Extracellular vesicles - vehicles that spread cancer genes

BioEssays

Volumn 34, Issue 6, 2012, Pages 489-497

  Rak, Janusz ^a   Guha, Abhijit ^b  

^a MONTREAL CHILDREN S HOSPITAL   (Canada)

^b UNIVERSITY HEALTH NETWORK   (Canada)

Author keywords

Cancer; EGFR; Exosomes; Microvesicles; Oncogenes

Indexed keywords

ANGIOGENIC FACTOR; BIOLOGICAL MARKER; CD147 ANTIGEN; CD63 ANTIGEN; CD81 ANTIGEN; CD9 ANTIGEN; CELL ADHESION MOLECULE; CHEMOKINE; CHEMOKINE RECEPTOR CCR4; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; EPIDERMAL GROWTH FACTOR RECEPTOR; EPSTEIN BARR VIRUS ANTIGEN 1; GELATINASE B; HEAT SHOCK PROTEIN 70; K RAS PROTEIN; MICRORNA 223; PADGEM PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P53; RAB27A PROTEIN; RAS PROTEIN;

ANGIOGENESIS; ARTICLE; BODY FLUID; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL FUNCTION; CELL MIGRATION; CELL TRANSFORMATION; CELL VACUOLE; DISEASE MARKER; EXTRACELLULAR VESICLE; GENE EXPRESSION; HUMAN; IMMUNITY; INFLAMMATION; MEDICAL TECHNOLOGY; NATURAL KILLER CELL; NEOPLASM; NONHUMAN; ONCOGENE; PATHOGENESIS; SIGNAL TRANSDUCTION; STEM CELL NICHE; STROMA; TUMOR GENE;

CELL LINE, TUMOR; HUMANS; NEOPLASMS; NEOPLASTIC PROCESSES; ONCOGENES; RAS PROTEINS; RECEPTOR, EPIDERMAL GROWTH FACTOR; SIGNAL TRANSDUCTION; TRANSPORT VESICLES;

EID: 84861228574     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201100169     Document Type: Article

References (100)

