CXCL12 in normal and pathological pregnancies: A review
Deng Ao
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Da-Jin Li
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
NHC Key Laboratory of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Correspondence
Ming-Qing Li and Da-Jin Li, Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University Shanghai Medical College, Shanghai, China.
Emails: [email protected] (M.Q.L); [email protected] (D.J.L.)
Search for more papers by this authorCorresponding Author
Ming-Qing Li
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
NHC Key Laboratory of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Correspondence
Ming-Qing Li and Da-Jin Li, Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University Shanghai Medical College, Shanghai, China.
Emails: [email protected] (M.Q.L); [email protected] (D.J.L.)
Search for more papers by this authorDeng Ao
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Search for more papers by this authorCorresponding Author
Da-Jin Li
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
NHC Key Laboratory of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Correspondence
Ming-Qing Li and Da-Jin Li, Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University Shanghai Medical College, Shanghai, China.
Emails: [email protected] (M.Q.L); [email protected] (D.J.L.)
Search for more papers by this authorCorresponding Author
Ming-Qing Li
Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
NHC Key Laboratory of Reproduction Regulation (Shanghai Institute of Planned Parenthood Research), Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Shanghai Key Laboratory of Female Reproductive Endocrine Related Diseases, Hospital of Obstetrics and Gynecology, Fudan University, Shanghai, China
Correspondence
Ming-Qing Li and Da-Jin Li, Laboratory for Reproductive Immunology, Hospital of Obstetrics and Gynecology, Fudan University Shanghai Medical College, Shanghai, China.
Emails: [email protected] (M.Q.L); [email protected] (D.J.L.)
Search for more papers by this authorAbstract
The survival of allogeneic fetuses during pregnancy is a rather paradoxical phenomenon with a complex mechanism. Chemokine ligand12 (CXCL12) and its receptors CXC chemokine receptor (CXCR)4 and 7 are extensively found in placenta tissues and cells, including trophoblast cells, vascular endothelial cells, and decidual stromal and decidual immune cells (eg, NK cells and regulatory T cells). Evidence has illustrated that the CXClL12/CXCR4/CXCR7 axis could enhance the cross talk at the maternal-fetal interface through multiple processes, such as invasion and placental angiogenesis, which appears to be critical signaling components in placentation and fetal outcome. In addition, an increasing number of studies have demonstrated that the CXCL12/CXCR4/CXCR7 axis also stands out for its pleiotropic roles in several pregnancy-associated diseases (eg, recurrent spontaneous abortion (RSA), pre-eclampsia (PE), and preterm labor). In the present review, the different biological properties and signaling in physiological and pathological pregnancy conditions of CXCL12/CXCR4/CXCR7 axis were discussed, with the aim of obtaining a further understanding of the regulatory mechanisms and highlighting their potential as a target for therapeutic approaches.
CONFLICT OF INTEREST
The authors have declared that no competing interest exists.
REFERENCES
- 1Herrler A, von Rango U, Beier HM. Embryo-maternal signalling: how the embryo starts talking to its mother to accomplish implantation. Reprod Biomed Online. 2003; 6(2): 244-256.
- 2Caballero-Campo P, Dominguez F, Coloma J, et al. Hormonal and embryonic regulation of chemokines IL-8, MCP-1 and RANTES in the human endometrium during the window of implantation. Mol Hum Reprod. 2002; 8(4): 375-384.
- 3Wood GW, Hausmann E, Choudhuri R. Relative role of CSF-1, MCP-1/JE, and RANTES in macrophage recruitment during successful pregnancy. Mol Reprod Dev. 1997; 46(1): 62-69; discussion 69–70.
10.1002/(SICI)1098-2795(199701)46:1<62::AID-MRD10>3.0.CO;2-5 CAS PubMed Web of Science® Google Scholar
- 4Fredriksson R, Lagerstrom MC, Lundin LG, Schioth HB. The G-protein-coupled receptors in the human genome form five main families. Phylogenetic analysis, paralogon groups, and fingerprints. Mol Pharmacol. 2003; 63(6): 1256-1272.
