The Journal of Experimental Medicine
Rockland Immunochemicals for Research
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Published 19 July 2004. doi:10.1084/jem.20041132
Rockefeller University Press, 0022-1007 $8.00
JEM, Volume 200, Number 2, 235-245
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Peyer's Patch Dendritic Cells Process Viral Antigen from Apoptotic Epithelial Cells in the Intestine of Reovirus-infected Mice

Marina N. Fleeton1, Nikhat Contractor1, Francisco Leon1, J. Denise Wetzel2,4, Terence S. Dermody2,3,4, and Brian L. Kelsall1

1 Laboratory of Clinical Investigation, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Bethesda, MD 20892
2 Department of Pediatrics, 3 Department of Microbiology and Immunology, and 4 Elizabeth B. Lamb Center for Pediatric Research, Vanderbilt University School of Medicine, Nashville, TN 37232

Address correspondence to Brian Kelsall, Laboratory of Molecular Immunology, National Institute of Allergy and Infectious Diseases, National Institutes of Health, Building 10, Room 11N228, Bethesda, MD 20892. Phone: (301) 496-7473; Fax: (301) 480-6768; email: Kelsall{at}nih.gov

We explored the role of Peyer's patch (PP) dendritic cell (DC) populations in the induction of immune responses to reovirus strain type 1 Lang (T1L). Immunofluorescence staining revealed the presence of T1L structural ({sigma}1) and nonstructural ({sigma}NS) proteins in PPs of T1L-infected mice. Cells in the follicle-associated epithelium contained both {sigma}1 and {sigma}NS, indicating productive viral replication. In contrast, {sigma}1, but not {sigma}NS, was detected in the subepithelial dome (SED) in association with CD11c+/CD8{alpha}–/CD11blo DCs, suggesting antigen uptake by these DCs in the absence of infection. Consistent with this possibility, PP DCs purified from infected mice contained {sigma}1, but not {sigma}NS, and PP DCs from uninfected mice could not be productively infected in vitro. Furthermore, {sigma}1 protein in the SED was associated with fragmented DNA by terminal deoxy-UTP nick-end labeling staining, activated caspase-3, and the epithelial cell protein cytokeratin, suggesting that DCs capture T1L antigen from infected apoptotic epithelial cells. Finally, PP DCs from infected mice activated T1L-primed CD4+ T cells in vitro. These studies show that CD8{alpha}–/CD11blo DCs in the PP SED process T1L antigen from infected apoptotic epithelial cells for presentation to CD4+ T cells, and therefore demonstrate the cross-presentation of virally infected cells by DCs in vivo during a natural viral infection.

Key Words: antigen processing • apoptosis • epithelial cells • immunity, mucosal • reovirus infection

M.N. Fleeton's present address is Virology Unit, Trinity College, Dublin 2, Ireland.

Abbreviations used in this paper: FAE, follicle-associated epithelium; PP, Peyer's patch; SED, subepithelial dome; T1L, reovirus strain type 1 Lang; TUNEL, terminal deoxy-UTP nick-end labeling.


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