Analysis of the Escherichia coli extracellular vesicle proteome identifies markers of purity and culture conditions

References

• Kaparakis-Liaskos M, Ferrero RL. Immune modulation by bacterial outer membrane vesicles. Nat Rev Immunol. 2015;15(6):375–16.
   PubMed Web of Science ®Google Scholar
• Kulkarni HM, Jagannadham MV. Biogenesis and multifaceted roles of outer membrane vesicles from gram-negative bacteria. Microbiol. 2014;160(Pt 10):2109–2121.
   Web of Science ®Google Scholar
• Orench-Rivera N, Kuehn MJ. Environmentally controlled bacterial vesicle-mediated export. Cell Microbiol. 2016;18(11):1525–1536.
   Web of Science ®Google Scholar
• Dauros-Singorenko P, Swift S. The transition from iron starvation to iron sufficiency as an important step in the progression of infection. Sci Prog. 2014;97(Pt 4):371–382.
   Google Scholar
• Prados-Rosales R, Weinrick BC, Pique DG, et al. Role for mycobacterium tuberculosis membrane vesicles in iron acquisition. J Bacteriol. 2014;196(6):1250–1256.
   PubMed Web of Science ®Google Scholar
• Roier S, Zingl FG, Cakar F, et al. A novel mechanism for the biogenesis of outer membrane vesicles in gram-negative bacteria. Nat Commun. 2016;7:10515.
   PubMed Web of Science ®Google Scholar
• Kuehn MJ, Kesty NC. Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005;19(22):2645–2655.
   PubMed Web of Science ®Google Scholar
• Kulp A, Kuehn MJ. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol. 2010;64:163–184.
   PubMed Web of Science ®Google Scholar
• Haurat MF, Elhenawy W, Feldman MF. Prokaryotic membrane vesicles: new insights on biogenesis and biological roles. Biol Chem. 2015;396(2):95–109.
   PubMed Web of Science ®Google Scholar
• Ellis TN, Kuehn MJ. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol Mol Biol Rev. 2010;74(1):81–94.
   PubMed Web of Science ®Google Scholar
• Jan AT. Outer membrane vesicles (OMVs) of gram-negative bacteria: a perspective update. Front Microbiol. 2017;8:1053.
   PubMed Web of Science ®Google Scholar
• Hoekstra D, van der Laan JW, de Leij L, et al. Release of outer membrane fragments from normally growing Escherichia coli. Biochim Biophys Acta. 1976;455(3):889–899.
   PubMed Web of Science ®Google Scholar
• Perez-Cruz C, Delgado L, Lopez-Iglesias C, et al. Outer-inner membrane vesicles naturally secreted by gram-negative pathogenic bacteria. PLoS One. 2015;10(1):e0116896.
   PubMed Web of Science ®Google Scholar
• Schwechheimer C, Kuehn MJ. Outer-membrane vesicles from gram-negative bacteria: biogenesis and functions. Nat Rev Microbiol. 2015;13(10):605–619.
   PubMed Web of Science ®Google Scholar
• Roier S, Zingl FG, Cakar F, et al. Bacterial outer membrane vesicle biogenesis: a new mechanism and its implications. Microb Cell. 2016;3(6):257–259.
   Web of Science ®Google Scholar
• Klimentova J, Stulik J. Methods of isolation and purification of outer membrane vesicles from gram-negative bacteria. Microbiol Res. 2015;170:1–9.
   Web of Science ®Google Scholar
• Dauros Singorenko P, Chang V, Whitcombe A, et al. Isolation of membrane vesicles from prokaryotes: a technical and biological comparison reveals heterogeneity. J Extracell Vesicles. 2017;6(1):1324731.
   PubMed Web of Science ®Google Scholar
• Wiese S, Reidegeld KA, Meyer HE, et al. Protein labeling by iTRAQ: a new tool for quantitative mass spectrometry in proteome research. Proteomics. 2007;7(3):340–350.
   PubMed Web of Science ®Google Scholar
• Knapp S, Hacker J, Jarchau T, et al. Large, unstable inserts in the chromosome affect virulence properties of uropathogenic Escherichia coli O6 strain 536. J Bacteriol. 1986;168(1):22–30.
   Web of Science ®Google Scholar
• Nissle A. Die antagonistische Behandlung chronischer Darmstörungen mit Colibakterien. Med Klin. 1918;2:29–33.
   Google Scholar
• Blenkiron C, Simonov D, Muthukaruppan A, et al. Uropathogenic Escherichia coli releases extracellular vesicles that are associated with RNA. Plos One. 2016;11(8):e0160440.
   PubMed Web of Science ®Google Scholar
• Wessel D, Flugge UI. A method for the quantitative recovery of protein in dilute solution in the presence of detergents and lipids. Anal Biochem. 1984;138(1):141–143.
   PubMed Web of Science ®Google Scholar
• Shilov IV, Seymour SL, Patel AA, et al. The Paragon algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol Cell Proteomics. 2007;6(9):1638–1655.
   PubMed Web of Science ®Google Scholar
• Tang WH, Shilov IV, Seymour SL. Nonlinear fitting method for determining local false discovery rates from decoy database searches. J Proteome Res. 2008;7(9):3661–3667.