- 5Du MR, Wang SC, Li DJ. The integrative roles of chemokines at the maternal-fetal interface in early pregnancy. Cell Mol Immunol. 2014; 11(5): 438-448.
- 6Colobran R, Pujol-Borrell R, Armengol MP, Juan M. The chemokine network. I. How the genomic organization of chemokines contains clues for deciphering their functional complexity. Clin Exp Immunol. 2007; 148(2): 208-217.
- 7Zlotnik A, Yoshie O. Chemokines: a new classification system and their role in immunity. Immunity. 2000; 12(2): 121-127.
- 8Balabanian K, Lagane B, Infantino S, et al. The chemokine SDF-1/CXCL12 binds to and signals through the orphan receptor RDC1 in T lymphocytes. J Biol Chem. 2005; 280(42): 35760-35766.
- 9Thelen M. Dancing to the tune of chemokines. Nat Immunol. 2001; 2(2): 129-134.
- 10Meng YH, Shao J, Li H, et al. CsA improves the trophoblasts invasiveness through strengthening the cross-talk of trophoblasts and decidual stromal cells mediated by CXCL12 and CD82 in early pregnancy. Int J Clin Exp Pathol. 2012; 5(4): 299-307.
- 11Li MQ, Tang CL, Du MR, et al. CXCL12 controls over-invasion of trophoblasts via upregulating CD82 expression in DSCs at maternal-fetal interface of human early pregnancy in a paracrine manner. Int J Clin Exp Pathol. 2011; 4(3): 276-286.
- 12Wu X, Li DJ, Yuan MM, Zhu Y, Wang MY. The expression of CXCR4/CXCL12 in first-trimester human trophoblast cells. Biol Reprod. 2004; 70(6): 1877-1885.
- 13Zhou WH, Du MR, Dong L, Yu J, Li DJ. Chemokine CXCL12 promotes the cross-talk between trophoblasts and decidual stromal cells in human first-trimester pregnancy. Hum Reprod. 2008; 23(12): 2669-2679.
- 14Zhao H-B, Tang C-L, Hou Y-L, et al. CXCL12/CXCR4 axis triggers the activation of EGF receptor and ERK signaling pathway in CsA-induced proliferation of human trophoblast cells. PLoS One. 2012; 7(7):e38375.
- 15Hanna J, Wald O, Goldman-Wohl D, et al. CXCL12 expression by invasive trophoblasts induces the specific migration of CD16- human natural killer cells. Blood. 2003; 102(5): 1569-1577.
- 16Schanz A, Winn VD, Fisher SJ, et al. Pre-eclampsia is associated with elevated CXCL12 levels in placental syncytiotrophoblasts and maternal blood. Eur J Obstet Gynecol Reprod Biol. 2011; 157(1): 32-37.
- 17Coulomb-L'Hermine A, Emilie D, Durand-Gasselin I, Galanaud P, Chaouat G. SDF-1 production by placental cells: a potential mechanism of inhibition of mother-to-fetus HIV transmission. AIDS Res Hum Retroviruses. 2000; 16(11): 1097-1098.
- 18Red-Horse K, Drake PM, Gunn MD, Fisher SJ. Chemokine ligand and receptor expression in the pregnant uterus: reciprocal patterns in complementary cell subsets suggest functional roles. Am J Pathol. 2001; 159(6): 2199-2213.
- 19Schanz A, Baston-Bust D, Krussel JS, Heiss C, Janni W, Hess AP. CXCR7 and syndecan-4 are potential receptors for CXCL12 in human cytotrophoblasts. J Reprod Immunol. 2011; 89(1): 18-25.
- 20Douglas GC, Thirkill TL, Sideris V, Rabieh M, Trollinger D, Nuccitelli R. Chemokine receptor expression by human syncytiotrophoblast. J Reprod Immunol. 2001; 49(2): 97-114.