1. Bishop JM. 1995. Cancer: the rise of the genetic paradigm. Genes Dev 9: 1309- 15.
2. Vogelstein B, Kinzler KW. 2004. Cancer genes and the pathways they control. Nat Med 10: 789- 99.
3. Miller FR, Heppner GH. 1990. Cellular interactions in metastasis. Cancer Metastasis Rev 9: 21- 34.
4. Hanahan D, Weinberg RA. 2011. Hallmarks of cancer: the next generation. Cell 144: 646- 74.
5. Belting M, Wittrup A. 2008. Nanotubes, exosomes, and nucleic acid-binding peptides provide novel mechanisms of intercellular communication in eukaryotic cells: implications in health and disease. J Cell Biol 183: 1187- 91.
6. Holmgren L. 2010. Horizontal gene transfer: you are what you eat. Biochem Biophys Res Commun 396: 147- 51.
7. Rechavi O, Goldstein I, Kloog Y. 2009. Intercellular exchange of proteins: the immune cell habit of sharing. FEBS Lett 583: 1792- 9.
8. Al-Nedawi K, Meehan B, Rak J. 2009. Microvesicles: messengers and mediators of tumor progression. Cell Cycle 8: 2014- 8.
9. Leung CT, Brugge JS. 2012. Outgrowth of single oncogene-expressing cells from suppressive epithelial environments. Nature 482: 410- 3.
10. Rak J. 2009. Ras oncogenes and tumour vascular interface. In Thomas-Tikhonenko A, ed; Cancer Genome and Tumor Microenvironment. New York: Springer. p. 133- 65.
11. Pylayeva-Gupta Y, Grabocka E, Bar-Sagi D. 2011. RAS oncogenes: weaving a tumorigenic web. Nat Rev Cancer 11: 761- 74.
12. Rak J, Yu JL, Luyendyk L, Mackman N. 2006. Oncogenes, trousseau syndrome, and cancer-related changes in the coagulome of mice and humans. Cancer Res 66: 10643- 6.
13. Bouck N, Stellmach V, Hsu SC. 1996. How tumors become angiogenic. Adv Cancer Res 69: 135- 74.
14. Hill R, Song Y, Cardiff RD, Van Dyke T. 2005. Selective evolution of stromal mesenchyme with p53 loss in response to epithelial tumorigenesis. Cell 123: 1001- 11.
15. Hida K, Hida Y, Amin DN, Flint AF, et al. 2004. Tumor-associated endothelial cells with cytogenetic abnormalities. Cancer Res 64: 8249- 55.
16. Ricci-Vitiani L, Pallini R, Biffoni M, Todaro M, et al. 2010. Tumour vascularization via endothelial differentiation of glioblastoma stem-like cells. Nature 468: 824- 8.
17. Slaughter DP, Southwick HW, Smejkal W. 1953. Field cancerization in oral stratified squamous epithelium; clinical implications of multicentric origin. Cancer 6: 963- 8.
18. Sinkovics JG. 2011. Horizontal gene transfers with or without cell fusions in all categories of the living matter. Adv Exp Med Biol 714: 5- 89.
19. Choi IG, Kim SH. 2007. Global extent of horizontal gene transfer. Proc Natl Acad Sci USA 104: 4489- 94.
20. Aguzzi A, Rajendran L. 2009. The transcellular spread of cytosolic amyloids, prions, and prionoids. Neuron 64: 783- 90.
21. Gyorgy B, Szabo TG, Pasztoi M, Pal Z, et al. 2011. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci 68: 2667- 88.
22. Poupot M, Fournie JJ. 2003. Spontaneous membrane transfer through homotypic synapses between lymphoma cells. J Immunol 171: 2517- 23.
23. Rafii A, Mirshahi P, Poupot M, Faussat AM, et al. 2008. Oncologic trogocytosis of an original stromal cells induces chemoresistance of ovarian tumours. PLoS One 3: e3894.
24. Thery C, Ostrowski M, Segura E. 2009. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol 9: 581- 93.
25. Lee TH, D'Asti E, Magnus N, Al-Nedawi K, et al. 2011. Microvesicles as mediators of intercellular communication in cancer-the emerging science of cellular 'debris'. Semin Immunopathol 33: 455- 67.
26. Mathivanan S, Ji H, Simpson RJ. 2010. Exosomes: extracellular organelles important in intercellular communication. J Proteomics 73: 1907- 20.
27. Chargaff E, West R. 1946. The biological significance of the thromboplastic protein of blood. J Biol Chem 166: 189- 97.
