Tumor cell-derived exosomes: A message in a bottle

Biochimica et Biophysica Acta - Reviews on Cancer

Volumn 1826, Issue 1, 2012, Pages 103-111

  Kharaziha, Pedram ^a   Ceder, Sophia ^a   Li, Qiao ^a   Panaretakis, Theocharis ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Cancer therapy; Exosomes; Metastatic niche; Microenvironment; Molecular profile; Multivesicular bodies

Indexed keywords

MICRORNA;

BIOCHEMISTRY; BIOGENESIS; CANCER IMMUNOTHERAPY; CELL COMMUNICATION; CELL DEATH; CELL FUSION; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CELL SECRETION; CELL STRUCTURE; CELL TRANSPORT; ENDOCYTOSIS; EXOSOME; FILTER; GENE TRANSFER; HEMOFILTRATION; HUMAN; LIPID COMPOSITION; METASTASIS; NANOTECHNOLOGY; NONHUMAN; ONCOGENE; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; RNA ANALYSIS; TUMOR CELL; TUMOR MICROENVIRONMENT;

ANIMALS; CELL TRANSFORMATION, NEOPLASTIC; EXOSOMES; HUMANS; NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84859927971     PISSN: 0304419X     EISSN: 18792561     Source Type: Journal    
DOI: 10.1016/j.bbcan.2012.03.006     Document Type: Review

References (96)

