Effect of pap copy number and receptor specificity on virulence of fimbriated Escherichia coli in a murine urinary tract colonization model

Hull, Richard A.; Nowicki, B.; Kaul, Anil; Runyan, Rebecca; Svanborg, Catharina; Hull, Sheila I.

doi:10.1006/mpat.1994.1054

Cited by 10 publications

(13 citation statements)

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“…1). These results are consistent with previous reports that transurethral inoculation of E. coli that express P fimbriae (Pϩ) results in increased amount of bacterial infection and a persistence to a greater amount than inoculation with equal amounts of the isogenic strain of E. coli without P fimbriae (PϪ) in the mouse UTI model in LPS-sensitive (C3H/HeN) mice as reported for LPS-insensitive (C3H/HeJ) mice (23,24,29). Hence, the persistence of P(ϩ) E. coli infection of the kidney may be due, in part, to the combined effects of the adhesion properties of P fimbriae and the ability of E. coli that express P fimbriae to impair IgA transport into the urinary space.…”

Section: Discussionsupporting

confidence: 93%

“…Animals were infused with 50 to 80 l of one of the following solutions through the urethra into the bladder via microbore tubing (Tygon; Fisher, Pittsburgh, PA) with: (1) PBS only (control); (2) 1 ϫ 10 8 E. coli bearing P fimbriae plasmid (Pϩ) in PBS; or (3) 1 ϫ 10 8 of the same strain E. coli bearing plasmid without P fimbriae (PϪ) in PBS (23). Three groups of mice were studied at 6, 24, or 48 h after infusion with either PBS or E. coli in PBS.…”

Section: Establishment Of Pyelonephritismentioning

confidence: 99%

“…All of the bacterial strains are derivatives of E. coli FN506, a nonadherent fecal strain (24). This strain of E. coli was transformed with either high copy number of the pBR322 recombinant plasmid encoding pap-1 (Pϩ) or the same plasmid without the pap-1 fimbriae (PϪ) (23). E. coli bacteria were grown overnight at 37°C on Luria agar, and the presence or absence of the P fimbriae expression on the strains was confirmed before bladder inoculation by the hemagglutination of 3% human blood cells that express the P antigen; E. coli express the P antigen P(ϩ) agglutinate human blood cells, whereas E. coli that lack the P antigen P(Ϫ) do not agglutinate human blood cells.…”

Section: Bacterial Culture and Induction Of Ascending Pyelonephritismentioning

confidence: 99%

“…Bacterial infection of the upper urinary tract (pyelonephritis) was confirmed by culturing kidney homogenate and quantified by determining the number of CFU of bacteria per gram of whole kidney tissue as described (23). Results are reported as the mean CFU per gram of kidney tissue homogenate on two to three separate cultures.…”

Section: Quantification Of Bacteria In Kidney Tissue Homogenatementioning

confidence: 99%

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Pyelonephritic Escherichia coli Expressing P Fimbriae Decrease Immune Response of the Mouse Kidney

