Proteomics analysis of cancer exosomes using a novel modified aptamer-based array (somascantm) platform

Molecular and Cellular Proteomics

Volumn 13, Issue 4, 2014, Pages 1050-1064

  Webber, Jason ^a   Stone, Timothy C ^a,b   Katilius, Evaldas ^c   Smith, Breanna C ^c   Gordon, Bridget ^c   Mason, Malcolm D ^a   Tabi, Zsuzsanna ^a   Brewis, Ian A ^b   Clayton, Aled ^a  

^a CARDIFF UNIVERSITY   (United Kingdom)

^b Innovation   (United Kingdom)

^c SomaLogic Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAM 9 PROTEIN; ADAM PROTEIN; ANTIBODY; APTAMER; CELL PROTEIN; CYCLOPHILIN A; HEAT SHOCK PROTEIN 70; INTEGRIN; INTER ALPHA TRYPSIN INHIBITOR HEAVY CHAIN FAMILY MEMBER 4; L1CAM PROTEIN; LACTADHERIN; LACTATE DEHYDROGENASE; NOTCH3 RECEPTOR; RAC1 PROTEIN; REAGENT; ROR1 PROTEIN; SCATTER FACTOR RECEPTOR; TUMOR MARKER; UNCLASSIFIED DRUG;

APTAMER BASED ARRAY PLATFORM; ARTICLE; BIOINFORMATICS; CANCER CELL; CANCER CELL CULTURE; CANCER EXOSOME; CELL LINE; CONTROLLED STUDY; DU145 CELL; EXOSOME; HUMAN; HUMAN CELL; IMMUNOBLOTTING; MALE; MICROARRAY KIT; MICROPLATE READER; PRIORITY JOURNAL; PROSTATE CANCER CELL LINE; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN MICROARRAY; PROTEOMICS; SUCROSE GRADIENT; WESTERN BLOTTING;

CELL LINE, TUMOR; EXOSOMES; GENES, ESSENTIAL; HUMANS; MALE; MICROARRAY ANALYSIS; NANOTECHNOLOGY; PROSTATIC NEOPLASMS; PROTEOMICS; TUMOR MARKERS, BIOLOGICAL;

EID: 84898764220     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M113.032136     Document Type: Article

References (54)