28. Wolf P. 1967. The nature and significance of platelet products in human plasma. Br J Haematol 13: 269- 88.
29. Taylor DD, Doellgast GJ. 1979. Quantitation of peroxidase-antibody binding to membrane fragments using column chromatography. Anal Biochem 98: 53- 9.
30. Dvorak HF, Quay SC, Orenstein NS, Dvorak AM, et al. 1981. Tumor shedding and coagulation. Science 212: 923- 4.
31. Trams EG, Lauter CJ, Salem N Jr, Heine U. 1981. Exfoliation of membrane ecto-enzymes in the form of micro-vesicles. Biochim Biophys Acta 645: 63- 70.
32. Johnstone RM. 2006. Exosomes biological significance: a concise review. Blood Cells Mol Dis 36: 315- 21.
33. Harding C, Heuser J, Stahl P. 1983. Receptor-mediated endocytosis of transferrin and recycling of the transferrin receptor in rat reticulocytes. J Cell Biol 97: 329- 39.
34. Cocucci E, Racchetti G, Meldolesi J. 2009. Shedding microvesicles: artefacts no more. Trends Cell Biol 19: 43- 51.
35. Heijnen HF, Schiel AE, Fijnheer R, Geuze HJ, et al. 1999. Activated platelets release two types of membrane vesicles: microvesicles by surface shedding and exosomes derived from exocytosis of multivesicular bodies and alpha-granules. Blood 94: 3791- 9.
36. Mathivanan S, Fahner CJ, Reid GE, Simpson RJ. 2011. ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 40: D1241- 4.
37. Bianco F, Perrotta C, Novellino L, Francolini M, et al. 2009. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J 28: 1043- 54.
38. Li B, Antonyak MA, Zhang J, Cerione RA. 2012. RhoA triggers a specific signaling pathway that generates transforming microvesicles in cancer cells. Oncogene, in press, DOI: 10.1038/onc.2011.636
39. Muralidharan-Chari V, Clancy J, Plou C, Romao M, et al. 2009. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 19: 1875- 85.
40. Di Vizio D, Kim J, Hager MH, Morello M, et al. 2009. Oncosome formation in prostate cancer: association with a region of frequent chromosomal deletion in metastatic disease. Cancer Res 69: 5601- 9.
41. Ostrowski M, Carmo NB, Krumeich S, Fanget I, et al. 2010. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat Cell Biol 12: 19- 30.
42. Shen B, Wu N, Yang JM, Gould SJ. 2011. Protein targeting to exosomes/microvesicles by plasma membrane anchors. J Biol Chem 286: 14383- 95.
43. Ratajczak J, Wysoczynski M, Hayek F, Janowska-Wieczorek A, et al. 2006. Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 20: 1487- 95.
44. Valadi H, Ekstrom K, Bossios A, Sjostrand M, et al. 2007. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 9: 654- 9.
45. Mause SF, Weber C. 2010. Microparticles: protagonists of a novel communication network for intercellular information exchange. Circ Res 107: 1047- 57.
46. Skog J, Wurdinger T, van Rijn RS, Meijer DH, et al. 2008. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 10: 1470- 6.
47. Orlowski RZ, Eswara JR, Lafond-Walker A, Grever AMR, et al. 1998. Tumor growth inhibition induced in a murine model of human Burkitt's lymphoma by a proteasome inhibitor. Cancer Res 58: 4342- 8.
48. Trajkovic K, Hsu C, Chiantia S, Rajendran L, et al. 2008. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 319: 1244- 7.
49. Dignat-George F, Boulanger CM. 2011. The many faces of endothelial microparticles. Arterioscler Thromb Vasc Biol 31: 27- 33.
50. Wang JG, Williams JC, Davis BK, Jacobson K, et al. 2011. Monocytic microparticles activate endothelial cells in an IL-1beta-dependent manner. Blood 118: 2366- 74.
51. Tushuizen ME, Diamant M, Sturk A, Nieuwland R. 2011. Cell-derived microparticles in the pathogenesis of cardiovascular disease: friend or foe? Arterioscler Thromb Vasc Biol 31: 4- 9.
52. Al-Nedawi K, Meehan B, Micallef J, Lhotak V, et al. 2008. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat Cell Biol 10: 619- 24.
