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Human Trophoblasts Recruited T Lymphocytes and Monocytes into Decidua by Secretion of Chemokine CXCL16 and Interaction with CXCR6 in the First-Trimester Pregnancy¹

Yu Huang^*,, Xiao-Yong Zhu^*, Mei-Rong Du^* and Da-Jin Li^2,*,

^* Laboratory for Reproductive Immunology, Hospital and Institute of Obstetrics and Gynecology, Shanghai Medical College, Fudan University, Shanghai, China; Department of Gynecology, Affiliated Hospital of Medical College, Qingdao University, Qingdao, China; and Department of Obstetrics and Gynecology, Affiliated Hospital, Hainan Medical College, Haikou, China

During human early pregnancy, fetus-derived trophoblasts come into direct contact with maternal immune cells at the maternofetal interface. At sites of placental attachment, invasive extravillous trophoblasts encounter decidual leukocytes (DLC) that accumulate within the decidua. Because we first found chemokine CXCL16 was highly expressed in and secreted by the first-trimester human trophoblasts previously, in this study we tested the hypothesis of whether the fetal trophoblasts can direct migration of maternal T lymphocyte and monocytes into decidua by secreting CXCL16. We analyzed the transcription and translation of CXCL16 in the isolated first-trimester human trophoblast, and examined the kinetic secretion of CXCL16 in the supernatant of the primary-cultured trophoblasts. We demonstrated that the sole receptor of CXCL16, CXCR6, is preferentially expressed in T lymphocytes, NKT cells, and monocytes, hardly expressed in two subsets of NK cells from either the peripheral blood or decidua. We further demonstrated the chemotactic activity of CXCL16 in the supernatant of the primary trophoblast on the peripheral mononuclear cells and DLC. Moreover, the CXCL16/CXCR6 interaction is involved in the migration of the peripheral T lymphocytes, T cells, and monocytes, but not NKT cells. In addition, the trophoblast-conditioned medium could enrich PBMC subsets selectively to constitute a leukocyte population with similar composition to that of DLC, which suggests that the fetus-derived trophoblasts can attract T cells, T cells, and monocytes by producing CXCL16 and interaction with CXCR6 on these cells, leading to forming a specialized immune milieu at the maternofetal interface.

The costs of publication of this article were defrayed in part by the payment of page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.

¹ This work was supported by the National Basic Research Program of China (2006CB944009, to D.-J.L.), the Key Project of the National Natural Science Foundation of China (30730087, to D.-J.L.), the National Natural Science Foundation of China (30670787 to D.-J.L. and 30700763 to Y.H.), Shanghai Leading Academic Discipline Project B117 (to D.-J.L.), and the Program for the Outstanding Medical Academic Leader of Shanghai (to D.-J.L.).

² Address correspondence and reprint requests to Dr. Da-Jin Li, Laboratory for Reproductive Immunology, Hospital and Institute of Obstetrics and Gynecology, Shanghai Medical College, Fudan University, Shanghai 200011, China. E-mail address: djli{at}shmu.edu.cn

³ Abbreviations used in this paper: EVCT, extravillous trophoblast; ST, syncytiotrophoblast; DLC, decidual leukocyte; VCT, villous trophoblast; rh, recombinant human.

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