Mass spectrometry-based proteome profiling of extracellular vesicles and their roles in cancer biology

다국어 초록 (Multilingual Abstract)

Over the past three decades, extracellular vesicles (EVs) have arisen as important mediators of intercellular communication that are involved in the transmission of biological signals between cells to regulate various biological processes. EVs are largely responsible for intercellular communication through the delivery of bioactive molecules, such as proteins, messenger RNAs (mRNAs), microRNAs (miRNAs), DNAs, lipids, and metabolites. EVs released from cancer cells play a significant role in signal transduction between cancer cells and the surrounding cells, which contributes to the formation of tumors and metastasis in the tumor microenvironment. In addition, EVs released from cancer cells migrate to blood vessels and flow into various biological fluids, including blood and urine. EVs and EVloaded functional cargoes, including proteins and miRNAs, found in these biological fluids are important biomarkers for cancer diagnosis. Therefore, EV proteomics greatly contributes to the understanding of carcinogenesis and tumor progression and is critical for the development of biomarkers for the early diagnosis of cancer. To explore the potential use of EVs as a gateway to understanding cancer biology and to develop cancer biomarkers, we discuss the mass spectrometric identification and characterization of EV proteins from different cancers. Information provided in this review may help in understanding recent progress regarding EV biology and the potential roles of EVs as new noninvasive biomarkers and therapeutic targets.

참고문헌 (Reference)

1 Gangoda, L., "proteomic profiling of exosomes secreted by breast cancer cells with varying metastatic potential" 17 : 2017

2 Harada, T., "Wnt5b-associated exosomes promote cancer cell migration and proliferation" 108 : 42-52, 2017

3 Shin, S. J., "Unexpected gain of function for the scaffolding protein plectin due to mislocalization in pancreatic cancer" 110 : 19414-19419, 2013

4 Baj-Krzyworzeka, M., "Tumour-derived microvesicles modulate biological activity of human monocytes" 113 : 76-82, 2007

5 Clark, D. J., "Triple SILAC quantitative proteomic analysis reveals differential abundance of cell signaling proteins between normal and lung cancer-derived exosomes" 133 : 161-169, 2016

6 Del Conde, I., "Tissue-factorbearing microvesicles arise from lipid rafts and fuse with activated platelets to initiate coagulation" 106 : 1604-1611, 2005

7 Perez-Hernandez, D., "The intracellular interactome of tetraspaninenriched microdomains reveals their function as sorting machineries toward exosomes" 288 : 11649-11661, 2013

8 Huang da, W., "Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources" 4 : 44-57, 2009

9 Castillo, J., "Surfaceome profiling enables isolation of cancer-specific exosomal cargo in liquid biopsies from pancreatic cancer patients" 29 : 223-229, 2018

10 Escrevente, C., "Sialoglycoproteins and N-glycans from secreted exosomes of ovarian carcinoma cells" 8 : e78631-, 2013

11 Ji, H., "Secretomebased proteomics reveals sulindac-modulated proteins released from colon cancer cells" 3 : 433-451, 2009

12 Zhang, Y., "Secreted monocytic miR-150 enhances targeted endothelial cell migration" 39 : 133-144, 2010

13 Ohno, S., "Roles of exosomes and microvesicles in disease pathogenesis" 65 : 398-401, 2013

14 Lim, J. W., "Restoration of full-length APC protein in SW480 colon cancer cells induces exosome-mediated secretion of DKK-4" 33 : 1873-1880, 2012

15 Clark, D. J., "Redefining the breast cancer exosome proteome by tandem mass tag quantitative proteomics and multivariate cluster analysis" 87 : 10462-10469, 2015

16 Jeppesen, D. K., "Quantitative proteomics of fractionated membrane and lumen exosome proteins from isogenic metastatic and nonmetastatic bladder cancer cells reveal differential expression of EMT factors" 14 : 699-712, 2014

17 Dong-Sic Choi, "Quantitative proteomics of extracellular vesicles derived from human primary and metastatic colorectal cancer cells" Informa UK Limited 1 (1): 18704-, 2012

18 Choi, D. S., "Proteomics, transcriptomics and lipidomics of exosomes and ectosomes" 13 : 1554-1571, 2013

19 Bilen, M. A., "Proteomics profiling of exosomes from primary mouse osteoblasts under proliferation versus mineralization conditions and characterization of their uptake into prostate cancer cells" 16 : 2709-2728, 2017

20 Dutta, S., "Proteomics profiling of cholangiocarcinoma exosomes : a potential role of oncogenic protein transferring in cancer progression" 1852 : 1989-1999, 2015