   PubMed Web of Science ®Google Scholar
• Vizcaino JA, Csordas A, del-Toro N, et al. 2016 update of the PRIDE database and its related tools. Nucleic Acids Res. 2016;44(D1):D447–D456.
   PubMed Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, et al. Gene ontology: tool for the unification of biology. The gene ontology consortium. Nat Genet. 2000;25(1):25–29.
   PubMed Web of Science ®Google Scholar
• Johnson JR. Virulence factors in Escherichia coli urinary tract infection. Clin Microbiol Rev. 1991;4(1):80–128.
   PubMed Web of Science ®Google Scholar
• Lee J, Kim OY, Gho YS. Proteomic profiling of Gram-negative bacterial outer membrane vesicles: current perspectives. Proteomics Clin Appl. 2016;10(9–10):897–909.
   PubMed Web of Science ®Google Scholar
• Wiles TJ, Kulesus RR, Mulvey MA. Origins and virulence mechanisms of uropathogenic Escherichia coli. Exp Mol Pathol. 2008;85(1):11–19.
   PubMed Web of Science ®Google Scholar
• Sonnenborn U, Schulze J. The non-pathogenic Escherichia coli strain Nissle 1917 – features of a versatile probiotic. Microb Ecol Health Dis. 2009;21(3–4):122–158.
   Google Scholar
• Aseev LV, Boni IV. Extraribosomal functions of bacterial ribosomal proteins. Mol Biol. 2011;45(5):739–750.
   Web of Science ®Google Scholar
• Wang W, Nag S, Zhang X, et al. Ribosomal proteins and human diseases: pathogenesis, molecular mechanisms, and therapeutic implications. Med Res Rev. 2015;35(2):225–285.
   PubMed Web of Science ®Google Scholar
• Grozdanov L, Raasch C, Schulze J, et al. Analysis of the genome structure of the nonpathogenic probiotic Escherichia coli strain Nissle 1917. J Bacteriol. 2004;186(16):5432–5441.
   PubMed Web of Science ®Google Scholar
• Chutkan H, Macdonald I, Manning A, et al. Quantitative and qualitative preparations of bacterial outer membrane vesicles. Methods Mol Biol. 2013;966:259–272.
   PubMedGoogle Scholar
• McBroom AJ, Johnson AP, Vemulapalli S, et al. Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J Bacteriol. 2006;188(15):5385–5392.
   PubMed Web of Science ®Google Scholar
• Bobrie A, Colombo M, Krumeich S, et al. Diverse subpopulations of vesicles secreted by different intracellular mechanisms are present in exosome preparations obtained by differential ultracentrifugation. J Extracell Vesicles. 2012;1:18397.
   PubMedGoogle Scholar
• Clark DJ, Fondrie WE, Liao Z, et al. Redefining the breast cancer exosome proteome by tandem mass tag quantitative proteomics and multivariate cluster analysis. Anal Chem. 2015;87(20):10462–10469.
   PubMed Web of Science ®Google Scholar
• Witwer KW, Buzas EI, Bemis LT, et al. Standardization of sample collection, isolation and analysis methods in extracellular vesicle research. J Extracell Vesicles. 2013;2:20360.
   PubMedGoogle Scholar
• Bai J, Kim SI, Ryu S, et al. Identification and characterization of outer membrane vesicle-associated proteins in Salmonella enterica serovar Typhimurium. Infect Immun. 2014;82(10):4001–4010.
   Web of Science ®Google Scholar
• Lee EY, Bang JY, Park GW, et al. Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics. 2007;7(17):3143–3153.
   PubMed Web of Science ®Google Scholar
• Aguilera L, Toloza L, Gimenez R, et al. Proteomic analysis of outer membrane vesicles from the probiotic strain Escherichia coli Nissle 1917. Proteomics. 2014;14(2–3):222–229.
   Web of Science ®Google Scholar
• Ristow LC, Welch RA. Hemolysin of uropathogenic Escherichia coli: A cloak or a dagger? Biochim Biophys Acta. 2016;1858(3):538–545.
   Web of Science ®Google Scholar
• Balsalobre C, Silvan JM, Berglund S, et al. Release of the type I secreted alpha-haemolysin via outer membrane vesicles from Escherichia coli. Mol Microbiol. 2006;59(1):99–112.
   Web of Science ®Google Scholar
• Fayet O, Ziegelhoffer T, Georgopoulos C. The groES and groEL heat shock gene products of Escherichia coli are essential for bacterial growth at all temperatures. J Bacteriol. 1989;171(3):1379–1385.
   PubMed Web of Science ®Google Scholar
• Kulkarni HM, Nagaraj R, Jagannadham MV. Protective role of E. coli outer membrane vesicles against antibiotics. Microbiol Res. 2015;181:1–7.
   PubMed Web of Science ®Google Scholar
• Bielaszewska M, Ruter C, Bauwens A, et al. Host cell interactions of outer membrane vesicle-associated virulence factors of enterohemorrhagic Escherichia coli O157: intracellular delivery, trafficking and mechanisms of cell injury. PLoS Pathog. 2017;13(2):e1006159.
