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Infection and Immunity, February 2000, p. 839-847, Vol. 68, No. 2
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.

Lack of a Role of Cytotoxic Necrotizing Factor 1 Toxin from Escherichia coli in Bacterial Pathogenicity and Host Cytokine Response in Infected Germfree Piglets

S. Fournout,1,2 C. M. Dozois,1,dagger M. Odin,2 C. Desautels,2 S. Pérès,3 F. Hérault,3 F. Daigle,3,dagger C. Segafredo,1 J. Laffitte,1 E. Oswald,3 J. M. Fairbrother,2 and I. P. Oswald1,*

Laboratoire de Pharmacologie Toxicologie1 and Laboratoire de Microbiologie Moléculaire Associé,3 Institut National de Recherche Agronomique, Toulouse, France, and GREMIP, Faculté de Médecine Vétérinaire, Saint-Hyacinthe, Québec, Canada2

Received 22 June 1999/Returned for modification 25 August 1999/Accepted 26 October 1999

Some Escherichia coli strains isolated from intestinal or extraintestinal infections in pigs produce cytotoxic necrotizing factor 1 (CNF1). In order to analyze the role of CNF1 in the pathogenesis of porcine colibacillosis, newborn colostrum-deprived germfree piglets were orally inoculated with a wild-type CNF1-producing strain (M623) or with an isogenic cnf1 mutant (M623Delta CNF1). The two isogenic strains induced a high mortality with similar lung and serosal inflammatory lesions, indicating that both strains were pathogenic in these piglets. Bacterial counts in various organs of inoculated piglets revealed an intestinal predisposition of M623 and M623Delta CNF1 strains for the cecum and colon. Extraintestinal organs (lungs, liver, spleen, and kidney) were also colonized by both strains. Similar colonization of intestinal and extraintestinal tissues in animals inoculated with either strain was observed, except in the ileum, where M623 showed a higher colonization than M623Delta CNF1. Intestinal (ileum and colon), extraintestinal (lung and kidney), and immune (mesenteric lymph nodes and spleen) tissues were sampled at 1 day postinoculation and analyzed for cytokine expression by a reverse transcriptase PCR technique. Inoculation with E. coli M623 induced an enhanced expression of inflammatory cytokines (interleukin-1alpha [IL-1alpha ], tumor necrosis factor alpha , and IL-12p40) in the intestinal organs compared to uninoculated piglets or piglets inoculated with nonpathogenic intestinal E. coli 862B, which is also able to colonize the intestinal tract. There was little difference in cytokine transcript levels in the intestinal and extraintestinal organs in piglets inoculated with E. coli strains M623 or M623Delta CNF1, except in the ileum, where IL-1alpha and IL-8 mRNA levels correlated with bacterial colonization. Expression of regulatory cytokines (gamma interferon and IL-4) was weak in immune tissues from piglets inoculated with M623 or M623Delta CNF1. Taken together, our data indicate that the CNF1-producing strain, M623, is pathogenic and induces inflammatory cytokine expression in germfree, colostrum-deprived piglets. Nevertheless, in this model, the CNF1 toxin does not appear to be a major factor for pathogenicity or cytokine response, as demonstrated by the use of an isogenic cnf1 mutant.

* Corresponding author. Mailing address: Laboratoire de Pharmacologie Toxicologie, INRA, 180 Chemin de Tournefeuille, 31931 Toulouse Cedex 9, France. Phone: 33 (0) 561285480. Fax: 33 (0) 561285310. E-mail: ioswald{at}toulouse.inra.fr.

dagger Present address: Department of Biology, Washington University, Saint Louis, MO 63130.

Infection and Immunity, February 2000, p. 839-847, Vol. 68, No. 2
0019-9567/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.


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