A novel protective vaccine antigen from the core Escherichia coli genome

mSphere

Volumn 1, Issue 6, 2016, Pages

  Moriel, Danilo G ^a,c   Tan, Lendl ^a   K Goh, Kelvin G ^a   Phan, Minh Duy ^a   Ipe, Deepak S ^b   Lo, Alvin W ^a   Peters, Kate M ^a   Ulett, Glen C ^b   Beatson, Scott A ^a   Schembri, Mark A ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

^b GRIFFITH UNIVERSITY   (Australia)

^c GSK   (Italy)

Author keywords

Escherichia coli; Vaccines; Virulence factors

Indexed keywords

EID: 85020872948     PISSN: None     EISSN: 23795042     Source Type: Journal    
DOI: 10.1128/mSphere.00326-16     Document Type: Article

References (57)

1. Rasko DA, Webster DR, Sahl JW, Bashir A, Boisen N, Scheutz F, Paxinos EE, Sebra R, Chin CS, Iliopoulos D, Klammer A, Peluso P, Lee L, Kislyuk AO, Bullard J, Kasarskis A, Wang S, Eid J, Rank D, Redman JC, Steyert SR, Frimodt-Møller J, Struve C, Petersen AM, Krogfelt KA, Nataro JP, Schadt EE, Waldor MK. 2011. Origins of the E. coli strain causing an outbreak of hemolytic-uremic syndrome in Germany. N Engl J Med 365:709-717. http://dx.doi.org/10.1056/NEJMoa1106920
2. Totsika M, Beatson SA, Sarkar S, Phan MD, Petty NK, Bachmann N, Szubert M, Sidjabat HE, Paterson DL, Upton M, Schembri MA. 2011. Insights into a multidrug resistant Escherichia coli pathogen of the globally disseminated ST131 lineage: genome analysis and virulence mechanisms. PLoS One 6:e26578. http://dx.doi.org/10.1371/journal.pone .0026578
3. Peirano G, Bradford PA, Kazmierczak KM, Badal RE, Hackel M, Hoban DJ, Pitout JD. 2014. Global incidence of carbapenemaseproducing Escherichia coli ST131. Emerg Infect Dis 20:1928-1931. http:// dx.doi.org/10.3201/eid2011.141388
4. Kaper JB, Nataro JP, Mobley HL. 2004. Pathogenic Escherichia coli. Nat Rev Microbiol 2:123-140. http://dx.doi.org/10.1038/nrmicro818
5. Didelot X, Méric G, Falush D, Darling AE. 2012. Impact of homologous and non-homologous recombination in the genomic evolution of Escherichia coli. BMC Genomics 13:256. http://dx.doi.org/10.1186/1471-2164-13-256
6. Jaureguy F, Landraud L, Passet V, Diancourt L, Frapy E, Guigon G, Carbonnelle E, Lortholary O, Clermont O, Denamur E, Picard B, Nassif X, Brisse S. 2008. Phylogenetic and genomic diversity of human bacteremic Escherichia coli strains. BMC Genomics 9:560. http:// dx.doi.org/10.1186/1471-2164-9-560
7. von Mentzer A, Connor TR, Wieler LH, Semmler T, Iguchi A, Thomson NR, Rasko DA, Joffre E, Corander J, Pickard D, Wiklund G, Svennerholm AM, Sjöling Å, Dougan G. 2014. Identification of enterotoxigenic Escherichia coli (ETEC) clades with long-term global distribution. Nat Genet 46:1321-1326. http://dx.doi.org/10.1038/ng.3145
8. Wirth T, Falush D, Lan R, Colles F, Mensa P, Wieler LH, Karch H, Reeves PR, Maiden MC, Ochman H, Achtman M. 2006. Sex and virulence in Escherichia coli: an evolutionary perspective. Mol Microbiol 60:1136-1151. http://dx.doi.org/10.1111/j.1365-2958.2006.05172.x
9. Karch H, Denamur E, Dobrindt U, Finlay BB, Hengge R, Johannes L, Ron EZ, Tønjum T, Sansonetti PJ, Vicente M. 2012. The enemy within us: lessons from the 2011 European Escherichia coli O104:H4 outbreak. EMBO Mol Med 4:841-848. http://dx.doi.org/10.1002/emmm .201201662
10. Moriel DG, Rosini R, Seib KL, Serino L, Pizza M, Rappuoli R. 2012. Escherichia coli: great diversity around a common core. mBio 3:e00118-12. http://dx.doi.org/10.1128/mBio.00118-12