Rice¹,

Peng²,

Spence³

et al. 2005

Journal of the American Society of Nephrology

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P fimbriae are proteinaceous appendages on the surface of Escherichia coli bacteria that mediate adherence to uroepithelial cells. E. coli that express P fimbriae account for the majority of ascending urinary tract infections in women with normal urinary tracts. The hypothesis that P fimbriae on uropathic E. coli attach to renal epithelia and may regulate the immune response to establish infection was investigated. The polymeric Ig receptor (pIgR), produced by renal epithelia, transports IgA into the urinary space. Kidney pIgR and urine IgA levels were analyzed in a mouse model of ascending pyelonephritis, using E. coli with (P؉) and without (P؊) P fimbriae, to determine whether P(؉) E. coli regulate epithelial pIgR expression and IgA transport into the urine. (P؉) E. coli establish infection and persist to a greater amount than P(؊) E. coli. P(؉)-infected mice downregulate pIgR mRNA and protein levels compared with P(؊)-infected or PBS controls at >48 h. The decrease in pIgR was associated with decreased urinary IgA levels in the P(؉)-infected group at 48 h. pIgR mRNA and protein also decline in P(؉) E. coli-infected LPS-hyporesponsive mice. These studies identify a novel virulence mechanism of E. coli that express P fimbriae. It is proposed that P fimbriae decrease pIgR expression in the kidney and consequently decrease IgA transport into the urinary space. This may explain, in part, how E. coli that bear P fimbriae exploit the immune system of human hosts to establish ascending pyelonephritis. Escherichia coli that express P fimbriae are the most common cause for upper urinary tract infections (UTI) or pyelonephritis (1). The P fimbriae mediate adherence to uroepithelial cells by binding to the Gal␣(1 to 4)Gal disaccharide on the apical surface of renal epithelial cells, glomeruli, and endothelia (2). The expression of P fimbriae on E. coli is important in establishing pyelonephritis, as P fimbriae-specific antibodies prevent the adherence of bacteria to uroepithelial cells in vitro (3) and protect animals from ascending E. coli pyelonephritis in vivo (4). Although P fimbriae are not the sole virulence factor on uropathic E. coli, pyelonephritis with P(ϩ) E. coli strains are more often associated with kidney histopathology than P(Ϫ) E. coli (5). In addition to its role as an adhesin, E. coli that express P fimbriae may determine the pattern of the local immune response via interaction with its P-specific glycosphingolipid receptors present on uroepithelial cells (6) and/or by signaling via inflammatory cytokines (7).The secretions that protect the mucosal surface of renal epithelia contain an array of host defense factors, including secretory immunoglobulins, of which IgA is the major class. The polymeric Ig receptor (pIgR) is responsible for transporting these secretory immunoglobulins (S-Ig) in vesicles from the basolateral to the apical surface of epithelial cells (8 -10), including renal tubule cells. The extracellular portion of the pIgR, termed secretory component (SC), is cleaved at the apical surface ...

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Section: Discussionsupporting

confidence: 93%

Section: Establishment Of Pyelonephritismentioning

confidence: 99%

Section: Bacterial Culture and Induction Of Ascending Pyelonephritismentioning

confidence: 99%

Section: Quantification Of Bacteria In Kidney Tissue Homogenatementioning

confidence: 99%

See 2 more Smart Citations

Pyelonephritic Escherichia coli Expressing P Fimbriae Decrease Immune Response of the Mouse Kidney

Rice¹,

Peng²,

Spence³

et al. 2005

Journal of the American Society of Nephrology

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“…The asymptomatic group contained the highest number of isolates that did not demonstrate MRHA, 31?25 %, while only 7?70 % of the cystitis and 14?29 % of the pyelonephritis isolates did not show MRHA. There was significant positive correlation between the level of MRHA and the number of P clusters for the isolates, Pearson correlation (r 2 ) of 0?321, P=0?023, showing that those isolates with more P clusters tended to show an increased level of MRHA, as expected from other studies (Blanco et al, 1997;Hull et al, 1994). It should be noted that although the use of human RBCs alone limits recognition to functional expression of PapG class II, since PapG class III binds preferentially to the Forssman antigen present in other species (Marklund et al, 1992), the majority of isolates were positive for agglutination, so MRHA with human RBCs was judged to be sufficient for the purposes of this study.…”

Section: Deletion Of P-related Fimbrial Clusters In the Clinical Isolsupporting

confidence: 83%

Demonstration of regulatory cross-talk between P fimbriae and type 1 fimbriae in uropathogenic Escherichia coli

