh M, Ghosh S, Piccolboni A, Sementchenko V, Tammana H, Gingeras TR (2007) RNA maps reveal new RNA classes and a possible function for pervasive transcription. Science 316:1484–1488

    Article  PubMed  CAS  Google Scholar 

  • Katayama S, Tomaru Y, Kasukawa T, Waki K, Nakanishi M, Nakamura M, Nishida H, Yap CC, Suzuki M, Kawai J, Suzuki H, Carninci P, Hayashizaki Y, Wells C, Frith M, Ravasi T, Pang KC, Hallinan J, Mattick J, Hume DA, Lipovich L, Batalov S, Engström PG, Mizuno Y, Faghihi MA, Sandelin A, Chalk AM, Mottagui-Tabar S, Liang Z, Lenhard B, Wahlestedt C (2005) Antisense transcription in the mammalian transcriptome. Science 309:1564–1566

    Article  PubMed  Google Scholar 

  • Kiss T (2002) Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109:145–148

    Article  PubMed  CAS  Google Scholar 

  • Kobayashi S, Boggon TJ, Dayaram T, Jänne PA, Kocher O, Meyerson M, Johnson BE, Eck MJ, Tenen DG, Halmos B (2005) EGFR mutation and resistance of non-small-cell lung cancer to gefitinib. N Engl J Med 352:786–792

    Article  PubMed  CAS  Google Scholar 

  • Kosaka N, Iguchi H, Yoshioka Y, Takeshita F, Matsuki Y, Ochiya T (2010) Secretory mechanisms and intercellular transfer of microRNAs in living cells. J Biol Chem 285:17442–17452

    Article  PubMed  CAS  Google Scholar 

  • Krämer-Albers EM, Bretz N, Tenzer S, Winterstein C, Möbius W, Berger H, Nave KA, Schild H, Trotter J (2007) Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons? Prot Clin 1:1446–1461

    Article  Google Scholar 

  • Lachenal G, Pernet-Gallay K, Chivet M, Hemming FJ, Belly A, Bodon G, Blot B, Haase G, Goldberg Y, Sadoul R (2011) Release of exosomes from differentiated neurons and its regulation by synaptic glutamatergic activity. Mol Cell Neurosci 46:409–418

    Article  PubMed  CAS  Google Scholar 

  • Lakkaraju A, Rodriguez-Boulan E (2008) Itinerant exosomes: emerging roles in cell and tissue polarity. Trends Cell Biol 18:199–209

    Article  PubMed  CAS  Google Scholar 

  • Lavie L, Kitova M, Maldener E, Meese E, Mayer J (2005) CpG methylation directly regulates transcriptional activity of the human endogenous retrovirus family HERV-K(HML-2). J Virol 79:876–883

    Article  PubMed  CAS  Google Scholar 

  • Lerner MR, Boyle JA, Hardin JA, Steitz JA (1981) Two novel classes of small ribonucleoproteins detected by antibodies associated with lupus erythematosus. Science 211:400

    Article  PubMed  CAS  Google Scholar 

  • Li X, Frank DN, Pace N, Zengel JM, Lindahl L (2002) Phylogenetic analysis of the structure of RNase MRP RNA in yeasts. RNA 8:740–751

    Article  PubMed  CAS  Google Scholar 

  • Macia A, Muñoz-Lopez M, Cortes JL, Hastings RK, Morell S, Lucena-Aguilar G, Marchal JA, Badge RM, Garcia-Perez JL (2011) Epigenetic control of retrotransposon expression in human embryonic stem cells. Mol Cell Biol 31:300–316

    Article  PubMed  CAS  Google Scholar 

  • Mack M, Kleinschmidt A, Bruhl H, Klier C, Nelson PJ, Cihak J, Plachy J, Stangassinger M, Erfle V, Schlondorff D (2000) Transfer of the chemokine receptor CCR5 between cells by membrane-derived microparticles: a mechanism for cellular human immunodeficiency virus 1 infection. Nat Med 6:769–775

    Article  PubMed  CAS  Google Scholar 

  • Mangiacasale R, Pittoggi C, Sciamanna I, Careddu A, Mattei E, Lorenzini R, Travaglini L, Landriscina M, Barone C, Nervi C, Lavia P, Spadafora C (2003) Exposure of normal and transformed cells to nevirapine, a reverse transcriptase inhibitor, reduces cell growth and promotes differentiation. Oncogene 22:2750–2751

