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Selective Priming and Expansion of Antigen-Specific Foxp3^–CD4⁺ T Cells during Listeria monocytogenes Infection¹

James M. Ertelt^*,, Jared H. Rowe^*,, Tanner M. Johanns^*,, Joseph C. Lai^*,, James B. McLachlan^* and Sing Sing Way^2,*,

Departments of ^* Pediatrics and Microbiology, Center for Infectious Disease and Microbiology Translational Research, University of Minnesota School of Medicine, Minneapolis, MN 55455

The Foxp3-expressing subset of regulatory CD4⁺ T cells have defined Ag specificity and play essential roles in maintaining peripheral tolerance by suppressing the activation of self-reactive T cells. Similarly, during chronic infection, pathogen-specific Foxp3-expressing CD4⁺ T cells expand and actively suppress pathogen-specific effector T cells. Herein, we used MHC class II tetramers and Foxp3^gfp knockin mice to track the kinetics and magnitude whereby pathogen-specific Foxp3⁺CD4⁺ and Foxp3^–CD4⁺ cells are primed and expand after acute infection with recombinant Listeria monocytogenes (Lm) expressing the non-"self"-Ag 2W1S_52–68. We demonstrate that Lm infection selectively primes proliferation, expansion, and subsequent contraction of Lm-specific Foxp3^– effector CD4⁺ cells, while the numbers of Lm-specific Foxp3⁺CD4⁺ regulatory cells remain essentially unchanged. In sharp contrast, purified 2W1S_52–68 peptide primes coordinated expansion of both Foxp3⁺ regulatory and Foxp3^– effector T cells with the same Ag specificity. Taken together, these results indicate selective priming and expansion of Foxp3^– CD4 T cells is a distinguishing feature for acute bacterial infection.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This study was supported by National Institute of Child Health and Human Development/National Institutes of Health Grant K08HD51584, the March of Dimes Basil O'Conner Research Award, the Minnesota Vikings Children’s Fund, and the Minnesota Medical Foundation.

² Address correspondence and reprint requests to Dr. Sing Sing Way, 2001 6th Street SE, Minneapolis, MN 55455. E-mail address: singsing{at}umn.edu

³ Abbreviations used in this paper: Treg, regulatory T cell; 2W1S-TET, 2W1S-tetramer; HA, hemagglutinin; Lm, Listeria monocytogenes; MHC II, MHC class II; WT, wild type.

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