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Molecular Pathogenesis

Characterization of the Novel Factor Paa Involved in the Early Steps of the Adhesion Mechanism of Attaching and Effacing Escherichia coli

Isabelle Batisson, Marie-Pierre Guimond, Francis Girard, Hongyan An, Chengru Zhu, Eric Oswald, John M. Fairbrother, Mario Jacques, Josée Harel
Isabelle Batisson
1Laboratoire de Biologie des Protistes, UMR 6023, Université Blaise Pascal, Aubière
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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Marie-Pierre Guimond
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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Francis Girard
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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Hongyan An
3Advantage International USA, Inc., Westport, Connecticut 06880
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Chengru Zhu
4Center for Vaccine Development, Division of Geographic Medicine, University of Maryland School of Medicine, Baltimore, Maryland 21201
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Eric Oswald
5Unité INRA-ENVT de Microbiologie Moléculaire, École Vétérinaire de Toulouse, 31076 Toulouse Cedex, France
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John M. Fairbrother
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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Mario Jacques
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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Josée Harel
2Groupe de Recherche sur les Maladies Infectieuses du Porc, Faculté de Médecine Vétérinaire, Université de Montréal, Saint-Hyacinthe, Québec J2S 7C6, Canada
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  • For correspondence: josee.harel@umontreal.ca
DOI: 10.1128/IAI.71.8.4516-4525.2003
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  • FIG. 1.
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    FIG. 1.

    Light microscopy micrographs of ileal explants inoculated with the wild-type O45 strain 86-1390 (A) or with the LEE-negative strain 862 (B). Strain 86-1390 showed a typical intimate-adherence pattern (arrowheads) with irregularity of the associated epithelial cells, whereas a loose association of bacteria with the intestinal mucosa of some villi with no obvious change in associated epithelial cells (arrow) was observed for negative-control strain 862. Magnification, ×400.

  • FIG. 2.
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    FIG. 2.

    Adherence of wild-type strains and their paa mutant strains. (A) paa mutant strain M155 (n = 18) showed a decreased number of intact ileal villi with bacterial adherence to epithelial cells, compared to wild-type PEPEC strain 86-1390 (n = 12) and to the complemented mutant strain M155c (n = 20). The porcine strain 862 (n = 15), which does not possess the LEE, was used as a negative control. (B) paa mutant strain E22Δpaa (n = 19) showed a decreased number of intact ileal villi compared to wild-type REPEC strain E22 (n = 19) and to the complemented mutant strain E22c (n = 10). Error bars, standard deviations of the means. Asterisk, statistically significant difference (P < 0.0001, when compared by Kruskal-Wallis test) from wild-type strains 86-1390 (A) and E22 (B).

  • FIG. 3.
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    FIG. 3.

    Transmission electron micrographs of ileal explants inoculated with the wild-type O45 strain 86-1390 (A; magnification, ×20,664), the complemented mutant strain M155c (B; magnification, ×20,702), or TnphoA mutant M155 (C; magnification, ×13,500). Typical A/E lesions were observed for both wild-type and complemented-mutant strains, whereas bacteria in the lumen without any direct contact with the epithelium were observed for the mutant M155.

  • FIG. 4.
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    FIG. 4.

    The nucleotide sequence of paa and its flanking sequences and the deduced amino acid sequences. The putative −10 and −35 promoter sites, the ribosome binding site (RBS), and the putative transcription terminator are underlined. The translation initiation codon and the TAG translation termination codon are in boldface. Vertical arrow, potential peptide signal cleavage site; arrowhead, insertion site of TnphoA.

  • FIG. 5.
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    FIG. 5.

    Alignment of the deduced amino acid sequences of the Paa of the 86-1390 strain and the Paa proteins of the O157:H7 EDL933 and Sakai E. coli strains, the AcfC protein of V. cholerae, and the PEB3 protein of C. jejuni. ∗, identical or conserved residues in all sequences in the alignment; colons, conserved substitutions; periods, semiconserved substitutions. The amino acid sequence alignment was performed with the Clustal W program.