- 21Athanassakis I, Papadimitriou L, Koumantakis E, Vassiliadis S. Th1- and Th2-type lymphokine-assisted induction and release of chemokine receptors from primary human trophoblast cells. Hum Immunol. 2000; 61(7): 651-657.
- 22Drake PM, Red-Horse K, Fisher SJ. Reciprocal chemokine receptor and ligand expression in the human placenta: implications for cytotrophoblast differentiation. Dev Dyn. 2004; 229(4): 877-885.
- 23Red-Horse K, Kapidzic M, Zhou Y, Feng KT, Singh H, Fisher SJ. EPHB4 regulates chemokine-evoked trophoblast responses: a mechanism for incorporating the human placenta into the maternal circulation. Development. 2005; 132(18): 4097-4106.
- 24Parry S, Zhang J, Koi H, Arechavaleta-Velasco F, Elovitz MA. Transcytosis of Human immunodeficiency virus 1 across the placenta is enhanced by treatment with tumour necrosis factor alpha. J Gen Virol. 2006; 87(Pt 8): 2269-2278.
- 25Jaleel MA, Tsai AC, Sarkar S, Freedman PV, Rubin LP. Stromal cell-derived factor-1 (SDF-1) signalling regulates human placental trophoblast cell survival. Mol Hum Reprod. 2004; 10(12): 901-909.
- 26Kumar A, Kumar S, Dinda AK, Luthra K. Differential expression of CXCR4 receptor in early and term human placenta. Placenta. 2004; 25(4): 347-351.
- 27Tripathi V, Verma R, Dinda A, Malhotra N, Kaur J, Luthra K. Differential expression of RDC1/CXCR7 in the human placenta. J Clin Immunol. 2009; 29(3): 379-386.
- 28Park DW, Lee HJ, Park CW, Hong SR, Kwak-Kim J, Yang KM. Peripheral blood NK cells reflect changes in decidual NK cells in women with recurrent miscarriages. Am J Reprod Immunol. 2010; 63(2): 173-180.
- 29Zhou WH, Ren L, Liu Y, Zhang YZ. Expression of chemokine receptor CXCR7 in human first-trimester trophoblasts and decidual stromal cells. Chin J Clin (Electronic Edition). 2013; 4: 1436-1440.
- 30Fear WR, Kesson AM, Naif H, Lynch GW, Cunningham AL. Differential tropism and chemokine receptor expression of human immunodeficiency virus type 1 in neonatal monocytes, monocyte-derived macrophages, and placental macrophages. J Virol. 1998; 72(2): 1334-1344.
- 31Vacca P, Moretta L, Moretta A, Mingari MC. Origin, phenotype and function of human natural killer cells in pregnancy. Trends Immunol. 2011; 32(11): 517-523.
- 32Lin Y, Xu L, Jin H, Zhong Y, Di J, Lin QD. CXCL12 enhances exogenous CD4+CD25+ T cell migration and prevents embryo loss in non-obese diabetic mice. Fertil Steril. 2009; 91(6): 2687-2696.
- 33Spencer HL, Jover E, Cathery W, et al. Role of TPBG (Trophoblast Glycoprotein) antigen in human pericyte migratory and angiogenic activity. Arterioscler Thromb Vasc Biol. 2019; 39(6): 1113-1124.
- 34Schanz A, Red-Horse K, Hess AP, Baston-Bust DM, Heiss C, Krussel JS. Oxygen regulates human cytotrophoblast migration by controlling chemokine and receptor expression. Placenta. 2014; 35(12): 1089-1094.
- 35Schanz A, Lukosz M, Hess AP, Baston-Bust DM, Krussel JS, Heiss C. hCG stimulates angiogenic signals in lymphatic endothelial and circulating angiogenic cells. J Reprod Immunol. 2015; 110: 102-108.
- 36Hao H, Hu S, Chen H, et al. Loss of endothelial CXCR7 impairs vascular homeostasis and cardiac remodeling after myocardial infarction: implications for cardiovascular drug discovery. Circulation. 2017; 135(13): 1253-1264.
