B7-H4 reduction induced by Toxoplasma gondii infection results in dysfunction of decidual dendritic cells by regulating the JAK2/STAT3 pathway

  • Parasit Vectors. 2022 May 3;15(1):157. doi: 10.1186/s13071-022-05263-1.
Xinyue Sun   #  1 Hongbing Xie   #  1 Haixia Zhang   #  1 Zhidan Li  1 Houbao Qi  1 Chunyan Yang  2 Xianbing Liu  1 Liqin Ren  3 Yuzhu Jiang  1 Xuemei Hu  4
Affiliations
  • 1. Department of Immunology, Binzhou Medical University, Yantai, 264003, Shandong, People's Republic of China.
  • 2. Department of Oral Biology, Binzhou Medical University, Yantai, 264003, Shandong, People's Republic of China.
  • 3. Department of Medical Genetics and Cell Biology, Binzhou Medical University, Yantai, 264003, Shandong, People's Republic of China.
  • 4. Department of Immunology, Binzhou Medical University, Yantai, 264003, Shandong, People's Republic of China. [email protected].
  • # Contributed equally.
Abstract

Background: Primary Infection of Toxoplasma gondii can cause serious abnormal pregnancy outcomes such as miscarriage and stillbirth. Inhibitory molecule B7-H4 is abundantly expressed in dendritic cells (DCs) and plays an important role in maintaining immune tolerance. However, the role of B7-H4 in decidual DCs (dDCs) in T. gondii-induced abnormal pregnancy outcomes is not clear.

Methods: We established T. gondii-infected abnormal pregnancy model in wild-type (WT) and B7-H4 knockout (B7-H4-/-) pregnant mice in vivo and cultured primary human dDCs in vitro. The abnormal pregnancy outcomes were observed and the expression of B7-H4, Functional Molecules (CD80, CD86, and MHC-II or HLA-DR), indoleamine 2,3-dioxygenase (IDO), cytokines (IL-10 and IL-12), and signaling molecules JAK2/STAT3 in dDCs was detected by flow cytometry and Western blot.

Results: Our results showed that T. gondii Infection significantly decreased B7-H4 expression in dDCs. In addition, B7-H4-/- infected pregnant mice showed much more severe abnormal pregnancy outcomes than their counterparts. Importantly, B7-H4-/- Infection further regulated the expression of molecules (CD80, CD86, and MHC-II or HLA-DR), enzyme IDO, and cytokines (IL-10 and IL-12) in dDCs. We further discovered that B7-H4-/- Infection impairs the JAK2/STAT3 pathway, contributing to dDC dysfunction.

Conclusions: Taken together, the results show that reduction of B7-H4 by T. gondii Infection significantly modulates the decrease in cytokine IL-10 and enzyme IDO and the increase in cytokine IL-12, contributing to dDC dysfunction. Moreover, the JAK2/STAT3 pathway is involved in the regulation of B7-H4 by T. gondii Infection and in the subsequent IDO and cytokine production, which ultimately contributes to abnormal pregnancy outcomes.

Keywords
Abnormal pregnancy; B7-H4; Decidual DCs; Inhibitory molecule; Maternal–fetal tolerance; Toxoplasma gondii.
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