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Research Article

Evaluation of serum extracellular vesicle isolation methods for profiling miRNAs by next-generation sequencing

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Article: 1481321 | Received 12 Feb 2018, Accepted 18 May 2018, Published online: 04 Jun 2018

References

  • Gardiner C, Di Vizio D, Sahoo S, et al. Techniques used for the isolation and characterization of extracellular vesicles: results of a worldwide survey. J Extracell Vesicles. 2016;5:1.
  • Cheng L, Sharples RA, Scicluna BJ, et al. Exosomes provide a protective and enriched source of miRNA for biomarker profiling compared to intracellular and cell-free blood. J Extracell Vesicles. 2014;3:23743
  • Mustapic M, Eitan E, Werner JK Jr., et al. Plasma extracellular vesicles enriched for neuronal origin: a potential window into brain pathologic processes. Front Neurosci. 2017;11:278.
  • Buschmann D, Haberberger A, Kirchner B, et al. Toward reliable biomarker signatures in the age of liquid biopsies – how to standardize the small RNA-Seq workflow. Nucleic Acids Res. 2016;44: 5995–18. Epub 2016/ 06/19.
  • El-Khoury V, Pierson S, Kaoma T, et al. Assessing cellular and circulating miRNA recovery: the impact of the RNA isolation method and the quantity of input material. Sci Rep. 2016;6:19529.
  • Guo Y, Vickers K, Xiong Y, et al. Comprehensive evaluation of extracellular small RNA isolation methods from serum in high throughput sequencing. BMC Genomics. 2017;18:50.
  • Danielson KM, Rubio R, Abderazzaq F, et al. High throughput sequencing of extracellular RNA from human plasma. PLoS One. 2017;12:e0164644.
  • 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. 2014;3:24858.
  • Alvarez ML, Khosroheidari M, Kanchi Ravi R, et al. Comparison of protein, microRNA, and mRNA yields using different methods of urinary exosome isolation for the discovery of kidney disease biomarkers. Kidney Int. 2012;82:1024–1032.
  • Royo F, Diwan I, Tackett MR, et al. Comparative miRNA analysis of urine extracellular vesicles isolated through five different methods. Cancers (Basel). 2016;8:112
  • Blans K, Hansen MS, Sorensen LV, et al. Pellet-free isolation of human and bovine milk extracellular vesicles by size-exclusion chromatography. J Extracell Vesicles. 2017;6:1294340.
  • Rekker K, Saare M, Roost AM, et al. Comparison of serum exosome isolation methods for microRNA profiling. Clin Biochem. 2014;47: 135–138. Epub 2013/ 11/05.
  • Muller L, Hong CS, Stolz DB, et al. Isolation of biologically-active exosomes from human plasma. J Immunol Methods. 2014;411:55–65.
  • Nielsen MH, Beck-Nielsen H, Andersen MN, et al. A flow cytometric method for characterization of circulating cell-derived microparticles in plasma. J Extracell Vesicles. 2017;3:20795.
  • Lasser C, Shelke GV, Yeri A, et al. Two distinct extracellular RNA signatures released by a single cell type identified by microarray and next-generation sequencing. RNA Biol. 2017;14:58–72.
  • Caponnetto F, Manini I, Skrap M, et al. Size-dependent cellular uptake of exosomes. Nanomedicine. 2017;13:1011–1020.
  • Zlotogorski-Hurvitz A, Dayan D, Chaushu G, et al. Human saliva-derived exosomes: comparing methods of isolation. J Histochem Cytochem. 2015;63:181–189.
  • Abramowicz A, Widlak P, Pietrowska M. Proteomic analysis of exosomal cargo: the challenge of high purity vesicle isolation. Mol Biosyst. 2016;12: 1407–1419. Epub 2016/ 04/01.
  • Royo F, Zuniga-Garcia P, Sanchez-Mosquera P, et al. Different EV enrichment methods suitable for clinical settings yield different subpopulations of urinary extracellular vesicles from human samples. J Extracell Vesicles. 2016;5: 29497. Epub 2016/ 02/20.
  • Mol EA, Goumans MJ, Doevendans PA, et al. Higher functionality of extracellular vesicles isolated using size-exclusion chromatography compared to ultracentrifugation. Nanomedicine. 2017;13:2061–2065.
  • Andreu Z, Rivas E, Sanguino-Pascual A, et al. Comparative analysis of EV isolation procedures for miRNAs detection in serum samples. J Extracell Vesicles. 2016;5:31655.
  • Crossland RE, Norden J, Bibby LA, et al. Evaluation of optimal extracellular vesicle small RNA isolation and qRT-PCR normalisation for serum and urine. J Immunol Methods. 2016;429:39–49.
