Contribution of proteomics to understanding the role of tumor-derived exosomes in cancer progression: State of the art and new perspectives

Proteomics

Volumn 13, Issue 10-11, 2013, Pages 1581-1594

  Fontana, Simona ^a   Saieva, Laura ^a   Taverna, Simona ^a   Alessandro, Riccardo ^a  

^a UNIVERSITY OF PALERMO   (Italy)

Author keywords

Cell biology; Tumor progression; Tumor derived exosome

Indexed keywords

AMPHIREGULIN; BETA 2 MICROGLOBULIN; BETA CATENIN; CADHERIN; CALPHOBINDIN II; CD147 ANTIGEN; CD151 ANTIGEN; CD82 ANTIGEN; CD9 ANTIGEN; CD97 ANTIGEN; CISPLATIN; CLAUDIN 3; CLAUDIN 7; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL PEPTIDASE IV; DNA DIRECTED DNA POLYMERASE DELTA; EPHRIN RECEPTOR B2; ESCRT PROTEIN; GLYCEROPHOSPHOINOSITOL INOSITOLPHOSPHODIESTERASE; LIPOCORTIN 1; LIPOCORTIN 2; LIPOCORTIN 5; MESSENGER RNA; MICRORNA; MICROSOMAL AMINOPEPTIDASE; MULTIDRUG RESISTANCE PROTEIN 2; PROTEIN 14 3 3; PROTEOCHONDROITIN SULFATE; SYNEXIN; TETRASPANIN;

APOPTOSIS; BLADDER CANCER; BREAST CANCER; CANCER CELL; CANCER GROWTH; CARCINOGENESIS; CELL MIGRATION; CELL SPREADING; EXOSOME; HUMAN; INSULINOMA; LUNG CANCER; MEDULLOBLASTOMA; MELANOMA; MESOTHELIOMA; NEOPLASM; NONHUMAN; OVARY CANCER; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONTENT; PROTEOMICS; REVIEW; TUMOR MICROENVIRONMENT;

EID: 84878653585     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201200398     Document Type: Review

References (86)