21 Welton, J. L., "Proteomics analysis of bladder cancer exosomes" 9 : 1324-1338, 2010

22 Mathivanan, S., "Proteomics analysis of A33 immunoaffinity-purified exosomes released from the human colon tumor cell line LIM1215 reveals a tissue-specific protein signature" 9 : 197-208, 2010

23 Duijvesz, D., "Proteomic profiling of exosomes leads to the identification of novel biomarkers for prostate cancer" 8 : e82589-, 2013

24 Graner, M. W., "Proteomic and immunologic analyses of brain tumor exosomes" 23 : 1541-1557, 2009

25 Wang, Z., "Proteomic analysis of urine exosomes by multidimensional protein identification technology(MudPIT)" 12 : 329-338, 2012

26 Sandvig, K., "Proteomic analysis of microvesicles released by the human prostate cancer cell line PC-3" 11 : M111-012914, 2012

27 Choi, D. S., "Proteomic analysis of microvesicles derived from human colorectal cancer cells" 6 : 4646-4655, 2007

28 Choi, D. S., "Proteomic analysis of microvesicles derived from human colorectal cancer ascites" 11 : 2745-2751, 2011

29 Demory Beckler, M., "Proteomic analysis of exosomes from mutant KRAS colon cancer cells identifies intercellular transfer of mutant KRAS" 12 : 343-355, 2013

30 Yao, Y., "Proteomic analysis of exosomes derived from human lymphoma cells" 20 : 8-, 2015

31 Palazzolo, G., "Proteomic analysis of exosome-like vesicles derived from breast cancer cells" 32 : 847-860, 2012

32 Ji, H., "Proteome profiling of exosomes derived from human primary and metastatic colorectal cancer cells reveal differential expression of key metastatic factors and signal transduction components" 13 : 1672-1686, 2013

33 Kavanagh, E. L., "Protein and chemotherapy profiling of extracellular vesicles harvested from therapeutic induced senescent triple negative breast cancer cells" 6 : e388-, 2017

34 Domenyuk, V., "Plasma exosome profiling of cancer patients by a next generation systems biology approach" 7 : 42741-, 2017

35 Guo, J., "Phosphoproteome characterization of human colorectal cancer SW620 cell-derived exosomes and new phosphosite discovery for C-HPP" 15 : 4060-4072, 2016

36 Vardaki, I., "Periostin is identified as a putative metastatic marker in breast cancer-derived exosomes" 7 : 74966-74978, 2016

37 Yu, Z., "Pancreatic cancer-derived exosomes promote tumor metastasis and liver pre-metastatic niche formation" 8 : 63461-63483, 2017

38 Costa-Silva, B., "Pancreatic cancer exosomes initiate pre-metastatic niche formation in the liver" 17 : 816-826, 2015

39 Wang, Y., "Oral cancer-derived exosomal NAP1 enhances cytotoxicity of natural killer cells via the IRF-3 pathway" 76 : 34-41, 2018

40 Suresh Mathivanan, "Oncogenic transformation of lung cells results in distinct exosome protein profile similar to the cell of origin" Wiley 17 (17): 1600432-, 2017

41 Klein-Scory, S., "New insights in the composition of extracellular vesicles from pancreatic cancer cells : implications for biomarkers and functions" 12 : 50-, 2014

42 Blomme, A., "Myoferlin is a novel exosomal protein and functional regulator of cancer-derived exosomes" 7 : 83669-83683, 2016

43 Jing Zhang, "Motile hepatocellular carcinoma cells preferentially secret sugar metabolism regulatory proteins via exosomes" Wiley 17 (17): 1700103-, 2017

44 Kharaziha, P., "Molecular profiling of prostate cancer derived exosomes may reveal a predictive signature for response to docetaxel" 6 : 21740-21754, 2015

45 Soekmadji, C., "Modulation of paracrine signaling by CD9 positive small extracellular vesicles mediates cellular growth of androgen deprived prostate cancer" 8 : 52237-52255, 2017

46 Gyorgy, B., "Membrane vesicles, current state-of-the-art : emerging role of extracellular vesicles" 68 : 2667-2688, 2011

47 Thery, C., "Membrane vesicles as conveyors of immune responses" 9 : 581-593, 2009

48 Kreimer, S., "Mass-spectrometry-based molecular characterization of extracellular vesicles : lipidomics and proteomics" 14 : 2367-2384, 2015

49 Chow, A., "Macrophage immunomodulation by breast cancer-derived exosomes requires Toll-like receptor 2-mediated activation of NF-kappaB" 4 : 5750-, 2014

50 Raimondo, S., "Label-free quantitative proteomic profiling of colon cancer cells identifies acetyl-CoA carboxylase alpha as antitumor target of Citrus limon-derived nanovesicles" 173 : 1-11, 2018

