Oncogenic extracellular vesicles in brain tumor progression

Frontiers in Physiology

Volumn 3 JUL, Issue , 2012, Pages

  D'Asti, Esterina ^a   Garnier, Delphine ^a   Lee, Tae H ^a   Montermini, Laura ^a   Meehan, Brian ^a   Rak, Janusz ^a  

^a RESEARCH INSTITUTE OF THE MCGILL UNIVERSITY HEALTH CENTRE   (Canada)

Author keywords

Brain; Cancer; Exosomes; Extracellular vesicles; Oncogenes

Indexed keywords

EID: 84866465336     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2012.00294     Document Type: Review

References (139)

1. Abusamra, A. J., Zhong, Z., Zheng, X., Li, M., Ichim, T. E., Chin, J. L., and Min, W. P. (2005). Tumor exo-somes expressing Fas ligand mediate CD8+ T-cell apoptosis. Blood Cells Mol. Dis. 35, 169-173.
2. Aharon, A., and Brenner, B. (2010). The role of breast cancer cells microparticles in thrombogenicity following chemotherapy. Thromb. Res. 125(SUPPL. 2), S179.
3. Al-Nedawi, K., Meehan, B., Kerbel, R. S., Allison, A. C., and Rak, J. (2009a). Endothelial expression of autocrine VEGF upon the uptake of tumorderived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. U.S.A. 106, 3794-3799.
4. Al-Nedawi, K., Meehan, B., and Rak, J. (2009b). Microvesicles: messengers and mediators of tumor progression. Cell Cycle 8, 2014-2018.
5. Al-Nedawi, K., Meehan, B., Micaleff, J., Guha, A., and Rak, J., (2010). "Phosphoproteome of tumour derived microvesicles as a source of biomarkers to monitor the effects of targeted agents in glioblastoma," in Society of Neurooncology, Annual Meeting, (Montreal, QC).
6. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V., May, L., Guha, A., and Rak, J. (2008). Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 10, 619-624.
7. Alvarez-Erviti, L., Seow, Y., Yin, H., Betts, C., Lakhal, S., and Wood, M. J. (2011). Delivery of siRNA to the mouse brain by systemic injection of targeted exosomes. Nat. Biotechnol. 29, 341-345.
8. Antonucci, F., Turola, E., Riganti, L., Caleo, M., Gabrielli, M., Perrotta, C., Novellino, L., Clementi, E., Giussani, P., Viani, P., Matteoli, M., and Verderio, C. (2012). Microvesicles released from microglia stimulate synaptic activity via enhanced sphingolipid metabolism. EMBO J. 31, 1231-1240.
9. Antonyak, M. A., Li, B., Boroughs, L. K., Johnson, J. L., Druso, J. E., Bryant, K. L., Holowka, D. A., and Cerione, R. A. (2011). Cancer cellderived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc. Natl. Acad. Sci. U.S.A. 108, 4852-4857.
10. Avraham, R., and Yarden, Y. (2011). Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nat. Rev. Mol. Cell Biol. 12, 104-117.
11. Baj-Krzyworzeka, M., Majka, M., Pratico, D., Ratajczak, J., Vilaire, G., Kijowski, J., Reca, R., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2002). Plateletderived microparticles stimulate proliferation, survival, adhesion, and chemotaxis of hematopoietic cells. Exp. Hematol. 30, 450-459.
12. Balaj, L., Chen, W., Liau, L. M., Soto, H., Garret, M., Zhu, L. D., Sivaraman, S., Wong, E. T., Carter, B., Hochberg, F. H., Breakefield, X. O., and Skog, J. (2012). BEAMing qRT-PCR analysis of IDH1 mutant in tumor microvesicles. J. Extracellular Ve s i c le s 1, 30.
13. Balaj, L., Lessard, R., Dai, L., Cho, Y. J., Pomeroy, S. L., Breakefield, X. O., and Skog, J. (2011). Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat. Commun. 2, 180.
14. Belting, M., and Wittrup, A. (2008). Nanotubes, exosomes, and nucleic acidbinding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease. J. Cell Biol. 183, 1187-1191.
15. Bergersen, L. H., and Gundersen, V. (2009). Morphological evidence for vesicular glutamate release from astrocytes. Neuroscience 158, 260-265.
16. Bergsmedh, A., Szeles, A., Henriksson, M., Bratt, A., Folkman, M. J., Spetz, A. L., and Holmgren, L. (2001). Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc. Natl. Acad. Sci. U.S.A. 98, 6407-6411.
17. Bianco, F., Perrotta, C., Novellino, L., Francolini, M., Riganti, L., Menna, E., Saglietti, L., Schuchman, E. H., Furlan, R., Clementi, E., Matteoli, M., and Verderio, C. (2009). Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 28, 1043-1054.