1. Johnstone R.M., et al. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 1987, 262(19):9412-9420.
2. Mathivanan S., Ji H., Simpson R.J. Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 2010, 73(10):1907-1920.
3. + dendritic cells capable of inducing antiviral T cell responses. J. Immunol. 2009, 182(7):4200-4207.
4. Thery C., Ostrowski M., Segura E. Membrane vesicles as conveyors of immune responses. Nat. Rev. Immunol. 2009, 9(8):581-593.
5. Cocucci E., Racchetti G., Meldolesi J. Shedding microvesicles: artefacts no more. Trends Cell Biol. 2009, 19(2):43-51.
6. Razi M., Futter C.E. Distinct roles for Tsg101 and Hrs in multivesicular body formation and inward vesiculation. Mol. Biol. Cell 2006, 17(8):3469-3483.
7. Fader C.M., Colombo M.I. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 2009, 16(1):70-78.
8. Babst M. A Protein's Final ESCRT. Traffic 2005, 6(1):2-9.
9. Trajkovic K., et al. Ceramide triggers budding of exosome vesicles into multivesicular endosomes. Science 2008, 319(5867):1244-1247.
10. Bianco F., et al. Acid sphingomyelinase activity triggers microparticle release from glial cells. EMBO J. 2009, 28(8):1043-1054.
11. Savina A., et al. Exosome release is regulated by a calcium-dependent mechanism in K562 cells. J. Biol. Chem. 2003, 278(22):20083-20090.
12. Merendino A.M., et al. Hsp60 is actively secreted by human tumor cells. PLoS One 2010, 5(2):e9247.
13. Fader C.M., et al. Induction of autophagy promotes fusion of multivesicular bodies with autophagic vacuoles in k562 cells. Traffic 2008, 9(2):230-250.
14. Fader C.M., Colombo M.I. Autophagy and multivesicular bodies: two closely related partners. Cell Death Differ. 2008, 16(1):70-78.
15. Parolini I., et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 2009, 284(49):34211-34222.
16. Ostrowski M., et al. Rab27a and Rab27b control different steps of the exosome secretion pathway. Nat. Cell Biol. 2010, 12(1):19-30. sup pp 1-13.
17. Hsu C., et al. Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J. Cell Biol. 2010, 189(2):223-232.
18. Taylor D.D., Gercel-Taylor C. MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 2008, 110(1):13-21.
19. Rosell R., Wei J., Taron M. Circulating microRNA signatures of tumor-derived exosomes for early diagnosis of non-small-cell lung cancer. Clin. Lung Cancer 2009, 10(1):8-9.
20. Higginbotham J.N., et al. Amphiregulin exosomes increase cancer cell invasion. Curr. Biol. 2011, 21(9):779-786.
21. Al-Nedawi K., et al. Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10(5):619-624.
22. Yu J.L., et al. Oncogenic events regulate tissue factor expression in colorectal cancer cells: implications for tumor progression and angiogenesis. Blood 2005, 105(4):1734-1741.
23. Yu X., Harris S.L., Levine A.J. The regulation of exosome secretion: a novel function of the p53 protein. Cancer Res. 2006, 66(9):4795-4801.
24. Lehmann B.D., et al. Senescence-associated exosome release from human prostate cancer cells. Cancer Res. 2008, 68(19):7864-7871.
25. Raposo G., et al. B lymphocytes secrete antigen-presenting vesicles. J. Exp. Med. 1996, 183(3):1161-1172.
26. Peters P.J., et al. Molecules relevant for T cell-target cell interaction are present in cytolytic granules of human T lymphocytes. Eur. J. Immunol. 1989, 19(8):1469-1475.
27. Zitvogel L., et al. Eradication of established murine tumors using a novel cell-free vaccine: dendritic cell-derived exosomes. J. Leukoc. Biol. 1998, 79.
28. Segurado A.A., et al. Laboratory characterization of human T cell lymphotropic virus types 1 (HTLV-1) and 2 (HTLV-2) infections in blood donors from Sao Paulo, Brazil. Am.J.Trop. Med. Hyg. 1997, 57(2):142-148.
29. Perez-Blas M., et al. Impaired T cell signal transduction through CD28 in a patient with idiopathic thrombocytopenia. Clin. Exp. Immunol. 1991, 85(3):424-428.
30. Potolicchio I., et al. Proteomic analysis of microglia-derived exosomes: metabolic role of the aminopeptidase CD13 in neuropeptide catabolism. J. Immunol. 2005, 175(4):2237-2243.
31. Ji H., et al. Difference gel electrophoresis analysis of Ras-transformed fibroblast cell-derived exosomes. Electrophoresis 2008, 29(12):2660-2671.
32. Luo S.S., et al. Human villous trophoblasts express and secrete placenta-specific microRNAs into maternal circulation via exosomes. Biol. Reprod. 2009, 81(4):717-729.
