T helper 1 response against Leishmania major in pregnant C57BL/6 mice increases implantation failure and fetal resorptions. Correlation with increased IFN-gamma and TNF and reduced IL-10 production by placental cells.

Lakshmi Krishnan, L.J. Guilbert, T Wegmann, Miodrag Belosevic, Timothy R. Mosmann

The Journal of Immunology · 1996 · 344 citations · 0 references

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TL;DR

Maternal immune responses affect fetal survival, with Th1 cytokines such as IFN‑γ and IL‑2 linked to fetal loss and Th2 cytokine IL‑10 protective, yet in leishmaniasis resistance is associated with a Th1 response while a Th2 response worsens disease. The study examined whether the protective Th1 response against Leishmania major in resistant C57BL/6 mice compromises concurrent pregnancy. In infected C57BL/6 mice, pregnancy failure increased, with more resorptions and pre‑implantation losses linked to higher IFN‑γ and TNF and lower IL‑4/IL‑10, whereas BALB/c mice were unaffected, indicating that a protective Th1 response can harm pregnancy.

Abstract

Maternal immune responses can influence fetal survival and several cytokines have harmful or protective effects on pregnancy. The Th1 cytokines IFN-gamma and IL-2 can cause fetal loss, whereas the Th2 cytokine IL-10 is protective. However, infections such as leishmaniasis show the opposite pattern: resistance is associated with the preferential mounting of a Th1 response, whereas a Th2 response exacerbates the disease. We therefore asked whether the curative Th1 response against Leishmania major in genetically resistant C57BL/6 mice, would compromise concurrent pregnancy. The number of resorptions as assessed by uterine scars was significantly increased in infected C57BL/6 mice and this was associated with a decreased production by placental cells of the Th2 cytokines IL-4 and IL-10 and increased production of IFN-gamma and TNF. Interestingly, the frequency of pregnancy failure before implantation in C57BL/6 mice was also substantially increased. In contrast to C57BL/6 mice, early infection did not reduce implantations in BALB/c mice that mount a Th2 anti-L. major response and succumb to infection. For both resorptions and implantations, there appeared to be a short period early in infection that was detrimental to pregnancy, followed by a period with lesser effects, and a later period that again induced higher resorptions or pre-implantation losses. These results suggest that a beneficial anti-parasite Th1 response can adversely affect pregnancy outcome. Furthermore, Th1 cytokines may be deleterious for not only placental maintenance but also preimplantation events.