RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization

Meng, Yuguang; Zhou, Wen‐Jie; Jin, Liping; Liu, Libing; Chang, Kai‐Kai; Mei, Jie; Li, Hui; Wang, Jian; Li, Da‐Jin; Li, Ming‐Qing

doi:10.1038/cddis.2017.505

Cited by 57 publications

(54 citation statements)

References 53 publications

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“…The immune cells at the maternal-fetal interface mainly include NK cells, macrophages (Mφ), regulatory T cells and DCs (92). Uterine NK cells and Mφ are the most prominent decidual immune cells; decidual NK cells account for ∼50-70% and decidual macrophages (DM) for 20-25% of all decidual immune cells (103,104). Decidual NK cells have low cytotoxicity as compared to peripheral blood NK cells (105).…”

Section: The Possible Role Of Lactic Acid At the Maternal-fetal Intermentioning

confidence: 99%

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Huang

Muyayalo

et al. 2020

Front. Immunol.

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Aerobic glycolysis is a recognized feature shared by tumors, leading to the accumulation of lactic acid in their local microenvironments. Like the tumors, the blastocysts, placenta, trophoblasts and decidual immune cells can also produce a large amount of lactic acid through aerobic glycolysis during the early pregnancy. Moreover, the placenta expresses the transporters of the lactic acid. While several studies have described the role of lactic acid in the tumor microenvironment, especially lactic acid's modulation of immune cells, the role of lactic acid produced during pregnancy is still unclear. In this paper, we reviewed the scientific evidence detailing the effects of lactic acid in the tumor microenvironment. Based on the influence of the lactic acid on immune cells and tumors, we proposed that lactic acid released in the unique uterine environment could have similar effects on the trophoblast cells and immune cells during the early pregnancy.

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Section: The Possible Role Of Lactic Acid At the Maternal-fetal Intermentioning

confidence: 99%

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Huang

Muyayalo

et al. 2020

Front. Immunol.

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“…38 DICs were used for dNK cell isolation using Human NK Cell Isolation Kit (Miltenyi Biotec) following the manufacturer's protocol. Using this method, 98% of cells obtained were vimentin + cytokeratin (CK)7 − DSCs and CD45 + DICs as previously reported.…”

Section: Cell Isolation and Culturementioning

confidence: 99%

“…Using this method, 98% of cells obtained were vimentin + cytokeratin (CK)7 − DSCs and CD45 + DICs as previously reported. 38 DICs were used for dNK cell isolation using Human NK Cell Isolation Kit (Miltenyi Biotec) following the manufacturer's protocol.…”

Section: Cell Isolation and Culturementioning

confidence: 99%

Trophoblast‐derived CXCL12 promotes CD56^brightCD82⁻CD29⁺ NK cell enrichment in the decidua

Han

Jin

Huang

et al. 2019

American J Rep Immunol

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Problem: Decidual natural killer (dNK) cells play key roles in maternal-fetal immune regulation, trophoblast invasion, and vascular remodeling, and most dNK cell populations are CD56 bright CD16 − NK cells. However, the enrichment and redistribution of dNK cells in the local decidua have not been clarified yet. Method of study:A total of 45 women with normal pregnancies and 8 unexplained recurrent spontaneous abortion (RSA) patients were included. We isolated primary human dNK (n = 53) and peripheral blood NK (pNK) cells (n = 5) from specimen and analyzed CD56, CD82, and CD29 by flow cytometry (FCM). We assessed their adhesion ability by cell counts of NK cells adhered to decidual stromal cells (DSCs) in a co-culture system. Results:We found that RSA patients had more CD56 dim dNK cells with lower CD82 and higher CD29 than women with normal pregnancies. There were negative correlations of CD82 to CD29 on CD56 dim and CD56 + dNK cells. In normal pregnancies, dNK cells had lower CD82 and higher CD29 expression with a stronger adhesion ability than pNK cells. Blocking CD82 on dNK cells increased the adhesive ability and CD29 expression, while blocking CD29 decreased the adhesive ability. Co-culturing dNK cells with trophoblast cells decreased CD82 expression and increased the adhesive ability of dNK cells and the percentage of CD56 bright NK cells, while blocking trophoblast-derived CXCL12 increased CD82 expression, decreased CD29 expression, and impaired the adhesive ability of NK cells. Conclusion: Trophoblast cells enhance the adhesive ability of NK cells to DSCs viathe CXCL12/CD82/CD29 signaling pathway and contribute to CD56 bright NK cell enrichment in the uterus. K E Y W O R D S abortion, adhesion, CD29, CD82, CXC12, decidua, NK, trophoblasts How to cite this article: Lu H, Jin L-P, Huang H-L, et al. Trophoblast-derived CXCL12 promotes CD56 bright CD82 − CD29 + NK cell enrichment in the decidua.Am J Reprod Immunol. 2020;83:e13203.

