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Journal of Virology, October 1999, p. 8657-8668, Vol. 73, No. 10
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.

Bovine Herpesvirus 1 Can Infect CD4+ T Lymphocytes and Induce Programmed Cell Death during Acute Infection of Cattle

M. T. C. Winkler, A. Doster, and C. Jones*

Department of Veterinary and Biomedical Sciences, Center for Biotechnology, University of Nebraska, Lincoln, Lincoln, Nebraska 68583-0905

Received 1 April 1999/Accepted 29 June 1999

Acute infection of cattle with bovine herpesvirus 1 (BHV-1) represses cell-mediated immunity, which can lead to secondary bacterial infections. Since BHV-1 can induce apoptosis of cultured lymphocytes, we hypothesized that these virus-host interactions occur in cattle. To test this hypothesis, we analyzed lymph nodes and peripheral blood mononuclear cells (PBMC) after calves were infected with BHV-1. In situ terminal deoxynucleotidyltransferase-mediated dUTP nick end-labeling (TUNEL) staining of lymphoid tissues (pharyngeal tonsil, cervical, retropharyngeal, and inguinal) was used to detect apoptotic cells. Calves infected with BHV-1 for 7 days revealed increased apoptotic cells near the corticomedullary junction in lymphoid follicles and in the subcapsular region. Increased frequency of apoptotic cells was also observed in the mucosa-associated lymphoid tissue lining the trachea and turbinate. Immunohistochemistry of consecutive sections from pharyngeal tonsil revealed that CD2+ T lymphocytes were positive for the BHV-1 envelope glycoprotein gD. The location of these CD2+ T lymphocytes in the germinal center suggested that they were CD4+ T cells. Electron microscopy and TUNEL also revealed apoptotic and herpesvirus-infected lymphocytes from this area. Fluorescence-activated cell sorting analyses demonstrated that CD4+ and CD8+ T cells decreased in lymph nodes and PBMC after infection. The decrease in CD4+ T cells correlated with an increase in apoptosis. CD4+ but not CD8+ lymphocytes were infected by BHV-1 as judged by in situ hybridization and PCR, respectively. Immediate-early (bovine ICP0) and early (ribonucleotide reductase) transcripts were detected in PBMC and CD4+ lymphocytes prepared from infected calves. In contrast, a late transcript (glycoprotein C) was not consistently detected suggesting productive infection was not efficient. Taken together, these results indicate that BHV-1 can infect CD4+ T cells in cattle, leading to apoptosis and suppression of cell-mediated immunity.

* Corresponding author. Mailing address: Department of Veterinary and Biomedical Sciences, Center for Biotechnology, University of Nebraska, Lincoln Fair St. at East Campus Loop, Lincoln, NE 68583-0905. Phone: (402) 472-1890. Fax: (402) 472-9690. E-mail: cj{at}unlinfo.unl.edu.

Journal of Virology, October 1999, p. 8657-8668, Vol. 73, No. 10
0022-538X/99/$04.00+0
Copyright © 1999, American Society for Microbiology. All rights reserved.


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