51 Kawakami, K., "Integrin beta4 and vinculin contained in exosomes are potential markers for progression of prostate cancer associated with taxaneresistance" 47 : 384-390, 2015

52 Sinha, A., "Indepth proteomic analyses of ovarian cancer cell line exosomes reveals differential enrichment of functional categories compared to the NCI 60 proteome" 445 : 694-701, 2014

53 Jang, S. C., "In vivo kinetic biodistribution of nano-sized outer membrane vesicles derived from bacteria" 11 : 456-461, 2015

54 Moon, P. G., "Identification of developmental endothelial locus-1 on circulating extracellular vesicles as a novel biomarker for early breast cancer detection" 22 : 1757-1766, 2016

55 Lee, J. E., "Identification of EDIL3 on extracellular vesicles involved in breast cancer cell invasion" 131 : 17-28, 2016

56 Valenti, R., "Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-beta-mediated suppressive activity on T lymphocytes" 66 : 9290-9298, 2006

57 Ristorcelli, E., "Human tumor nanoparticles induce apoptosis of pancreatic cancer cells" 22 : 3358-3369, 2008

58 Yi, H., "High-grade ovarian cancer secreting effective exosomes in tumor angiogenesis" 8 : 5062-5070, 2015

59 He, M., "Hepatocellular carcinoma-derived exosomes promote motility of immortalized hepatocyte through transfer of oncogenic proteins and RNAs" 36 : 1008-1018, 2015

60 Ono, K., "HSP-enriched properties of extracellular vesicles involve survival of metastatic oral cancer cells" 119 : 7350-7362, 2018

61 Skog, J., "Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers" 10 : 1470-1476, 2008

62 Choi, D. Y., "Extracellular vesicles shed from gefitinib-resistant nonsmall cell lung cancer regulate the tumor microenvironment" 14 : 1845-1856, 2014

63 Minciacchi, V. R., "Extracellular vesicles in cancer : exosomes, microvesicles and the emerging role of large oncosomes" 40 : 41-51, 2015

64 de Andrade, A., "Extracellular vesicles from oral squamous carcinoma cells display pro-and anti-angiogenic properties" 24 : 725-731, 2018

65 Raposo, G., "Extracellular vesicles : exosomes, microvesicles, and friends" 200 : 373-383, 2013

66 Andaloussi, E. L., "Extracellular vesicles : biology and emerging therapeutic opportunities" 12 : 347-357, 2013

67 Mulvey, H. E., "Extracellular vesicle-mediated phenotype switching in malignant and non-malignant colon cells" 15 : 571-, 2015

68 Kim, C. W., "Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin" 62 : 6312-6317, 2002

69 Zheng, J., "Extracellular matrix proteins and carcinoembryonic antigenrelated cell adhesion molecules characterize pancreatic duct fluid exosomes in patients with pancreatic cancer" 20 : 597-604, 2018

70 Suresh Mathivanan, "Extracellular Vesicles in the Adaptive Process of Prostate Cancer during Inhibition of Androgen Receptor Signaling by Enzalutamide" Wiley 17 (17): 1600427-, 2017

71 O’Driscoll, L., "Expanding on exosomes and ectosomes in cancer" 372 : 2359-2362, 2015

72 Harris, D. A., "Exosomes released from breast cancer carcinomas stimulate cell movement" 10 : e0117495-, 2015

73 Wang, S., "Exosomes released by hepatocarcinoma cells endow adipocytes with tumor-promoting properties" 11 : 82-, 2018

74 Paggetti, J., "Exosomes released by chronic lymphocytic leukemia cells induce the transition of stromal cells into cancer-associated fibroblasts" 126 : 1106-1117, 2015

75 Yi, H., "Exosomes mediated pentose phosphate pathway in ovarian cancer metastasis : a proteomics analysis" 8 : 15719-15728, 2015

76 Kahlert, C., "Exosomes in tumor microenvironment influence cancer progression and metastasis" 91 : 431-437, 2013

77 Schillaci, O., "Exosomes from metastatic cancer cells transfer amoeboid phenotype to non-metastatic cells and increase endothelial permeability : their emerging role in tumor heterogeneity" 7 : 4711-, 2017

78 Hosseini-Beheshti, E., "Exosomes as biomarker enriched microvesicles : characterization of exosomal proteins derived from a panel of prostate cell lines with distinct AR phenotypes" 11 : 863-885, 2012

