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Infection and Immunity, May 2003, p. 2468-2477, Vol. 71, No. 5
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.5.2468-2477.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.

Gamma Interferon Production by Hepatic NK T Cells during Escherichia coli Infection Is Resistant to the Inhibitory Effects of Oxidative Stress

Guochi Zhang,1 Robert Dru Nichols,1 Masaru Taniguchi,2 Toshinori Nakayama,2 and Michael J. Parmely1*

Department of Microbiology, Molecular Genetics and Immunology, University of Kansas Medical Center, Kansas City, KS 66160-7420,1 Core Research for Evolutional Science and Technology Project and Department of Molecular Immunology, Graduate School of Medicine, Chiba University, Chiba 260-8670, Japan2

Received 3 January 2003/ Returned for modification 4 February 2003/ Accepted 18 February 2003

The reductive-oxidative status of tissues regulates the expression of many inflammatory genes that are induced during gram-negative bacterial infections. The cytokine gamma interferon (IFN-{gamma}) is a potent stimulus for host inflammatory gene expression, and oxidative stress has been shown to inhibit its production in mice challenged with Escherichia coli bacteria. The objective of the present study was to characterize the cells that produced IFN-{gamma} in a mouse bacterial peritonitis model and determine the effects of oxidative stress on their activation. The liver contained large numbers of IFN-{gamma}-expressing lymphocytes following challenge with viable E. coli bacteria. The surface phenotypes of IFN-{gamma}-expressing hepatic lymphocytes were those of natural killer (NK) cells (NK1.1+ CD3-), conventional T cells (NK1.1- CD3+), and NK T cells (NK1.1+ CD3+). Treating mice with diethyl maleate to deplete tissue thiols significantly impaired IFN-{gamma} production by NK cells, conventional T cells, and CD1d-restricted NK T cells in response to E. coli challenge. However, IFN-{gamma} expression by a subset of NK T cells, which did not bind {alpha}-galactosylceramide-CD1d tetramers, was resistant to the inhibitory effects of tissue oxidative stress. Stress-resistant IFN-{gamma}-expressing cells were also predominantly CD8+ and bore {gamma}{delta} T-cell antigen receptors. The residual IFN-{gamma} response by NK T cells may explain previous reports of hepatic gene expression following gram-negative bacterial challenge in thiol-depleted mice. The finding also demonstrates that innate immune cells differ significantly in their responses to altered tissue redox status.

* Corresponding author. Mailing address: Department of Microbiology, Molecular Genetics and Immunology, University of Kansas Medical Center, 3901 Rainbow Blvd., Kansas City, KS 66160-7420. Phone: (913) 588-7053. Fax: (913) 588-7295. E-mail: mparmely{at}kumc.edu.

Editor: J. T. Barbieri

Infection and Immunity, May 2003, p. 2468-2477, Vol. 71, No. 5
0019-9567/03/$08.00+0     DOI: 10.1128/IAI.71.5.2468-2477.2003
Copyright © 2003, American Society for Microbiology. All Rights Reserved.



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