    Article  PubMed  CAS  Google Scholar 

  • Mariner PD, Walters RD, Espinoza CA, Drullinger LF, Wagner SD, Kugel JF, Goodrich JA (2008) Human Alu RNA is a modular transacting repressor of mRNA transcription during heat shock. Mol Cell 29:499–509

    Article  PubMed  CAS  Google Scholar 

  • Marzesco AM, Janich P, Wilsch-Bräuninger M, Dubreuil V, Langenfeld K, Corbeil D, Huttner WB (2005) Release of extracellular membrane particles carrying the stem cell marker prominin-1 (CD133) from neural progenitors and other epithelial cells. J Cell Sci 118:2849–2858

    Article  PubMed  CAS  Google Scholar 

  • Mattick JS (2004) RNA regulation: a new genetics? Nat Rev Genet 5:316–323

    Article  PubMed  CAS  Google Scholar 

  • Mills RE, Bennett EA, Iskow RC, Devine SE (2007) Which transposable elements are active in the human genome? Trends Genet 23:183–191

    Article  PubMed  CAS  Google Scholar 

  • Miranda KC, Bond DT, McKee M, Skog J, Păunescu TG, Da Silva N, Brown D, Russo LM (2010) Nucleic acids within urinary exosomes/microvesicles are potential biomarkers for renal disease. Kidney Int 78:191–199

    Article  PubMed  Google Scholar 

  • Mwenda JM (1993) Biochemical characterization of a reverse transcriptase activity associated with retroviral-like particles isolated from human placental villous tissue. Cell Mol Biol Noisy-le-grand 39:317–328

    PubMed  CAS  Google Scholar 

  • Nelson SJ, Cha S (2003) Imaging glioblastoma multiforme. Cancer J 9:134–145

    Article  PubMed  CAS  Google Scholar 

  • Ng K, Pullirsch D, Leeb M, Wutz A (2007) Xist and the order of silencing. EMBO Rep 8:34–39

    Article  PubMed  CAS  Google Scholar 

  • Nilsson J, Skog J, Nordstrand A, Baranov V, Mincheva-Nilsson L, Breakefield XO, Widmark A (2009) Prostate cancer-derived urine exosomes: a novel approach to biomarkers for prostate cancer. Brit J Cancer 100:1603–1607

    Article  PubMed  CAS  Google Scholar 

  • Ohshima K, Inoue K, Fujiwara A, Hatakeyama K, Kanto K, Watanabe Y, Muramatsu K, Fukuda Y, Ogura S, Yamaguchi K, Mochizuki T (2010) Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 5:e13247

    Article  PubMed  Google Scholar 

  • Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, Hopmans E, Lindengey JL, de Gruijl TD, Wurdinger T, Middeldorp JM (2010) Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107:6328–6333

    Article  PubMed  CAS  Google Scholar 

  • Potolicchio I, Carven GJ, Xu X, Stipp C, Riese RJ, Stern LJ, Santambrogio L (2005) Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J Immunol 175:2237–2243

    PubMed  CAS  Google Scholar 

  • Poznanski AA, Calarco PG (1991) The expression of intracisternal A particle genes in the preimplantation mouse embryo. Dev Biol 143:271–281

    Article  PubMed  CAS  Google Scholar 

  • Qiu LX, Mao C, Zhang J, Zhu XD, Liao RY, Xue K, Li J, Chen Q (2010) Predictive and prognostic value of KRAS mutations in metastatic colorectal cancer patients treated with cetuximab: a meta-analysis of 22 studies. Eur J Cancer 46:2781–2787

    Article  PubMed  CAS  Google Scholar 

  • Rabinowits G, Gerçel-Taylor C, Day JM, Taylor DD, Kloecker GH (2009) Exosomal microRNA: a diagnostic marker for lung cancer. Clin Lung Cancer 10:42–46

    Article  PubMed  CAS  Google Scholar 

  • Rajendran L, Honsho M, Zahn TR, Keller P, Geiger KD, Verkade P, Simons K (2006) Alzheimer’s disease beta-amyloid peptides are released in association with exosomes. Proc Natl Acad Sci USA 103:11172–11177