- 37Zheng J, Wang H, Zhou W. Modulatory effects of trophoblast-secreted CXCL12 on the migration and invasion of human first-trimester decidual epithelial cells are mediated by CXCR4 rather than CXCR7. Reprod Biol Endocrinol. 2018; 16(1): 17.
- 38Quinn KE, Ashley AK, Reynolds LP, Grazul-Bilska AT, Ashley RL. Activation of the CXCL12/CXCR4 signaling axis may drive vascularization of the ovine placenta. Domest Anim Endocrinol. 2014; 47: 11-21.
- 39Giakoumelou S, Wheelhouse N, Brown J, et al. Chlamydia trachomatis infection of human endometrial stromal cells induces defective decidualisation and chemokine release. Sci Rep. 2017; 7(1): 2001.
- 40Zhou WH, Wu X, Hu WD, Du MR. Co-expression of CXCR4 and CXCR7 in human endometrial stromal cells is modulated by steroid hormones. Int J Clin Exp Pathol. 2015; 8(3): 2449-2460.
- 41Ruiz A, Ruiz L, Colón-Caraballo M, et al. Pharmacological blockage of the CXCR4-CXCL12 axis in endometriosis leads to contrasting effects in proliferation, migration, and invasion. Biol Reprod. 2018; 98(1): 4-14.
- 42Mei J, Zhu XY, Jin LP, Duan ZL, Li DJ, Li MQ. Estrogen promotes the survival of human secretory phase endometrial stromal cells via CXCL12/CXCR4 up-regulation-mediated autophagy inhibition. Hum Reprod. 2015; 30(7): 1677-1689.
- 43Hwang JH, Lee MJ, Seok OS, et al. Cytokine expression in placenta-derived mesenchymal stem cells in patients with pre-eclampsia and normal pregnancies. Cytokine. 2010; 49(1): 95-101.
- 44Lei G-Q, Wu Z-Y, Jiang W-B, et al. Effect of CXCL12/CXCR4 on migration of decidua-derived mesenchymal stem cells from pregnancies with preeclampsia. Am J Reprod Immunol. 2019; 82(5):e13180.
- 45Zhu B, Xu D, Deng X, et al. CXCL12 enhances human neural progenitor cell survival through a CXCR7- and CXCR4-mediated endocytotic signaling pathway. Stem Cells. 2012; 30(11): 2571-2583.
- 46Fujita D, Tanabe A, Sekijima T, et al. Role of extracellular signal-regulated kinase and AKT cascades in regulating hypoxia-induced angiogenic factors produced by a trophoblast-derived cell line. J Endocrinol. 2010; 206(1): 131-140.
- 47Tamaru S, Mizuno Y, Tochigi H, et al. MicroRNA-135b suppresses extravillous trophoblast-derived HTR-8/SVneo cell invasion by directly down regulating CXCL12 under low oxygen conditions. Biochem Biophys Res Commun. 2015; 461(2): 421-426.
- 48Chim SSC, Shing TKF, Hung ECW, et al. Detection and characterization of placental microRNAs in maternal plasma. Clin Chem. 2008; 54(3): 482-490.
- 49Tsuzuki T, Okada H, Cho H, et al. Hypoxic stress simultaneously stimulates vascular endothelial growth factor via hypoxia-inducible factor-1alpha and inhibits stromal cell-derived factor-1 in human endometrial stromal cells. Hum Reprod. 2012; 27(2): 523-530.
- 50Ceradini DJ, Kulkarni AR, Callaghan MJ, et al. Progenitor cell trafficking is regulated by hypoxic gradients through HIF-1 induction of SDF-1. Nat Med. 2004; 10(8): 858-864.
- 51Wang K, Jiang YZ, Chen DB, Zheng J. Hypoxia enhances FGF2- and VEGF-stimulated human placental artery endothelial cell proliferation: roles of MEK1/2/ERK1/2 and PI3K/AKT1 pathways. Placenta. 2009; 30(12): 1045-1051.