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“…23 In addition to important roles in immune surveillance, dNK participates in two processes necessary for implantation of the blastocyst and development of the placenta: (a) participation in the process of invasion of the trophoblast and (b) a role in angiogenesis. [24][25][26] Decidual NK may differentiate locally under the influence of tissue-derived TGF-β produced by DSCs. [24][25][26] Decidual NK may differentiate locally under the influence of tissue-derived TGF-β produced by DSCs.…”

Section: Discussionmentioning

confidence: 99%

“…7 Numerous studies have demonstrated that DSCs act as key gatekeepers and chief modulators of immune cells at the maternal-fetal interface. [24][25][26] Decidual NK may differentiate locally under the influence of tissue-derived TGF-β produced by DSCs. 21 Progesterone, human chorionic gonadotropin, and prolactin may have an indirect role in priming DSCs or directly acting on NK cells.…”

Section: Discussionmentioning

confidence: 99%

Decidual stromal cells promote the differentiation of CD56^brightCD16⁻NK cells by secreting IL‐24 in early pregnancy

Yang

Zhou

Han

et al. 2019

American J Rep Immunol

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Problem Decidual stromal cells (DSCs) are important origins of cytokines to modulate maternal‐fetal immunotolerance and provide a feasible environment for embryo implantation and development. Interleukin (IL)‐24 is a multifunctional cancer killing cytokine and a pleiotropic immunoregulator with complex potency according to tissue or cell types. Its role in establishment and maintenance of normal pregnancy is largely unknown. The aim of our study was to investigate the function and significance of IL‐24 and its receptor in the coordination between DSCs and natural killer cells (NK) in early pregnancy. Method of study The levels of IL‐24 in DSC, endometrial stromal cell (ESC), peripheral blood NK cells (pNK), or decidual NK cells (dNK) culture supernatants were detected by enzyme‐linked immunosorbent assay (ELISA), and the levels of IL‐24 receptors were determined by real‐time reverse transcriptase‐polymerase chain reaction (RT‐PCR) and flow cytometry assays. The effect of IL‐24 on the functions of decidual NK cells was analyzed by flow cytometry assays in vitro. Results The concentration of IL‐24 in culture supernatant of DSCs was significantly higher than that of ESCs. Both eNK (endometrial NK cells) and dNK highly expressed IL‐24 receptors (IL‐20R1 and IL‐22R1), especially on CD56dim eNK. However, there were extremely low levels of IL‐20R1 and IL‐22R1 on pNK. Recombinant human IL‐24 or DSCs‐secreted IL‐24 downregulated the levels of CD16, Granzyme B, perforin, and interferon (IFN)‐γ and upregulated the levels of inhibitory receptors killer‐cell immunoglobulin‐like receptor (KIR)2DL1 and KIR3DL1, or immunotolerant or angiogenic cytokines (eg, transforming growth factor (TGF)‐β, IL‐10, and IL‐8), and elevated the percentage of CD56brightCD16−dNK in vitro. Conclusion These data suggest that DSCs promote the differentiation of CD56brightCD16−NK with high levels of inhibitory receptors, immunotolerant, and angiogenic cytokines by secreting IL‐24 during decidualization in early pregnancy.

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RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization

Cited by 57 publications

References 53 publications

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Trophoblast‐derived CXCL12 promotes CD56^brightCD82⁻CD29⁺ NK cell enrichment in the decidua

Decidual stromal cells promote the differentiation of CD56^brightCD16⁻NK cells by secreting IL‐24 in early pregnancy

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RANKL-mediated harmonious dialogue between fetus and mother guarantees smooth gestation by inducing decidual M2 macrophage polarization

Cited by 57 publications

References 53 publications

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Lactic Acid: A Novel Signaling Molecule in Early Pregnancy?

Trophoblast‐derived CXCL12 promotes CD56brightCD82−CD29+ NK cell enrichment in the decidua

Decidual stromal cells promote the differentiation of CD56brightCD16−NK cells by secreting IL‐24 in early pregnancy

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Trophoblast‐derived CXCL12 promotes CD56^brightCD82⁻CD29⁺ NK cell enrichment in the decidua

Decidual stromal cells promote the differentiation of CD56^brightCD16⁻NK cells by secreting IL‐24 in early pregnancy