Previous Article | Next Article 
Infection and Immunity, September 1999, p. 4499-4509, Vol. 67, No. 9
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
Invasive Ability of an Escherichia coli
Strain Isolated from the Ileal Mucosa of a Patient with Crohn's
Disease
Jerome
Boudeau,
Anne-Lise
Glasser,
Estelle
Masseret,
Bernard
Joly, and
Arlette
Darfeuille-Michaud*
Pathogénie Bactérienne
Intestinale, Laboratoire de Bactériologie, Faculté de
Pharmacie, 63001 Clermont-Ferrand, France
Received 12 April 1999/Returned for modification 1 June
1999/Accepted 21 June 1999
Crohn's disease (CD) is an inflammatory bowel disease in which
Escherichia coli strains have been suspected of being
involved. We demonstrated previously that ileal lesions of CD are
colonized by E. coli strains able to adhere to intestinal
Caco-2 cells but devoid of the virulence genes so far described in the
pathogenic E. coli strains involved in gastrointestinal
infections. In the present study we compared the invasive ability of
one of these strains isolated from an ileal biopsy of a patient with
CD, strain LF82, with that of reference enteroinvasive (EIEC),
enteropathogenic (EPEC), enterotoxigenic (ETEC), enteraggregative
(EAggEC), enterohemorrhagic (EHEC), and diffusely adhering (DAEC)
E. coli strains. Gentamicin protection assays showed that
E. coli LF82 was able to efficiently invade HEp-2 cells.
Its invasive level was not significantly different from that of EIEC
and EPEC strains (P > 0.5) but significantly higher
than that of ETEC (P < 0.03), EHEC
(P < 0.005), EAggEC (P < 0.004) and
DAEC (P < 0.02) strains. Strain LF82 also
demonstrated efficient ability to invade intestinal epithelial cultured
Caco-2, Intestine-407, and HCT-8 cells. Electron microscopy examination of infected HEp-2 cells revealed the presence of numerous intracellular bacteria located in vacuoles or free in the host cell cytoplasm. In
addition, the interaction of strain LF82 with epithelial cells was
associated with the elongation of microvillar extensions that extruded
from the host cell membranes and engulfed the bacteria. This
internalization mechanism strongly resembles Salmonella- or
Shigella-induced macropinocytosis. The use of cytochalasin D and colchicine showed that the uptake of strain LF82 by HEp-2 cells
was mediated by both an actin microfilament-dependent mechanism and
microtubule involvement. In addition, strain LF82 survived for at least
24 h in HEp-2 and Intestine-407 cells and efficiently replicated
intracellularly in HEp-2 cells. PCR and hybridization experiments did
not reveal the presence of any of the genetic determinants encoding
EIEC, EPEC, or ETEC proteins involved in bacterial invasion. Thus,
these findings show that LF82, which colonized the ileal mucosa of a
patient with CD, is a true invasive E. coli strain and
suggest the existence of a new potentially pathogenic group of E. coli, which we propose be designated adherent-invasive E. coli.
*
Corresponding author. Mailing address: Pathogénie
Bactérienne Intestinale, Laboratoire de Bactériologie,
Faculté de Pharmacie, 63001 Clermont-Ferrand, France. Phone: 33 4 73 60 80 52. Fax: 33 4 73 27 74 94. E-mail:
arlette.darfeuille-michaud{at}u-clermont1.fr.
Infection and Immunity, September 1999, p. 4499-4509, Vol. 67, No. 9
0019-9567/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Carvalho, F. A., Barnich, N., Sivignon, A., Darcha, C., Chan, C. H.F., Stanners, C. P., Darfeuille-Michaud, A.
(2009). Crohn's disease adherent-invasive Escherichia coli colonize and induce strong gut inflammation in transgenic mice expressing human CEACAM. JEM
206: 2179-2189
[Abstract]
[Full Text]
-
Fearnley, C., Manning, G., Bagnall, M., Javed, M. A., Wassenaar, T. M., Newell, D. G.
(2008). Identification of hyperinvasive Campylobacter jejuni strains isolated from poultry and human clinical sources. J Med Microbiol
57: 570-580
[Abstract]
[Full Text]
-
Roselli, M., Finamore, A., Britti, M. S., Konstantinov, S. R., Smidt, H., de Vos, W. M., Mengheri, E.