    Article  PubMed  CAS  Google Scholar 

  • Ratajczak J, Miekus K, Kucia M, Zhang J, Reca R, Dvorak P, Ratajczak MZ (2006) Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20:847–856

    Article  PubMed  CAS  Google Scholar 

  • Rinn JL, Kertesz M, Wang JK, Squazzo SL, Xu X, Brugmann SA, Goodnough LH, Helms JA, Farnham PJ, Segal E, Chang HY (2007) Functional demarcation of active and silent chromatin domains in human HOX loci by noncoding RNAs. Cell 129:1311–1323

    Article  PubMed  CAS  Google Scholar 

  • Ruprecht K, Mayer J, Sauter M, Roemer K, Mueller-Lantzsch N (2008) Endogenous retroviruses and cancer. Cell Mol Life Sci 65:3366–3382

    Article  PubMed  CAS  Google Scholar 

  • Simons M, Raposo G (2009) Exosomes–vesicular carriers for intercellular communication. Curr Opin Cell Biol 21:575–581

    Article  PubMed  CAS  Google Scholar 

  • Singer T, McConnell MJ, Marchetto MC, Coufal NG, Gage FH (2010) LINE-1 retrotransposons: mediators of somatic variation in neuronal genomes? Trends Neurosci 33:345–354

    Article  PubMed  CAS  Google Scholar 

  • Skog J, Würdinger T, van Rijn S, Meijer D, Gainche L, Curry WTJ, Carter BS, Krichevsky AM, Breakefield XO (2008) Glioblastoma microvesicles transport RNA and protein that promote tumor growth and provide diagnostic biomarkers. Nat Cell Biol 10:1470–1476

    Article  PubMed  CAS  Google Scholar 

  • Smalheiser NR (2007) Exosomal transfer of proteins and RNAs at synapses in the nervous system. Biol Direct 2:35

    Article  PubMed  Google Scholar 

  • Smalley KS (2010) PLX-4032, a small-molecule B-Raf inhibitor for the potential treatment of malignant melanoma. Cur Opin Investig Drugs 11:699–706

    CAS  Google Scholar 

  • Srikantan V, Zou Z, Petrovics G, Xu L, Augustus M, Davis L, Livezey JR, Connell T, Sesterhenn IA, Yoshino K, Buzard GS, Mostofi FK, McLeod DG, Moul JW, Srivastava S (2000) PCGEM1, a prostate-specific gene, is overexpressed in prostate cancer. Proc Natl Acad Sci USA 97:12216–12221

    Article  PubMed  CAS  Google Scholar 

  • Storlazzi CT, Fioretos T, Surace C, Lonoce A, Mastrorilli A, Strömbeck B, D’Addabbo P, Iacovelli F, Minervini C, Aventin A, Dastugue N, Fonatsch C, Hagemeijer A, Jotterand M, Mühlematter D, Lafage-Pochitaloff M, Nguyen-Khac F, Schoch C, Slovak ML, Smith A, Solè F, Van Roy N, Johansson B, Rocchi M (2006) MYC-containing double minutes in hematologic malignancies: evidence in favor of the episome model and exclusion of MYC as the target gene. Hum Mol Genet 15:933–942

    Article  PubMed  CAS  Google Scholar 

  • Szpakowski S, Sun X, Lage JM, Dyer A, Rubinstein J, Kowalski D, Sasaki C, Costa J, Lizardi PM (2009) Loss of epigenetic silencing in tumors preferentially affects primate-specific retroelements. Gene 448:151–167

    Article  PubMed  CAS  Google Scholar 

  • Taft RJ, Mattick JS (2003) Increasing biological complexity is positively correlated with relative genome-wide expansion of non-protein coding DNA sequences. Genome Biol. http://www.genomebiology.com/2003/5/1/P1. Accessed 1 Dec 2003

  • Taft RJ, Pang KC, Mercer TR, Dinger M, Mattick JS (2010) Non-coding RNAs: regulators of disease. J Pathol 220:126–139

    Article  PubMed  CAS  Google Scholar 

  • Taylor DD, Gercel-Taylor C (2008) MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110:13–21