1. Thery, C., Zitvogel, L., Amigorena, S., Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2002, 2, 569-579.
2. Simpson, R. J., Jensen, S. S., Lim, J. W., Proteomic profiling of exosomes: current perspectives. Proteomics 2008, 8, 4083-4099.
3. Caby, M. P., Lankar, D., Vincendeau-Scherrer, C., Raposo, G. et al., Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 2005, 17, 879-887.
4. Pisitkun, T., Shen, R. F., Knepper, M. A., Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. USA 2004, 101, 13368-13373.
5. Skriner, K., Adolph, K., Jungblut, P. R., Burmester, G. R., Association of citrullinated proteins with synovial exosomes. Arthritis Rheum. 2006, 54, 3809-3814.
6. Andre, F., Schartz, N. E., Movassagh, M., Flament, C. et al., Malignant effusions and immunogenic tumour-derived exosomes. Lancet 2002, 360, 295-305.
7. Gatti, J. L., Metayer, S., Belghazi, M., Dacheux, F. et al., Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod. 2005, 72, 1452-1465.
8. Ronquist, G., Brody, I., The prostasome: its secretion and function in man. Biochim. Biophys. Acta 1985, 822, 203-218.
9. Thery, C., Boussac, M., Veron, P., Ricciardi-Castagnoli, P. et al., Proteomic analysis of dendritic cell-derived exosomes: a secreted subcellular compartment distinct from apoptotic vesicles. J. Immunol. 2001, 166, 7309-7318.
10. Valadi, H., Ekstrom, K., Bossios, A., Sjostrand, M. et al., Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat. Cell Biol. 2007, 9, 654-659.
11. Keller, S., Sanderson, M. P., Stoeck, A., Altevogt, P., Exosomes: from biogenesis and secretion to biological function. Immunol. Lett. 2006, 107, 102-108.
12. Pan, B. T., Johnstone, R. M., Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 1983, 33, 967-978.
13. Fevrier, B., Raposo, G., Exosomes: endosomal-derived vesicles shipping extracellular messages. Curr. Opin. Cell Biol. 2004, 16, 415-421.
14. Ludwig, A. K., Giebel, B., Exosomes: small vesicles participating in intercellular communication. Int. J. Biochem. Cell Biol. 2012, 44, 11-15.
15. Feng, D., Zhao, W. L., Ye, Y. Y., Bai, X. C. et al., Cellular internalization of exosomes occurs through phagocytosis. Traffic 2010, 11, 675-687.
16. Mathivanan, S., Lim, J. W., Tauro, B. J., Ji, H. 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, 197-208.
17. Simons, M., Raposo, G., Exosomes-vesicular carriers for intercellular communication. Curr. Opin. Cell Biol. 2009, 21, 575-581.
18. Zhang, H. G., Grizzle, W. E., Exosomes and cancer: a newly described pathway of immune suppression. Clin. Cancer Res. 2011, 17, 959-964.
19. Al-Nedawi, K., Meehan, B., Rak, J., Microvesicles: messengers and mediators of tumor progression. Cell Cycle 2009, 8, 2014-2018.
20. Ratajczak, J., Wysoczynski, M., Hayek, F., Janowska-Wieczorek, A. et al., Membrane-derived microvesicles: important and underappreciated mediators of cell-to-cell communication. Leukemia 2006, 20, 1487-1495.
21. Valenti, R., Huber, V., Filipazzi, P., Pilla, L. et al., Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes. Cancer Res. 2006, 66, 9290-9298.
22. Zomer, A., Vendrig, T., Hopmans, E. S., van Eijndhoven, M. et al., Exosomes: fit to deliver small RNA. Commun. Integr. Biol. 2010, 3, 447-450.
23. Andre, F., Schartz, N. E., Chaput, N., Flament, C. et al., Tumor-derived exosomes: a new source of tumor rejection antigens. Vaccine 2002, 20(Suppl 4), A28-A31.
24. Dolo, V., Adobati, E., Canevari, S., Picone, M. A. et al., Membrane vesicles shed into the extracellular medium by human breast carcinoma cells carry tumor-associated surface antigens. Clin. Exp. Metastasis 1995, 13, 277-286.