(2007). The Novel Porcine Lactobacillus sobrius Strain Protects Intestinal Cells from Enterotoxigenic Escherichia coli K88 Infection and Prevents Membrane Barrier Damage. J. Nutr.
137: 2709-2716
[Abstract]
[Full Text]
-
Claret, L., Miquel, S., Vieille, N., Ryjenkov, D. A., Gomelsky, M., Darfeuille-Michaud, A.
(2007). The Flagellar Sigma Factor FliA Regulates Adhesion and Invasion of Crohn Disease-associated Escherichia coli via a Cyclic Dimeric GMP-dependent Pathway. J. Biol. Chem.
282: 33275-33283
[Abstract]
[Full Text]
-
Bringer, M.-A., Rolhion, N., Glasser, A.-L., Darfeuille-Michaud, A.
(2007). The Oxidoreductase DsbA Plays a Key Role in the Ability of the Crohn's Disease-Associated Adherent-Invasive Escherichia coli Strain LF82 To Resist Macrophage Killing. J. Bacteriol.
189: 4860-4871
[Abstract]
[Full Text]
-
Conte, M P, Schippa, S, Zamboni, I, Penta, M, Chiarini, F, Seganti, L, Osborn, J, Falconieri, P, Borrelli, O, Cucchiara, S
(2006). Gut-associated bacterial microbiota in paediatric patients with inflammatory bowel disease. Gut
55: 1760-1767
[Abstract]
[Full Text]
-
Simpson, K. W., Dogan, B., Rishniw, M., Goldstein, R. E., Klaessig, S., McDonough, P. L., German, A. J., Yates, R. M., Russell, D. G., Johnson, S. E., Berg, D. E., Harel, J., Bruant, G., McDonough, S. P., Schukken, Y. H.
(2006). Adherent and Invasive Escherichia coli Is Associated with Granulomatous Colitis in Boxer Dogs.. Infect. Immun.
74: 4778-4792
[Abstract]
[Full Text]
-
Nazli, A., Wang, A., Steen, O., Prescott, D., Lu, J., Perdue, M. H., Soderholm, J. D., Sherman, P. M., McKay, D. M.
(2006). Enterocyte Cytoskeleton Changes Are Crucial for Enhanced Translocation of Nonpathogenic Escherichia coli across Metabolically Stressed Gut Epithelia. Infect. Immun.
74: 192-201
[Abstract]
[Full Text]
-
Sherman, P. M., Johnson-Henry, K. C., Yeung, H. P., Ngo, P. S. C., Goulet, J., Tompkins, T. A.
(2005). Probiotics Reduce Enterohemorrhagic Escherichia coli O157:H7- and Enteropathogenic E. coli O127:H6-Induced Changes in Polarized T84 Epithelial Cell Monolayers by Reducing Bacterial Adhesion and Cytoskeletal Rearrangements. Infect. Immun.
73: 5183-5188
[Abstract]
[Full Text]
-
Ingrassia, I., Leplingard, A., Darfeuille-Michaud, A.
(2005). Lactobacillus casei DN-114 001 Inhibits the Ability of Adherent-Invasive Escherichia coli Isolated from Crohn's Disease Patients To Adhere to and To Invade Intestinal Epithelial Cells. Appl. Environ. Microbiol.
71: 2880-2887
[Abstract]
[Full Text]
-
Luck, S. N., Bennett-Wood, V., Poon, R., Robins-Browne, R. M., Hartland, E. L.
(2005). Invasion of Epithelial Cells by Locus of Enterocyte Effacement-Negative Enterohemorrhagic Escherichia coli. Infect. Immun.
73: 3063-3071
[Abstract]
[Full Text]
-
Servin, A. L.
(2005). Pathogenesis of Afa/Dr Diffusely Adhering Escherichia coli. Clin. Microbiol. Rev.
18: 264-292
[Abstract]
[Full Text]
-
Rolhion, N., Barnich, N., Claret, L., Darfeuille-Michaud, A.
(2005). Strong Decrease in Invasive Ability and Outer Membrane Vesicle Release in Crohn's Disease-Associated Adherent-Invasive Escherichia coli Strain LF82 with the yfgL Gene Deleted. J. Bacteriol.
