Quantitative proteomics of extracellular vesicles derived from human primary and metastatic colorectal cancer cells

Abstract

Cancer cells actively release extracellular vesicles (EVs), including exosomes and microvesicles, into surrounding tissues. These EVs play pleiotropic roles in cancer progression and metastasis, including invasion, angiogenesis, and immune modulation. However, the proteomic differences between primary and metastatic cancer cell‐derived EVs remain unclear. Here, we conducted comparative proteomic analysis between EVs derived from human primary colorectal cancer cells (SW480) and their metastatic derivatives (SW620). Using label‐free quantitation, we identified 803 and 787 proteins in SW480 EVs and SW620 EVs, respectively. Based on comparison between the estimated abundance of EV proteins, we identified 368 SW480 EV‐enriched and 359 SW620 EV‐enriched proteins. SW480 EV‐enriched proteins played a role in cell adhesion, but SW620 EV‐enriched proteins were associated with cancer progression and functioned as diagnostic indicators of metastatic cancer; they were overexpressed in metastatic colorectal cancer and played roles in multidrug resistance. As the first proteomic analysis comparing primary and metastatic cancer‐derived EVs, this study increases our understanding of the pathological function of EVs in the metastatic process and provides useful biomarkers for cancer metastasis.

Shown for reading. Its publisher allows quoting it, not republishing it.

References 68

1. 1.

   Thery C, Ostrowski M, Segura E. Membrane vesicles as conveyors of immune responses. Nat Rev Immunol. 2009;9:581-93.

   Not in our library10.1038/nri2567 (opens in a new tab)

2. 2.

   Valadi H, Ekstrom K, Bossios A, Sjostrand M, Lee JJ, Lotvall JO. Exosome-mediated transfer of mRNAs and microRNAs is a novel mechanism of genetic exchange between cells. Nat Cell Biol. 2007;9:654-9.

   Not in our library10.1038/ncb1596 (opens in a new tab)

3. 3.

   Kim CW, Lee HM, Lee TH, Kang C, Kleinman HK, Gho YS. Extracellular membrane vesicles from tumor cells promote angiogenesis via sphingomyelin. Cancer Res. 2002;62:6312-7.

   Not in our library

4. 4.

   Gyorgy B, Szabo TG, Pasztoi M, Pal Z, Misjak P, Aradi B, et al. Membrane vesicles, current state-of-the-art: emerging role of extracellular vesicles. Cell Mol Life Sci. 2011;68:2667-88.

   Not in our library10.1007/s00018-011-0689-3 (opens in a new tab)

5. 5.

   Choi DS, Yang JS, Choi EJ, Jang SC, Park S, Kim OY, et al. The protein interaction network of extracellular vesicles derived from human colorectal cancer cells. J Proteome Res. 2012;11:1144-51.

   Not in our library10.1021/pr200842h (opens in a new tab)

6. 6.

   Huber V, Fais S, Iero M, Lugini L, Canese P, Squarcina P, et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology. 2005;128:1796-804.

   Not in our library10.1053/j.gastro.2005.03.045 (opens in a new tab)

7. 7.

   Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, 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;66:9290-8.

   Not in our library10.1158/0008-5472.can-06-1819 (opens in a new tab)

8. 8.

   Choi DS, Lee JM, Park GW, Lim HW, Bang JY, Kim YK, et al. Proteomic analysis of microvesicles derived from human colorectal cancer cells. J Proteome Res. 2007;6:4646-55.

   Not in our library10.1021/pr070192y (opens in a new tab)

9. 9.

   Lee HM, Choi EJ, Kim JH, Kim TD, Kim YK, Kang C, et al. A membranous form of ICAM-1 on exosomes efficiently blocks leukocyte adhesion to activated endothelial cells. Biochem Biophys Res Commun. 2010;397:251-6.

   Not in our library10.1016/j.bbrc.2010.05.094 (opens in a new tab)

10. 10.
    Colorectal cancer cell-derived microvesicles are enriched in cell cycle-related mRNAs that promote proliferation of endothelial cells · 2009

    No notice
11. 11.

    Xue H, Lu B, Zhang J, Wu M, Huang Q, Wu Q, et al. Identification of serum biomarkers for colorectal cancer metastasis using a differential secretome approach. J Proteome Res. 2010;9:545-55.

    Not in our library10.1021/pr9008817 (opens in a new tab)

12. 12.

    Ghosh D, Yu H, Tan XF, Lim TK, Zubaidah RM, Tan HT, et al. Identification of key players for colorectal cancer metastasis by iTRAQ quantitative proteomics profiling of isogenic SW480 and SW620 cell lines. J Proteome Res. 2011;10:4373-87.

