Abstract
Pregnancy is a state where high and stage-dependent plasticity of the maternal immune system is necessary in order to equilibrate between immunosuppression of harmful responses towards the fetus and ability to fight infections. TCR γδ cells have been implicated in the responses in infectious diseases, in the regulation of immune responses, and in tissue homeostasis and repair. The variety of functions makes γδ T cells a particularly interesting population during pregnancy. In this study, we investigated the proportion, phenotype and TCR γ and δ repertoires of γδ T cells at the maternal–fetal interface and in the blood of pregnant women using FACS, immunohistochemistry and spectratyping. We found an enrichment of activated and terminally differentiated pro-inflammatory γδ T-cell effectors with specific location in the human decidua during early pregnancy, while no significant changes in their counterparts in the blood of pregnant women were observed. Our spectratyping data revealed polyclonal CDR3 repertoires of the δ1, δ2 and δ3 chains and γ2, γ3, γ4 and γ5 chains and oligoclonal and highly restricted CDR3γ9 repertoire of γδ T cells in the decidua and blood of pregnant women. Early pregnancy induces recruitment of differentiated pro-inflammatory γδ T-cell effectors with diverse TCR repertoires at the maternal–fetal interface.
Highlights
Implantation, as a part of early pregnancy, is a dynamic process when the semi-allogeneic embryo “signals” its presence in the uterus and should be recognized and tolerated by the maternal immune system
In interstitial implantation and hemochorial type of placenta, there are two surfaces of contact—one maternal–fetal interface (MFI) is that wherein decidua basalis-based maternal immune cells contact with the extravillous cytotrophoblasts (EVTs), and another one, increasing in volume as pregnancy progresses, is formed between the chorionic villi and maternal blood, wherein the maternal immune cells in the peripheral circulation are in contact with syncytiotrophoblast, covering placental villi
We demonstrated that γδ T lymphocytes with diverse TCR repertoires can expand, differentiate, and acquire effector phenotypes at the MFI during early human pregnancy, while no significant changes in their counterparts in the blood of pregnant women were observed
Summary
Implantation, as a part of early pregnancy, is a dynamic process when the semi-allogeneic embryo “signals” its presence in the uterus and should be recognized and tolerated by the maternal immune system. The type of implantation determines to what extent maternal immune cells interact with fetal tissues and cells. It is well accepted that a successful pregnancy requires a robust, dynamic and responsive maternal immune system and the immunological milieu at the MFI is unique, modulated and definitely not suppressed [1]. The unique composition and phenotype of decidua-based immune cells as a part of decidua-associated lymphoid tissue (DALT) as well as their interaction with stromal decidual cells, and trophoblast (embryonic) cells is crucial for pregnancy recognition and establishment of tolerogenic environment for the embryo. In species with hemochorial placenta, leukocytes are about 10% of the decidual cells in the proliferative phase of the cycle, increasing to ~20% in the late secretory phase and >40% in early pregnancy [2]
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