11. Clermont O, Gordon D, Denamur E. 2015. Guide to the various phylogenetic classification schemes for Escherichia coli and the correspondence among schemes. Microbiology 161:980-988. http://dx.doi.org/ 10.1099/mic.0.000063
12. Salipante SJ, Roach DJ, Kitzman JO, Snyder MW, Stackhouse B, Butler-Wu SM, Lee C, Cookson BT, Shendure J. 2015. Large-scale genomic sequencing of extraintestinal pathogenic Escherichia coli strains. Genome Res 25:119-128. http://dx.doi.org/10.1101/gr .180190.114
13. Ahmed SA, Awosika J, Baldwin C, Bishop-Lilly KA, Biswas B, Broomall S, Chain PS, Chertkov O, Chokoshvili O, Coyne S, Davenport K, Detter JC, Dorman W, Erkkila TH, Folster JP, Frey KG, George M, Gleasner C, Henry M, Hill KK, Hubbard K, Insalaco J, Johnson S, Kitzmiller A, Krepps M, Lo CC, Luu T, McNew LA, Minogue T, Munk CA, Osborne B, Patel M, Reitenga KG, Rosenzweig CN, Shea A, Shen X, Strockbine N, Tarr C, Teshima H, van Gieson E, Verratti K, Wolcott M, Xie G, Sozhamannan S, Gibbons HS. 2012. Genomic comparison of Escherichia coli O104:H4 isolates from 2009 and 2011 reveals plasmid, and prophage heterogeneity, including Shiga toxin encoding phage stx2. PLoS One 7:e48228. http://dx.doi.org/10.1371/journal.pone .0048228
14. Brzuszkiewicz E, Thürmer A, Schuldes J, Leimbach A, Liesegang H, Meyer FD, Boelter J, Petersen H, Gottschalk G, Daniel R. 2011. Genome sequence analyses of two isolates from the recent Escherichia coli outbreak in Germany reveal the emergence of a new pathotype: entero-aggregative-haemorrhagic Escherichia coli (EAHEC). Arch Microbiol 193:883-891. http://dx.doi.org/10.1007/s00203-011-0725-6
15. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, Prior K, Szczepanowski R, Ji Y, Zhang W, McLaughlin SF, Henkhaus JK, Leopold B, Bielaszewska M, Prager R, Brzoska PM, Moore RL, Guenther S, Rothberg JM, Karch H. 2011. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS One 6:e22751. http://dx.doi.org/10.1371/journal.pone.0022751
16. Toval F, Schiller R, Meisen I, Putze J, Kouzel IU, Zhang W, Karch H, Bielaszewska M, Mormann M, Müthing J, Dobrindt U. 2014. Characterization of urinary tract infection-associated Shiga toxin-producing Escherichia coli. Infect Immun 82:4631-4642. http://dx.doi.org/10.1128/ IAI.01701-14
17. Petty NK, Ben Zakour NL, Stanton-Cook M, Skippington E, Totsika M, Forde BM, Phan MD, Gomes Moriel D, Peters KM, Davies M, Rogers BA, Dougan G, Rodriguez-Baño J, Pascual A, Pitout JD, Upton M, Paterson DL, Walsh TR, Schembri MA, Beatson SA. 2014. Global dissemination of a multidrug resistant Escherichia coli clone. Proc Natl Acad Sci U S A 111:5694-5699. http://dx.doi.org/10.1073/pnas .1322678111
18. Price LB, Johnson JR, Aziz M, Clabots C, Johnston B, Tchesnokova V, Nordstrom L, Billig M, Chattopadhyay S, Stegger M, Andersen PS, Pearson T, Riddell K, Rogers P, Scholes D, Kahl B, Keim P, Sokurenko EV. 2013. The epidemic of extended-spectrum-beta-lactamaseproducing Escherichia coli ST131 is driven by a single highly pathogenic subclone, H30-Rx. mBio 4:e00377-13. http://dx.doi.org/10.1128/mBio .00377-13
19. Luo C, Walk ST, Gordon DM, Feldgarden M, Tiedje JM, Konstantinidis KT. 2011. Genome sequencing of environmental Escherichia coli expands understanding of the ecology and speciation of the model bacterial species. Proc Natl Acad Sci U S A 108:7200-7205. http:// dx.doi.org/10.1073/pnas.1015622108