33. Denzer K., et al. Exosome: from internal vesicle of the multivesicular body to intercellular signaling device. J. Cell Sci. 2000, 113(Pt 19):3365-3374.
34. Lai R.C., et al. Exosome secreted by MSC reduces myocardial ischemia/reperfusion injury. Stem Cell Res. 2010, 4(3):214-222.
35. Garrett J.T., Arteaga C.L. Resistance to HER2-directed antibodies and tyrosine kinase inhibitors: mechanisms and clinical implications. Cancer Biol. Ther. 2011, 11(9).
36. Alevizos I., et al. Exosomes from human saliva as a source of microRNA biomarkers. Oral Dis. 2010, 16(1):34-38.
37. Enattah N.S., et al. Evidence of still-ongoing convergence evolution of the lactase persistence T-13910 alleles in humans. Am. J. Hum. Genet. 2007, 81(3):615-625.
38. Andre F., et al. Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002, 360(9329):295-305.
39. Admyre C., et al. Exosomes with major histocompatibility complex class II and co-stimulatory molecules are present in human BAL fluid. Eur. Respir. J. 2003, 22(4):578-583.
40. Keller S., et al. CD24 is a marker of exosomes secreted into urine and amniotic fluid. Kidney Int. 2007, 72(9):1095-1102.
41. Gatti J.L., et al. Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod. 2005, 72(6):1452-1465.
42. Poliakov A., et al. Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 2009, 69(2):159-167.
43. Admyre C., et al. Exosomes with immune modulatory features are present in human breast milk. J. Immunol. 2007, 179(3):1969-1978.
44. Harrington M.G., et al. The morphology and biochemistry of nanostructures provide evidence for synthesis and signaling functions in human cerebrospinal fluid. Cerebrospinal Fluid Res. 2009, 6:10.
45. Rabinowits G., et al. Exosomal microRNA: a diagnostic marker for lung cancer. Clin. Lung Cancer 2009, 10(1):42-46.
46. Staubach S., Razawi H., Hanisch F.G. Proteomics of MUC1-containing lipid rafts from plasma membranes and exosomes of human breast carcinoma cells MCF-7. Proteomics 2009, 9(10):2820-2835.
47. Graner M.W., et al. Proteomic and immunologic analyses of brain tumor exosomes. FASEB J. 2009, 23(5):1541-1557.
48. Hegmans J.P., et al. Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. 2004, 164(5):1807-1815.
49. Mears R., et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004, 4(12):4019-4031.
50. Merendino A.M., et al. Hsp60 is actively secreted by human tumor cells. PLoS One 2010, 5(2):e9247.
51. Djerf E.A., et al. ErbB receptor tyrosine kinases contribute to proliferation of malignant melanoma cells: inhibition by gefitinib (ZD1839). Melanoma Res. 2009, 19(3):156-166.
52. Logozzi M., et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS One 2009, 4(4):e5219.
53. van Niel G., et al. Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121(2):337-349.
54. Mathivanan S., et al. Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature. Mol. Cell. Proteomics 2010, 9(2):197-208.
55. Valadi H., et al. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9(6):654-659.
56. Kogure T., et al. Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011.
57. Nagata S., et al. Identification of Tim4 as a phosphatidylserine receptor. Nature 2007, 450(7168):435-439.
58. Nolte-'t Hoen E.N., et al. Activated T cells recruit exosomes secreted by dendritic cells via LFA-1. Blood 2009, 113(9):1977-1981.
59. Segura E., et al. ICAM-1 on exosomes from mature dendritic cells is critical for efficient naive T-cell priming. Blood 2005, 106(1):216-223.
60. Tian T., et al. Visualizing of the cellular uptake and intracellular trafficking of exosomes by live-cell microscopy. J. Cell. Biochem. 2010, 111(2):488-496.
61. Escrevente C., et al. Interaction and uptake of exosomes by ovarian cancer cells. BMC Cancer 2011, 11:108.
62. Sui S.F., et al. Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11(5):675-687.
63. Zhang H.G., Grizzle W.E. Exosomes and cancer: a newly described pathway of immune suppression. Clin. Cancer Res. 2011, 17(5):959-964.
64. Simons M., Raposo G. Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21(4):575-581.
65. Webber J., et al. Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010, 70(23):9621-9630.
66. Al-Nedawi K., et al. Endothelial expression of autocrine VEGF upon the uptake of tumor-derived microvesicles containing oncogenic EGFR. Proc. Natl. Acad. Sci. U. S. A. 2009, 106(10):3794-3799.