    Not in our library10.1021/pr2005617 (opens in a new tab)

13. 13.

    Lu P, Vogel C, Wang R, Yao X, Marcotte EM. Absolute protein expression profiling estimates the relative contributions of transcriptional and translational regulation. Nat Biotechnol. 2007;25:117-24.

    Not in our library10.1038/nbt1270 (opens in a new tab)

14. 14.

    Gercel-Taylor C, Atay S, Tullis RH, Kesimer M, Taylor DD. Nanoparticle analysis of circulating cell-derived vesicles in ovarian cancer patients. Anal Biochem. 2012;428:44-53.

    Not in our library10.1016/j.ab.2012.06.004 (opens in a new tab)

15. 15.

    Bjornson RD, Carriero NJ, Colangelo C, Shifman M, Cheung KH, Miller PL, et al. X!!Tandem, an improved method for running X!tandem in parallel on collections of commodity computers. J Proteome Res. 2008;7:293-9.

    Not in our library10.1021/pr0701198 (opens in a new tab)

16. 16.

    Keller A, Eng J, Zhang N, Li XJ, Aebersold R. A uniform proteomics MS/MS analysis platform utilizing open XML file formats. Mol Syst Biol. 2005;1.

    Not in our library10.1038/msb4100024 (opens in a new tab)

17. 17.

    Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.

    Not in our library10.1038/nprot.2008.211 (opens in a new tab)

18. 18.

    Mears R, Craven RA, Hanrahan S, Totty N, Upton C, Young SL, et al. Proteomic analysis of melanoma-derived exosomes by two-dimensional polyacrylamide gel electrophoresis and mass spectrometry. Proteomics. 2004;4:4019-31.

    Not in our library10.1002/pmic.200400876 (opens in a new tab)

19. 19.

    Choi DS, Park JO, Jang SC, Yoon YJ, Jung JW, Choi DY, et al. Proteomic analysis of microvesicles derived from human colorectal cancer ascites. Proteomics. 2011;11:2745-51.

    Not in our library10.1002/pmic.201100022 (opens in a new tab)

20. 20.

    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.

    Not in our library10.1074/mcp.m900152-mcp200 (opens in a new tab)

21. 21.

    Raimondo F, Morosi L, Chinello C, Magni F, Pitto M. Advances in membranous vesicle and exosome proteomics improving biological understanding and biomarker discovery. Proteomics. 2011;11:709-20.

    Not in our library10.1002/pmic.201000422 (opens in a new tab)

22. 22.

    Roberson CD, Atay S, Gercel-Taylor C, Taylor DD. Tumor-derived exosomes as mediators of disease and potential diagnostic biomarkers. Cancer Biomark. 2010;8:281-91.

    Not in our library10.3233/cbm-2011-0211 (opens in a new tab)

23. 23.

    Mathivanan S, Simpson RJ. ExoCarta: a compendium of exosomal proteins and RNA. Proteomics. 2009;9:4997-5000.

    Not in our library10.1002/pmic.200900351 (opens in a new tab)

24. 24.

    Zhang Y, Ye Y, Shen D, Jiang K, Zhang H, Sun W, et al. Identification of transgelin-2 as a biomarker of colorectal cancer by laser capture microdissection and quantitative proteome analysis. Cancer Sci. 2010;101:523-9.

    Not in our library10.1111/j.1349-7006.2009.01424.x (opens in a new tab)

25. 25.

    Buda A, Pignatelli M. Cytoskeletal network in colon cancer: from genes to clinical application. Int J Biochem Cell Biol. 2004;36:759-65.

    Not in our library10.1016/j.biocel.2003.09.004 (opens in a new tab)

26. 26.

    Gupta GP, Massague J. Cancer metastasis: building a framework. Cell. 2006;127:679-95.

    Not in our library10.1016/j.cell.2006.11.001 (opens in a new tab)

27. 27.

    Andre M, Le Caer JP, Greco C, Planchon S, El Nemer W, Boucheix C, et al. Proteomic analysis of the tetraspanin web using LC-ESI-MS/MS and MALDI-FTICR-MS. Proteomics. 2006;6:1437-49.

    Not in our library10.1002/pmic.200500180 (opens in a new tab)

28. 28.

    Kubens BS, Zanker KS. Differences in the migration capacity of primary human colon carcinoma cells (SW480) and their lymph node metastatic derivatives (SW620). Cancer Lett. 1998;131:55-64.

    Not in our library10.1016/s0304-3835(98)00201-8 (opens in a new tab)

29. 29.

    Chairoungdua A, Smith DL, Pochard P, Hull M, Caplan MJ. Exosome release of beta-catenin: a novel mechanism that antagonizes Wnt signaling. J Cell Biol. 2010;190:1079-91.