25. Hegmans, J. P., Bard, M. P., Hemmes, A., Luider, T. M. et al., Proteomic analysis of exosomes secreted by human mesothelioma cells. Am. J. Pathol. 2004, 164, 1807-1815.
26. Mears, R., Craven, R. A., Hanrahan, S., Totty, N. et al., Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics 2004, 4, 4019-4031.
27. Cho, J. A., Yeo, D. J., Son, H. Y., Kim, H. W. et al., Exosomes: a new delivery system for tumor antigens in cancer immunotherapy. Int. J. Cancer 2005, 114, 613-622.
28. Filipazzi, P., Burdek, M., Villa, A., Rivoltini, L. et al., Recent advances on the role of tumor exosomes in immunosuppression and disease progression. Semin. Cancer Biol. 2012, 22, 342-349.
29. Yang, C., Robbins, P. D., The roles of tumor-derived exosomes in cancer pathogenesis. Clin. Dev. Immunol. 2011, doi:10.1155/2011/842849.
30. Peinado, H., Lavotshkin, S., Lyden, D., The secreted factors responsible for pre-metastatic niche formation: old sayings and new thoughts. Semin. Cancer Biol. 2011, 21, 139-146.
31. Safaei, R., Larson, B. J., Cheng, T. C., Gibson, M. A. et al., Abnormal lysosomal trafficking and enhanced exosomal export of cisplatin in drug-resistant human ovarian carcinoma cells. Mol. Cancer Ther. 2005, 4, 1595-1604.
32. Battke, C., Ruiss, R., Welsch, U., Wimberger, P. et al., Tumour exosomes inhibit binding of tumour-reactive antibodies to tumour cells and reduce ADCC. Cancer Immunol. Immunother. 2011, 60, 639-648.
33. Kogure, T., Lin, W. L., Yan, I. K., Braconi, C. et al., Intercellular nanovesicle-mediated microRNA transfer: a mechanism of environmental modulation of hepatocellular cancer cell growth. Hepatology 2011, 54, 1237-1248.
34. Al-Nedawi, K., Meehan, B., Micallef, J., Lhotak, V. et al., Intercellular transfer of the oncogenic receptor EGFRvIII by microvesicles derived from tumour cells. Nat. Cell Biol. 2008, 10, 619-624.
35. Khan, S., Jutzy, J. M., Aspe, J. R., McGregor, D. W. et al., Survivin is released from cancer cells via exosomes. Apoptosis 2011, 16, 1-12.
36. Webber, J., Steadman, R., Mason, M. D., Tabi, Z. et al., Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 2010, 70, 9621-9630.
37. Sidhu, S. S., Mengistab, A. T., Tauscher, A. N., LaVail, J. et al., The microvesicle as a vehicle for EMMPRIN in tumor-stromal interactions. Oncogene 2004, 23, 956-963.
38. Dolo, V., Ginestra, A., Cassara, D., Violini, S. et al., Selective localization of matrix metalloproteinase 9, beta1 integrins, and human lymphocyte antigen class I molecules on membrane vesicles shed by 8701-BC breast carcinoma cells. Cancer Res. 1998, 58, 4468-4474.
39. Ginestra, A., Miceli, D., Dolo, V., Romano, F. M. et al., Membrane vesicles in ovarian cancer fluids: a new potential marker. Anticancer Res. 1999, 19, 3439-3445.
40. Giusti, I., D'Ascenzo, S., Millimaggi, D., Taraboletti, G. et al., Cathepsin B mediates the pH-dependent proinvasive activity of tumor-shed microvesicles. Neoplasia 2008, 10, 481-488.
41. Escola, J. M., Kleijmeer, M. J., Stoorvogel, W., Griffith, J. M. et al., Selective enrichment of tetraspan proteins on the internal vesicles of multivesicular endosomes and on exosomes secreted by human B-lymphocytes. J. Biol. Chem. 1998, 273, 20121-20127.
42. Charrin, S., le Naour, F., Silvie, O., Milhiet, P. E. et al., Lateral organization of membrane proteins: tetraspanins spin their web. Biochem. J. 2009, 420, 133-154.
43. Berditchevski, F., Complexes of tetraspanins with integrins: more than meets the eye. J. Cell Sci. 2001, 114, 4143-4151.
44. Hemler, M. E., Tetraspanin proteins mediate cellular penetration, invasion, and fusion events and define a novel type of membrane microdomain. Annu. Rev. Cell Dev. Biol. 2003, 19, 397-422.
