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Journal of Virology, February 2003, p. 1703-1717, Vol. 77, No. 3
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.3.1703-1717.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Vigorous Innate and Virus-Specific Cytotoxic T-Lymphocyte Responses to Murine Cytomegalovirus in the Submaxillary Salivary Gland

Victoria J. Cavanaugh,1 Yuping Deng,2 Mark P. Birkenbach,3 Jacquelyn S. Slater,1 and Ann E. Campbell1*

Department of Microbiology and Molecular Cell Biology, Glennan Center for Geriatrics and Gerontology,1 Department of Internal Medicine,2 Department of Pathology and Anatomy, Eastern Virginia Medical School, Norfolk, Virginia 235013

Received 1 March 2002/ Accepted 22 October 2002

To better understand the immunological mechanisms that permit prolonged shedding of murine cytomegalovirus (MCMV) from the salivary gland, the phenotypic and functional characteristics of leukocytes infiltrating the submaxillary gland (SMG) were analyzed in infected BALB/c mice. A robust innate immune response, comprised of CD11c+ major histocompatibility complex class II+ CD11b- CD8{alpha}+ dendritic cells and {gamma}/{delta} T-cell receptor-bearing CD3+ T cells was prominent through at least 28 days postinfection. Concurrently, a dramatic increase in pan-NK (DX5+) CD3+ and CD8+ T cells was observed, while CD4+ T cells, known to be essential for viral clearance from this tissue, increased slightly. The expression particularly of gamma interferon but also of interleukin-10 and CC chemokines was extraordinarily high in the SMG in response to MCMV infection. The gamma interferon was produced primarily by CD4+ and CD8+ T lymphocytes and DX5+ CD3+ T cells. The SMG CD8+ T cells were highly cytolytic ex vivo, and a significant proportion of these cells were specific to an immunodominant MCMV peptide. These peptide-specific clones were not exhausted by the presence of high virus titers, which persisted in the SMG despite the strength of the cell-mediated responses. In contrast, MCMV replication was efficiently cleared from the draining cervical and periglandular lymph nodes, a tissue displaying a substantially weaker antiviral response. Our data indicated that vigorous innate and acquired immune responses are elicited, activated, and retained in response to mucosal inflammation from persistent MCMV infection of the submaxillary gland.

* Corresponding author. Mailing address: Department of Microbiology and Molecular Cell Biology, Eastern Virginia Medical School, P. O. Box 1980, Norfolk, VA 23501-1980. Phone: (757) 446-5667. Fax: (757) 624-2255. E-mail: campbeae{at}evms.edu.

Journal of Virology, February 2003, p. 1703-1717, Vol. 77, No. 3
0022-538X/03/$08.00+0     DOI: 10.1128/JVI.77.3.1703-1717.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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