   PubMed Web of Science ®Google Scholar
• Chan KW, Shone C, Hesp JR. Antibiotics and iron-limiting conditions and their effect on the production and composition of outer membrane vesicles secreted from clinical isolates of extraintestinal pathogenic E. coli. Proteomics Clin Appl. 2017;11(1–2). DOI:10.1002/prca.201600091
   Web of Science ®Google Scholar
• Keenan JI, Allardyce RA. Iron influences the expression of helicobacter pylori outer membrane vesicle-associated virulence factors. Eur J Gastroenterol Hepatol. 2000;12(12):1267–1273.
   Web of Science ®Google Scholar
• Folsom JP, Parker AE, Carlson RP. Physiological and proteomic analysis of Escherichia coli iron-limited chemostat growth. J Bacteriol. 2014;196(15):2748–2761.
   Web of Science ®Google Scholar
• Lim CK, Hassan KA, Tetu SG, et al. The effect of iron limitation on the transcriptome and proteome of pseudomonas fluorescens Pf-5. PLoS One. 2012;7(6):e39139.
   Web of Science ®Google Scholar
• Lima DC, Duarte FT, Medeiros VK, et al. The influence of iron on the proteomic profile of chromobacterium violaceum. BMC Microbiol. 2014;14:267.
   Web of Science ®Google Scholar
• Pieper R, Fisher CR, Suh MJ, et al. Analysis of the proteome of intracellular Shigella flexneri reveals pathways important for intracellular growth. Infect Immun. 2013;81(12):4635–4648.
   PubMed Web of Science ®Google Scholar
• Kagawa W, Sagawa T, Niki H, et al. Structural basis for the DNA-binding activity of the bacterial beta-propeller protein YncE. Acta Crystallogr D Biol Crystallogr. 2011;67(Pt 12):1045–1053.
   Google Scholar
• Wurpel DJ, Moriel DG, Totsika M, et al. Comparative analysis of the uropathogenic Escherichia coli surface proteome by tandem mass-spectrometry of artificially induced outer membrane vesicles. J Proteomics. 2015;115:93–106.
   Web of Science ®Google Scholar
• Wurpel DJ, Totsika M, Allsopp LP, et al. Comparative proteomics of uropathogenic Escherichia coli during growth in human urine identify UCA-like (UCL) fimbriae as an adherence factor involved in biofilm formation and binding to uroepithelial cells. J Proteomics. 2016;131:177–189.
   Web of Science ®Google Scholar
• Moriel DG, Tan L, Goh KG, et al. A novel protective vaccine antigen from the core Escherichia coli genome. mSphere. 2016;1(6):pii: e00326–16.
   Web of Science ®Google Scholar
• McHugh JP, Rodriguez-Quinones F, Abdul-Tehrani H, et al. Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem. 2003;278(32):29478–29486.
   PubMed Web of Science ®Google Scholar
• Sturm A, Schierhorn A, Lindenstrauss U, et al. YcdB from Escherichia coli reveals a novel class of Tat-dependently translocated hemoproteins. J Biol Chem. 2006;281(20):13972–13978.
   Web of Science ®Google Scholar
• Elmi A, Watson E, Sandu P, et al. Campylobacter jejuni outer membrane vesicles play an important role in bacterial interactions with human intestinal epithelial cells. Infect Immun. 2012;80(12):4089–4098.
   Web of Science ®Google Scholar
• Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol. 2013;200(4):373–383.
   PubMed Web of Science ®Google Scholar
• Rowe MC, Withers HL, Swift S. Uropathogenic Escherichia coli forms biofilm aggregates under iron restriction that disperse upon the supply of iron. FEMS Microbiol Lett. 2010;307(1):102–109.
   Web of Science ®Google Scholar
• Fuller HR, Morris GE. Quantitative proteomics using iTRAQ labeling and mass spectrometry. In: Leung HE, editor. Integrative proteomics; 2012. 347–362. London (England): InTechOpen.
   Google Scholar
• Bourassa S, Fournier F, Nehme B, et al. Evaluation of iTRAQ and SWATH-MS for the quantification of proteins associated with insulin resistance in human duodenal biopsy samples. PLoS One. 2015;10(5):e0125934.
   PubMed Web of Science ®Google Scholar
• Yang W, Ding D, Zhang C, et al. iTRAQ-based proteomic profiling of Vibrio parahaemolyticus under various culture conditions. Proteome Sci. 2015;13:19.
   Web of Science ®Google Scholar
• Liang V, Ullrich M, Lam H, et al. Altered proteostasis in aging and heat shock response in C. elegans revealed by analysis of the global and de novo synthesized proteome. Cell Mol Life Sci. 2014;71(17):3339–3361.
   Web of Science ®Google Scholar
• Rhein V, Song X, Wiesner A, et al. Amyloid-beta and tau synergistically impair the oxidative phosphorylation system in triple transgenic Alzheimer’s disease mice. Proc Natl Acad Sci U S A. 2009;106(47):20057–20062.
   PubMed Web of Science ®Google Scholar