45. Gesierich, S., Berezovskiy, I., Ryschich, E., Zoller, M., Systemic induction of the angiogenesis switch by the tetraspanin D6.1A/CO-029. Cancer Res. 2006, 66, 7083-7094.
46. Pant, S., Hilton, H., Burczynski, M. E., The multifaceted exosome: biogenesis, role in normal and aberrant cellular function, and frontiers for pharmacological and biomarker opportunities. Biochem. Pharmacol. 2012, 83, 1484-1494.
47. Hood, J. L., Pan, H., Lanza, G. M., Wickline, S. A., Paracrine induction of endothelium by tumor exosomes. Lab Invest. 2009, 89, 1317-1328.
48. Taverna, S., Flugy, A., Saieva, L., Kohn, E. C. et al., Role of exosomes released by chronic myelogenous leukemia cells in angiogenesis. Int. J. Cancer 2012, 130, 2033-2043.
49. Rivoltini, L., Canese, P., Huber, V., Iero, M. et al., Escape strategies and reasons for failure in the interaction between tumour cells and the immune system: how can we tilt the balance towards immune-mediated cancer control? Expert Opin. Biol. Ther. 2005, 5, 463-476.
50. Valenti, R., Huber, V., Iero, M., Filipazzi, P. et al., Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res. 2007, 67, 2912-2915.
51. Andreola, G., Rivoltini, L., Castelli, C., Huber, V. et al., Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J. Exp. Med. 2002, 195, 1303-1316.
52. Liu, C., Yu, S., Zinn, K., Wang, J. et al., Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J. Immunol. 2006, 176, 1375-1385.
53. Ashiru, O., Boutet, P., Fernandez-Messina, L., Aguera-Gonzalez, S. et al., Natural killer cell cytotoxicity is suppressed by exposure to the human NKG2D ligand MICA*008 that is shed by tumor cells in exosomes. Cancer Res. 2010, 70, 481-489.
54. Clayton, A., Mitchell, J. P., Court, J., Linnane, S. et al., Human tumor-derived exosomes down-modulate NKG2D expression. J. Immunol. 2008, 180, 7249-7258.
55. Xiang, X., Poliakov, A., Liu, C., Liu, Y. et al., Induction of myeloid-derived suppressor cells by tumor exosomes. Int. J. Cancer 2009, 124, 2621-2633.
56. Chen, K. G., Valencia, J. C., Lai, B., Zhang, G. et al., Melanosomal sequestration of cytotoxic drugs contributes to the intractability of malignant melanomas. Proc. Natl. Acad. Sci. USA 2006, 103, 9903-9907.
57. Yan, X., Yin, J., Yao, H., Mao, N. et al., Increased expression of annexin A3 is a mechanism of platinum resistance in ovarian cancer. Cancer Res. 2010, 70, 1616-1624.
58. Yin, J., Yan, X., Yao, X., Zhang, Y. et al., Secretion of annexin A3 from ovarian cancer cells and its association with platinum resistance in ovarian cancer patients. J. Cell. Mol. Med. 2012, 16, 337-348.
59. Ramachandran, S., Palanisamy, V., Horizontal transfer of RNAs: exosomes as mediators of intercellular communication. Wiley Interdiscip. Rev. RNA 2012, 3, 286-293.
60. Fabbri, M., Paone, A., Calore, F., Galli, R. et al., MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc. Natl. Acad. Sci. USA 2012, 109, E2110-E2116.
61. Umezu, T., Ohyashiki, K., Kuroda, M., Ohyashiki, J. H., Leukemia cell to endothelial cell communication via exosomal miRNAs. Oncogene 2012, doi: 10.1038/onc.2012.295.
62. Bard, M. P., Hegmans, J. P., Hemmes, A., Luider, T. M. et al., Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am. J. Respir. Cell. Mol. Biol. 2004, 31, 114-121.
63. Choi, D. S., Park, J. O., Jang, S. C., Yoon, Y. J. et al., Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics 2011, 11, 2745-2751.
64. Simpson, R. J., Lim, J. W., Moritz, R. L., Mathivanan, S., Exosomes: proteomic insights and diagnostic potential. Expert Rev. Proteomics 2009, 6, 267-283.