  • Helwa I, Cai J, Drewry MD, et al. A comparative study of serum exosome isolation using differential ultracentrifugation and three commercial reagents. PLoS One. 2017;12:e0170628.
  • Bellingham SA, Shambrook M, Hill AF. Quantitative analysis of exosomal miRNA via qPCR and digital PCR. Methods Mol Biol. 2017;1545: 55–70. Epub 2016/ 12/13.
  • Zeringer E, Li M, Barta T, et al. Methods for the extraction and RNA profiling of exosomes. World J Methodol. 2013;3: 11–18. Epub 2013/ 03/26.
  • Takahashi K, Yan IK, Kim C, et al. Analysis of extracellular RNA by digital PCR. Front Oncol. 2014;4: 129. Epub 2014/ 06/14.
  • Li M, Zeringer E, Barta T, et al. Analysis of the RNA content of the exosomes derived from blood serum and urine and its potential as biomarkers. Philos Trans R Soc Lond B Biol Sci. 2014;369 ( Epub 2014/ 08/20).
  • Huang X, Yuan T, Tschannen M, et al. Characterization of human plasma-derived exosomal RNAs by deep sequencing. BMC Genomics. 2013;14: 319. Epub 2013/ 05/15.
  • Tsang EK, Abell NS, Li X, et al. Small RNA sequencing in cells and exosomes identifies eQTLs and 14q32 as a region of active export. G3 (Bethesda). 2017;7: 31–39. Epub 2016/ 11/04.
  • Tang YT, Huang YY, Zheng L, et al. Comparison of isolation methods of exosomes and exosomal RNA from cell culture medium and serum. Int J Mol Med. 2017;40: 834–844. Epub 2017/ 07/25.
  • Nimah M, Brilli RJ. Coagulation dysfunction in sepsis and multiple organ system failure. Crit Care Clin. 2003;19:441–458.
  • SepNet Critical Care Trials G. Incidence of severe sepsis and septic shock in German intensive care units: the prospective, multicentre INSEP study. Intensive Care Med. 2016;42:1980–1989.
  • Charlson ME, Pompei P, Ales KL, et al. A new method of classifying prognostic comorbidity in longitudinal studies: development and validation. J Chronic Dis. 1987;40:373–383.
  • Reithmair M, Buschmann D, Märte M, et al. Cellular and extracellular miRNAs are blood-compartment-specific diagnostic targets in sepsis. J Cell Mol Med. 2017;21:2403–2411.
  • Spornraft M, Kirchner B, Haase B, et al. Optimization of extraction of circulating RNAs from plasma – enabling small RNA sequencing. PLoS One. 2014;9:e107259.
  • Andrews S FastQC: a quality control tool for high throughput sequence data; 2010.
  • Kong Y. Btrim: a fast, lightweight adapter and quality trimming program for next-generation sequencing technologies. Genomics. 2011;98:152–153.
  • Consortium RN. RNAcentral: an international database of ncRNA sequences. Nucleic Acids Res. 2015;43:D123–D129.
  • Kozomara A, Griffiths-Jones S. miRBase: annotating high confidence microRNAs using deep sequencing data. Nucleic Acids Research. 2014;42:D68–D73.
  • Langmead B, Trapnell C, Pop M, et al. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biology. 2009;10:R25.
  • Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology. 2014;15:550.
  • R Core Team. R: a language and environment for statistical computing. Vienna, Austria; 2017.
  • Gregory R, Warnes BB, Bonebakker L, et al. Various R Programming Tools for Plotting Data; 2016.
  • Wickham H ggplot2: Elegant Graphics for data analysis; 2009.
  • Neuwirth E RColorBrewer: ColorBrewer Palettes. 2014.
  • Galili T. dendextend: an R package for visualizing, adjusting and comparing trees of hierarchical clustering. Bioinformatics. 2015;31:3718–3720.
  • Yuan Tang MH, Wenxuan L. ggfortify: unified interface to visualize statistical result of popular R Packages; 2016.
  • Chen H VennDiagram: generate high-resolution Venn and Euler plots; 2016.
  • Eitan E, Green J, Bodogai M, et al. Age-related changes in plasma extracellular vesicle characteristics and internalization by leukocytes. Sci Rep. 2017;7:1342.
  • Webber J, Clayton A. How pure are your vesicles? J Extracell Vesicles. 2013;2:19861.
  • Kalra H, Adda CG, Liem M, et al. Comparative proteomics evaluation of plasma exosome isolation techniques and assessment of the stability of exosomes in normal human blood plasma. Proteomics. 2013;13: 3354–3364. Epub 2013/ 10/12.
  • Eldh M, Lotvall J, Malmhall C, et al. Importance of RNA isolation methods for analysis of exosomal RNA: evaluation of different methods. Mol Immunol. 2012;50:278–286.