20. Walk ST, Alm EW, Gordon DM, Ram JL, Toranzos GA, Tiedje JM, Whittam TS. 2009. Cryptic lineages of the genus Escherichia. Appl Environ Microbiol 75:6534-6544. http://dx.doi.org/10.1128/AEM.01262-09
21. Keseler IM, Mackie A, Peralta-Gil M, Santos-Zavaleta A, Gama-Castro S, Bonavides-Martínez C, Fulcher C, Huerta AM, Kothari A, Krummenacker M, Latendresse M, Muñiz-Rascado L, Ong Q, Paley S, Schröder I, Shearer AG, Subhraveti P, Travers M, Weerasinghe D, Weiss V, Collado-Vides J, Gunsalus RP, Paulsen I, Karp PD. 2013. EcoCyc: fusing model organism databases with systems biology. Nucleic Acids Res 41:D605-D612. http://dx.doi.org/10.1093/nar/gks1027
22. Phan MD, Peters KM, Sarkar S, Lukowski SW, Allsopp LP, Moriel DG, Achard ME, Totsika M, Marshall VM, Upton M, Beatson SA, Schembri MA. 2013. The serum resistome of a globally disseminated multidrug resistant uropathogenic clone. PLoS Genet 9:e1003834. http:// dx.doi.org/10.1371/journal.pgen.1003834
23. Blattner FR, Plunkett G, III, Bloch CA, Perna NT, Burland V, Riley M, Collado-Vides J, Glasner JD, Rode CK, Mayhew GF, Gregor J, Davis NW, Kirkpatrick HA, Goeden MA, Rose DJ, Mau B, Shao Y. 1997. The complete genome sequence of Escherichia coli K-12. Science 277: 1453-1462. http://dx.doi.org/10.1126/science.277.5331.1453
24. Njamkepo E, Fawal N, Tran-Dien A, Hawkey J, Strockbine N, Jenkins C, Talukder KA, Bercion R, Kuleshov K, Kolínská R, Russell JE, Kaftyreva L, Accou-Demartin M, Karas A, Vandenberg O, Mather AE, Mason CJ, Page AJ, Ramamurthy T, Bizet C, Gamian A, Carle I, Sow AG, Bouchier C, Wester AL, Lejay-Collin M, Fonkoua MC, Hello SL, Blaser MJ, Jernberg C, Ruckly C, Mérens A, Page AL, Aslett M, Roggentin P, Fruth A, Denamur E, Venkatesan M, Bercovier H, Bodhidatta L, Chiou CS, Clermont D, Colonna B, Egorova S, Pazhani GP, Ezernitchi AV, Guigon G, Harris SR, Izumiya H, Korzeniowska-Kowal A. 2016. Global phylogeography and evolutionary history of Shigella dysenteriae type 1. Nat Microbiol 1:16027. http://dx.doi.org/ 10.1038/nmicrobiol.2016.27
25. Ingle DJ, Tauschek M, Edwards DJ, Hocking DM, Pickard DJ, Azzopardi KI, Amarasena T, Bennett-Wood V, Pearson JS, Tamboura B, Antonio M, Ochieng JB, Oundo J, Mandomando I, Qureshi S, Ramamurthy T, Hossain A, Kotloff KL, Nataro JP, Dougan G, Levine MM, Robins-Browne RM, Holt KE. 2016. Evolution of atypical enteropathogenic E. coli by repeated acquisition of LEE pathogenicity island variants. Nat Microbiol 1:15010. http://dx.doi.org/10.1038/nmicrobiol.2015.10
26. Moriel DG, Bertoldi I, Spagnuolo A, Marchi S, Rosini R, Nesta B, Pastorello I, Corea VA, Torricelli G, Cartocci E, Savino S, Scarselli M, Dobrindt U, Hacker J, Tettelin H, Tallon LJ, Sullivan S, Wieler LH, Ewers C, Pickard D, Dougan G, Fontana MR, Rappuoli R, Pizza M, Serino L. 2010. Identification of protective and broadly conserved vaccine antigens from the genome of extraintestinal pathogenic Escherichia coli. Proc Natl Acad Sci U S A 107:9072-9077. http://dx.doi.org/10.1073/ pnas.0915077107
27. Smith SN, Hagan EC, Lane MC, Mobley HLT. 2010. Dissemination and systemic colonization of uropathogenic Escherichia coli in a murine model of bacteremia. mBio 1:e00262-10. http://dx.doi.org/10.1128/ mBio.00262-10
28. Zhang W, Sack DA. 2012. Progress and hurdles in the development of vaccines against enterotoxigenic Escherichia coli in humans. Expert Rev Vaccines 11:677-694. http://dx.doi.org/10.1586/erv.12.37