et al. 2006

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The majority of Escherichia coli strains isolated from urinary tract infections have the potential to express multiple fimbriae. Two of the most common fimbrial adhesins are type 1 fimbriae and pyelonephritis-associated pili (Pap). Previous research has shown that induced, plasmid-based expression of a Pap regulator, papB, and its close homologues can prevent inversion of the fim switch controlling the expression of type 1 fimbriae. The aim of the present study was to determine if this cross-regulation occurs when PapB is expressed from its native promoter in the chromosome of E. coli K-12 and clinical isolates. The regulation was examined in three ways: (1) mutated alleles of the pap regulatory region, including papB and papI, that maintain the pap promoter in either the off or the on phase were exchanged into the chromosome of both E. coli K-12 and the clinical isolate E. coli CFT073, and the effect on type 1 fimbrial expression was measured; (2) type 1 fimbrial expression was determined using a novel fimS : : gfp + reporter system in mutants of the clinical isolate E. coli 536 in which combinations of complete fimbrial clusters had been deleted; (3) type 1 fimbrial expression was determined in a range of clinical isolates and compared with both the number of P clusters and their expression. All three approaches demonstrated that P expression represses type 1 fimbrial expression. Using a number of novel genetic approaches, this work extends the initial finding that PapB inhibits FimB recombination to the impact of this regulation in clinical isolates. INTRODUCTIONUrinary tract infections (UTIs) are common, affecting a large proportion of the population. It is estimated that 20 % of women develop a UTI in their lifetime, and antibiotic treatment results in approximately 110 000 prescriptions per million inhabitants per annum in Europe (Naber, 2000). Escherichia coli strains are the predominant cause of uncomplicated UTIs, responsible for between 60 and 80 % of the cases reported in the UK each year (Graham & Galloway, 2001). Many infections are asymptomatic, especially in the elderly (Nicolle, 2001), but others result in cystitis. If the infection ascends to the kidney, then pyelonephritis can occur. Such infections are a significant origin of Gramnegative sepsis.Fimbrial adhesins are important virulence factors that allow binding of the bacteria to specific receptors on epithelial cells of the urinary tract. The two adhesins most commonly associated with UTI are type 1 fimbriae, and pyelonephritisassociated pili (Pap) and Pap-related fimbriae (Prf); the last two are collectively termed P fimbriae in this study. Type 1 fimbriae mediate binding to a-D-mannose-containing receptors and extracellular matrix components, whereas P fimbriae bind to glycoreceptors containing the aGal(1-4)bGal moiety (Lindberg et al., 1984). Although type 1 fimbriae are common to the majority of E. coli isolates, the FimH adhesin has been shown to be important in a mouse model of UTI, and a degranulation response to the fimbriae is asso...

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P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract

Wullt

Bergsten

Connell

et al. 2000

Molecular Microbiology

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SummaryThis study examined the role of P fimbriae in the establishment of bacteriuria. Patients (n 17) were subjected to intravesical inoculation with an asymptomatic bacteriuria strain, Escherichia coli 83972, or its P-fimbriated (pap 1 /prs 1 ) transformants. As shown by groupwise analysis, the pap 1 /prs 1 transformants established bacteriuria more rapidly than E. coli 83972 (P 0.021) and required a lower number of inoculations to reach 10 5 cfu ml 21 (P 0.018). Intraindividual analysis showed that the pap 1 /prs 1 transformants established bacteriuria more rapidly than E. coli 83972 in the patients who subsequently became carriers of both strains. Finally, bacterial establishment was shown to vary with the in vivo expression of P fimbriae. Bacterial counts were higher when P-fimbrial expression was detected than when the pap 1 /prs 1 strain showed a negative phenotype. The results suggested that P fimbriae enhance the establishment of bacteriuria and fulfil the molecular Koch postulates as a colonization factor in the human urinary tract.

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Effect of pap copy number and receptor specificity on virulence of fimbriated Escherichia coli in a murine urinary tract colonization model

Cited by 10 publications

References 0 publications

Pyelonephritic Escherichia coli Expressing P Fimbriae Decrease Immune Response of the Mouse Kidney

Pyelonephritic Escherichia coli Expressing P Fimbriae Decrease Immune Response of the Mouse Kidney

Demonstration of regulatory cross-talk between P fimbriae and type 1 fimbriae in uropathogenic Escherichia coli

P fimbriae enhance the early establishment of Escherichia coli in the human urinary tract

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