    Not in our library10.1083/jcb.201002049 (opens in a new tab)

30. 30.

    Dusek RL, Attardi LD. Desmosomes: new perpetrators in tumour suppression. Nat Rev Cancer. 2011;11:317-23.

    Not in our library10.1038/nrc3051 (opens in a new tab)

31. 31.

    Hurley JH, Hanson PI. Membrane budding and scission by the ESCRT machinery: it's all in the neck. Nat Rev Mol Cell Biol. 2010;11:556-66.

    Not in our library10.1038/nrm2937 (opens in a new tab)

32. 32.

    Simons M, Raposo G. Exosomes – vesicular carriers for intercellular communication. Curr Opin Cell Biol. 2009;21:575-81.

    Not in our library10.1016/j.ceb.2009.03.007 (opens in a new tab)

33. 33.

    Vignjevic D, Schoumacher M, Gavert N, Janssen KP, Jih G, Lae M, et al. Fascin, a novel target of beta-catenin-TCF signaling, is expressed at the invasive front of human colon cancer. Cancer Res. 2007;67:6844-53.

    Not in our library10.1158/0008-5472.can-07-0929 (opens in a new tab)

34. 34.

    Techasen A, Loilome W, Namwat N, Takahashi E, Sugihara E, Puapairoj A, et al. Myristoylated alanine-rich C kinase substrate phosphorylation promotes cholangiocarcinoma cell migration and metastasis via the protein kinase C-dependent pathway. Cancer Sci. 2010;101:658-65.

    Not in our library10.1111/j.1349-7006.2009.01427.x (opens in a new tab)

35. 35.

    Eswaran J, Soundararajan M, Knapp S. Targeting group II PAKs in cancer and metastasis. Cancer Metastasis Rev. 2009;28:209-17.

    Not in our library10.1007/s10555-008-9181-4 (opens in a new tab)

36. 36.

    Chen N, Sun W, Deng X, Hao Y, Chen X, Xing B, et al. Quantitative proteome analysis of HCC cell lines with different metastatic potentials by SILAC. Proteomics. 2008;8:5108-18.

    Not in our library10.1002/pmic.200800280 (opens in a new tab)

37. 37.

    Song B, Tang JW, Wang B, Cui XN, Hou L, Sun L, et al. Identify lymphatic metastasis-associated genes in mouse hepatocarcinoma cell lines using gene chip. World J Gastroenterol. 2005;11:1463-72.

    Not in our library10.3748/wjg.v11.i10.1463 (opens in a new tab)

38. 38.

    Yang HJ, Chen JZ, Zhang WL, Ding YQ. Focal adhesion plaque associated cytoskeletons are involved in the invasion and metastasis of human colorectal carcinoma. Cancer Invest. 2010;28:127-34.

    Not in our library10.3109/07357900903147184 (opens in a new tab)

39. 39.

    Seaman S, Stevens J, Yang MY, Logsdon D, Graff-Cherry C, St Croix B. Genes that distinguish physiological and pathological angiogenesis. Cancer Cell. 2007;11:539-54.

    Not in our library10.1016/j.ccr.2007.04.017 (opens in a new tab)

40. 40.

    O'Brien CA, Pollett A, Gallinger S, Dick JE. A human colon cancer cell capable of initiating tumour growth in immunodeficient mice. Nature. 2007;445:106-10.

    Not in our library10.1038/nature05372 (opens in a new tab)

Cited by papers we hold 9

• Recent advances of small extracellular vesicle biomarkers in breast cancer diagnosis and prognosis · 2023
  No notice
• Biodistribution of Exosomes and Engineering Strategies for Targeted Delivery of Therapeutic Exosomes · 2021
  No notice
• Mass spectrometry-based proteome profiling of extracellular vesicles and their roles in cancer biology · 2019
  No notice
• Focus on Extracellular Vesicles: New Frontiers of Cell-to-Cell Communication in Cancer · 2016
  No notice
• Large oncosomes contain distinct protein cargo and represent a separate functional class of tumor-derived extracellular vesicles · 2015
  No notice
• Emerging roles of extracellular vesicles in the adaptive response of tumour cells to microenvironmental stress · 2013
  No notice
• Extracellular Vesicle (EV) Array: microarray capturing of exosomes and other extracellular vesicles for multiplexed phenotyping · 2013
  No notice
• Characterization of RNA in exosomes secreted by human breast cancer cell lines using next-generation sequencing · 2013
  No notice
• EVpedia: an integrated database of high‐throughput data for systemic analyses of extracellular vesicles · 2013
  No notice

Questions about this paper

Reads

A person counts once a day per paper. We keep no cookie and no address: a reader is a hash that changes every day. Any month under five reads shows no number.