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Research Article

Ultracentrifugation Versus Kit Exosome Isolation: NanoLC–MS and Other Tools Reveal Similar Performance Biomarkers, But Also Contaminations

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Article: FSO359 | Received 27 Sep 2018, Accepted 23 Oct 2018, Published online: 09 Nov 2018

References

  • Théry C, Zitvogel L, Amigorena S. Exosomes: composition, biogenesis and function. Nat. Rev. Immunol. 2, 569 (2002).
  • Lener T, Gimona M, Aigner L et al. Applying extracellular vesicles based therapeutics in clinical trials - an ISEV position paper. J. Extracell. Vesicles 4, 31 (2015).
  • Zhao H, Yang L, Baddour J et al. Tumor microenvironment derived exosomes pleiotropically modulate cancer cell metabolism. Elife 5, e10250 (2016).
  • Skotland T, Sandvig K, Llorente A. Lipids in exosomes: current knowledge and the way forward. Prog. Lipid Res. 66, 30–41 (2017).
  • Beach A, Zhang H-G, Ratajczak MZ, Kakar SS. Exosomes: an overview of biogenesis, composition and role in ovarian cancer. J. Ovarian Res. 7, 14–14 (2014).
  • Li P, Kaslan M, Lee SH, Yao J, Gao Z. Progress in exosome isolation techniques. Theranostics 7(3), 789–804 (2017).
  • Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H, Lyden D. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell 30(6), 836–848 (2016).
  • Pocsfalvi G, Stanly C, Fiume I, Vekey K. Chromatography and its hyphenation to mass spectrometry for extracellular vesicle analysis. J. Chromatogr. A 1439, 26–41 (2016).
  • Farahani M, Rubbi C, Liu L, Slupsky JR, Kalakonda N. CLL exosomes modulate the transcriptome and behaviour of recipient stromal cells and are selectively enriched in miR-202-3p. PLoS ONE 10(10), e0141429 (2015).
  • Logozzi M, De Milito A, Lugini L et al. High levels of exosomes expressing CD63 and caveolin-1 in plasma of melanoma patients. PLoS ONE 4(4), 10 (2009).
  • Parolini I, Federici C, Raggi C et al. Microenvironmental pH is a key factor for exosome traffic in tumor cells. J. Biol. Chem. 284(49), 34211–34222 (2009).
  • Peinado H, Alečković M, Lavotshkin S et al. Melanoma exosomes educate bone marrow progenitor cells toward a pro-metastatic phenotype through MET. Nat. Med. 18(6), 883–891 (2012).
  • Harris DA, Patel SH, Gucek M, Hendrix A, Westbroek W, Taraska JW. Exosomes released from breast cancer carcinomas stimulate cell movement. PLoS ONE 10(3), e0117495 (2015).
  • Desantis CE, Lin CC, Mariotto AB et al. Cancer treatment and survivorship statistics, 2014. CA Cancer J. Clin. 64(4), 252–271 (2014).
  • Redig AJ, Mcallister SS. Breast cancer as a systemic disease: a view of metastasis. J. Intern. Med. 274(2), 113–126 (2013).
  • Touat M, Duran-Pena A, Alentorn A, Lacroix L, Massard C, Idbaih A. Emerging circulating biomarkers in glioblastoma: promises and challenges. Expert Rev. Mol. Diagn. 15(10), 1311–1323 (2015).
  • Molina JR, Hayashi Y, Stephens C, Georgescu MM. Invasive glioblastoma cells acquire stemness and increased akt activation. Neoplasia 12(6), 453–U437 (2010).
  • Preusser M, De Ribaupierre S, Wohrer A et al. Current concepts and management of glioblastoma. Ann. Neurol. 70(1), 9–21 (2011).
  • Jan Chrastina ZN, Milan Brazdil, Marketa Hermanova. Glioblastoma multiforme in a patient with isolated hemimegalencephaly. J. Neurol. Surg. Rep. 76(1), 160–163 (2015).
  • Shao HL, Chung J, Lee K et al. Chip-based analysis of exosomal mRNA mediating drug resistance in glioblastoma. Nat. Commun. 6, 9 (2015).
  • Best MG, Sol N, Zijl S, Reijneveld JC, Wesseling P, Wurdinger T. Liquid biopsies in patients with diffuse glioma. Acta Neuropathol. 129(6), 849–865 (2015).
  • Cristofanilli M, Budd GT, Ellis MJ et al. Circulating tumor cells, disease progression, and survival in metastatic breast cancer. N. Engl. J. Med 351(8), 781–791 (2004).
  • He M, Zeng Y. Microfluidic exosome analysis toward liquid biopsy for cancer. J. Lab. Autom. 21(4), 599–608 (2016).