1. Thompson, I. M., Pauler, D. K., Goodman, P. J., Tangen, C. M., Lucia, M. S., Parnes, H. L., Minasian, L. M., Ford, L. G., Lippman, S. M., Crawford, E. D., Crowley, J. J., and Coltman, C. A., Jr. (2004) Prevalence of prostate cancer among men with a prostate-specific antigen level-4.0 ng per milliliter. N. Engl. J. Med. 350, 2239-2246
2. Selley, S., Donovan, J., Faulkner, A., Coast, J., and Gillatt, D. (1997) Diagnosis, management and screening of early localised prostate cancer. Health Technol. Assess. 1(2), 1-96
3. Caby, M., Lankar, D., Vincendeau-Scherrer, C., Raposo, G., and Bonnerot, C. (2005) Exosomal-like vesicles are present in human blood plasma. Int. Immunol. 17, 879-887
4. Pisitkun, T., Shen, R., and Knepper, M. (2004) Identification and proteomic profiling of exosomes in human urine. Proc. Natl. Acad. Sci. U.S.A. 101, 13369-13373
5. Admyre, C., Johansson, S. M., Qazi, K. R., Filen, J.-J., Lahesmaa, R., Norman, M., Neve, E. P., Scheynius, A., and Gabrielsson, S. (2007) Exosomes with immune modulatory features are present in human breast milk. J. Immunol. 179, 1969-1978
6. Gatti, J.-L., Metayer, S., Belghazi, M., Dacheux, F., and Dacheux, J.-L. (2005) Identification, proteomic profiling, and origin of ram epididymal fluid exosome-like vesicles. Biol. Reprod. 72(6), 1452-1465
7. Bard, M. P., Hegmans, J. P., Hemmes, A., Luider, T. M., Willemsen, R., Severijnen, L.-A. A., van Meerbeeck, J. P., Burgers, S. A., Hoogsteden, H. C., and Lambrecht, B. N. (2004) Proteomic analysis of exosomes isolated from human malignant pleural effusions. Am. J. Respir. Cell Mol. Biol. 31, 114-121
8. Raposo, G., Nijman, H. W., Stoorvogel, W., Leijendekker, R., Harding, C. V., Melief, C. J. M., and Geuze, H. J. (1996) B Lymphocytes secrete antigenpresenting vesicles. J. Exp. Med. 183, 1161-1172
9. Booth, A. M., Fang, Y., Fallon, J. K., Yang, J.-M., Hildreth, J. E. K., and Gould, S. J. (2006) Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane. J. Cell Biol. 172, 923-935
10. Simpson, R. J., Lim, J. W., Moritz, R. L., and Mathivanan, S. (2009) Exosomes: proteomic insights and diagnostic potential. Exp. Rev. Proteomics 6, 267-283
11. Park, J. E., Tan, H. S., Datta, A., Lai, R. C., Zhang, H., Meng, W., Lim, S. K., and Sze, S. K. (2010) Hypoxic tumor cell modulates its microenvironment to enhance angiogenic and metastatic potential by secretion of proteins and exosomes. Mol. Cell. Proteomics 9, 1085-1099
12. Khan, S., Jutzy, J. M., Aspe, J. R., McGregor, D. W., Neidigh, J. W., and Wall, N. R. (2011) Survivin is released from cancer cells via exosomes. Apoptosis 16, 1-12
13. Clayton, A., Turkes, A., Navabi, H., Mason, M. D., and Tabi, Z. (2005) Induction of heat shock proteins in B-cell exosomes. J. Cell Sci. 118(Pt 16), 3631-3638
14. Hosseini-Beheshti, E., Pham, S., Adomat, H., Li, N., and Tomlinson Guns, E. S. (2012) Exosomes as biomarker enriched microvesicles: characterization of exosomal proteins derived from a panel of prostate cell lines with distinct AR phenotypes. Mol. Cell. Proteomics 11, 863-885
15. Sandvig, K., and Llorente, A. (2012) Proteomic analysis of microvesicles released by the human prostate cancer cell line PC-3. Mol. Cell. Proteomics 11(7), M111.012914
16. Jansen, F. H., Krijgsveld, J., van Rijswijk, A., van den Bemd, G.-J., van den Berg, M. S., van Weerden, W. M., Willemsen, R., Dekker, L. J., Luider, T. M., and Jenster, G. (2009) Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol. Cell. Proteomics 8, 1192-1205
17. Poliakov, A., Spilman, M., Dokland, T., Amling, C. L., and Mobley, J. A. (2009) Structural heterogeneity and protein composition of exosome-like vesicles (prostasomes) in human semen. Prostate 69, 159-167
18. Zichi, D., Eaton, B., Singer, B., and Gold, L. (2008) Proteomics and diagnostics: let's get specific, again. Curr. Opin. Chem. Biol. 12, 78-85
19. Ostroff, R. M., Bigbee, W. L., Franklin, W., Gold, L., Mehan, M., Miller, Y. E., Pass, H. I., Rom, W. N., Siegfried, J. M., Stewart, A., Walker, J. J., Weissfeld, J. L., Williams, S., Zichi, D., and Brody, E. N. (2010) Unlocking biomarker discovery: large scale application of aptamer proteomic technology for early detection of lung cancer. PLoS One 5, e15003