    Article  PubMed  CAS  Google Scholar 

  • Taylor AR, Robinson MB, Gifondorwa DJ, Tytell M, Milligan CE (2007) Regulation of heat shock protein 70 release in astrocytes: role of signaling kinases. Dev Neurobiol 67:1815–1829

    Article  PubMed  CAS  Google Scholar 

  • Théry C, Ostrowski M, Segura E (2009) Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9:581–593

    Article  PubMed  Google Scholar 

  • Ting DT, Lipson D, Paul S, Brannigan BW, Akhavanfard S, Coffman EJ, Contino G, Deshpande V, Iafrate AJ, Letovsky S, Rivera MN, Bardeesy N, Maheswaran S, Haber DA (2011) Aberrant overexpression of satellite repeats in pancreatic and other epithelial cancers. Science 331:593–596

    Article  PubMed  CAS  Google Scholar 

  • Trajkovic K, Hsu C, Chiantia S, Rajendran L, Wenzel D, Wieland F, Schwille P, Brügger B, Simons M (2008) Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319:1244–1247

    Article  PubMed  CAS  Google Scholar 

  • Tseng JJ, Hsieh YT, Hsu SL, Chou MM (2009) Metastasis associated lung adenocarcinoma transcript 1 is up-regulated in placenta previa increta/percreta and strongly associated with trophoblast-like cell invasion in vitro. Mol Hum Reprod 15:725–731

    Article  PubMed  CAS  Google Scholar 

  • Valadi H, Ekström K, Bossios A, Sjöstrand M, Lee JJ, Lötvall JO (2007) Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9:654–659

    Article  PubMed  CAS  Google Scholar 

  • Valadkhan S (2010) Role of the snRNAs in spliceosomal active site. RNA Biol 7:345–353

    Article  PubMed  CAS  Google Scholar 

  • Yang YG, Lindahl T, Barnes DE (2007) Trex1 exonuclease degrades ssDNA to prevent chronic checkpoint activation and autoimmune disease. Cell 1313:873–886

    Article  Google Scholar 

  • Yuan A, Farber EL, Rapoport AL, Tejada D, Deniskin R, Akhmedov NB, Farber DB (2009) Transfer of microRNAs by embryonic stem cell microvesicles. PLoS One 4:e4722

    Article  PubMed  Google Scholar 

  • Zhang Y, Liu D, Chen X, Li J, Li L, Bian Z, Sun F, Lu J, Yin Y, Cai X, Sun Q, Wang K, Ba Y, Wang Q, Wang D, Yang J, Liu P, Xu T, Yan Q, Zhang J, Zen K, Zhang CY (2010) Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol Cell 39:133–144

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This commentary is written in deep appreciation of the inspiring mentorship of Dr. Marshall Nirenberg. The authors have tried to include exciting new scientific ideas, which he always relished. The authors would like to thank Ms. Suzanne McDavitt for skilled editorial assistance and Drs. Charles Lai and David Corey for contributing figures. The Breakefield laboratory is funded by NINDS and NCI. Dr. Skog has a grant from the American Brain Tumor Association (ABTA).

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Authors and Affiliations

  1. Department of Neurology, Boston, MA, USA

    Kristan E. van der Vos, Leonora Balaj, Johan Skog & Xandra O. Breakefield

  2. Department of Radiology, Massachusetts General Hospital, Boston, MA, USA

    Kristan E. van der Vos, Leonora Balaj, Johan Skog & Xandra O. Breakefield

  3. Neuroscience Program, Harvard Medical School, Boston, MA, 02114, USA

    Kristan E. van der Vos, Leonora Balaj, Johan Skog & Xandra O. Breakefield

  4. Exosome Diagnostics, Inc, New York, NY, 10032, USA

    Johan Skog

  5. Molecular Neurogenetics Unit, Massachusetts General Hospital-East, 13th Street, Building 149, Charlestown, MA, 02129, USA

    Xandra O. Breakefield

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  1. Kristan E. van der Vos
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Correspondence to Xandra O. Breakefield.

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van der Vos, K.E., Balaj, L., Skog, J. et al. Brain Tumor Microvesicles: Insights into Intercellular Communication in the Nervous System. Cell Mol Neurobiol 31, 949–959 (2011). https://doi.org/10.1007/s10571-011-9697-y

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