29. Horne C, Vallance BA, Deng W, Finlay BB. 2002. Current progress in enteropathogenic and enterohemorrhagic Escherichia coli vaccines. Expert Rev Vaccines 1:483-493. http://dx.doi.org/10.1586/14760584 .1.4.483
30. Garcia-Angulo VA, Kalita A, Torres AG. 2013. Advances in the development of enterohemorrhagic Escherichia coli vaccines using murine models of infection. Vaccine 31:3229-3235. http://dx.doi.org/10.1016/ j.vaccine.2013.05.013
31. Moriel DG, Schembri MA. 2013. Vaccination approaches for the prevention of urinary tract infection. Curr Pharm Biotechnol 14:967-974. http://dx.doi.org/10.2174/1389201014666131226144824
32. Hacker J, Carniel E. 2001. Ecological fitness, genomic islands and bacterial pathogenicity. A Darwinian view of the evolution of microbes. EMBO Rep 2:376-381. http://dx.doi.org/10.1093/embo-reports/kve097
33. Kulp A, Kuehn MJ. 2010. Biological functions and biogenesis of secreted bacterial outer membrane vesicles. Annu Rev Microbiol 64: 163-184. http://dx.doi.org/10.1146/annurev.micro.091208.073413
34. Nesta B, Valeri M, Spagnuolo A, Rosini R, Mora M, Donato P, Alteri CJ, Del Vecchio M, Buccato S, Pezzicoli A, Bertoldi I, Buzzigoli L, Tuscano G, Falduto M, Rippa V, Ashhab Y, Bensi G, Fontana MR, Seib KL, Mobley HL, Pizza M, Soriani M, Serino L. 2014. SslE elicits functional antibodies that impair in vitro mucinase activity and in vivo colonization by both intestinal and extraintestinal Escherichia coli strains. PLoS Pathog 10:e1004124. http://dx.doi.org/10.1371/journal.ppat .1004124
35. Webb CT, Selkrig J, Perry AJ, Noinaj N, Buchanan SK, Lithgow T. 2012. Dynamic association of BAM complex modules includes surface exposure of the lipoprotein BamC. J Mol Biol 422:545-555. http:// dx.doi.org/10.1016/j.jmb.2012.05.035
36. Baba-Dikwa A, Thompson D, Spencer NJ, Andrews SC, Watson KA. 2008. Overproduction, purification and preliminary X-ray diffraction analysis of YncE, an iron-regulated Sec-dependent periplasmic protein from Escherichia coli. Acta Crystallogr Sect F Struct Biol Cryst Commun 64:966-969. http://dx.doi.org/10.1107/S1744309108029515
37. Baars L, Ytterberg AJ, Drew D, Wagner S, Thilo C, van Wijk KJ, de Gier JW. 2006. Defining the role of the Escherichia coli chaperone SecB using comparative proteomics. J Biol Chem 281:10024-10034. http:// dx.doi.org/10.1074/jbc.M509929200
38. Kagawa W, Sagawa T, Niki H, Kurumizaka H. 2011. Structural basis for the DNA-binding activity of the bacterial beta-propeller protein YncE. Acta Crystallogr D Biol Crystallogr 67:1045-1053. http://dx.doi.org/ 10.1107/S0907444911045033
39. Wurpel DJ, Moriel DG, Totsika M, Easton DM, Schembri MA. 2014. Comparative analysis of the uropathogenic Escherichia coli surface proteome by tandem mass-spectrometry of artificially induced outer membrane vesicles. J Proteomics 115:93-106. http://dx.doi.org/10.1016/ j.jprot.2014.12.005
40. McHugh JP, Rodríguez-Quinoñes F, Abdul-Tehrani H, Svistunenko DA, Poole RK, Cooper CE, Andrews SC. 2003. Global iron-dependent gene regulation in Escherichia coli. A new mechanism for iron homeostasis. J Biol Chem 278:29478-29486. http://dx.doi.org/10.1074/ jbc.M303381200
41. Hays MP, Ericsson AC, Yang Y, Hardwidge PR. 2016. Vaccinating with conserved Escherichia coli antigens does not alter the mouse intestinal microbiome. BMC Res Notes 9:401. http://dx.doi.org/10.1186/s13104-016-2208-y
42. Pearson WR, Wood T, Zhang Z, Miller W. 1997. Comparison of DNA sequences with protein sequences. Genomics 46:24-36. http:// dx.doi.org/10.1006/geno.1997.4995