20. Gold, L., Ayers, D., Bertino, J., Bock, C., Bock, A., Brody, E. N., Carter, J., Dalby, A. B., Eaton, B. E., Fitzwater, T., Flather, D., Forbes, A., Foreman, T., Fowler, C., Gawande, B., Goss, M., Gunn, M., Gupta, S., Halladay, D., Heil, J., Heilig, J., Hicke, B., Husar, G., Janjic, N., Jarvis, T., Jennings, S., Katilius, E., Keeney, T. R., Kim, N., Koch, T. H., Kraemer, S., Kroiss, L., Le, N., Levine, D., Lindsey, W., Lollo, B., Mayfield, W., Mehan, M., Mehler, R., Nelson, S. K., Nelson, M., Nieuwlandt, D., Nikrad, M., Ochsner, U., Ostroff, R. M., Otis, M., Parker, T., Pietrasiewicz, S., Resnicow, D. I., Rohloff, J., Sanders, G., Sattin, S., Schneider, D., Singer, B., Stanton, M., Sterkel, A., Stewart, A., Stratford, S., Vaught, J. D., Vrkljan, M., Walker, J. J., Watrobka, M., Waugh, S., Weiss, A., Wilcox, S. K., Wolfson, A., Wolk, S. K., Zhang, C., and Zichi, D. (2010) Aptamer-based multiplexed proteomic technology for biomarker discovery. PLoS One 5, e15004
21. Gold, L., Walker, J. J., Wilcox, S. K., and Williams, S. (2012) Advances in human proteomics at high scale with the SOMAscan proteomics platform. Nat. Biotechnol. 29, 543-549
22. Ostroff, R. M., Mehan, M. R., Stewart, A., Ayers, D., Brody, E. N., Williams, S. A., Levin, S., Black, B., Harbut, M., Carbone, M., Goparaju, C., and Pass, H. I. (2012) Early detection of malignant pleural mesothelioma in asbestos-exposed individuals with a noninvasive proteomics-based surveillance tool. PLoS One 7, e46091
23. Mehan, M. R., Ayers, D., Thirstrup, D., Xiong, W., Ostroff, R. M., Brody, E. N., Walker, J. J., Gold, L., Jarvis, T. C., Janjic, N., Baird, G. S., and Wilcox, S. K. (2012) Protein signature of lung cancer tissues. PLoS One 7, e35157
24. Baird, G. S., Nelson, S. K., Keeney, T. R., Stewart, A., Williams, S., Kraemer, S., Peskind, E. R., and Montine, T. J. (2012) Age-dependent changes in the cerebrospinal fluid proteome by slow off-rate modified aptamer array. Am. J. Pathol. 180, 446-456
25. Stone, K. R., Mickey, D. D., Wunderli, H., Mickey, G. H., and Paulson, D. F. (1978) Isolation of a human prostate carcinoma cell line (DU 145). Int. J. Cancer 21, 274-281
26. Mitchell, J. P., Court, J., Mason, M. D., Tabi, Z., and Clayton, A. (2008) Increased exosome production from tumour cell cultures using the Integra CELLine Culture System. J. Immunol. Methods 335, 98-105
27. Thé ry, C., Amigorena, S., Raposo, G., and Clayton, A. (2006) Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Cell Biol. Unit 3.22
28. Webber, J., Steadman, R., Mason, M. D., Tabi, Z., and Clayton, A. (2010) Cancer exosomes trigger fibroblast to myofibroblast differentiation. Cancer Res. 70, 9621-9630
29. Welton, J. L., Khanna, S., Giles, P. J., Brennan, P., Brewis, I. A., Staffurth, J., Mason, M. D., and Clayton, A. (2010) Proteomics analysis of bladder cancer exosomes. Mol. Cell. Proteomics 9, 1324-1338
30. Kalra, H., Simpson, R. J., Ji, H., Aikawa, E., Altevogt, P., Askenase, P., et al. (2012) Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol. 10(12), e1001450
31. Hulsen, T., Vlieg, J. D., and Alkema, W. (2008) BioVenn-a web application for the comparison and visualization of biological lists using area-proportional Venn diagrams. BMC Genomics 9, 488
32. Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2008) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57
33. Huang, D. W., Sherman, B. T., and Lempicki, R. A. (2009) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res. 37, 1-13
34. Cline, M. S., Smoot, M., Cerami, E., Kuchinsky, A., Landys, N., Workman, C., Christmas, R., Avila-Campilo, I., Creech, M., Gross, B., Hanspers, K., Isserlin, R., Kelley, R., Killcoyne, S., Lotia, S., Maere, S., Morris, J., Ono, K., Pavlovic, V., Pico, A. R., Vailaya, A., Wang, P. L., Adler, A., Conklin, B. R., Hood, L., Kuiper, M., Sander, C., Schmulevich, I., Schwikowski, B., Warner, G. J., Ideker, T., and Bader, G. D. (2007) Integration of biological networks and gene expression data using Cytoscape. Nat. Protoc. 2, 2366-2382