18. Biernat, W., Huang, H., Yokoo, H., Kleihues, P., and Ohgaki, H. (2004). Predominant expression of mutant EGFR (EGFRvIII) is rare in primary glioblastomas. Brain Pathol. 14, 131-136.
19. Bolukbasi, M. F., Mizrak, A., Ozdener, G. B., Madlener, S., Strobel, T., Erkan, E. P., Fan, J.-B., Breakefield, X. O., and Saydam, O. (2012). miR-1289 and "zipcode" -like sequence enrich mRNA in microvesicles. J. Extracellular Vesicles 1, 2.
20. Brase, J. C., Johannes, M., Schlomm, T., Falth, M., Haese, A., Steuber, T., Beissbarth, T., Kuner, R., and Sultmann, H. (2011). Circulating miRNAs are correlated with tumor progression in prostate cancer. Int. J. Cancer 128, 608-616.
21. Burnier, L., Fontana, P., Kwak, B. R., and ngelillo-Scherrer, A. (2009). Cell-derived microparticles in haemostasis and vascular medicine. Thromb. Haemost. 101, 439-451.
22. Camussi, G., Deregibus, M. C., Bruno, S., Cantaluppi, V., and Biancone, L. (2010). Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 78, 838-848.
23. Ceruti, S., Colombo, L., Magni, G., Vigano, F., Boccazzi, M., Deli, M. A., Sperlagh, B., Abbracchio, M. P., and Kittel, A. (2011). Oxygenglucose deprivation increases the enzymatic activity and the microvesicle-mediated release of ectonucleotidases in the cells composing the blood-brain barrier. Neurochem. Int. 59, 259-271.
24. Chen, J., Chen, S., Chen, Y., Zhang, C., Wang, J., Zhang, W., Liu, G., Zhao, B., and Chen, Y. (2011). Circulating endothelial progenitor cells and cellular membrane microparticles in db/db diabetic mouse: possible implications in cerebral ischemic damage. Am. J. Physiol. Endocrinol. Metab. 301, E62-E71.
25. Chen, X., Liang, H., Zhang, J., Zen, K., and Zhang, C. Y. (2012). Secreted microRNAs: a new form of intercellular communication. Trends Cell Biol. 22, 125-132.
26. Choi, I. G., and Kim, S. H. (2007). Global extent of horizontal gene transfer. Proc. Natl. Acad. Sci. U.S.A. 104, 4489-4494.
27. Collino, F., Deregibus, M. C., Bruno, S., Sterpone, L., Aghemo, G., Viltono, L., Tetta, C., and Camussi, G. (2010). Microvesicles derived from adult human bone marrow and tissue specific mesenchymal stem cells shuttle selected pattern of miRNAs. PLoS ONE. 5:e11803. doi: 10.1371/journal.pone.0011803
28. Colombo, E., Borgiani, B., Verderio, C., and Furlan, R. (2012). Microvesicles: novel biomarkers for neurological disorders. Front. Physiol. 3:63. doi: 10.3389/fphys. 2012.00063
29. Cortez, M. A., Bueso-Ramos, C., Ferdin, J., Lopez-Berestein, G., Sood, A. K., and Calin, G. A. (2011). MicroRNAs in body fluids-the mix of hormones and biomarkers. Nat. Rev. Clin. Oncol. 8, 467-477.
30. Court, F. A., Hendriks, W. T., MacGillavry, H. D., Alvarez, J., and van, M. 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.
31. D'Asti, E., Huang, A., and Rak, J. (2012). "Downregulation of tissue factor (TF) in medulloblastoma cells expressing miR-520g," in Proceedings of Keystone Syposia, (Snowmass, CO).
32. de Vrij, J., Kwappenberg, K. M. C., Maas, S. L. N., Kleijn, A., Lamfers, M. L., Dirven, C. M. F., Schilham, M. W., and Broekman, M. L. D. (2012). Immune modulatory properties of glioblastoma multiforme exosomes. J. Extracellular Vesicles 1, 62.
33. Del Conde, I., Shrimpton, C. N., Thiagarajan, P., and Lopez, J. A. (2005). Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106, 1604-1611.
34. Deregibus, M. C., Cantaluppi, V., Calogero, R., Lo, I. M., Tetta, C., Biancone, L., Bruno, S., Bussolati, B., and 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.
35. Di Vizio, D., Kim, J., Hager, M. H., Morello, M., Yang, W., Lafargue, C. J., True, L. D., Rubin, M. A., Adam, R. M., Beroukhim, R., Demichelis, F., and Freeman, M. R. (2009). Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res. 69, 5601-5609.
36. Dolo, V., D'Ascenzo, S., Giusti, I., Millimaggi, D., Taraboletti, G., and Pavan, A. (2005). Shedding of membrane vesicles by tumor and endothelial cells. Ital. J. Anat. Embryol. 110, 127-133.