  • Melo SA, Luecke LB, Kahlert C et al. Glypican-1 identifies cancer exosomes and detects early pancreatic cancer. Nature 523(7559), 177–182 (2015).
  • Taylor DD, Gercel-Taylor C. microRNA signatures of tumor-derived exosomes as diagnostic biomarkers of ovarian cancer. Gynecol. Oncol. 110(1), 13–21 (2008).
  • Roberg-Larsen H, Lund K, Seterdal KE et al. Mass spectrometric detection of 27-hydroxycholesterol in breast cancer exosomes. J. Steroid Biochem. Mol. Biol. 169, 22–28 (2017).
  • Skog J, Würdinger T, Van Rijn S et al. Glioblastoma microvesicles transport RNA and proteins that promote tumour growth and provide diagnostic biomarkers. Nat. Cell Biol. 10(12), 1470–1476 (2008).
  • Hochberg FH, Atai NA, Gonda D et al. Glioma diagnostics and biomarkers: an ongoing challenge in the field of medicine and science. Expert Rev. Mol. Diagn. 14(4), 439–452 (2014).
  • Saadatpour L, Fadaee E, Fadaei S et al. Glioblastoma: exosome and microRNA as novel diagnosis biomarkers. Cancer Gene Ther. 23(12), 415–418 (2016).
  • Mondal A, Singh DK, Panda S, Shiras A. Extracellular vesicles as modulators of tumor microenvironment and disease progression in glioma. Front. Oncol. 7, 8 (2017).
  • Keller S, Ridinger J, Rupp A-K, Janssen JW, Altevogt P. Body fluid derived exosomes as a novel template for clinical diagnostics. J. Transl. Med. 9(1), 86 (2011).
  • Théry C, Amigorena S, Raposo G, Clayton A. Isolation and characterization of exosomes from cell culture supernatants and biological fluids. Curr. Protoc. Mol. Biol. 30, 3.22.1–3.22.29 (2006).
  • Cantin R, Diou J, Bélanger D, Tremblay AM, Gilbert C. Discrimination between exosomes and HIV-1: purification of both vesicles from cell-free supernatants. J. Immunol. Methods 338(1), 21–30 (2008).
  • Greening DW, Xu R, Ji H, Tauro BJ, Simpson RJ. A protocol for exosome isolation and characterization: evaluation of ultracentrifugation, density-gradient separation, and immunoaffinity capture methods. Methods Mol. Biol. 1295, 179–209 (2015).
  • Cvjetkovic A, Lötvall J, Lässer C. The influence of rotor type and centrifugation time on the yield and purity of extracellular vesicles. J. Extracell. Vesicles 3, doi: 10.3402/jev.v3403.23111 (2014) ( Epub ahead of print).
  • 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 12(3), 587–598 (2013).
  • Bhatia SN, Ingber DE. Microfluidic organs-on-chips. Nat. Biotechnol. 32(8), 760–772 (2014).
  • Böing AN, Van Der Pol E, Grootemaat AE, Coumans FA, Sturk A, Nieuwland R. Single-step isolation of extracellular vesicles by size-exclusion chromatography. J. Extracell. Vesicles 3, doi: 10.3402/jev.v3403.23430 (2014) ( Epub ahead of print).
  • Gámez-Valero A, Monguió-Tortajada M, Carreras-Planella L. Size-exclusion chromatography-based isolation minimally alters extracellular vesicles’ characteristics compared to precipitating agents. Sci. Rep. 6, doi: 10.1038/srep33641 (2016) ( Epub ahead of print).
  • Grant R, Ansa-Addo E, Stratton D et al. A filtration-based protocol to isolate human plasma membrane-derived vesicles and exosomes from blood plasma. J. Immunol. Methods 371(1), 143–151 (2011).
  • Clayton A, Court J, Navabi H et al. Analysis of antigen presenting cell derived exosomes, based on immuno-magnetic isolation and flow cytometry. J. Immunol. Methods 247(1), 163–174 (2001).
  • Yang JS, Lee JC, Byeon SK, Rha KH, Moon MH. Size dependent lipidomic analysis of urinary exosomes from patients with prostate cancer by flow field-flow fractionation and nanoflow liquid chromatography-tandem mass spectrometry. Anal. Chem. 89, 2488–2496 (2017).
  • Abramowicz A, Widlak P, Pietrowska M. Proteomic analysis of exosomal cargo: the challenge of high purity vesicle isolation. Mol. Biosyst. 12(5), 1407–1419 (2016).
  • Ku A, Lim HC, Evander M et al. Rapid acoustic enrichment of extracellular vesicles from biological fluids. Anal. Chem. 90(13), 8011–8019 (2018).
  • Rider MA, Hurwitz SN, Meckes DG Jr. ExtraPEG: a polyethylene glycol-based method for enrichment of extracellular vesicles. Sci. Rep. 6, 23978 (2016).
