New insights in the composition of extracellular vesicles from pancreatic cancer cells: Implications for biomarkers and functions

Proteome Science

Volumn 12, Issue 1, 2014, Pages

  Klein Scory, Susanne ^a   Tehrani, Mahnaz Moradian ^b   Eilert Micus, Christina ^a   Adamczyk, Kamila A ^a   Wojtalewicz, Nathalie ^a   Schnölzer, Martina ^b   Hahn, Stephan A ^c   Schmiegel, Wolff ^a   Schwarte Waldhoff, Irmgard ^a  

^a RUHR UNIVERSITY BOCHUM   (Germany)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c RUHR UNIVERSITY BOCHUM   (Germany)

Author keywords

Affinity purification; Biomarker; Exosome; Extracellular vesicles; Pancreatic cancer; Proteomics; Secretome

Indexed keywords

CELL PROTEIN; GLYCOPROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; MEMBRANE PROTEIN; PROTEASOME; RIBOSOME PROTEIN; TUMOR MARKER;

ARTICLE; CARCINOGENESIS; CELL INTERACTION; EXOSOME; EXTRACELLULAR MATRIX; HUMAN; HUMAN CELL; PANCREAS CANCER; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN SECRETION; PROTEOMICS; SECRETOME;

EID: 84988614406     PISSN: None     EISSN: 14775956     Source Type: Journal    
DOI: 10.1186/s12953-014-0050-5     Document Type: Article

References (54)

1. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JWW, Comber H, Forman D, Bray F: Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 2013, 49:1374-1403.
2. Gukovsky I, Li N, Todoric J, Gukovskaya A, Karin M: Inflammation, autophagy, and obesity: common features in the pathogenesis of pancreatitis and pancreatic cancer. Gastroenterology 2013, 144:1199-1209. e4.
3. Shah MM, Saif MW: Pancreatic cancer and thrombosis. highlights from the "2010 ASCO Annual Meeting". Chicago, IL, USA. June 4-8, 2010. JOP 2010, 11:331-333.
4. Caccia D, Zanetti Domingues L, Miccichè F, de Bortoli M, Carniti C, Mondellini P, Bongarzone I: Secretome compartment is a valuable source of biomarkers for cancer-relevant pathways. J Proteome Res 2011, 10:4196-4207.
5. Cocucci E, Racchetti G, Meldolesi J: Shedding microvesicles: artefacts no more. Trends Cell Biol 2009, 19:43-51.
6. Choi D, Lee J, Go G, Kim Y, Gho YS: Circulating extracellular vesicles in cancer diagnosis and monitoring: an appraisal of clinical potential. Mol Diagn Ther 2013, 17:265-271.
7. Webber J, Clayton A: How pure are your vesicles? J Extracell Vesicles 2013, 2:19861.
8. Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C: Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 2010, 123:1603-1611.
9. D'Souza-Schorey C, Clancy JW: Tumor-derived microvesicles: shedding light on novel microenvironment modulators and prospective cancer biomarkers. Genes Dev 2012, 26:1287-1299.
10. Raposo G, Stoorvogel W: Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013, 200:373-383.
11. Chaput N, Théry C: Exosomes: immune properties and potential clinical implementations. Semin Immunopathol 2011, 33:419-440.
12. Henderson MC, Azorsa DO: The genomic and proteomic content of cancer cell-derived exosomes. Front Oncol 2012, 2:38.
13. Bang C, Thum T: Exosomes: new players in cell-cell communication. Int J Biochem Cell Biol 2012, 44:2060-2064.
14. Garcia-Contreras M, Ricordi C, Robbins PD, Oltra E: Exosomes in the pathogenesis, diagnosis and treatment of pancreatic diseases. CellR4 2014, 2:e807.
15. Mathivanan S, Fahner CJ, Reid GE, Simpson RJ: ExoCarta 2012: database of exosomal proteins, RNA and lipids. Nucleic Acids Res 2012, 40:D1241-D1244.
16. Raposo G, Nijman HW, Stoorvogel W, Liejendekker R, Harding CV, Melief CJ, Geuze HJ: B lymphocytes secrete antigen-presenting vesicles. J Exp Med 1996, 183:1161-1172.
17. Mathivanan S, Lim JW, Tauro BJ, Ji H, Moritz RL, Simpson RJ: 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.
18. Choi D, Kim D, Kim Y, Gho YS: Proteomics, transcriptomics and lipidomics of exosomes and ectosomes. Proteomics 2013, 13:1554-1571.
19. Cirulli V, Crisa L, Beattie GM, Mally MI, Lopez AD, Fannon A, Ptasznik A, Inverardi L, Ricordi C, Deerinck T, Ellisman M, Reisfeld RA, Hayek A: KSA antigen Ep-CAM mediates cell-cell adhesion of pancreatic epithelial cells: morphoregulatory roles in pancreatic islet development. J Cell Biol 1998, 140:1519-1534.
20. Moore PS, Sipos B, Orlandini S, Sorio C, Real FX, Lemoine NR, Gress T, Bassi C, Kloppel G, Kalthoff H, Ungefroren H, Lohr M, Scarpa A: Genetic profile of 22 pancreatic carcinoma cell lines. analysis of K-ras, p53, p16 and DPC4/Smad4. Virchows Arch 2001, 439:798-802.
21. Jansen FH, Krijgsveld J, van Rijswijk A, van den Bemd G-J, van den Berg MS, van Weerden WM, Willemsen R, Dekker LJ, Luider TM, Jenster G: Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins. Mol Cell Proteomics 2009, 8:1192-1205.
22. Kalra H, Simpson RJ, Ji H, Aikawa E, Altevogt P, Askenase P, Bond VC, Borràs FE, Breakefield X, Budnik V, Buzas E, Camussi G, Clayton A, Cocucci E, Falcon-Perez JM, Gabrielsson S, Gho YS, Gupta D, Harsha HC, Hendrix A, Hill AF, Inal JM, Jenster G, Krämer-Albers E, Lim SK, Llorente A, Lötvall J, Marcilla A, Mincheva-Nilsson L, Nazarenko I, et al: Vesiclepedia: a compendium for extracellular vesicles with continuous community annotation. PLoS Biol 2012, 10:e1001450.
23. Kuo L, Freed EO: ARRDC1 as a mediator of microvesicle budding. Proc Natl Acad Sci U S A 2012, 109:4025-4026.
24. Nabhan JF, Hu R, Oh RS, Cohen SN, Lu Q: Formation and release of arrestin domain-containing protein 1-mediated microvesicles (ARMMs) at plasma membrane by recruitment of TSG101 protein. Proc Natl Acad Sci U S A 2012, 109:4146-4151.
25. Chelala C, Hahn SA, Whiteman HJ, Barry S, Hariharan D, Radon TP, Lemoine NR, Crnogorac-Jurcevic T: Pancreatic expression database: a generic model for the organization, integration and mining of complex cancer datasets. BMC Genomics 2007, 8:439.
26. Erkan M: Antifibrotic therapy in pancreatic diseases. Gut 2013, 62:1244-1245.
27. Wolfers J, Lozier A, Raposo G, Regnault A, Thery C, Masurier C, Flament C, Pouzieux S, Faure F, Tursz T, Angevin E, Amigorena S, Zitvogel L: Tumorderived exosomes are a source of shared tumor rejection antigens for CTL cross-priming. Nat Med 2001, 7:297-303.
28. Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO: Exosomemediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol 2007, 9:654-659.