37. Dvorak, H. F., Van DeWater, L., Bitzer, A. M., Dvorak, A. M., Anderson, D., Harvey, V. S., Bach, R., Davis, G. L., DeWolf, W., and Carvalho, A. C. (1983). Procoagulant activity associated with plasma membrane vesicles shed by cultured tumor cells. Cancer Res. 43, 4434-4442.
38. Faure, 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., and Sadoul, R. (2006). Exosomes are released by cultured cortical neurones. Mol. Cell. Neurosci. 31, 642-648.
39. Fernando, R. I., Litzinger, M., Trono, P., Hamilton, D. H., Schlom, J., and Palena, C. (2010). The T-box transcription factor Brachyury promotes epithelialmesenchymal transition in human tumor cells. J. Clin. Invest. 120, 533-544.
40. Finak, G., Bertos, N., Pepin, F., Sadekova, S., Souleimanova, M., Zhao, H., Chen, H., Omeroglu, G., Meterissian, S., Omeroglu, A., Hallett, M., and Park, M. (2008). Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 14, 518-527.
41. Fitzner, D., Schnaars, M., van, R. D., Krishnamoorthy, G., Dibaj, P., Bakhti, M., Regen, T., Hanisch, U. K., and Simons, M. (2011). Selective transfer of exosomes from oligodendrocytes to microglia by macropinocytosis. J. Cell Sci. 124, 447-458.
42. Franklin, J. L., Beckler, M. D., Higginbotham, J. N., and Coffey, R. J. Jr. (2012). Exosomes from mutant KRAS cells transfer KRAS and transform wild type KRAS recipient cells. J. Extracellular Vesicles 1, 26.
43. Frye, B. C., Halfter, S., Djudjaj, S., Muehlenberg, P., Weber, S., Raffetseder, U., En-Nia, A., Knott, H., Baron, J. M., Dooley, S., Bernhagen, J., and Mertens, P. R. (2009). Y-box protein-1 is actively secreted through a non-classical pathway and acts as an extracellular mitogen. EMBO Rep. 10, 783-789.
44. Garcia-Olmo, D. C., Dominguez, C., Garcia-Arranz, M., Anker, P., Stroun, M., Garcia-Verdugo, J. M., and Garcia-Olmo, D. (2010). Cellfree nucleic acids circulating in the plasma of colorectal cancer patients induce the oncogenic transformation of susceptible cultured cells. Cancer Res. 70, 560-567.
45. Garnier, D., Milsom, C. C., Magnus, N., Bentley, V., Lee, T.-H., Meehan, B., Montermini, L., and Rak, J. (2012). Epithelial-to-Mesenchymal Transition (EMT) Alters Vesiculation of Cancer Cells Expressing Oncogenic Epidermal Growth Factor Receptor (EGFR): implications for the Aggressive, Procoagulant and Proangiogenic Properties. Abstract 1018 (Minisymposium, TB05.01 Tumor Angiogenesis and Antiangiogenic Therapy).
46. Garzon, R., Marcucci, G., and Croce, C. M. (2010). Targeting microRNAs in cancer: rationale, strategies and challenges. Nat. Rev. Drug Discov. 9, 775-789.
47. Gesierich, S., Berezovskiy, I., Ryschich, E., and Zoller, M. (2006). Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res. 66, 7083-7094.
48. Ghosh, A. K., Secreto, C. R., Knox, T. R., Ding, W., Mukhopadhyay, D., and Kay, N. E. (2010). Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood 115, 1755-1764.
49. Graner, M. W., Alzate, O., Dechkovskaia, A. M., Keene, J. D., Sampson, J. H., Mitchell, D. A., and Bigner, D. D. (2009). Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 23, 1541-1557.
50. Grange, C., Tapparo, M., Collino, F., Vitillo, L., Damasco, C., Deregibus, M. C., Tetta, C., Bussolati, B., and Camussi, G. (2011). Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 71, 5346-5356.
51. Guescini, M., Genedani, S., Stocchi, V., and Agnati, L. F. (2010). Astrocytes and Glioblastoma cells release exosomes carrying mtDNA. J. Neural Tr a n s m. 117, 1-4.
52. Hendrix, A., Westbroek, W., Bracke, M., and De, W. O. (2010). An ex(o)citing machinery for invasive tumor growth. Cancer Res. 70, 9533-9537.
53. Heneghan, H. M., Miller, N., Lowery, A. J., Sweeney, K. J., Newell, J., and Kerin, M. J. (2010). Circulating microRNAs as novel minimally invasive biomarkers for breast cancer. Ann. Surg. 251, 499-505.
54. Holmgren, L., Szeles, A., Rajnavolgyi, E., Folkman, J., Klein, G., Ernberg, I., and Falk, K. I. (1999). Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood 93, 3956-3963.
55. Hood, J. L., San, R. S., and Wickline, S. A. (2011). Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 71, 3792-3801.