187: 2286-2296
[Abstract]
[Full Text]
-
Bringer, M.-A., Barnich, N., Glasser, A.-L., Bardot, O., Darfeuille-Michaud, A.
(2005). HtrA Stress Protein Is Involved in Intramacrophagic Replication of Adherent and Invasive Escherichia coli Strain LF82 Isolated from a Patient with Crohn's Disease. Infect. Immun.
73: 712-721
[Abstract]
[Full Text]
-
Wada, Y., Kato, M., Yamamoto, S., Shibahara, T., Ishikawa, Y., Kadota, K.
(2004). Invasive Ability of Escherichia coli O18 Isolated from Swine Neonatal Diarrhea. Vet Pathol
41: 433-437
[Abstract]
[Full Text]
-
Barnich, N., Bringer, M.-A., Claret, L., Darfeuille-Michaud, A.
(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
[Abstract]
[Full Text]
-
Schuppler, M., Lotzsch, K., Waidmann, M., Autenrieth, I. B.
(2004). An Abundance of Escherichia coli Is Harbored by the Mucosa- Associated Bacterial Flora of Interleukin-2-Deficient Mice. Infect. Immun.
72: 1983-1990
[Abstract]
[Full Text]
-
Tamboli, C P, Neut, C, Desreumaux, P, Colombel, J F
(2004). Dysbiosis in inflammatory bowel disease. Gut
53: 1-4
[Abstract]
[Full Text]
-
Betis, F., Brest, P., Hofman, V., Guignot, J., Kansau, I., Rossi, B., Servin, A., Hofman, P.
(2003). Afa/Dr Diffusely Adhering Escherichia coli Infection in T84 Cell Monolayers Induces Increased Neutrophil Transepithelial Migration, Which in Turn Promotes Cytokine-Dependent Upregulation of Decay-Accelerating Factor (CD55), the Receptor for Afa/Dr Adhesins. Infect. Immun.
71: 1774-1783
[Abstract]
[Full Text]
-
Blanc-Potard, A.-B., Tinsley, C., Scaletsky, I., Le Bouguenec, C., Guignot, J., Servin, A. L., Nassif, X., Bernet-Camard, M.-F.
(2002). Representational Difference Analysis between Afa/Dr Diffusely Adhering Escherichia coli and Nonpathogenic E. coli K-12. Infect. Immun.
70: 5503-5511
[Abstract]
[Full Text]
-
Uhlich, G. A., Keen, J. E., Elder, R. O.
(2002). Variations in the csgD Promoter of Escherichia coli O157:H7 Associated with Increased Virulence in Mice and Increased Invasion of HEp-2 Cells. Infect. Immun.
70: 395-399
[Abstract]
[Full Text]
-
Glasser, A.-L., Boudeau, J., Barnich, N., Perruchot, M.-H., Colombel, J.-F., Darfeuille-Michaud, A.
(2001). Adherent Invasive Escherichia coli Strains from Patients with Crohn's Disease Survive and Replicate within Macrophages without Inducing Host Cell Death. Infect. Immun.
69: 5529-5537
[Abstract]
[Full Text]
-
Guignot, J., Bernet-Camard, M.-F., Pous, C., Plancon, L., Le Bouguenec, C., Servin, A. L.
(2001). Polarized Entry of Uropathogenic Afa/Dr Diffusely Adhering Escherichia coli Strain IH11128 into Human Epithelial Cells: Evidence for {alpha}5{beta}1 Integrin Recognition and Subsequent Internalization through a Pathway Involving Caveolae and Dynamic Unstable Microtubules. Infect. Immun.
69: 1856-1868
[Abstract]
[Full Text]
-
Masseret, E, Boudeau, J, Colombel, J F, Neut, C, Desreumaux, P, Joly, B, Cortot, A, Darfeuille-Michaud, A
(2001). Genetically related Escherichia coli strains associated with Crohn's disease. Gut
48: 320-325
[Abstract]
[Full Text]
-
Caradonna, L., Amati, L., Magrone, T., Pellegrino, N.M., Jirillo, E., Caccavo, D.
(2000). Invited review: Enteric bacteria, lipopolysaccharides and related cytokines in inflammatory bowel disease: biological and clinical significance. Innate Immunity
6: 205-214
[Abstract]