65. Welton, J. L., Khanna, S., Giles, P. J., Brennan, P. et al., Proteomics analysis of bladder cancer exosomes. Mol. Cell. Proteomics 2010, 9, 1324-1338.
66. Xiao, Z., Blonder, J., Zhou, M., Veenstra, T. D., Proteomic analysis of extracellular matrix and vesicles. J. Proteomics 2009, 72, 34-45.
67. Raimondo, F., Morosi, L., Chinello, C., Magni, F. et al., Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics 2011, 11, 709-720.
68. Li, Y., Zhang, Y., Qiu, F., Qiu, Z., Proteomic identification of exosomal LRG1: a potential urinary biomarker for detecting NSCLC. Electrophoresis 2011, 32, 1976-1983.
69. Fontana, S., De Leo, G., Sedic, M., Alessandro, R., Proteomics in antitumor research. Drug Discov. Today Technol. 2006, 3, 441-449.
70. Palazzolo, G., Albanese, N. N., Di Cara, G., Gygax, D. et al., Proteomic analysis of exosome-like vesicles derived from breast cancer cells. Anticancer Res. 2012, 32, 847-860.
71. Lee, H. S., Jeong, J., Lee, K. J., Characterization of vesicles secreted from insulinoma NIT-1 cells. J. Proteome Res. 2009, 8, 2851-2862.
72. Mann, M., Hendrickson, R. C., Pandey, A., Analysis of proteins and proteomes by mass spectrometry. Annu. Rev. Biochem. 2001, 70, 437-473.
73. Gonzalez-Begne, M., Lu, B., Han, X., Hagen, F. K. et al., Proteomic analysis of human parotid gland exosomes by multidimensional protein identification technology (MudPIT). J. Proteome Res. 2009, 8, 1304-1314.
74. Tauro, B. J., Greening, D. W., Mathias, R. A., Ji, H. et al., Comparison of ultracentrifugation, density gradient separation, and immunoaffinity capture methods for isolating human colon cancer cell line LIM1863-derived exosomes. Methods 2012, 56, 293-304.
75. Choi, D. S., Lee, J. M., Park, G. W., Lim, H. W. et al., Proteomic analysis of microvesicles derived from human colorectal cancer cells. J. Proteome Res. 2007, 6, 4646-4655.
76. Hanahan, D., Weinberg, R. A., The hallmarks of cancer. Cell 2000, 100, 57-70.
77. Kim, S., Takahashi, H., Lin, W. W., Descargues, P. et al., Carcinoma-produced factors activate myeloid cells through TLR2 to stimulate metastasis. Nature 2009, 457, 102-106.
78. Hashino, J., Fukuda, Y., Oikawa, S., Nakazato, H. et al., Metastatic potential of human colorectal carcinoma SW1222 cells transfected with cDNA encoding carcinoembryonic antigen. Clin. Exp. Metastasis 1994, 12, 324-328.
79. Thompson, J. A., Grunert, F., Zimmermann, W., Carcinoembryonic antigen gene family: molecular biology and clinical perspectives. J. Clin. Lab. Anal. 1991, 5, 344-366.
80. Epple, L. M., Griffiths, S. G., Dechkovskaia, A. M., Dusto, N. L. et al., Medulloblastoma exosome proteomics yield functional roles for extracellular vesicles. PLoS One 2012, 7, e42064.
81. Cox, J., Mann, M., Quantitative, high-resolution proteomics for data-driven systems biology. Annu. Rev. Biochem. 2011, 80, 273-299.
82. Park, J. E., Tan, H. S., Datta, A., Lai, R. C. 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, 1085-1099.
83. Bantscheff, M., Lemeer, S., Savitski, M. M., Kuster, B., Quantitative mass spectrometry in proteomics: critical review update from 2007 to the present. Anal. Bioanal. Chem. 2012, 404, 939-965.
84. Cappadona, S., Baker, P. R., Cutillas, P. R., Heck, A. J. et al., Current challenges in software solutions for mass spectrometry-based quantitative proteomics. Amino Acids 2012, 43, 1087-1108.
85. Gonzalez-Galarza, F. F., Lawless, C., Hubbard, S. J., Fan, J. et al., A critical appraisal of techniques, software packages, and standards for quantitative proteomic analysis. OMICS 2012, 16, 431-442.
86. Choi, D. S., Yang, J. S., Choi, E. J., Jang, S. C. et al., The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. J. Proteome Res. 2012, 11, 1144-1151.