  • Wang H, Zhang P, Chen W, et al. Serum microRNA signatures identified by Solexa sequencing predict sepsis patients’ mortality: a prospective observational study. PLoS One. 2012;7: e38885. Epub 2012/ 06/22.
  • Caserta S, Kern F, Cohen J, et al. Circulating plasma microRNAs can differentiate human sepsis and systemic inflammatory response syndrome (SIRS). Sci Rep. 2016;6: 28006. Epub 2016/ 06/21.
  • Jiang X, Xu C, Lei F, et al. MiR-30a targets IL-1alpha and regulates islet functions as an inflammation buffer and response factor. Sci Rep. 2017;7: 5270. Epub 2017/ 07/15.
  • Cheng Y, Kuang W, Hao Y, et al. Downregulation of miR-27a* and miR-532-5p and upregulation of miR-146a and miR-155 in LPS-induced RAW264.7. Macrophage Cells Inflammation. 2012;35:1308–1313.
  • Tili E, Michaille JJ, Cimino A, et al. Modulation of miR-155 and miR-125b levels following lipopolysaccharide/TNF-alpha stimulation and their possible roles in regulating the response to endotoxin shock. J Immunol. 2007;179: 5082–5089. Epub 2007/ 10/04.
  • Zhou Y, Song Y, Shaikh Z, et al. MicroRNA-155 attenuates late sepsis-induced cardiac dysfunction through JNK and beta-arrestin 2. Oncotarget. 2017;8: 47317–47329. Epub 2017/ 05/20.
  • Liu J, Shi K, Chen M, et al. Elevated miR-155 expression induces immunosuppression via CD39(+) regulatory T-cells in sepsis patient. Int J Infect Dis. 2015;40: 135–141. Epub 2015/ 10/04.
  • Tacke F, Roderburg C, Benz F, et al. Levels of circulating miR-133a are elevated in sepsis and predict mortality in critically ill patients. Crit Care Med. 2014;42: 1096–1104. Epub 2014/ 01/15.
  • Sari AN, Korkmaz B, Serin MS, et al. Effects of 5,14-HEDGE, a 20-HETE mimetic, on lipopolysaccharide-induced changes in MyD88/TAK1/IKKbeta/IkappaB-alpha/NF-kappaB pathway and circulating miR-150, miR-223, and miR-297 levels in a rat model of septic shock. Inflamm Res. 2014;63: 741–756. Epub 2014/ 06/12.
  • Vasilescu C, Rossi S, Shimizu M, et al. MicroRNA fingerprints identify miR-150 as a plasma prognostic marker in patients with sepsis. PLoS One. 2009;4: e7405. Epub 2009/ 10/14.
  • Lin H, Ewing LE, Koturbash I, et al. MicroRNAs as biomarkers for liver injury: current knowledge, challenges and future prospects. Food Chem Toxicol. 2017;110: 229–239. Epub 2017/ 10/19.
  • Wang H, Yu B, Deng J, et al. Serum miR-122 correlates with short-term mortality in sepsis patients. Crit Care. 2014;18: 704. Epub 2015/ 02/13.
  • Wang HJ, Deng J, Wang JY, et al. Serum miR-122 levels are related to coagulation disorders in sepsis patients. Clin Chem Lab Med. 2014;52: 927–933. Epub 2014/ 01/15.
  • Roderburg C, Benz F, Vargas Cardenas D, et al. Elevated miR-122 serum levels are an independent marker of liver injury in inflammatory diseases. Liver Int. 2015;35: 1172–1184. Epub 2014/ 07/22.
  • Linares R, Tan S, Gounou C, et al. High-speed centrifugation induces aggregation of extracellular vesicles. J Extracell Vesicles. 2015;4:29509.
  • Dominguez-Medina S, McDonough S, Swanglap P, et al. In situ measurement of bovine serum albumin interaction with gold nanospheres. Langmuir. 2012;28:9131–9139.
  • Stranska R, Gysbrechts L, Wouters J, et al. Comparison of membrane affinity-based method with size-exclusion chromatography for isolation of exosome-like vesicles from human plasma. J Transl Med. 2018;16: 1. Epub 2018/ 01/11.
  • Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15: 375–387. Epub 2015/ 05/16.
  • Alexander M, Hu R, Runtsch MC, et al. Exosome-delivered microRNAs modulate the inflammatory response to endotoxin. Nat Commun. 2015;6: 7321. Epub 2015/ 06/19.
  • Sodar BW, Kittel A, Paloczi K, et al. Low-density lipoprotein mimics blood plasma-derived exosomes and microvesicles during isolation and detection. Sci Rep. 2016;6: 24316. Epub 2016/ 04/19.