67. Chairoungdua A., et al. Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling. J. Cell Biol. 2010, 190(6):1079-1091.
68. Deregibus M.C., et al. Endothelial progenitor cell derived microvesicles activate an angiogenic program in endothelial cells by a horizontal transfer of mRNA. Blood 2007, 110(7):2440-2448.
69. Grange C., et al. Microvesicles released from human renal cancer stem cells stimulate angiogenesis and formation of lung premetastatic niche. Cancer Res. 2011, 71(15):5346-5356.
70. Ciravolo V., et al. Potential role of HER2-overexpressing exosomes in countering Trastuzumab-based therapy. J. Cell. Physiol. 2011.
71. Verweij F.J., et al. LMP1 association with CD63 in endosomes and secretion via exosomes limits constitutive NF-kappaB activation. EMBO J. 2011, 30(11):2115-2129.
72. Zoller M. Tetraspanins: push and pull in suppressing and promoting metastasis. Nature reviews. Cancer 2009, 9(1):40-55.
73. Kuhn S., et al. A complex of EpCAM, claudin-7, CD44 variant isoforms, and tetraspanins promotes colorectal cancer progression. Mol. Cancer Res. 2007, 5(6):553-567.
74. Funakoshi T., et al. Expression of tetraspanins in human lung cancer cells: frequent downregulation of CD9 and its contribution to cell motility in small cell lung cancer. Oncogene 2003, 22(5):674-687.
75. Ohshima K., et al. Let-7 microRNA family is selectively secreted into the extracellular environment via exosomes in a metastatic gastric cancer cell line. PLoS One 2010, 5(10):e13247.
76. Pegtel D.M., et al. Functional delivery of viral miRNAs via exosomes. Proc. Natl. Acad. Sci. 2010.
77. Zhang Y., et al. Secreted monocytic miR-150 enhances targeted endothelial cell migration. Mol. Cell 2010, 39(1):133-144.
78. Skog J., et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 2008, 10(12):1470-1476.
79. Lim P.K., et al. Gap junction-mediated import of microRNA from bone marrow stromal cells can elicit cell cycle quiescence in breast cancer cells. Cancer Res. 2011, 71(5):1550-1560.
80. Taverna S., et al. Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int. J. Cancer 2011.
81. Hood J.L., San R.S., Wickline S.A. Exosomes released by melanoma cells prepare sentinel lymph nodes for tumor metastasis. Cancer Res. 2011, 71(11):3792-3801.
82. Ristorcelli E., et al. Human tumor nanoparticles induce apoptosis of pancreatic cancer cells. FASEB J. 2008, 22(9):3358-3369.
83. Camussi G., et al. Exosomes/microvesicles as a mechanism of cell-to-cell communication. Kidney Int. 2010, 78(9):838-848.
84. Khan S., et al. Survivin is released from cancer cells via exosomes. Apoptosis 2011, 16(1):1-12.
85. + T-cell apoptosis. Blood Cells Mol. Dis. 2005, 35(2):169-173.
86. Safaei R., et al. Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol. Cancer Ther. 2005, 4(10):1595-1604.
87. Shedden K., et al. Expulsion of small molecules in vesicles shed by cancer cells: association with gene expression and chemosensitivity profiles. Cancer Res. 2003, 63(15):4331-4337.
88. Park J.E., et al. Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol. Cell. Proteomics 2010, 9(6):1085-1099.
89. Jung T., et al. CD44v6 dependence of premetastatic niche preparation by exosomes. Neoplasia 2009, 11(10):1093-1105.
90. Hao S., et al. Epigenetic transfer of metastatic activity by uptake of highly metastatic B16 melanoma cell-released exosomes. Exp. Oncol. 2006, 28(2):126-131.
91. Wolfers J., et al. Tumor-derived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat. Med. 2001, 7(3):297-303.
92. Viaud S., et al. Dendritic cell-derived exosomes for cancer immunotherapy: what's next?. Cancer Res. 2010, 70(4):1281-1285.
93. Zhuang X., et al. Treatment of brain inflammatory diseases by delivering exosome encapsulated anti-inflammatory drugs from the nasal region to the brain. Mol. Ther. 2011, 19(10):1769-1779.
94. Lakhal S., Wood M.J.A. Exosome nanotechnology: an emerging paradigm shift in drug delivery. BioEssays 2011, 33(10):737-741.
95. Mathivanan S., Fahner C.J., Reid G.E., Simpson R.J. ExoCarta 2012: database of exosomal proteins RNA and lipids. Nucleic Acids Res. 2012.
96. Mathivanan S., Simpson R.J. ExoCarta: A compendium of exosomal proteins and RNA. Proteomics 2009, 21:4997-5000.