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Infect Immun, April 1998, p. 1570-1578, Vol. 66, No. 4
0019-9567/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Role of Intimin and Bundle-Forming Pili in
Enteropathogenic Escherichia coli Adhesion to Pediatric
Intestinal Tissue In Vitro
Susan
Hicks,1
Gad
Frankel,2
James B.
Kaper,3
Gordon
Dougan,2 and
Alan
D.
Phillips1,*
University Department of Paediatric
Gastroenterology, Royal Free Hospital, London, NW3
2QG,1 and
Department of
Biochemistry, Imperial College of Science, Technology, and
Medicine, London, SW7 2AZ,2 United Kingdom,
and
Center for Vaccine Development, Baltimore, Maryland,
212013
Received 8 October 1997/Returned for modification 13 November
1997/Accepted 22 January 1998
Attaching and effacing (A/E) lesion formation is central to
enteropathogenic Escherichia coli (EPEC) pathogenesis.
In vitro experiments with human epithelial cell lines have implicated
virulence plasmid-encoded bundle-forming pili (BFP) in initial
binding and intimin in intimate attachment and A/E lesion formation.
This study investigated the role of BFP and intimin in EPEC
interactions with pediatric small intestinal biopsy tissue in in vitro
organ culture. Organ culture infections (2 to 8 h) were performed
with E2348/69 (a wild-type EPEC O127:H6 clinical isolate) and
E2348/69 derivatives including CVD206 (eae deficient),
CVD206(pCVD438) (eae-complemented CVD206),
CVD206(pCVD438/01) (expressing intimin, which is nonfunctional due
to a single amino acid substitution), JPN15 (spontaneous EPEC
adherence factor virulence plasmid-cured E2348/69), and 31-6-1(1)
(E2348/69 with a TnphoA insertion inactivation mutation in
the virulence plasmid-encoded bfpA gene). Scanning and
transmission electron microscopy revealed that after 8 h E2348/69 and CVD206(pCVD438) (both Int+ BFP+)
adhered to all specimens, causing A/E lesions with surrounding microvillous elongation. JPN15 and 31-6-1(1) (both Int+
BFP
) adhered and caused A/E lesions although bacteria
adhered in "flat," two-dimensional groups. CVD206 and
CVD206(pCVD438/01) (both Int
BFP+) did
not adhere to any sample, and no pathological tissue changes were seen.
Thus, in human intestinal organ culture, BFP do not appear to be
involved in the initial stages of EPEC nonintimate adhesion but are
implicated in the formation of complex, three-dimensional colonies via
bacterium-bacterium interactions. Intimin appears to play an essential
role in establishing colonization of EPEC on pediatric small intestinal
tissue.
*
Corresponding author. Mailing address: University
Department of Paediatric Gastroenterology, Royal Free Hospital, Pond
St., London, NW3 2QG, United Kingdom. Phone: 171 8302783. Fax: 171 8302146. E-mail: adphill{at}rfhsm.ac.uk.
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-
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-
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-
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-
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[Full Text]
-
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[Abstract]
[Full Text]
-
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[Abstract]
[Full Text]
-
Zhang, X.-L., Tsui, I. S. M., Yip, C. M. C., Fung, A. W. Y., Wong, D. K.-H., Dai, X., Yang, Y., Hackett, J., Morris, C.
(2000). Salmonella enterica Serovar Typhi Uses Type IVB Pili To Enter Human Intestinal Epithelial Cells. Infect. Immun.
68: 3067-3073
[Abstract]
[Full Text]
-
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(2000). Intimin from enteropathogenic Escherichia coli mediates remodelling of the eukaryotic cell surface. Microbiology
146: 1333-1344
[Abstract]
[Full Text]
-
Marches, O., Nougayrede, J.-P., Boullier, S., Mainil, J., Charlier, G., Raymond, I., Pohl, P., Boury, M., De Rycke, J., Milon, A., Oswald, E.
(2000). Role of Tir and Intimin in the Virulence of Rabbit Enteropathogenic Escherichia coli Serotype O103:H2. Infect. Immun.
68: 2171-2182
[Abstract]
[Full Text]
-
Sperandio, V., Mellies, J. L., Nguyen, W., Shin, S., Kaper, J. B.
(1999). Quorum sensing controls expression of the type III secretion gene transcription and protein secretion in enterohemorrhagic and enteropathogenic Escherichia coli. Proc. Natl. Acad. Sci. USA
96: 15196-15201
[Abstract]
[Full Text]
-
Batchelor, M., Knutton, S., Caprioli, A., Huter, V., Zanial, M., Dougan, G., Frankel, G.
(1999). Development of a Universal Intimin Antiserum and PCR Primers. J. Clin. Microbiol.
37: 3822-3827
[Abstract]
[Full Text]
-
Vanmaele, R. P., Heerze, L. D., Armstrong, G. D.
(1999). Role of Lactosyl Glycan Sequences in Inhibiting Enteropathogenic Escherichia coli Attachment. Infect. Immun.
67: 3302-3307
[Abstract]
[Full Text]
-
Boerlin, P., McEwen, S. A., Boerlin-Petzold, F., Wilson, J. B., Johnson, R. P., Gyles, C. L.
(1999). Associations between Virulence Factors of Shiga Toxin-Producing Escherichia coli and Disease in Humans. J. Clin. Microbiol.
37: 497-503
[Abstract]
[Full Text]
-
Adu-Bobie, J., Trabulsi, L. R., Carneiro-Sampaio, M. M. S., Dougan, G., Frankel, G.
(1998). Identification of Immunodominant Regions within the C-Terminal Cell Binding Domain of Intimin alpha and Intimin beta from Enteropathogenic Escherichia coli. Infect. Immun.
66: 5643-5649
[Abstract]
[Full Text]
-
PHILLIPS, A D
(1998). The medium is the messenger. Gut
43: 456-457
[Full Text]
-
Sinclair, J. F., O'Brien, A. D.
(2002). Cell Surface-localized Nucleolin Is a Eukaryotic Receptor for the Adhesin Intimin-gamma of Enterohemorrhagic Escherichia coli O157:H7. J. Biol. Chem.
277: 2876-2885
[Abstract]
[Full Text]