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Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37.

Kai-Larsen Y, Lüthje P, Chromek M, Peters V, Wang X, Holm A, Kádas L, Hedlund KO, Johansson J, Chapman MR, Jacobson SH, Römling U, Agerberth B, Brauner A - PLoS Pathog. (2010)

Bottom Line: Our results suggest that curli and cellulose exhibit differential and complementary functions.Cellulose production, on the other hand, reduced immune induction and hence delayed bacterial elimination from the kidneys.Thus, even relatively low concentrations of LL-37 inhibited curli-mediated biofilm formation in vitro.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden.

ABSTRACT
Bacterial growth in multicellular communities, or biofilms, offers many potential advantages over single-cell growth, including resistance to antimicrobial factors. Here we describe the interaction between the biofilm-promoting components curli fimbriae and cellulose of uropathogenic E. coli and the endogenous antimicrobial defense in the urinary tract. We also demonstrate the impact of this interplay on the pathogenesis of urinary tract infections. Our results suggest that curli and cellulose exhibit differential and complementary functions. Both of these biofilm components were expressed by a high proportion of clinical E. coli isolates. Curli promoted adherence to epithelial cells and resistance against the human antimicrobial peptide LL-37, but also increased the induction of the proinflammatory cytokine IL-8. Cellulose production, on the other hand, reduced immune induction and hence delayed bacterial elimination from the kidneys. Interestingly, LL-37 inhibited curli formation by preventing the polymerization of the major curli subunit, CsgA. Thus, even relatively low concentrations of LL-37 inhibited curli-mediated biofilm formation in vitro. Taken together, our data demonstrate that biofilm components are involved in the pathogenesis of urinary tract infections by E. coli and can be a target of local immune defense mechanisms.

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Biofilm expression by uropathogenic and fecal E. coli isolates.(A) Adhesion capacity and thickness of biofilm produced by E. coli isolates collected from urine of patients with urinary tract infections (UTI, n = 99) and from fecal samples of healthy individuals (Fecal, n = 77) was measured. Individual values and medians are presented, depicted as optical density (OD) at 570 nm after dissolution of crystal violet. The difference is significant (P<0.0001, Mann-Whitney U test). (B) Isolates from urine samples were investigated by electron microscopy. The left image shows an overview, the right image is a magnification showing immunogold-labelled curli. The scale bars show 0.5 µm (left) and 100 nm (right), respectively.
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ppat-1001010-g001: Biofilm expression by uropathogenic and fecal E. coli isolates.(A) Adhesion capacity and thickness of biofilm produced by E. coli isolates collected from urine of patients with urinary tract infections (UTI, n = 99) and from fecal samples of healthy individuals (Fecal, n = 77) was measured. Individual values and medians are presented, depicted as optical density (OD) at 570 nm after dissolution of crystal violet. The difference is significant (P<0.0001, Mann-Whitney U test). (B) Isolates from urine samples were investigated by electron microscopy. The left image shows an overview, the right image is a magnification showing immunogold-labelled curli. The scale bars show 0.5 µm (left) and 100 nm (right), respectively.

Mentions: A total of 99 E. coli isolates were collected from urine of patients with UTI and 77 isolates were obtained from fecal samples of healthy individuals. Each isolate was assessed for biofilm formation using a standard microtiter assay (see Materials and Methods). On average, uropathogenic bacteria adhered significantly better and formed more biofilm as compared to fecal isolates (P<0.0001, Figure 1A).


Uropathogenic Escherichia coli modulates immune responses and its curli fimbriae interact with the antimicrobial peptide LL-37.

Kai-Larsen Y, Lüthje P, Chromek M, Peters V, Wang X, Holm A, Kádas L, Hedlund KO, Johansson J, Chapman MR, Jacobson SH, Römling U, Agerberth B, Brauner A - PLoS Pathog. (2010)

Biofilm expression by uropathogenic and fecal E. coli isolates.(A) Adhesion capacity and thickness of biofilm produced by E. coli isolates collected from urine of patients with urinary tract infections (UTI, n = 99) and from fecal samples of healthy individuals (Fecal, n = 77) was measured. Individual values and medians are presented, depicted as optical density (OD) at 570 nm after dissolution of crystal violet. The difference is significant (P<0.0001, Mann-Whitney U test). (B) Isolates from urine samples were investigated by electron microscopy. The left image shows an overview, the right image is a magnification showing immunogold-labelled curli. The scale bars show 0.5 µm (left) and 100 nm (right), respectively.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2908543&req=5

ppat-1001010-g001: Biofilm expression by uropathogenic and fecal E. coli isolates.(A) Adhesion capacity and thickness of biofilm produced by E. coli isolates collected from urine of patients with urinary tract infections (UTI, n = 99) and from fecal samples of healthy individuals (Fecal, n = 77) was measured. Individual values and medians are presented, depicted as optical density (OD) at 570 nm after dissolution of crystal violet. The difference is significant (P<0.0001, Mann-Whitney U test). (B) Isolates from urine samples were investigated by electron microscopy. The left image shows an overview, the right image is a magnification showing immunogold-labelled curli. The scale bars show 0.5 µm (left) and 100 nm (right), respectively.
Mentions: A total of 99 E. coli isolates were collected from urine of patients with UTI and 77 isolates were obtained from fecal samples of healthy individuals. Each isolate was assessed for biofilm formation using a standard microtiter assay (see Materials and Methods). On average, uropathogenic bacteria adhered significantly better and formed more biofilm as compared to fecal isolates (P<0.0001, Figure 1A).

Bottom Line: Our results suggest that curli and cellulose exhibit differential and complementary functions.Cellulose production, on the other hand, reduced immune induction and hence delayed bacterial elimination from the kidneys.Thus, even relatively low concentrations of LL-37 inhibited curli-mediated biofilm formation in vitro.

View Article: PubMed Central - PubMed

Affiliation: Department of Medical Biochemistry and Biophysics, Karolinska Institutet, Stockholm, Sweden.

ABSTRACT
Bacterial growth in multicellular communities, or biofilms, offers many potential advantages over single-cell growth, including resistance to antimicrobial factors. Here we describe the interaction between the biofilm-promoting components curli fimbriae and cellulose of uropathogenic E. coli and the endogenous antimicrobial defense in the urinary tract. We also demonstrate the impact of this interplay on the pathogenesis of urinary tract infections. Our results suggest that curli and cellulose exhibit differential and complementary functions. Both of these biofilm components were expressed by a high proportion of clinical E. coli isolates. Curli promoted adherence to epithelial cells and resistance against the human antimicrobial peptide LL-37, but also increased the induction of the proinflammatory cytokine IL-8. Cellulose production, on the other hand, reduced immune induction and hence delayed bacterial elimination from the kidneys. Interestingly, LL-37 inhibited curli formation by preventing the polymerization of the major curli subunit, CsgA. Thus, even relatively low concentrations of LL-37 inhibited curli-mediated biofilm formation in vitro. Taken together, our data demonstrate that biofilm components are involved in the pathogenesis of urinary tract infections by E. coli and can be a target of local immune defense mechanisms.

Show MeSH
Related in: MedlinePlus