56. Hunter, K. (2006). Host genetics influence tumour metastasis. Nat. Rev. Cancer 6, 141-146.
57. Inda, M. M., Bonavia, R., Mukasa, A., Narita, Y., Sah, D. W., Vandenberg, S., Brennan, C., Johns, T. G., Bachoo, R., Hadwiger, P., Tan, P., DePinho, R. A., Cavenee, W., and Furnari, F. (2010). Tumor heterogeneity is an active process maintained by a mutant EGFR-induced cytokine circuit in glioblastoma. Genes Dev. 24, 1731-1745.
58. Jaiswal, R., Gong, J., Sambasivam, S., Combes, V., Mathys, J. M., Davey, R., Grau, G. E., and Bebawy, M. (2012). Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J. 1, 420-429.
59. Janowska-Wieczorek, A., Marquez-Curtis, L. A., Wysoczynski, M., and Ratajczak, M. Z. (2006). Enhancing effect of platelet-derived microvesi-cles on the invasive potential of breast cancer cells. Transfusion 46, 1199-1209.
60. Janowska-Wieczorek, A., Wysoczynski, M., Kijowski, J., Marquez-Curtis, L., Machalinski, B., Ratajczak, J., and Ratajczak, M. Z. (2005). Microvesicles derived from activated platelets induce metastasis and angiogenesis in lung cancer. Int. J. Cancer 113, 752-760.
61. Jones, D. T., Kocialkowski, S., Liu, L., Pearson, D. M., Ichimura, K., and Collins, V. P. (2009). Oncogenic RAF1 rearrangement and a novel BRAF mutation as alternatives to KIAA1549, BRAF fusion in activating the MAPK pathway in pilo-cytic astrocytoma. Oncogene 28, 2119-2123.
62. Jung, T., Castellana, D., Klingbeil, P., Cuesta, H. I., Vitacolonna, M., Orlicky, D. J., Roffler, S. R., Brodt, P., and Zoller, M. (2009). CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 11, 1093-1105.
63. Key, N. S., Chantrathammachart, P., Moody, P. W., and Chang, J.-Y. (2010). Membrane microparticles in VTE and cancer. Thromb. Res. 125, S80-S83.
64. Khorana, A. A. (2010). Venous throm-boembolism and prognosis in cancer. Thromb. Res. 125, 490-493.
65. Koga, K., Matsumoto, K., Akiyoshi, T., Kubo, M., Yamanaka, N., Tasaki, A., Nakashima, H., Nakamura, M., Kuroki, S., Tanaka, M., and Katano, M. (2005). Purification, characterization and biological significance of tumor-derived exosomes. Anticancer Res. 25, 3703-3707.
66. Kosaka, N., Iguchi, H., and Ochiya, T. (2010). Circulating microRNA in body fluid: a new potential biomarker for cancer diagnosis and prognosis. Cancer Sci. 101, 2087-2092.
67. Kramer-Albers, E. M., Bretz, N., Tenzer, S., Winterstein, C., Mobius, W., Berger, H., Nave, K. A., Schild, H., and Trotter, J. (2007). Oligodendrocytes secrete exosomes containing major myelin and stress-protective proteins: trophic support for axons? Proteomics Clin. Appl. 1, 1446-1461.
68. Lavon, I., Refael, M., Zelikovitch, B., Shalom, E., and Siegal, T. (2010). Serum DNA can define tumor-specific genetic and epigenetic markers in gliomas of various grades. Neuro Oncol. 12, 173-180.
69. Lee, T. H., D'Asti, E., Magnus, N., Al-Nedawi, K., Meehan, B., and Rak, J. (2011a). Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular 'debris'. Semin. Immunopathol. 33, 455-467.
70. Lee, T. H., Montermini, L., Meehan, B., Guha, A., and Rak, J. (2011b). "Microvesicles as intercellular messengers carrying oncogenic and tumour suppressory signals," in Poster Presentation, The Canadian Cancer Research Conference, (Toronto, ON).
71. Lespagnol, A., Duflaut, D., Beekman, C., Blanc, L., Fiucci, G., Marine, J. C., Vidal, M., Amson, R., and Telerman, A. (2008). Exosome secretion, including the DNA damage-induced p53-dependent secretory pathway, is severely compromised in TSAP6/Steap3-null mice. Cell Death Differ. 15, 1723-1733.
72. Li, J., Sulman, E., and Aldape, K. (2012). Molecular biology of brain tumors. Handb. Clin. Neurol. 104, 23-34.
73. Li, M., Lee, K. F., Lu, Y., Clarke, I., Shih, D., Eberhart, C., Collins, V. P., Van, M. T., Picard, D., Zhou, L., Boutros, P. C., Modena, P., Liang, M. L., Scherer, S. W., Bouffet, E., Rutka, J. T., Pomeroy, S. L., Lau, C. C., Taylor, M. D., Gajjar, A., Dirks, P. B., Hawkins, C. E., and Huang, A. (2009). Frequent amplification of a chr19q13.41 microRNA polycistron in aggressive primitive neuroecto-dermal brain tumors. Cancer Cell 16, 533-546.