29. Skog J, Würdinger T, van Rijn S, Meijer DH, Gainche L, Sena-Esteves M, Curry WT, Carter BS, Krichevsky AM, Breakefield XO: Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat Cell Biol 2008, 10:1470-1476.
30. Colombo M, Moita C, Van Niel G, Kowal J, Vigneron J, Benaroch P, Manel N, Moita LF, Théry C, Raposo G: Analysis of ESCRT functions in exosome biogenesis, composition and secretion highlights the heterogeneity of extracellular vesicles. J Cell Sci 2013, 126:5553-5565.
31. Gress TM, Menke A, Bachem MG, Muller-Pillasch F, Ellenrieder V, Weidenbach H, Wagner M, Adler G: Role of extracellular matrix in pancreatic diseases. Digestion 1998, 59:625-637.
32. Tauro BJ, Greening DW, Mathias RA, Mathivanan S, Ji H, Simpson RJ: Two distinct populations of exosomes are released from LIM1863 colon carcinoma cell-derived organoids. Mol Cell Proteomics 2013, 12:587-598.
33. Donaldson JG, Jackson CL: ARF family G proteins and their regulators: roles in membrane transport, development and disease. Nat Rev Mol Cell Biol 2011, 12:362-375.
34. Lau C, Kim Y, Chia D, Spielmann N, Eibl G, Elashoff D, Wei F, Lin Y, Moro A, Grogan T, Chiang S, Feinstein E, Schafer C, Farrell J, Wong DTW: Role of pancreatic cancer-derived exosomes in salivary biomarker development. J Biol Chem 2013, 288:26888-26897.
35. Mu W, Rana S, Zöller M: Host matrix modulation by tumor exosomes promotes motility and invasiveness. Neoplasia 2013, 15:875-887.
36. Sleeman JP: The metastatic niche and stromal progression. Cancer Metastasis Rev 2012, 31:429-440.
37. Iacono KT, Brown AL, Greene MI, Saouaf SJ: CD147 immunoglobulin superfamily receptor function and role in pathology. Exp Mol Pathol 2007, 83:283-295.
38. Gao W, Chen L, Ma Z, Du Z, Zhao Z, Hu Z, Li Q: Isolation and phenotypic characterization of colorectal cancer stem cells with organ-specific metastatic potential. Gastroenterology 2013, 145:636-646. e5.
39. Adamczyk KA, Klein-Scory S, Tehrani MM, Warnken U, Schmiegel W, Schnölzer M, Schwarte-Waldhoff I: Characterization of soluble and exosomal forms of the EGFR released from pancreatic cancer cells. Life Sci 2011, 89:304-312.
40. Valenti R, Huber V, Iero M, Filipazzi P, Parmiani G, Rivoltini L: Tumorreleased microvesicles as vehicles of immunosuppression. Cancer Res 2007, 67:2912-2915.
41. Corrado C, Raimondo S, Chiesi A, Ciccia F, Leo de G, Alessandro R: Exosomes as intercellular signaling organelles involved in health and disease: basic science and clinical applications. Int J Mol Sci 2013, 14:5338-5366.
42. Clayton A, Al-Taei S, Webber J, Mason MD, Tabi Z: Cancer exosomes express CD39 and CD73, which suppress T cells through adenosine production. J Immunol 2011, 187:676-683.
43. Beavis PA, Stagg J, Darcy PK, Smyth MJ: CD73: a potent suppressor of antitumor immune responses. Trends Immunol 2012, 33:231-237.
44. Taylor DD, Gercel-Taylor C: MicroRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol Oncol 2008, 110:13-21.
45. Tauro BJ, Greening DW, Mathias RA, Ji H, Mathivanan S, Scott AM, Simpson RJ: 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.
46. Rupp A, Rupp C, Keller S, Brase JC, Ehehalt R, Fogel M, Moldenhauer G, Marmé F, Sültmann H, Altevogt P: Loss of EpCAM expression in breast cancer derived serum exosomes: role of proteolytic cleavage. Gynecol Oncol 2011, 122:437-446.
47. Wu X, He X, Chen Y, Yuan R, Zeng Y, Lian L, Zou Y, Lan N, Wu X, Lan P: High expression of CD73 as a poor prognostic biomarker in human colorectal cancer. J Surg Oncol 2012, 106:130-137.
48. van Niel G, Raposo G, Candalh C, Boussac M, Hershberg R, Cerf-Bensussan N, Heyman M: Intestinal epithelial cells secrete exosome-like vesicles. Gastroenterology 2001, 121:337-349.
49. Taylor DD, Zacharias W, Gercel-Taylor C: Exosome isolation for proteomic analyses and RNA profiling. Methods Mol Biol 2011, 728:235-246.
50. Battke C, Ruiss R, Welsch U, Wimberger P, Lang S, Jochum S, Zeidler R: Tumour exosomes inhibit binding of tumour-reactive antibodies to tumour cells and reduce ADCC. Cancer Immunol Immunother 2011, 60:639-648.
51. Liu C, Yu S, Zinn K, Wang J, Zhang L, Jia Y, Kappes JC, Barnes S, Kimberly RP, Grizzle WE, Zhang H: Murine mammary carcinoma exosomes promote tumor growth by suppression of NK cell function. J Immunol 2006, 176:1375-1385.
52. Piersma SR, Fiedler U, Span S, Lingnau A, Pham TV, Hoffmann S, Kubbutat MHG, Jiménez CR: Workflow comparison for label-free, quantitative secretome proteomics for cancer biomarker discovery: method evaluation, differential analysis, and verification in serum. J Proteome Res 2010, 9:1913-1922.
53. Huang DW, Sherman BT, Lempicki RA: Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. DAVID Bioinformatics Resources. Nat Protoc 2009, 57:44-57.
54. Chen J, Bardes EE, Aronow BJ, Jegga AG: ToppGene Suite for gene list enrichment analysis and candidate gene prioritization. Nucleic Acids Res 2009, 37:W305.