  • Gyorgy B, Szabo TG, Turiak L, et al. Improved flow cytometric assessment reveals distinct microvesicle (cell-derived microparticle) signatures in joint diseases. PLoS One. 2012;7: e49726. Epub 2012/ 11/28.
  • Mork M, Handberg A, Pedersen S, et al. Prospects and limitations of antibody-mediated clearing of lipoproteins from blood plasma prior to nanoparticle tracking analysis of extracellular vesicles. J Extracell Vesicles. 2017;6: 1308779. Epub 2017/ 05/06.
  • Gardiner C, Ferreira YJ, Dragovic RA, et al. Extracellular vesicle sizing and enumeration by nanoparticle tracking analysis. J Extracell Vesicles. 2013;2: 19671. Epub 2013/ 09/07.
  • Ghosal A. Importance of secreted bacterial RNA in bacterial-host interactions in the gut. Microb Pathog. 2017;104: 161–163. Epub 2017/ 01/24.
  • Ghosal A, Upadhyaya BB, Fritz JV, et al. The extracellular RNA complement of Escherichia coli. Microbiologyopen. 2015;4: 252–266. Epub 2015/ 01/23.
  • Soo CY, Song Y, Zheng Y, et al. Nanoparticle tracking analysis monitors microvesicle and exosome secretion from immune cells. Immunology. 2012;136: 192–197. Epub 2012/ 02/22.
  • Zabeo D, Cvjetkovic A, Lasser C, et al. Exosomes purified from a single cell type have diverse morphology. J Extracell Vesicles. 2017;6: 1329476. Epub 2017/ 07/19.
  • Enderle D, Spiel A, Coticchia CM, et al. Characterization of RNA from exosomes and other extracellular vesicles isolated by a novel spin column-based method. PLoS One. 2015;10:e0136133.
  • Koliha N, Wiencek Y, Heider U, et al. A novel multiplex bead-based platform highlights the diversity of extracellular vesicles. J Extracell Vesicles. 2016;5:29975.
  • Kowal J, Arras G, Colombo M, et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A. 2016;113:E968–77.
  • Gamez-Valero A, Monguio-Tortajada M, Carreras-Planella L, et al. Size-exclusion chromatography-based isolation minimally alters extracellular vesicles’ characteristics compared to precipitating agents. Sci Rep. 2016;6:33641.
  • Zarovni N, Corrado A, Guazzi P, et al. Integrated isolation and quantitative analysis of exosome shuttled proteins and nucleic acids using immunocapture approaches. Methods. 2015;87:46–58.
  • Lotvall 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. 2014;3: 26913. Epub 2014/ 12/30.
  • Lobb RJ, Becker M, Wen SW, et al. Optimized exosome isolation protocol for cell culture supernatant and human plasma. J Extracell Vesicles. 2015;4: 27031. Epub 2015/ 07/22.
  • Welton JL, Webber JP, Botos LA, et al. Ready-made chromatography columns for extracellular vesicle isolation from plasma. J Extracell Vesicles. 2015;4:27269.
  • Baranyai T, Herczeg K, Onodi Z, et al. Isolation of exosomes from blood plasma: qualitative and quantitative comparison of ultracentrifugation and size exclusion chromatography methods. PLoS One. 2015;10:e0145686.
  • Quek C, Bellingham SA, Jung CH, et al. Defining the purity of exosomes required for diagnostic profiling of small RNA suitable for biomarker discovery. RNA Biol. 2017;14:245–258.
  • Deregibus MC, Figliolini F, D’Antico S, et al. Charge-based precipitation of extracellular vesicles. Int J Mol Med. 2016;38:1359–1366.
  • Witwer KW, Soekmadji C, Hill AF, et al. Updating the MISEV minimal requirements for extracellular vesicle studies: building bridges to reproducibility. J Extracell Vesicles. 2017;6: 1396823. Epub 2017/ 12/01.
  • Arroyo JD, Chevillet JR, Kroh EM, et al. Argonaute2 complexes carry a population of circulating microRNAs independent of vesicles in human plasma. Proc Natl Acad Sci U S A. 2011;108: 5003–5008. Epub 2011/ 03/09.
  • Mateescu B, Kowal EJ, van Balkom BW, et al. Obstacles and opportunities in the functional analysis of extracellular vesicle RNA – an ISEV position paper. J Extracell Vesicles. 2017;6: 1286095. Epub 2017/ 03/23.
  • van Eijndhoven MA, Zijlstra JM, Groenewegen NJ, et al. Plasma vesicle miRNAs for therapy response monitoring in Hodgkin lymphoma patients. JCI Insight. 2016;1: e89631. Epub 2016/ 11/25.