74. Liu, C., Yu, S., Zinn, K., Wang, J., Zhang, L., Jia, Y., Kappes, J. C., Barnes, S., Kimberly, R. P., Grizzle, W. E., and Zhang, H. G. (2006). Murine mammary carcinoma exo-somes promote tumor growth by suppression of NK cell function. J. Immunol. 176, 1375-1385.
75. Lleonart, M. E., Garcia-Foncillas, J., Sanchez-Prieto, R., Martin, P., Moreno, A., Salas, C., and Cajal, S. (1998). Microsatellite instability and p53 mutations in sporadic right and left colon carcinoma: different clinical and molecular implications. Cancer 83, 889-895.
76. Mani, S. A., Guo, W., Liao, M. J., Eaton, E. N., Ayyanan, A., Zhou, A. Y., Brooks, M., Reinhard, F., Zhang, C. C., Shipitsin, M., Campbell, L. L., Polyak, K., Brisken, C., Yang, J., and Weinberg, R. A. (2008). The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133, 704-715.
77. Marzesco, A. M., Janich, P., Wilsch-Brauninger, M., Dubreuil, V., Langenfeld, K., Corbeil, D., and Huttner, W. B. (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.
78. Mathivanan, S., Fahner, C. J., Reid, G. E., and Simpson, R. J. (2012). ExoCarta 2012, database of exosomal proteins, RNA and lipids. Nucleic Acids Res. 40, D1241-D1244.
79. Mathivanan, S., Ji, H., and Simpson, R. J. (2010). Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73, 1907-1920.
80. Mause, S. F., and Weber, C. (2010). Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ. Res. 107, 1047-1057.
81. Meckes, D. G. Jr., Shair, K. H., Marquitz, A. R., Kung, C. P., Edwards, R. H., and Raab-Traub, N. (2010). Human tumor virus utilizes exosomes for intercellular communication. Proc. Natl. Acad. Sci. U.S.A.107, 20370-20375.
82. Milsom, C. C., Yu, J. L., Mackman, N., Micallef, J., Anderson, G. M., Guha, A., and Rak, J. W. (2008). Tissue factor regulation by epidermal growth factor receptor and epithelial-to-mesenchymal transitions: effect on tumor initiation and angiogenesis. Cancer Res. 68, 10068-10076.
83. Mitchell, P. S., Parkin, R. K., Kroh, E. M., Fritz, B. R., Wyman, S. K., Pogosova-Agadjanyan, E. L., Peterson, A., Noteboom, J., O'Briant, K. C., Allen, A., Lin, D. W., Urban, N., Drescher, C. W., Knudsen, B. S., Stirewalt, D. L., Gentleman, R., Vessella, R. L., Nelson, P. S., Martin, D. B., and Tewari, M. (2008). Circulating microRNAs as stable blood-based markers for cancer detection. Proc. Natl. Acad. Sci. U.S.A. 105, 10513-10518.
84. Mittelbrunn, M., and Sanchez-Madrid, F.(2012). Intercellular commu nication: diverse structures for exchange of genetic informa tion. Nat. Rev. Mol. Cell Biol. 13, 328-335.
85. Muralidharan-Chari, V., Clancy, J. W., Sedgwick, A., and Souza-Schorey, C. (2010). Microvesicles: mediators of extracellular communication during cancer progression. J. Cell Sci. 123, 1603-1611.
86. Nilsson, R. J., Balaj, L., Hulleman, E., van, R. S., Pegtel, D. M., Walraven, M., Widmark, A., Gerritsen, W. R., Verheul, H. M., Vandertop, W. P., Noske, D. P., Skog, J., and Wurdinger, T. (2011). Blood platelets contain tumor-derived RNA biomarkers. Blood 118, 3680-3683.
87. Noerholm, M., Balaj, L., Limperg, T., Salehi, A., Zhu, L. D., Hochberg, F. H., Breakefield, X. O., Carter, B. S., and Skog, J. (2012). RNA expression patterns in serum microvesicles from patients with glioblastoma multiforme and controls. BMC Cancer 12, 22.
88. Ohgaki, H., and Kleihues, P. (2009). Genetic alterations and signaling pathways in the evolution of gliomas. Cancer Sci. 100, 2235-2241.