- 52Tuuli MG, Longtine MS, Nelson DM. Review: oxygen and trophoblast biology–a source of controversy. Placenta. 2011; 32(Suppl 2): S109-118.
- 53Kong D, Park EJ, Stephen AG, et al. Echinomycin, a small-molecule inhibitor of hypoxia-inducible factor-1 DNA-binding activity. Cancer Res. 2005; 65(19): 9047-9055.
- 54Tsutsumi A, Okada H, Nakamoto T, Okamoto R, Yasuda K, Kanzaki H. Estrogen induces stromal cell-derived factor 1 (SDF-1/CXCL12) production in human endometrial stromal cells: a possible role of endometrial epithelial cell growth. Fertil Steril. 2011; 95(1): 444-447.
- 55Okada H, Okamoto R, Tsuzuki T, Tsuji S, Yasuda K, Kanzaki H. Progestins inhibit estradiol-induced vascular endothelial growth factor and stromal cell-derived factor 1 in human endometrial stromal cells. Fertil Steril. 2011; 96(3): 786-791.
- 56Boudot A, Kerdivel G, Habauzit D, et al. Differential estrogen-regulation of CXCL12 chemokine receptors, CXCR4 and CXCR7, contributes to the growth effect of estrogens in breast cancer cells. PLoS One. 2011; 6(6):e20898.
- 57Salvucci O, Yao L, Villalba S, Sajewicz A, Pittaluga S, Tosato G. Regulation of endothelial cell branching morphogenesis by endogenous chemokine stromal-derived factor-1. Blood. 2002; 99(8): 2703-2711.
- 58Salcedo R, Oppenheim JJ. Role of chemokines in angiogenesis: CXCL12/SDF-1 and CXCR4 interaction, a key regulator of endothelial cell responses. Microcirculation. 2003; 10(3–4): 359-370.
- 59Barrientos G, Tirado-González I, Freitag N, et al. CXCR4(+) dendritic cells promote angiogenesis during embryo implantation in mice. Angiogenesis. 2013; 16(2): 417-427.
- 60Li L, Tu J, Jiang Y, Zhou J, Yabe S, Schust DJ. Effects of lipopolysaccharide on human first trimester villous cytotrophoblast cell function in vitro. Biol Reprod. 2016; 94(2): 33.
- 61Du MR, Zhou WH, Piao HL, Li MQ, Tang CL, Li DJ. Cyclosporin A promotes crosstalk between human cytotrophoblast and decidual stromal cell through up-regulating CXCL12/CXCR4 interaction. Hum Reprod. 2012; 27(7): 1955-1965.
- 62Tang C, Chen L, Gu W, et al. Cyclosporin A enhances the ability of trophoblasts to displace the activated human umbilical vein endothelial cell monolayers. Int J Clin Exp Pathol. 2013; 6(11): 2441-2450.
- 63Grasso E, Gori S, Paparini D, et al. VIP induces the decidualization program and conditions the immunoregulation of the implantation process. Mol Cell Endocrinol. 2018; 460: 63-72.
- 64Chen TG, Zhong ZY, Sun GF, Zhou YX, Zhao Y. Effects of tumour necrosis factor-alpha on activity and nitric oxide synthase of endothelial progenitor cells from peripheral blood. Cell Prolif. 2011; 44(4): 352-359.
- 65Piao H-L, Tao YU, Zhu R, et al. The CXCL12/CXCR4 axis is involved in the maintenance of Th2 bias at the maternal/fetal interface in early human pregnancy. Cell Mol Immunol. 2012; 9(5): 423-430.
- 66Iikura M, Miyamasu M, Yamaguchi M, et al. Chemokine receptors in human basophils: inducible expression of functional CXCR4. J Leukoc Biol. 2001; 70(1): 113-120.
- 67Gupta SK, Lysko PG, Pillarisetti K, Ohlstein E, Stadel JM. Chemokine receptors in human endothelial cells. Functional expression of CXCR4 and its transcriptional regulation by inflammatory cytokines. J Biol Chem. 1998; 273(7): 4282-4287.
