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ToxSci Advance Access published online on August 19, 2004
Toxicological Sciences, doi:10.1093/toxsci/kfh255
Toxicological Sciences © Society of Toxicology 2004; all rights reserved
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Received March 26, 2004
Accepted August 9, 2004

Immunotoxiocology

Roles of Reactive Oxygen Species and Heme Oxygenase-1 in Modulation of Alveolar Macrophage-Mediated Pulmonary Immune Responses to Listeria monocytogenes by Diesel Exhaust Particles

Xuejun J. Yin 1, Jane Y. C. Ma 2, James M. Antonini 2, Vincent Castranova 2, Joseph K. H. Ma 1*

1 School of Pharmacy, West Virginia University, Morgantown, West Virginia 26506
2 Health Effects Laboratory Division, National Institute for Occupational Safety and Health, Morgantown, West Virginia 26505

* To whom correspondence should be addressed. E-mail: jma{at}hsc.wvu.edu.


  Abstract

Diesel exhaust particles (DEP) have been shown to suppress alveolar macrophage (AM)-mediated pulmonary immune responses to Listeria monocytogenes in vivo. In this study, effects of DEP-derived reactive oxygen species (ROS) and heme oxygenase (HO)-1 on AM-mediated immune responses to L. monocytogenes were investigated. Brown Norway rats were intratracheally inoculated with 100,000 L. monocytogenes and AM were isolated at 7 days post-infection. Exposure to DEP or their organic extract (eDEP), but not the washed DEP (wDEP) or carbon black, increased intracellular ROS and HO-1 expression in AM. Induction of ROS and HO-1 by eDEP was partially reversed by {alpha}-naphthoflavone, a cytochrome P450 1A1 inhibitor, and totally blocked by N-acetylcysteine. In addition, exposure to eDEP, but not wDEP, inhibited lipopolysacchride-stimulated secretion of tumor necrosis factor- (TNF-){alpha} and interleukin- (IL-)12, but augmented production of IL-10 by AM. Kinetic studies showed that modulation of cytokines by eDEP was preceded by ROS and HO-1 induction. Furthermore, pretreatment of AM with superoxide dismutase (SOD) or zinc protoporphrin IX (Znpp), which attenuated eDEP-induced HO-1 expression/activity, substantially inhibited eDEP effect on IL-10. Finally, direct stimulation with pyrogallol (PYR), a superoxide donor, up-regulated HO-1 and IL-10 but decreased secretion of IL-12 in L. monocytogenes-infected AM. These results show that DEP, through eDEP-mediated ROS, induce HO-1 expression and IL-10 production and at the same time inhibit AM production of TNF-{alpha} and IL-12 to dampen the host immune responses. The results also suggest that HO-1 may play an important role in regulating production of IL-10 by DEP-exposed and L. monocytogenes-infected AM.

Keywords: Diesel exhaust particles; Listeria monocytogenes; heme oxygenase-1; reactive oxygen species; cytokines.
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