89. Parsons, D. W., Jones, S., Zhang, X., Lin, J. C., Leary, R. J., Angenendt, P., Mankoo, P., Carter, H., Siu, I. M., Gallia, G. L., Olivi, A., McLendon, R., Rasheed, B. A., Keir, S., Nikolskaya, T., Nikolsky, Y., Busam, D. A., Tekleab, H., Diaz, L. A. Jr., Hartigan, J., Smith, D. R., Strausberg, R. L., Marie, S. K., Shinjo, S. M., Yan, H., Riggins, G.J., Bigner, D. D., Karchin, R., Papadopoulos, N., Parmigiani, G., Vogelstein, B., Velculescu, V. E ., and Kinzler, K. W. (2008). An inte grated genomic analysis of human glioblastoma multiforme. Science 321, 1807-1812.
90. Paugh, B. S., Broniscer, A., Qu, C., Miller, C. P., Zhang, J., Tatevossian, R. G., Olson, J. M., Geyer, J. R., Chi, S. N., da Silva, N. S., Onar-Thomas, A., Baker, J. N., Gajjar, A., Ellison, D. W., and Baker, S. J. (2011). Genome-wide analyses identify recurrent amplifications of receptor tyrosine kinases and cell-cycle regulatory genes in diffuse intrinsic pontine glioma. J. Clin. Oncol. 29, 3999-4006.
91. Peinado, H., Lavotshkin, S., and Lyden, D. (2011). The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 21, 139-146.
92. Phillips, H. S., Kharbanda, S., Chen, R., Forrest, W. F., Soriano, R. H., Wu, T. D., Misra, A., Nigro, J. M., Colman, H., Soroceanu, L., Williams, P. M., Modrusan, Z., Feuerstein, B. G., and Aldape, K. (2006). Molecular subclasses of high-grade glioma predict prognosis, delineate a pattern of disease progression, and resemble stages in neurogenesis. Cancer Cell 9,157-173.
93. Piccin, A., Murphy, W. G., and Smith, O. P. (2007). Circulating micropar-ticles: pathophysiology and clinical implications. Blood Rev. 21, 157-171.
94. Potolicchio, I., Carven, G. J., Xu, X., Stipp, C., Riese, R. J., Stern, L. J., and Santambrogio, L. (2005). Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neu-ropeptide catabolism. J. Immunol. 175, 2237-2243.
95. Rafii, A., Mirshahi, P., Poupot, M., Faussat, A. M., Simon, A., Ducros, E., Mery, E., Couderc, B., Lis, R., Capdet, J., Bergalet, J., Querleu, D., Dagonnet, F., Fournie, J. J., Marie, J. P., Pujade-Lauraine, E., Favre, G., Soria, J., and Mirshahi, M. (2008). Oncologic trogocyto-sis of an original stromal cells induces chemoresistance of ovarian tumours. PLoS ONE. 3:e3894. doi: 10.1371/journal.pone.0003894
96. Rak, J., and Guha, A. (2012). Extracellular vesicles - vehicles that spread cancer genes. Bioessays 10,489-497.
97. Ramachandran, A., Yan, H., Bentink, S., Noerholm, M., Berking, C., Flaherty, K., Hochberg, F. H., and Skog, J. (2011). "Detection of BRAF mutations in serum/plasma microvesicles (exosomes) of malignant melanoma patients. Molecular Cancer Therapeutics 10," in Proceedings of the AACR-NCI-EORTC International Conference: Molecular Targets and Cancer Therapeutics, 2011 Nov 12-16; San Francisco: CA; Philadelphia: PA. AACR; Mol. Cancer Ther. 2011; 10(11 SUPPL.): Abstract nr C139.
98. Ratajczak, J., Miekus, K., Kucia, M., Zhang, J., Reca, R., Dvorak, P., and Ratajczak, M. Z. (2006a). Embryonic stem cell-derived microvesicles reprogram hematopoietic progenitors: evidence for horizontal transfer of mRNA and protein delivery. Leukemia 20, 847-856.
99. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A., and Ratajczak, M. Z. (2006b). Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20, 1487-1495.
100. Rohan, R. M., Fernandez, A., Udagawa, T., Yuan, J., and D'Amato, R. J. (2000). Genetic heterogeneity of angiogenesis in mice. FASEB J. 14, 871-876.
101. Schwartzentruber, J., Korshunov, A., Liu, X. Y., Jones, D. T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A. M., Quang, D. A., Tonjes, M., Hovestadt, V., Albrecht, S., Kool, M., Nantel, A., Konermann, C., Lindroth, A., Jager, N., Rausch, T., Ryzhova, M., Korbel, J. O., Hielscher, T., Hauser, P., Garami, M., Klekner, A., Bognar, L., Ebinger, M., Schuhmann, M. U., Scheurlen, W., Pekrun, A., Fruhwald, M. C., Roggendorf, W., Kramm, C., Durken, M., Atkinson, J., Lepage, P., Montpetit, A., Zakrzewska, M., Zakrzewski, K., Liberski, P. P., Dong, Z., Siegel, P., Kulozik, A. E., Zapatka, M., Guha, A., Malkin, D., Felsberg, J., Reifenberger, G., von, D. A., Ichimura, K., Collins, V. P., Witt, H., Milde, T., Witt, O., Zhang, C., Castelo-Branco, P., Lichter, P., Faury, D., Tabori, U., Plass, C., Majewski, J., Pfister, S. M., and Jabado, N. (2012). Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature 482, 226-231.
