A subset of mucosa-associated Escherichia coli isolates from patients with colon cancer, but not Crohn's disease, share pathogenicity islands with urinary pathogenic E. coli
Adherent and invasive mucosa-associated Escherichia coli have been implicated in the pathogenesis of colon cancer and inflammatory bowel diseases. It has been reported that such isolates share features of extraintestinal E. coli (ExPEC) and particularly uropathogenic E. coli (UPEC). We used suppression subtractive hybridization (SSH) to subtract the genome of E. coli K-12 from that of a colon cancer mucosal E. coli isolate. Of the subtracted sequences, 53 % were present in the genomes of one or more of three sequenced UPEC strains but absent from the genome of an enterohaemorrhagic E. coli (EHEC) strain. Of the subtracted sequences, 80 % matched at least one UPEC genome, whereas only 4 % were absent from the UPEC genomes but present in the genome of the EHEC strain. A further genomic subtraction against the UPEC strain 536 enriched for sequences matching mobile genetic elements, other ExPEC strains, and other UPEC strains or commensals, rather than strains associated with gastrointestinal disease. We analysed the distribution of selected subtracted sequences and UPEC-associated pathogenicity islands (PAIs) amongst a panel of mucosa-associated E. coli isolated from colonoscopic biopsies of patients with colon cancer, patients with Crohn's disease and controls. This enabled us to identify a group of isolates from colon cancer (30–40 %) carrying multiple genes previously categorized as UPEC-specific and implicated in virulence.
BarnichN.,
BringerM. A.,
ClaretL.,
Darfeuille-MichaudA.2004; Involvement of lipoprotein NlpI in the virulence of adherent invasive Escherichia coli strain LF82 isolated from a patient with Crohn's disease. Infect Immun 72:2484–2493
BrzuszkiewiczE.,
BruggemannH.,
LiesegangH.,
EmmerthM.,
OlschlagerT.,
NagyG.,
AlbermannK.,
WagnerC.,
BuchrieserC.other authors2006; How to become a uropathogen: comparative genomic analysis of extraintestinal pathogenic Escherichia coli strains. Proc Natl Acad Sci U S A 103:12879–12884
ChenS. L.,
HungC. S.,
XuJ.,
ReigstadC. S.,
MagriniV.,
SaboA.,
BlasiarD.,
BieriT.,
MeyerR. R.other authors2006; Identification of genes subject to positive selection in uropathogenic strains of Escherichia coli : a comparative genomics approach. Proc Natl Acad Sci U S A 103:5977–5982
DobrindtU.,
Blum-OehlerG.,
NagyG.,
SchneiderG.,
JohannA.,
GottschalkG.,
HackerJ.2002; Genetic structure and distribution of four pathogenicity islands (PAI I536 to PAI IV536) of uropathogenic Escherichia coli strain 536. Infect Immun 70:6365–6372
EwersC.,
LiG.,
WilkingH.,
KiebetalingS.,
AltK.,
AntaoE. M.,
LaturnusC.,
DiehlI.,
GloddeS.other authors2007; Avian pathogenic, uropathogenic, and newborn meningitis-causing Escherichia coli : how closely related are they?. Int J Med Microbiol 297:163–176
GretenF. R.,
EckmannL.,
GretenT. F.,
ParkJ. M.,
LiZ. W.,
EganL. J.,
KagnoffM. F.,
KarinM.2004; IKK β links inflammation and tumorigenesis in a mouse model of colitis-associated cancer. Cell 118:285–296
GuyerD. M.,
KaoJ. S.,
MobleyH. L.1998; Genomic analysis of a pathogenicity island in uropathogenic Escherichia coli CFT073: distribution of homologous sequences among isolates from patients with pyelonephritis, cystitis, and catheter-associated bacteriuria and from fecal samples. Infect Immun 66:4411–4417
JohnsonJ. R.,
StellA. L.2000; Extended virulence genotypes of Escherichia coli strains from patients with urosepsis in relation to phylogeny and host compromise. J Infect Dis 181:261–272
JohnsonJ. R.,
BrownJ. J.,
MaslowJ. N.1998; Clonal distribution of the three alleles of the Gal( α 1–4)Gal-specific adhesin gene papG among Escherichia coli strains from patients with bacteremia. J Infect Dis 177:651–661
JohnsonJ. R.,
ScheutzF.,
UllerydP.,
KuskowskiM. A.,
O'BryanT. T.,
SandbergT.2005; Phylogenetic and pathotypic comparison of concurrent urine and rectal Escherichia coli isolates from men with febrile urinary tract infection. J Clin Microbiol 43:3895–3900
KotlowskiR.,
BernsteinC. N.,
SepehriS.,
KrauseD. O.2007; High prevalence of Escherichia coli belonging to the B2+D phylogenetic group in inflammatory bowel disease. Gut 56:669–675
OelschlaegerT. A.,
DobrindtU.,
HackerJ.2002a; Pathogenicity islands of uropathogenic E. coli and the evolution of virulence. Int J Antimicrob Agents 19:517–521
RaskoD. A.,
PhillipsJ. A.,
LiX.,
MobleyH. L.2001; Identification of DNA sequences from a second pathogenicity island of uropathogenic Escherichia coli CFT073: probes specific for uropathogenic populations. J Infect Dis 184:1041–1049
Rodriguez-SiekK. E.,
GiddingsC. W.,
DoetkottC.,
JohnsonT. J.,
FakhrM. K.,
NolanL. K.2005; Comparison of Escherichia coli isolates implicated in human urinary tract infection and avian colibacillosis. Microbiology 151:2097–2110
RolhionN.,
CarvalhoF. A.,
Darfeuille-MichaudA.2007; OmpC and the σ E regulatory pathway are involved in adhesion and invasion of the Crohn's disease-associated Escherichia coli strain LF82. Mol Microbiol 63:1684–1700
RyanP.,
KellyR. G.,
LeeG.,
CollinsJ. K.,
O'SullivanG. C.,
O'ConnellJ.,
ShanahanF.2004; Bacterial DNA within granulomas of patients with Crohn's disease – detection by laser capture microdissection and PCR. Am J Gastroenterol 99:1539–1543
SimpsonK. W.,
DoganB.,
RishniwM.,
GoldsteinR. E.,
KlaessigS.,
McDonoughP. L.,
GermanA. J.,
YatesR. M.,
RussellD. G.other authors2006; Adherent and invasive Escherichia coli is associated with granulomatous colitis in boxer dogs. Infect Immun 74:4778–4792
WelchR. A.,
BurlandV.,
PlunkettG.III,
RedfordP.,
RoeschP.,
RaskoD.,
BucklesE. L.,
LiouS. R.,
BoutinA.other authors2002; Extensive mosaic structure revealed by the complete genome sequence of uropathogenic Escherichia coli . Proc Natl Acad Sci U S A 99:17020–17024
WulltB.,
BergstenG.,
ConnellH.,
RollanoP.,
GebretsadikN.,
HullR.,
SvanborgC.2000; P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract. Mol Microbiol 38:456–464
WulltB.,
BergstenG.,
SamuelssonM.,
SvanborgC.2002; The role of P fimbriae for Escherichia coli establishment and mucosal inflammation in the human urinary tract. Int J Antimicrob Agents 19:522–538
A subset of mucosa-associated Escherichia coli isolates from patients with colon cancer, but not Crohn's disease, share pathogenicity islands with urinary pathogenic E. coli