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Infection and Immunity, September 2003, p. 5077-5086, Vol. 71, No. 9
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.9.5077-5086.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Central Role for B Lymphocytes and CD4+ T Cells in Immunity to Infection by the Attaching and Effacing Pathogen Citrobacter rodentium

Cameron P. Simmons,1* Simon Clare,1 Marjan Ghaem-Maghami,1 Tania K. Uren,2 Joanna Rankin,1 Allan Huett,1 Rob Goldin,3 David J. Lewis,4 Thomas T. MacDonald,5 Richard A. Strugnell,2 Gad Frankel,1 and Gordon Dougan1

Centre for Molecular Microbiology and Infection, Department of Biological Sciences, Imperial College of Science, Technology and Medicine, South Kensington, London SW6 1SJ,1 Department of Infection, Inflammation and Repair, University of Southampton, Southampton SO16 6YD,5 Imperial College Faculty of Medicine at St. Mary's, Paddington, London W2 1PG,3 Microbiology, St. George's Hospital Medical School, London SW17 0RE, United Kingdom,4 Department of Microbiology and Immunology, University of Melbourne, Parkville, Victoria, Australia 30522

Received 18 November 2002/ Returned for modification 27 January 2003/ Accepted 5 June 2003

Citrobacter rodentium, an attaching-effacing bacterial pathogen, establishes an acute infection of the murine colonic epithelium and induces a mild colitis in immunocompetent mice. This study describes the role of T-cell subsets and B lymphocytes in immunity to C. rodentium. C57Bl/6 mice orally infected with C. rodentium resolved infection within 3 to 4 weeks. Conversely, systemic and colonic tissues of RAG1-/- mice orally infected with C. rodentium contained high and sustained pathogen loads, and in the colon this resulted in a severe colitis. C57Bl/6 mice depleted of CD4+ T cells, but not CD8+ T cells, were highly susceptible to infection and also developed severe colitis. Mice depleted of CD4+ T cells also had diminished immunoglobulin G (IgG) and IgA antibody responses to two C. rodentium virulence-associated determinants, i.e., EspA and intimin, despite having a massively increased pathogen burden. Mice with an intact T-cell compartment, but lacking B cells (µMT mice), were highly susceptible to C. rodentium infection. Systemic immunity, but not mucosal immunity, could be restored by adoptive transfer of convalescent immune sera to infected µMT mice. Adoptive transfer of immune B cells, but not naïve B cells, provided highly variable immunity to recipient µMT mice. The results suggest that B-cell-mediated immune responses are central to resolution of a C. rodentium infection but that the mechanism through which this occurs requires further investigation. These data are relevant to understanding immunity to enteric attaching and effacing bacterial pathogens of humans.

* Corresponding author. Present address: Oxford-Wellcome Trust Clinical Research Unit, Centre for Tropical Diseases, 190 Ben Ham Tu, Ho Chi Minh City, Vietnam. Phone: 84 89237954. Fax: 84 89238904. E-mail: csimmons{at}hcm.vnn.vn.

Editor: B. B. Finlay

Infection and Immunity, September 2003, p. 5077-5086, Vol. 71, No. 9
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.9.5077-5086.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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