102. Serrano, M., Gomez-Lahoz, E., DePinho, R. A., Beach, D., and Bar-Sagi, D. (1995). Inhibition of ras-induced proliferation and cellular transformation by p16INK4. Science 267, 249-252.
103. Shao, H., Chung, J., Balaj, L., Charest, A., Bigner, D. D., Carter, B. S., Hochberg, F. H., Breakefield, X. O., Weissleder, R., and Lee, H. (2012). Protein typing of circulating microvesicles allows real-time monitoring of glioblastoma therapy. J. Extracellular Vesicles 1, 26.
104. Sheldon, H., Heikamp, E., Turley, H., Dragovic, R., Thomas, P., Oon, C. E., Leek, R., Edelmann, M., Kessler, B., Sainson, R. C., Sargent, I., Li, J. L., and Harris, A. L. (2010). New mechanism for Notch signaling to endothelium at a distance by Deltalike 4 incorporation into exosomes. Blood 116, 2385-2394.
105. Shen, B., Wu, N., Yang, J. M., and Gould, S. J. (2011). Protein targeting to exosomes/microvesicles by plasma membrane anchors. J. Biol. Chem. 286, 14383-14395.
106. Simons, M., and Raposo, G. (2009). Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 21, 575-581.
107. Sinkovics, J. G. (2011). Horizontal gene transfers with or without cell fusions in all categories of the living matter. Adv. Exp. Med. Biol. 714, 5-89.
108. Skog, J., Wurdinger, T., van, R. S., Meijer, D. H., Gainche, L., Curry, W. T. Jr., Carter, B. S., Krichevsky, A. M., and Breakefield, X. O. (2008). Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10, 1470-1476.
109. Smalheiser, N. R. (2009). Do neural cells communicate with endothe-lial cells via secretory exosomes and microvesicles? Cardiovasc. Psychiatry Neurol. 2009, 383086.
110. Snuderl, M., Fazlollahi, L., Le, L. P., Nitta, M., Zhelyazkova, B. H., Davidson, C. J., Akhavanfard, S., Cahill, D. P., Aldape, K. D., Betensky, R. A., Louis, D. N., and Iafrate, A. J. (2011). Mosaic amplification of multiple receptor tyrosine kinase genes in glioblastoma. Cancer Cell 20, 810-817.
111. Steeg, P. S., Camphausen, K. A., and Smith, Q. R. (2011). Brain metas-tases as preventive and therapeutic targets. Nat. Rev. Cancer 11, 352-363.
112. Stiles, C. D., and Rowitch, D. H. (2008). Glioma stem cells: a midterm exam. Neuron 58, 832-846.
113. Svensson, K. J., Kucharzewska, P., Christianson, H. C., Skold, S., Lofstedt, T., Johansson, M. C., Morgelin, M., Bengzon, J., Ruf, W., and Belting, M. (2011). 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. 108, 13147-13152.
114. Swisher, E. M., Wollan, M., Mahtani, S. M., Willner, J. B., Garcia, R., Goff, B. A., and King, M. C. (2005). Tumor-specific p53 sequences in blood and peritoneal fluid of women with epithelial ovarian cancer. Am. J. Obstet. Gynecol. 193, 662-667.
115. Taraboletti, G., D'Ascenzo, S., Giusti, I., Marchetti, D., Borsotti, P., Millimaggi, D., Giavazzi, R., Pavan, A., and Dolo, V. (2006). Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH. Neoplasia 8, 96-103.
116. Tauro, B., Mathias, R., Greening, D., Le, V. P. A., Ji, H., Mathivanan, S., Zhu, J. L., and Simpson, R. J. (2012). Oncogenic Ras-induced epithelial-mesenchymal transition in MDCK cells alters proteome profiles of secreted exosomes. J. Extracellular Ve s i c le s 1, 28.
117. Taylor, D. D., and Gercel-Taylor, C. (2005). Tumour-derived exosomes and their role in cancer-associated T-cell signalling defects. Br. J. Cancer 92, 305-311.
118. Taylor, D. D., and Gercel-Taylor, C. (2008). MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110, 13-21.
119. Tesselaar, M. E., Romijn, F. P., Van Der Linden, I. K., Prins, F. A., Bertina, R. M., and Osanto, S. (2007). Microparticle-associated tissue factor activity: a link between cancer and thrombosis? J. Thromb. Haemost. 5, 520-527.
120. Thery, C., Ostrowski, M., and Segura, E. (2009). Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 9, 581-593.
121. Thiery, J. P., Acloque, H., Huang, R. Y., and Nieto, M. A. (2009). Epithelial-mesenchymal transitions in development and disease. Cell 139, 871-890.
