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Infection and Immunity, June 2007, p. 2833-2840, Vol. 75, No. 6
0019-9567/07/$08.00+0     doi:10.1128/IAI.01826-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.

Environmental Strains of Mycobacterium avium Interfere with Immune Responses Associated with Mycobacterium bovis BCG Vaccination{triangledown}

Sarah L. Young,1 Lynn Slobbe,1 Rachel Wilson,1 Bryce M. Buddle,2 Geofferey W. de Lisle,2 and Glenn S. Buchan1*

Department of Microbiology & Immunology, University of Otago, Dunedin, New Zealand,1 AgResearch, Wallaceville Animal Research Centre, Upper Hutt, New Zealand2

Received 16 November 2006/ Returned for modification 18 December 2006/ Accepted 9 March 2007

Prior exposure of a vaccinee to certain species of environmental mycobacteria can prime the immune system against common mycobacterial antigens, which can in turn reduce the subsequent efficacy of live attenuated mycobacterial vaccines (such as Mycobacterium bovis BCG), in both human and livestock vaccination programs. In this study, two strains of Mycobacterium avium, both isolated from New Zealand livestock, were investigated to determine their growth characteristics and effects on the immune system in murine models. Markedly different effects on the immune system were observed; an IS901-negative strain (WAg 207) induced significant up-regulation of cell surface activation markers (major histocompatibility complex II, CD80, and CD86) on in vitro-derived dendritic cells and induced the release of proinflammatory monokines (interleukin-1β [IL-1β], IL-6, and tumor necrosis factor alpha) in dendritic cell-macrophage cocultures following direct in vitro contact of cells with bacteria. In contrast, an IS901-positive strain (WAg 206) had none of these effects. When mice were exposed to M. avium via oral infection prior to BCG parenteral immunization, both strains were shown to be capable of decreasing subsequent antigen-stimulated gamma interferon secretion by splenic lymphocytes, although this effect was more significant for strain WAg 206. Both strains also induced a mycobacterial antigen-specific serological response in M. avium-sensitized and BCG-immunized mice; this response was greater in WAg 206-sensitized mice, and there was a predominance of immunoglobulin G1 antibody. The down-regulation of IFN-{gamma} responses and the up-regulation of antibody responses are characteristic of a switch to a type 2 immune response. The different results may be linked to the inherent growth characteristics of the two strains, since WAg 206 was shown to grow slowly in murine macrophages in vitro and to cause a persistent systemic infection following infection in vivo, while WAg 207 grew fast and did not persist in mice. The implications of these findings for BCG vaccination protocols are discussed.

* Corresponding author. Mailing address: Department of Microbiology & Immunology, University of Otago, Box 56, Dunedin, New Zealand. Phone: 64 3479 7708. Fax: 64 3479 8540. E-mail: glen.buchan{at}stonebow.otago.ac.nz

{triangledown} Published ahead of print on 19 March 2007.

Editor: J. L. Flynn

Infection and Immunity, June 2007, p. 2833-2840, Vol. 75, No. 6
0019-9567/07/$08.00+0     doi:10.1128/IAI.01826-06
Copyright © 2007, American Society for Microbiology. All Rights Reserved.



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