  • Tang Y-T, Huang Y-Y, Zheng L et al. Comparison of isolation methods of exosomes and exosomal RNA from cell culture medium and serum. Int. J. Mol. Med. 40(3), 834 (2017).
  • Vik-Mo EO, Sandberg C, Olstorn H et al. Brain tumor stem cells maintain overall phenotype and tumorigenicity after in vitro culturing in serum-free conditions. Neuro. Oncol. 12(12), 1220–1230 (2010).
  • Pan B-T, Teng K, Wu C, Adam M, Johnstone RM. Electron microscopic evidence for externalization of the transferrin receptor in vesicular form in sheep reticulocytes. J. Cell. Biol. 101(3), 942–948 (1985).
  • Pan B-T, Johnstone RM. Fate of the transferrin receptor during maturation of sheep reticulocytes in vitro: selective externalization of the receptor. Cell 33(3), 967–978 (1983).
  • Lobb RJ, Becker M, Wen SW et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J. Extracell. Vesicles 4, 11 (2015).
  • Jenjaroenpun P, Kremenska Y, Nair VM, Kremenskoy M, Joseph B, Kurochkin IV. Characterization of RNA in exosomes secreted by human breast cancer cell lines using next-generation sequencing. PeerJ 1, e201 (2013).
  • Palazzolo G, Albanese NN, Di Cara G, Gygax D, Vittorelli ML, Pucci-Minafra I. Proteomic analysis of exosome-like vesicles derived from breast cancer cells. Anticancer Res. 32(3), 847–860 (2012).
  • Van Deun J, Mestdagh P, Sormunen R et al. The impact of disparate isolation methods for extracellular vesicles on downstream RNA profiling. J. Extracell. Vesicles 3(1), 24858 (2014).
  • Liu F, Vermesh O, Mani V et al. The exosome total isolation chip. ACS Nano 11(11), 10712–10723 (2017).
  • Lötvall J, Hill AF, Hochberg F et al. Minimal experimental requirements for definition of extracellular vesicles and their functions: a position statement from the International Society for Extracellular Vesicles. J. Extracell. Vesicles 3, 26913–23078 (2014).
  • Kim J, Tan Z, Lubman DM. Exosome enrichment of human serum using multiple cycles of centrifugation. Electrophoresis 36(17), 2017–2026 (2015).
  • Berg HS, Seterdal KE, Smetop T et al. Self-packed core shell nano liquid chromatography columns and silica-based monolithic trap columns for targeted proteomics. J. Chromatogr. A 1498, 111–119 (2017).
  • De Vrij J, Maas SLN, Kwappenberg KMC et al. Glioblastoma-derived extracellular vesicles modify the phenotype of monocytic cells. Int. J. Cancer 137(7), 1630–1642 (2015).
  • Redzic JS, Ung TH, Graner MW. Glioblastoma extracellular vesicles: reservoirs of potential biomarkers. Pharmacogenomics Person. Med. 7, 65–77 (2014).
  • Thuringer D, Hammann A, Benikhlef N et al. Transactivation of the epidermal growth factor receptor by heat shock protein 90 via Toll-like receptor 4 contributes to the migration of glioblastoma cells. J. Biol. Chem. 286(5), 3418–3428 (2011).
  • Graner MW, Cumming RI, Bigner DD. The heat shock response and chaperones/heat shock proteins in brain tumors: surface expression, release, and possible immune consequences. J. Neurosci. 27(42), 11214–11227 (2007).
  • Wade A, Robinson AE, Engler JR, Petritsch C, James CD, Phillips JJ. Proteoglycans and their roles in brain cancer. FEBS J. 280(10), 2399–2417 (2013).
  • Mooney KL, Choy W, Sidhu S et al. The role of CD44 in glioblastoma multiforme. J. Clin. Neurosci. 34, 1–5 (2016).
  • Kraan J, Van Den Broek P, Verhoef C et al. Endothelial CD276 (B7-H3) expression is increased in human malignancies and distinguishes between normal and tumour-derived circulating endothelial cells. Br. J. Cancer 111(1), 149–156 (2014).
  • Beliakoff J, Whitesell L. Hsp90: an emerging target for breast cancer therapy. Anticancer Drugs 15(7), 651–662 (2004).
  • Price JT, Tiganis T, Agarwal A, Djakiew D, Thompson EW. Epidermal growth factor promotes MDA-MB-231 breast cancer cell migration through a phosphatidylinositol 3′-kinase and phospholipase C-dependent mechanism. Cancer Res. 59(21), 5475–5478 (1999).
  • Hoshino A, Costa-Silva B, Shen T-L et al. Tumour exosome integrins determine organotropic metastasis. Nature 527, 329 (2015).