- 68Nagase H, Miyamasu M, Yamaguchi M, et al. Cytokine-mediated regulation of CXCR4 expression in human neutrophils. J Leukoc Biol. 2002; 71(4): 711-717.
- 69Ruiz A, Salvo VA, Ruiz LA, Baez P, Garcia M, Flores I. Basal and steroid hormone-regulated expression of CXCR4 in human endometrium and endometriosis. Reprod Sci. 2010; 17(10): 894-903.
- 70Tripathi V, Kumar R, Dinda AK, Kaur J, Luthra K. CXCL12-CXCR7 signaling activates ERK and Akt pathways in human choriocarcinoma cells. Cell Commun Adhes. 2014; 21(4): 221-228.
- 71Knofler M, Pollheimer J. IFPA Award in Placentology lecture: molecular regulation of human trophoblast invasion. Placenta. 2012; 33(Suppl): S55-62.
- 72Soares MJ, Chakraborty D, Renaud SJ, et al. Regulatory pathways controlling the endovascular invasive trophoblast cell lineage. J Reprod Dev. 2012; 58(3): 283-287.
- 73Kent LN, Rumi MA, Kubota K, Lee DS, Soares MJ. FOSL1 is integral to establishing the maternal-fetal interface. Mol Cell Biol. 2011; 31(23): 4801-4813.
- 74Du M-R, Zhou W-H, Yan F-T, et al. Cyclosporine A induces titin expression via MAPK/ERK signalling and improves proliferative and invasive potential of human trophoblast cells. Hum Reprod. 2007; 22(9): 2528-2537.
- 75Ren L, Liu YQ, Zhou WH, Zhang YZ. Trophoblast-derived chemokine CXCL12 promotes CXCR4 expression and invasion of human first-trimester decidual stromal cells. Hum Reprod. 2012; 27(2): 366-374.
- 76Zhang Y, Zhao H, Zhao D, et al. SDF-1/CXCR4 axis in myelodysplastic syndromes: correlation with angiogenesis and apoptosis. Leuk Res. 2012; 36(3): 281-286.
- 77Lockwood CJ, Krikun G, Hickey M, Huang SJ, Schatz F. Decidualized human endometrial stromal cells mediate hemostasis, angiogenesis, and abnormal uterine bleeding. Reprod Sci. 2009; 16(2): 162-170.
- 78Oh YS, Kim HY, Song IC, et al. Hypoxia induces CXCR4 expression and biological activity in gastric cancer cells through activation of hypoxia-inducible factor-1alpha. Oncol Rep. 2012; 28(6): 2239-2246.
- 79Sun Y, Cheng Z, Ma L, Pei G. Beta-arrestin2 is critically involved in CXCR4-mediated chemotaxis, and this is mediated by its enhancement of p38 MAPK activation. J Biol Chem. 2002; 277(51): 49212-49219.
- 80Tang CL, Zhao HB, Li MQ, Du MR, Meng YH, Li DJ. Focal adhesion kinase signaling is necessary for the Cyclosporin A-enhanced migration and invasion of human trophoblast cells. Placenta. 2012; 33(9): 704-711.
- 81Warner JA, Zwezdaryk KJ, Day B, Sullivan DE, Pridjian G, Morris CA. Human cytomegalovirus infection inhibits CXCL12- mediated migration and invasion of human extravillous cytotrophoblasts. Virol J. 2012; 9: 255.
- 82Sanchez-Martin L, Sanchez-Mateos P, Cabanas C. CXCR7 impact on CXCL12 biology and disease. Trends Mol Med. 2013; 19(1): 12-22.
- 83Hartmann TN, Grabovsky V, Pasvolsky R, et al. A crosstalk between intracellular CXCR7 and CXCR4 involved in rapid CXCL12-triggered integrin activation but not in chemokine-triggered motility of human T lymphocytes and CD34+ cells. J Leukoc Biol. 2008; 84(4): 1130-1140.
