Journal of Leukocyte Biology BioLegend: Treg, Th17, Stem Cell
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Originally published online as doi:10.1189/jlb.0207130 on March 17, 2008

Published online before print March 17, 2008
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(Journal of Leukocyte Biology. 2008;83:1413-1422.)
© 2008 by Society for Leukocyte Biology

Pregnancy enhances the innate immune response in experimental cutaneous leishmaniasis through hormone-modulated nitric oxide production

Yaneth Osorio*,{dagger},{ddagger},1, Diana L. Bonilla{dagger}, Alex G. Peniche{dagger}, Peter C. Melby*,{ddagger} and Bruno L. Travi*,{dagger},{ddagger},1,2

* Department of Medicine, University of Texas, Health Science Center, San Antonio, Texas, USA;
{dagger} Centro Internacional de Entrenamiento e Investigaciones Medicas-CIDEIM, Cali, Colombia; and
{ddagger} Research Service, Department of Veterans Affairs Medical Center, South Texas Veterans Health Care System, San Antonio, Texas, USA

2Correspondence: Department of Medicine, University of Texas, Health Science Center, 7703 Floyd Curl Dr., Mailcode 7881, San Antonio, TX 78229-3900, USA. E-mail: travi{at}uthscsa.edu

The maintenance of host defense during pregnancy may depend on heightened innate immunity. We evaluated the immune response of pregnant hamsters during early infection with Leishmania (Viannia) panamensis, a cause of American cutaneous leishmaniasis. At 7 days post-infection, pregnant animals showed a lower parasite burden compared with nonpregnant controls at the cutaneous infection site (P=0.0098) and draining lymph node (P=0.02). Resident peritoneal macrophages and neutrophils from pregnant animals had enhanced Leishmania killing capacity compared with nonpregnant controls (P=0.018 each). This enhanced resistance during pregnancy was associated with increased expression of inducible NO synthase (iNOS) mRNA in lymph node cells (P=0.02) and higher NO production by neutrophils (P=0.0001). Macrophages from nonpregnant hamsters infected with L. panamensis released high amounts of NO upon estrogen exposure (P=0.05), and addition of the iNOS inhibitor L-N6-(1-iminoethyl) lysine blocked the induction of NO production (P=0.02). Infected, nonpregnant females treated with estrogen showed a higher percentage of cells producing NO at the infection site than controls (P=0.001), which correlated with lower parasite burdens (P=0.036). Cultured macrophages or neutrophils from estrogen-treated hamsters showed significantly increased NO production and Leishmania killing compared with untreated controls. iNOS was identified as the likely source of estrogen-induced NO in primed and naïve macrophages, as increased transcription was evident by real-time PCR. Thus, the innate defense against Leishmania infection is heightened during pregnancy, at least in part as a result of estrogen-mediated up-regulation of iNOS expression and NO production.

Key Words: Leishmania • hamster • estrogen






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