  • FIG. 6.
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    FIG. 6.

    Reduction of the percentage of intact villi showing intimate adherence when pig ileal explants are inoculated with PEPEC strain 86-1390 following treatment with anti-Paa antibodies, compared to percentages for explants inoculated with strain 86-1390 following treatment with antibodies from hens immunized with a sonicate preparation from host strain M15(pREP4) (T −). The porcine strain 862, which does not have the LEE, was used as a negative control. Asterisk, statistically significant difference (P < 0.0001, when compared by Kruskal-Wallis tests) from the T (−) treatment.

  • FIG. 7.
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    FIG. 7.

    Transmission electron micrographs showing the uniform distribution of immunogold-labeled Paa protein (arrow) over the bacterial surface of the complemented strain M155c (A) following overnight growth at 37°C in TSB. When anti-Paa serum was adsorbed against the Paa protein, only a few gold beads were observed for strain M155c, mostly in the background (B). Bars = 300 nm.

Tables

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  • TABLE 1.

    Integrity of the yciDE region in paa-positive strains

    Strain typeNo. of strainsa
    TotalyciDE negativebyciDE positive
    EHEC431
    REPEC72 (E22, RDEC-1)5
    PEPEC149 (86-1390)5
    Total2514 (56%)11 (44%)
    • ↵ a Strains considered positive amplified a 1,122-bp fragment, whereas no amplification was seen in the negative strains.

    • ↵ b Strains 86-1390 and E22 were used for testing the role of Paa; RDEC-1 is an REPEC strain.

  • TABLE 2.

    Clinical and histopathological findings in piglets inoculated with porcine E. coli O45 isolates

    StraineNo. of pigs with diarrhea/no. inoculatedOnset of diarrhea (h)bExtent of A/E lesionsdPresence of paa gene
    81-44202/224+++++
    86-13902/230+++++
    91-19-1722/235+++++
    90-20612/239++++
    90-15132/241++++
    88-42991/1a44+++
    86-47332/270++
    83-23152/283++−
    88-18611/1a91−−
    89-56-1961/296−−
    82-43780/2NMc+−
    81-17861/285−−
    • ↵ a One piglet died of causes unrelated to the infection within 20 h after birth.

    • ↵ b Mean time of onset of diarrhea p.i.

    • ↵ c NM, nonmeasurable data.

    • ↵ d ++++, extensive bacterial colonization and severe effacement of microvilli; +++, large areas of bacterial colonization and heavy effacement; ++, focal lesions; +, small scattered focal lesions; −, no lesions observed.

    • ↵ e Strains were eae and LEE positive, except for 81-1786, which was a control eae-negative strain.

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Characterization of the Novel Factor Paa Involved in the Early Steps of the Adhesion Mechanism of Attaching and Effacing Escherichia coli
Isabelle Batisson, Marie-Pierre Guimond, Francis Girard, Hongyan An, Chengru Zhu, Eric Oswald, John M. Fairbrother, Mario Jacques, Josée Harel
Infection and Immunity Jul 2003, 71 (8) 4516-4525; DOI: 10.1128/IAI.71.8.4516-4525.2003

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Characterization of the Novel Factor Paa Involved in the Early Steps of the Adhesion Mechanism of Attaching and Effacing Escherichia coli
Isabelle Batisson, Marie-Pierre Guimond, Francis Girard, Hongyan An, Chengru Zhu, Eric Oswald, John M. Fairbrother, Mario Jacques, Josée Harel
Infection and Immunity Jul 2003, 71 (8) 4516-4525; DOI: 10.1128/IAI.71.8.4516-4525.2003
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KEYWORDS

Adhesins, Escherichia coli
Bacterial Adhesion
Escherichia coli

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