122. Trajkovic, K., Hsu, C., Chiantia, S., Rajendran, L., Wenzel, D., Wieland, F., Schwille, P., Brugger, B., and Simons, M. (2008). Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319, 1244-1247.
123. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M., Lee, J. J., and Lotvall, J. O. (2007). Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 9, 654-659.
124. Valenti, R., Huber, V., Iero, M., Filipazzi, P., Parmiani, G., and Rivoltini, L. (2007). Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res. 67, 2912-2915.
125. van der Vos, K. E., Balaj, L., Skog, J., and Breakefield, X. O. (2011). Brain tumor microvesicles: insights into intercellular communication in the nervous system. Cell. Mol. Neurobiol. 31, 949-959.
126. Verhaak, R. G., Hoadley, K. A., Purdom, E., Wang, V., Qi, Y., Wilkerson, M. D., Miller, C. R., Ding, L., Golub, T., Mesirov, J. P., Alexe, G., Lawrence, M., O'Kelly, M., Tamayo, P., Weir, B. A., Gabriel, S., Winckler, W., Gupta, S., Jakkula, L., Feiler, H. S., Hodgson, J. G., James, C. D., Sarkaria, J. N., Brennan, C., Kahn, A., Spellman, P. T., Wilson, R. K., Speed, T. P., Gray, J. W., Meyerson, M., Getz, G., Perou, C. M., and Hayes, D. N. (2010). Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 19, 98-110.
127. von Bartheld, C. S., and Altick, A. L. (2011). Multivesicular bodies in neurons: distribution, protein content, and trafficking functions. Prog. Neurobiol. 93, 313-340.
128. Wen, P. Y., and Kesari, S. (2008). Malignant gliomas in adults. N. Engl. J. Med. 359, 492-507.
129. Williams, R. L., and Urbe, S. (2007). The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell Biol. 8, 355-368.
130. Wolf, P. (1967). The nature and significance of platelet products in human plasma. Br. J. Haematol. 13, 269-288.
131. Wolfers, J., Lozier, A., Raposo, G., Regnault, A., Thery, C., Masurier, C., Flament, C., Pouzieux, S., Faure, F., Tursz, T., Angevin, E., Amigorena, S., and Zitvogel, L. (2001). Tumor-derived exo-somes are a source of shared tumor rejection antigens for CTL cross-priming. Nat. Med. 7, 297-303.
132. Wrensch, M., Minn, Y., Chew, T., Bondy, M., and Berger, M. S. (2002). Epidemiology of primary brain tumors: current concepts and review of the literature. Neuro Oncol. 4, 278-299.
133. Wu, X., Northcott, P. A., Dubuc, A., Dupuy, A. J., Shih, D. J., Witt, H., Croul, S., Bouffet, E., Fults, D. W., Eberhart, C. G., Garzia, L., Van, M. T., Zagzag, D., Jabado, N., Schwartzentruber, J., Majewski, J., Scheetz, T. E., Pfister, S. M., Korshunov, A., Li, X. N., Scherer, S. W., Cho, Y. J., Akagi, K., MacDonald, T. J., Koster, J., McCabe, M. G., Sarver, A. L., Collins, V. P., Weiss, W. A., Largaespada, D. A., Collier, L. S., and Taylor, M. D. (2012). Clonal selection drives genetic divergence of metastatic medulloblastoma. Nature 482, 529-533.
134. Yan, H., Parsons, D. W., Jin, G., McLendon, R., Rasheed, B. A., Yuan, W., Kos, I., Batinic-Haberle, I., Jones, S., Riggins, G. J., Friedman, H., Friedman, A., Reardon, D., Herndon, J., Kinzler, K. W., Velculescu, V. E., Vogelstein, B., and Bigner, D. D. (2009). IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 360, 765-773.
135. Yu, X., Harris, S. L., and Levine, A. J. (2006). The regulation of exo-some secretion: a novel function of the p53 protein. Cancer Res. 66, 4795-4801.
136. Yu, J. L., May, L., Lhotak, V., Shahrzad, S., Shirasawa, S., Weitz, J. I., Coomber, B. L., Mackman, N., and Rak, J. W. (2005). Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 105, 1734-1741.
137. Yu, J. L., and Rak, J. W. (2004). Shedding of tissue factor (TF)-containing microparticles rather than alternatively spliced TF is the main source of TF activity released from human cancer cells. J. Thromb. Haemost. 2, 2065-2067.
138. Zhu, Y., and Parada, L. F. (2002). The molecular and genetic basis of neurological tumours. Nat. Rev. Cancer 2, 616-626.
139. Zwicker, J. I. (2010). Predictive value of tissue factor bearing microparticles in cancer associated thrombosis. Thromb. Res. 125, S89-S91.