- 84Chen Q, Zhang M, Li Y, et al. CXCR7 Mediates Neural Progenitor Cells Migration to CXCL12 Independent of CXCR4. Stem Cells. 2015; 33(8): 2574-2585.
- 85Wu X, Jin LP, Yuan MM, Zhu Y, Wang MY, Li DJ. Human first-trimester trophoblast cells recruit CD56brightCD16- NK cells into decidua by way of expressing and secreting of CXCL12/stromal cell-derived factor 1. J Immunol. 2005; 175(1): 61-68.
- 86Tao YU, Li Y-H, Piao H-L, et al. CD56(bright)CD25+ NK cells are preferentially recruited to the maternal/fetal interface in early human pregnancy. Cell Mol Immunol. 2015; 12(1): 77-86.
- 87Lu H, Jin LP, Huang HL, et al. Trophoblast-derived CXCL12 promotes CD56(bright) CD82(-) CD29(+) NK cell enrichment in the decidua. Am J Reprod Immunol. 2020; 83(2). e13203
- 88Lin Y, Wang H, Wang W, Zeng S, Zhong Y, Li DJ. Prevention of embryo loss in non-obese diabetic mice using adoptive ITGA2(+)ISG20(+) natural killer-cell transfer. Reproduction. 2009; 137(6): 943-955.
- 89Ramhorst R, Grasso E, Paparini D, et al. Decoding the chemokine network that links leukocytes with decidual cells and the trophoblast during early implantation. Cell Adh Migr. 2016; 10(1–2): 197-207.
- 90Piao HL, Wang SC, Tao Y, Fu Q, Du MR, Li DJ. CXCL12/CXCR4 signal involved in the regulation of trophoblasts on peripheral NK cells leading to Th2 bias at the maternal-fetal interface. Eur Rev Med Pharmacol Sci. 2015; 19(12): 2153-2161.
- 91Wang Y, Underwood J, Vaughan R, Harmer A, Doyle C, Lehner T. Allo-immunization elicits CCR5 antibodies, SDF-1 chemokines, and CD8-suppressor factors that inhibit transmission of R5 and X4 HIV-1 in women. Clin Exp Immunol. 2002; 129(3): 493-501.
- 92Fraccaroli L, Grasso E, Hauk V, et al. Defects in the vasoactive intestinal peptide (VIP)/VPAC system during early stages of the placental-maternal leucocyte interaction impair the maternal tolerogenic response. Clin Exp Immunol. 2012; 170(3): 310-320.
- 93Hwang HS, Kwon HS, Sohn IS, Park YW, Kim YH. Increased CXCL12 expression in the placentae of women with pre-eclampsia. Eur J Obstet Gynecol Reprod Biol. 2012; 160(2): 137-141.
- 94Lu J, Zhou WH, Ren L, Zhang YZ. CXCR4, CXCR7, and CXCL12 are associated with trophoblastic cells apoptosis and linked to pathophysiology of severe preeclampsia. Exp Mol Pathol. 2016; 100(1): 184-191.
- 95Torbe A, Czajka R, Kordek A, Rzepka R, Kwiatkowski S, Rudnicki J. Maternal serum proinflammatory cytokines in preterm labor with intact membranes: neonatal outcome and histological associations. Eur Cytokine Netw. 2007; 18(2): 102-107.
- 96Combs CA, Gravett M, Garite TJ, et al. Amniotic fluid infection, inflammation, and colonization in preterm labor with intact membranes. Am J Obstet Gynecol. 2014; 210(2): 125e121-125e115.
- 97Tseng JJ, Chen YF, Hsieh YT, Chou MM. Elevated amniotic fluid stromal cell-derived factor-1alpha (SDF-1alpha) concentration in mid-gestation as a predictor of adverse birth outcomes. J Chin Med Assoc. 2009; 72(12): 638-642.
- 98Aminzadeh F, Ghorashi Z, Nabati S, et al. Differential expression of CXC chemokines CXCL10 and CXCL12 in term and pre-term neonates and their mothers. Am J Reprod Immunol. 2012; 68(4): 338-344.