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A more recent version of this article appeared on June 1, 2008

Published online before print March 17, 2008
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© by The Society for Leukocyte Biology
Journal of Leukocyte Biology, doi:10.1189/jlb.0207130

Received for publication February 26, 2007.
Revised January 11, 2008.
Accepted for publication January 22, 2008.

Article

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

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

*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

@ To whom correspondence should be addressed. E-mail: travi{at}uthscsa.edu.


  Abstract

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 • draining lymph node • iNOS






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