53. Yu X, Harris SL, Levine LA. 2006. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res 66: 4795- 801.
54. Lespagnol A, Duflaut D, Beekman C, Blanc L, et al. 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- 33.
55. Flaumenhaft R, Mairuhu AT, Italiano JE. 2010. Platelet- and megakaryocyte-derived microparticles. Semin Thromb Hemost 36: 881- 7.
56. Dolo V, D'Ascenzo S, Giusti I, Millimaggi D, et al. 2005. Shedding of membrane vesicles by tumor and endothelial cells. Ital J Anat Embryol 110: 127- 33.
57. Hendrix A, Westbroek W, Bracke M, De Wever WO. 2010. An ex(o)citing machinery for invasive tumor growth. Cancer Res 70: 9533- 7.
58. Greco V, Hannus M, Eaton S. 2001. Argosomes: a potential vehicle for the spread of morphogens through epithelia. Cell 106: 633- 45.
59. Simons M, Raposo G. 2009. Exosomes - vesicular carriers for intercellular communication. Curr Opin Cell Biol 21: 575- 81.
60. Del Conde I, Shrimpton CN, Thiagarajan P, Lopez JA. 2005. Tissue-factor-bearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation. Blood 106: 1604- 11.
61. Yu JL, May L, Milsom C, Anderson GM, et al. 2008. Contribution of host-derived tissue factor to tumor neovascularization. Arterioscler Thromb Vasc Biol 28: 1975- 81.
62. Martinez MC, Andriantsitohaina R. 2011. Microparticles in angiogenesis: therapeutic potential. Circ Res 109: 110- 9.
63. Mack M, Kleinschmidt A, Bruhl H, Klier C, et al. 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- 75.
64. Balaj L, Lessard R, Dai L, Cho YJ, et al. 2011. Tumour microvesicles contain retrotransposon elements and amplified oncogene sequences. Nat Commun 2: 180.
65. Jaiswal R, Gong J, Sambasivam S, Combes V, et al. 2012. Microparticle-associated nucleic acids mediate trait dominance in cancer. FASEB J 26: 420- 9.
66. Janowska-Wieczorek A, Marquez-Curtis LA, Wysoczynski M, Ratajczak MZ. 2006. Enhancing effect of platelet-derived microvesicles on the invasive potential of breast cancer cells. Transfusion 46: 1199- 209.
67. Yang MY, Chaudhary A, Seaman S, Dunty J, et al. 2011. The cell surface structure of tumor endothelial marker 8 (TEM8) is regulated by the actin cytoskeleton. Biochim Biophys Acta 1813: 39- 49.
68. Camussi G, Deregibus MC, Bruno S, Cantaluppi V, et al. 2010. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int 78: 838- 48.
69. Taraboletti G, D'Ascenzo S, Giusti I, Marchetti D, et al. 2006. Bioavailability of VEGF in tumor-shed vesicles depends on vesicle burst induced by acidic pH. Neoplasia 8: 96- 103.
70. Sheldon H, Heikamp E, Turley H, Dragovic R, et al. 2010. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 116: 2385- 94.
71. Al-Nedawi K, Meehan B, Kerbel RS, Allison AC, et al. 2009. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc Natl Acad Sci USA 106: 3794- 9.
72. Wolfers J, Lozier A, Raposo G, Regnault A, et al. 2001. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 7: 297- 303.
73. Taylor DD, Gercel-Taylor C. 2008. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 110: 13- 21.
74. Fritzsching B, Schwer B, Kartenbeck J, Pedal A, et al. 2002. Release and intercellular transfer of cell surface CD81 via microparticles. J Immunol 169: 5531- 7.
75. Ghosh AK, Secreto CR, Knox TR, Ding W, et al. 2010. Circulating microvesicles in B-cell chronic lymphocytic leukemia can stimulate marrow stromal cells: implications for disease progression. Blood 115: 1755- 64.
76. Gesierich S, Berezovskiy I, Ryschich E, Zoller M. 2006. Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res 66: 7083- 94.
77. Zwicker JI, Trenor CC III, Furie BC, Furie B. 2011. Tissue factor-bearing microparticles and thrombus formation. Arterioscler Thromb Vasc Biol 31: 728- 33.