79 Booth, A. M., "Exosomes and HIV Gag bud from endosome-like domains of the T cell plasma membrane" 172 : 923-935, 2006

80 Keller, S., "Exosomes : from biogenesis and secretion to biological function" 107 : 102-108, 2006

81 Mathivanan, S., "Exosomes : extracellular organelles important in intercellular communication" 73 : 1907-1920, 2010

82 Thery, C., "Exosomes : composition, biogenesis and function" 2 : 569-579, 2002

83 Ramakrishnaiah, V., "Exosome-mediated transmission of hepatitis C virus between human hepatoma Huh7.5 cells" 110 : 13109-13113, 2013

84 Jin, H., "Exosomal zinc transporter ZIP4 promotes cancer growth and is a novel diagnostic biomarker for pancreatic cancer" 109 : 2946-2956, 2018

85 Jansen, F. H., "Exosomal secretion of cytoplasmic prostate cancer xenograft-derived proteins" 8 : 1192-1205, 2009

86 Thomas, S. N., "Exosomal proteome profiling : a potential multi-marker cellular phenotyping tool to characterize hypoxia-induced radiation resistance in breast cancer" 1 : 87-108, 2013

87 Rauschenberger, L., "Exosomal particles secreted by prostate cancer cells are potent mRNA and protein vehicles for the interference of tumor and tumor environment" 76 : 409-424, 2016

88 Fu, H., "Exosomal TRIM3 is a novel marker and therapy target for gastric cancer" 37 : 162-, 2018

89 Kharmate, G., "Epidermal growth factor receptor in prostate cancer derived exosomes" 11 : e0154967-, 2016

90 Chaiyawat, P., "Elevated O-GlcNAcylation of extracellular vesicle proteins derived from metastatic colorectal cancer cells" 13 : 387-398, 2016

91 Kim, D. K., "EVpedia : a community web portal for extracellular vesicles research" 31 : 933-939, 2015

92 Bobrie, A., "Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation" 1 : 2012

93 Griffiths, S. G., "Differential proteome analysis of extracellular vesicles from breast cancer cell lines by chaperone affinity enrichment" 5 : pii: E25-, 2017

94 Khoontawad, J., "Differential protein expression marks the transition from infection with opisthorchis viverrini to cholangiocarcinoma" 16 : 911-923, 2017

95 Taverna, S., "Curcumin modulates chronic myelogenous leukemia exosomes composition and affects angiogenic phenotype via exosomal miR-21" 7 : 30420-30439, 2016

96 Gabrilovich, D. I., "Coordinated regulation of myeloid cells by tumours" 12 : 253-268, 2012

97 Huan, J., "Coordinate regulation of residual bone marrow function by paracrine trafficking of AML exosomes" 29 : 2285-2295, 2015

98 Bosque, A., "Comparative proteomics of exosomes secreted by tumoral Jurkat T cells and normal human T cell blasts unravels a potential tumorigenic role for valosin-containing protein" 7 : 29287-29305, 2016

99 Kalra, H., "Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma" 13 : 3354-3364, 2013

100 Barteneva, N. S., "Circulating microparticles : square the circle" 14 : 23-, 2013

101 Silvers, C. R., "Characterization of urinary extracellular vesicle proteins in muscle-invasive bladder cancer" 8 : 91199-91208, 2017

102 Adamczyk, K. A., "Characterization of soluble and exosomal forms of the EGFR released from pancreatic cancer cells" 89 : 304-312, 2011

103 Liang, B., "Characterization and proteomic analysis of ovarian cancerderived exosomes" 80 : 171-182, 2013

104 Chaiyadet, S., "Carcinogenic liver fluke secretes extracellular vesicles that promote cholangiocytes to adopt a tumorigenic phenotype" 212 : 1636-1645, 2015

105 Tucker, R., "Blood-derived non-extracellular vesicle proteins as potential biomarkers for the diagnosis of early ER + breast cancer and detection of lymph node involvement" 7 : 283-, 2018

106 Beckham, C. J., "Bladder cancer exosomes contain EDIL-3/Del1 and facilitate cancer progression" 192 : 583-592, 2014

107 Colombo, M., "Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles" 30 : 255-289, 2014

108 Akers, J. C., "Biogenesis of extracellular vesicles(EV) : exosomes, microvesicles, retrovirus-like vesicles, and apoptotic bodies" 113 : 1-11, 2013

109 Kowal, J., "Biogenesis and secretion of exosomes" 29 : 116-125, 2014

110 Gould, S. J., "As we wait: coping with an imperfect nomenclature for extracellular vesicles" 2 : 2013

111 van der Mijn, J. C., "Analysis of AKT and ERK1/2 protein kinases in extracellular vesicles isolated from blood of patients with cancer" 3 : 25657-, 2014

112 Raimondo, F., "Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery" 11 : 709-720, 2011

113 Sun, Y., "A novel TP53 pathway influences the HGS-mediated exosome formation in colorectal cancer" 6 : 28083-, 2016