35. Saito, R., Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P.-L., Lotia, S., Pico, A. R., Bader, G. D., and Ideker, T. (2012) A travel guide to Cytoscape plugins. Nat. Methods 9, 1069-1076
36. Peinado, H., Aleckovic, M., Lavotshkin, S., Matei, I., Costa-Silva, B., Moreno-Bueno, G., Hergueta-Redondo, M., Williams, C., García-Santos, G., Ghajar, C., Nitadori-Hoshino, A., Hoffman, C., Badal, K., Garcia, B. A., Callahan, M. K., Yuan, J., Martins, V. R., Skog, J., Kaplan, R. N., Brady, M. S., Wolchok, J. D., Chapman, P. B., Kang, Y., Bromberg, J., and Lyden, D. (2012) Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18, 883-891
37. Anderson, H. A., Maylock, C. A., Williams, J. A., Paweletz, C. P., Shu, H., and Shacter, E. (2003) Serum-derived protein S binds to phosphatidylserine and stimulates the phagocytosis of apoptotic cells. Nat. Immunol. 4, 87-91
38. Zeelenberg, I. S., Ostrowski, M., Krumeich, S., Bobrie, A., Jancic, C., Boissonnas, A., Delcayre, A., Le Pecq, J. B., Combadie re, B., Amigorena, S., and The ry, C. (2008) Targeting tumor antigens to secreted membrane vesicles in vivo induces efficient antitumor immune responses. Cancer Res. 68, 1228-1235
39. Saraon, P., Musrap, N., Cretu, D., Karagiannis, G. S., Batruch, I., Smith, C., Drabovich, A. P., Trudel, D., van der Kwast, T., Morrissey, C., Jarvi, K. A., and Diamandis, E. P. (2012) Proteomic profiling of androgen-independent prostate cancer cell lines reveals a role for protein S during the development of high grade and castration-resistant prostate cancer. J. Biol. Chem. 287, 34019-34031
40. Rabesandrata, H., Toutant, J., Reggio, H., and Vidal, M. (1998) Decayaccelerating factor (CD55) and membrane inhibitor of reactive lysis (CD59) are released within exosomes during in vitro maturation of reticulocytes. Blood 91, 2573-2580
41. 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
42. Lynch, S., Santos, S. G., Campbell, E. C., Nimmo, A. M. S., Botting, C., Prescott, A., Antoniou, A. N., and Powis, S. J. (2009) Novel MHC Class I structures on exosomes. J. Immunol. 183, 1884-1891
43. 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
44. Skog, J., Wurdinger, T., van Rijn, 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
45. Heijnen, H. F. G., Schiel, A. E., Fijnheer, R., Geuze, H. J., and Sixma, J. J. (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, 3791-3799
46. Pilzer, D., Gasser, O., Moskovich, O., Schifferli, J. A., and Fishelson, Z. (2005) Emission of membrane vesicles: roles in complement resistance, immunity and cancer. Springer Semin. Immunopathol. 27, 375-387
47. Franz, C., Boing, A. N., Hau, C. M., Montag, M., Strowitzki, T., Nieuwland, R., and Toth, B. (2013) Procoagulant tissue factor-exposing vesicles in human seminal fluid. J. Reprod. Immunol. 98, 45-51
48. Mu, W., Rana, S., and Zoller, M. (2013) Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 8, 875-887
49. Clayton, A., Harris, C. L., Court, J., Mason, M. D., and Morgan, B. P. (2003) Antigen presenting cell exosomes are protected from complement mediated lysis by expression of CD55 and CD59. Eur. J. Immunol. 33, 525-531
50. Gastpar, R., Gehrmann, M., Bausero, M., Asea, A., Gross, C., Schroeder, J. A., and Multhoff, G. (2005) Heat shock protein 70 surface-positive tumor exosomes stimulate migratory and cytolytic activity of natural killer cells. Cancer Res. 65, 5238-5247
51. Johnstone, R., Adam, M., Hammond, J., Orr, L., and Turbide, C. (1987) Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J. Biol. Chem. 262, 9412-9420
52. Johnstone, R. M., Mathew, A., Mason, A. B., and Teng, K. (1991) Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalisation of obsolete membrane proteins. J. Cell Pathol. 147, 27-36
53. Katzmann, D., Stefan, C., Babst, M., and Emr, S. (2003) Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162, 413-423
54. Chua, C. E. L., Lim, Y. S., Lee, M. G., and Tang, B. L. (2012) Non-classical membrane trafficking processes galore. J. Cell. Physiol. 227, 3722-3730