78. Hood JL, San RS, Wickline SA. 2011. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res 71: 3792- 801.
79. Jung T, Castellana D, Klingbeil P, Cuesta H, et al. 2009. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 11: 1093- 105.
80. Grange C, Tapparo M, Collino F, Vitillo L, et al. 2011. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res 71: 5346- 56.
81. Peinado H, Lavotshkin S, Lyden D. 2011. The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin Cancer Biol 21: 139- 46.
82. Lima LG, Chammas R, Monteiro RQ, Moreira ME, et al. 2009. Tumor-derived microvesicles modulate the establishment of metastatic melanoma in a phosphatidylserine-dependent manner. Cancer Lett 283: 168- 75.
83. Milsom C, Magnus N, Meehan B, Al-Nedawi K, et al. 2009. Tissue factor and cancer stem cells. Is there a linkage? Arterioscler Thromb Vasc Biol 29: 2005- 14.
84. Holmgren L, Szeles A, Rajnavolgyi E, Folkman J, et al. 1999. Horizontal transfer of DNA by the uptake of apoptotic bodies. Blood 93: 3956- 63.
85. Bergsmedh A, Szeles A, Henriksson M, Bratt A, et al. 2001. Horizontal transfer of oncogenes by uptake of apoptotic bodies. Proc Natl Acad Sci USA 98: 6407- 11.
86. Sanderson MP, Keller S, Alonso A, Riedle S, et al. 2008. Generation of novel, secreted epidermal growth factor receptor (EGFR/ErbB1) isoforms via metalloprotease-dependent ectodomain shedding and exosome secretion. J Cell Biochem 103: 1783- 97.
87. Koga K, Matsumoto K, Akiyoshi T, Kubo M, et al. 2005. Purification, characterization and biological significance of tumor-derived exosomes. Anticancer Res 25: 3703- 7.
88. Meckes DG Jr, Shair KH, Marquitz AR, Kung CP, et al. 2010. Human tumor virus utilizes exosomes for intercellular communication. Proc Natl Acad Sci USA 107: 20370- 5.
89. Rak J, Al-Nedawi K, Meehan B, Guha A. 2010. Tumor cell-derived microvesicles. Patent application, CIP-05001770-379US-1.
90. Yu JL, May L, Lhotak V, Shahrzad S, et al. 2005. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 105: 1734- 41.
91. Pegtel DM, Cosmopoulos K, Thorley-Lawson DA, van Eijndhoven MA, et al. 2010. Functional delivery of viral miRNAs via exosomes. Proc Natl Acad Sci USA 107: 6328- 33.
92. Barth S, Meister G, Grasser FA. 2011. EBV-encoded miRNAs. Biochim Biophys Acta 1809: 631- 40.
93. Thery C, Clayton A, Amigorena S, Raposo G. 2006. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. In Bonifacino JS, Dasso M, Harford JB, Lippincott-Schwartz J, Yamada KM, eds; Current Protocols in Cell Biology. John Wiley & Sons. Unit 3.22:1-29.
94. Li J, Sulman E, Aldape K. 2012. Molecular biology of brain tumors. Handb Clin Neurol 104: 23- 34.
95. Nilsson RJ, Balaj L, Hulleman E, Van Rijn RS, et al. 2011. Blood platelets contain tumor-derived RNA biomarkers. Blood 118: 3680- 3.
96. Serrano M, Gomez-Lahoz E, DePinho RA, Beach D, et al. 1995. Inhibition of ras-induced proliferation and cellular transformation by p16INK4. Science 267: 249- 52.
97. Ding H, Roncari L, Shannon P, Wu X, et al. 2001. Astrocyte-specific expression of activated p21-ras results in malignant astrocytoma formation in a transgenic mouse model of human gliomas. Cancer Res 61: 3826- 36.
98. Denko NC, Giaccia AJ, Stringer JR, Stambrook PJ. 1994. The human Ha-ras oncogene induces genomic instability in murine fibroblasts within one cell cycle. Proc Natl Acad Sci USA 91: 5124- 8.
99. Shahrzad S, Quayle L, Stone C, Plumb C, et al. 2005. Ischemia-induced K-ras mutations in human colorectal cancer cells: role of microenvironmental regulation of MSH2 expression. Cancer Res 65: 8134- 41.
100. Antonyak MA, Li B, Boroughs LK, Johnson JL, et al. 2011. Cancer cell-derived microvesicles induce transformation by transferring tissue transglutaminase and fibronectin to recipient cells. Proc Natl Acad Sci USA 108: 4852- 7.