43. Yu NY, Wagner JR, Laird MR, Melli G, Rey S, Lo R, Dao P, Sahinalp SC, Ester M, Foster LJ, Brinkman FS. 2010. PSORTb 3.0: improved protein subcellular localization prediction with refined localization subcategories and predictive capabilities for all prokaryotes. Bioinformatics 26: 1608-1615. http://dx.doi.org/10.1093/bioinformatics/btq249
44. Juncker AS, Willenbrock H, Von Heijne G, Brunak S, Nielsen H, Krogh A. 2003. Prediction of lipoprotein signal peptides in Gramnegative bacteria. Protein Sci 12:1652-1662. http://dx.doi.org/10.1110/ ps.0303703
45. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 4:363-371. http:// dx.doi.org/10.1038/nprot.2009.2
46. Clermont O, Bonacorsi S, Bingen E. 2000. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl Environ Microbiol 66:4555-4558. http://dx.doi.org/10.1128/AEM.66.10.4555-4558.2000
47. Escobar-Páramo P, Le Menac'h A, Le Gall T, Amorin C, Gouriou S, Picard B, Skurnik D, Denamur E. 2006. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ Microbiol 8:1975-1984. http://dx.doi.org/ 10.1111/j.1462-2920.2006.01077.x
48. Clermont O, Christenson JK, Denamur E, Gordon DM. 2013. The Clermont Escherichia coli phylo-typing method revisited: improvement of specificity and detection of new phylo-groups. Environ Microbiol Rep 5:58-65. http://dx.doi.org/10.1111/1758-2229.12019
49. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol 30:2725-2729. http://dx.doi.org/10.1093/molbev/mst197
50. Krzywinski M, Schein J, Birol I, Connors J, Gascoyne R, Horsman D, Jones SJ, Marra MA. 2009. Circos: an information aesthetic for compar-ative genomics. Genome Res 19:1639-1645. http://dx.doi.org/10.1101/ gr.092759.109
51. Moriel DG, Beatson SA, Wurpel DJ, Lipman J, Nimmo GR, Paterson DL, Schembri MA. 2013. Identification of novel vaccine candidates against multidrug-resistant Acinetobacter baumannii. PLoS One 8:e77631. http://dx.doi.org/10.1371/journal.pone.0077631
52. Donnelly MI, Zhou M, Millard CS, Clancy S, Stols L, Eschenfeldt WH, Collart FR, Joachimiak A. 2006. An expression vector tailored for large-scale, high-throughput purification of recombinant proteins. Protein Expr Purif 47:446-454. http://dx.doi.org/10.1016/j.pep.2005.12.011
53. Allsopp LP, Beloin C, Ulett GC, Valle J, Totsika M, Sherlock O, Ghigo JM, Schembri MA. 2012. Molecular characterization of UpaB and UpaC, two new autotransporter proteins of uropathogenic Escherichia coli CFT073. Infect Immun 80:321-332. http://dx.doi.org/10.1128/IAI.05322-11
54. Nichols KB, Totsika M, Moriel DG, Lo AW, Yang J, Wurpel DJ, Rossiter AE, Strugnell RA, Henderson IR, Ulett GC, Beatson SA, Schembri MA. 2016. Molecular characterisation of the vacuolating autotransporter toxin in uropathogenic Escherichia coli. J Bacteriol 198: 1487-1498. http://dx.doi.org/10.1128/JB.00791-15
55. Kakkanat A, Totsika M, Schaale K, Duell BL, Lo AW, Phan MD, Moriel DG, Beatson SA, Sweet MJ, Ulett GC, Schembri MA. 2015. The role of H4 flagella in Escherichia coli ST131 virulence. Sci Rep 5:16149. http:// dx.doi.org/10.1038/srep16149
56. Studier FW. 2005. Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41:207-234. http://dx.doi.org/ 10.1016/j.pep.2005.01.016
57. Brumbaugh AR, Smith SN, Mobley HL. 2013. Immunization with the yersiniabactin receptor, FyuA, protects against pyelonephritis in a murine model of urinary tract infection. Infect Immun 81:3309-3316. http:// dx.doi.org/10.1128/IAI.00470-13