Mechanism of human chorionic gonadotrophin-mediated immunomodulation in pregnancy

References

• Cole LA. HCG variants, the growth factors which drive human malignancies. Am. J. Cancer Res. 2(1), 22–35 (2012).
   PubMed Web of Science ®Google Scholar
• Angioni S, Spedicato M, Rizzo A et al. In vitro activity of human chorionic gonadotropin (hCG) on myometrium contractility. Gynecol. Endocrinol. 27(3), 180–184 (2011).
   PubMed Web of Science ®Google Scholar
• Norris W, Nevers T, Sharma S, Kalkunte S. Review: hCG, preeclampsia and regulatory T cells. Placenta 32(Suppl. 2), S182–S185 (2011).
   PubMed Web of Science ®Google Scholar
• Bansal AS. Joining the immunological dots in recurrent miscarriage. Am. J. Reprod. Immunol. 64(5), 307–315 (2010).
   PubMed Web of Science ®Google Scholar
• Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat. Immunol. 5(3), 266–271 (2004).
   PubMed Web of Science ®Google Scholar
• Somerset DA, Zheng Y, Kilby MD, Sansom DM, Drayson MT. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112(1), 38–43 (2004).
   PubMed Web of Science ®Google Scholar
• Santner-Nanan B, Peek MJ, Khanam R et al. Systemic increase in the ratio between Foxp3+ and IL-17-producing CD4+ T cells in healthy pregnancy but not in preeclampsia. J. Immunol. 183(11), 7023–7030 (2009).
   PubMed Web of Science ®Google Scholar
• Herr F, Baal N, Reisinger K et al. HCG in the regulation of placental angiogenesis. Results of an in vitro study. Placenta 28(Suppl. A), S85–S93 (2007).
   PubMedGoogle Scholar
• Kayisli UA, Selam B, Guzeloglu-Kayisli O, Demir R, Arici A. Human chorionic gonadotropin contributes to maternal immunotolerance and endometrial apoptosis by regulating Fas–Fas ligand system. J. Immunol. 171(5), 2305–2313 (2003).
   PubMed Web of Science ®Google Scholar
• Fluhr H, Krenzer S, Stein GM et al. Interferon-γ and tumor necrosis factor-α sensitize primarily resistant human endometrial stromal cells to Fas-mediated apoptosis. J. Cell. Sci. 120(Pt 23), 4126–4133 (2007).
   PubMed Web of Science ®Google Scholar
• Stahn R, Goletz S, Stahn R et al. Human chorionic gonadotropin (hCG) as inhibitior of E-selectin-mediated cell adhesion. Anticancer Res. 25(3A), 1811–1816 (2005).
   PubMedGoogle Scholar
• Kalkunte S, Nevers T, Norris W et al. Presence of non-functional hCG in preeclampsia and rescue of normal pregnancy by recombinant hCG. Placenta 31, A126 (2010).
   PubMedGoogle Scholar
• Chen JZ, Sheehan PM, Brennecke SP, Keogh RJ. Vessel remodelling, pregnancy hormones and extravillous trophoblast function. Mol. Cell. Endocrinol. 349(2), 138–144 (2012).
   PubMed Web of Science ®Google Scholar
• Foidart JM, Schaaps JP, Chantraine F, Munaut C, Lorquet S. Dysregulation of anti-angiogenic agents (sFlt-1, PLGF, and sEndoglin) in preeclampsia – a step forward but not the definitive answer. J. Reprod. Immunol. 82(2), 106–111 (2009).
   PubMed Web of Science ®Google Scholar
• Licht P, Fluhr H, Neuwinger J, Wallwiener D, Wildt L. Is human chorionic gonadotropin directly involved in the regulation of human implantation? Mol. Cell. Endocrinol. 269(1–2), 85–92 (2007).
   PubMed Web of Science ®Google Scholar
• Berndt S, Perrier d’Hauterive S, Blacher S et al. Angiogenic activity of human chorionic gonadotropin through LH receptor activation on endothelial and epithelial cells of the endometrium. FASEB J. 20(14), 2630–2632 (2006).
   PubMed Web of Science ®Google Scholar
• Weedon-Fekjær MS, Taskén K. Review: spatiotemporal dynamics of hCG/cAMP signaling and regulation of placental function. Placenta 33(Suppl.), S87–S91 (2012).
   PubMedGoogle Scholar
• Fluhr H, Bischof-Islami D, Krenzer S, Licht P, Bischof P, Zygmunt M. Human chorionic gonadotropin stimulates matrix metalloproteinases-2 and -9 in cytotrophoblastic cells and decreases tissue inhibitor of metalloproteinases-1, -2, and -3 in decidualized endometrial stromal cells. Fertil. Steril. 90(Suppl. 4), 1390–1395 (2008).
   PubMedGoogle Scholar
• Tsampalas M, Gridelet V, Berndt S, Foidart JM, Geenen V, Perrier d’Hauterive S. Human chorionic gonadotropin: a hormone with immunological and angiogenic properties. J. Reprod. Immunol. 85(1), 93–98 (2010).
   PubMed Web of Science ®Google Scholar
• Fuchs T, Hammarström L, Smith CI, Brundin J. In vitro induction of murine suppressor T-cells by human chorionic gonadotropin. Acta Obstet. Gynecol. Scand. 59(4), 355–359 (1980).
   PubMed Web of Science ®Google Scholar
• Fuchs T, Hammarström L, Smith CI, Brundin J. In vitro induction of human suppressor T cells by a chorionic gonadotropin preparation. J. Reprod. Immunol. 3(2), 75–84 (1981).
   PubMed Web of Science ®Google Scholar
• Yamauchi S, Izumi S, Shiotsuka Y, Watanabe K, Ozawa A. Demonstration of HCG on the surface of maternal lymphocytes and discrimination of T and B cells by esterase cytochemistry. Tokai J. Exp. Clin. Med. 8(4), 333–337 (1983).
   PubMedGoogle Scholar
• Lin J, Lojun S, Lei ZM, Wu WX, Peiner SC, Rao CV. Lymphocytes from pregnant women express human chorionic gonadotropin/luteinizing hormone receptor gene. Mol. Cell. Endocrinol. 111(1), R13–R17 (1995).
   Web of Science ®Google Scholar
• Eblen AC, Gerçel-Taylor C, Nakajima ST, Taylor DD. Modulation of T-cell CD3-zeta chain expression in early pregnancy. Am. J. Reprod. Immunol. 47(3), 167–173 (2002).
   PubMedGoogle Scholar
• Khil LY, Jun HS, Kwon H et al. Human chorionic gonadotropin is an immune modulator and can prevent autoimmune diabetes in NOD mice. Diabetologia 50(10), 2147–2155 (2007).
   PubMedGoogle Scholar
• Ueno A, Cho S, Cheng L et al. Transient upregulation of indoleamine 2,3-dioxygenase in dendritic cells by human chorionic gonadotropin downregulates autoimmune diabetes. Diabetes 56(6), 1686–1693 (2007).
   PubMedGoogle Scholar
• Wan H, Versnel MA, Leijten LM et al. Chorionic gonadotropin induces dendritic cells to express a tolerogenic phenotype. J. Leukoc. Biol. 83(4), 894–901 (2008).
   PubMed Web of Science ®Google Scholar
• Dong M, Ding G, Zhou J, Wang H, Zhao Y, Huang H. The effect of trophoblasts on T lymphocytes: possible regulatory effector molecules – a proteomic analysis. Cell Physiol. Biochem. 21(5–6), 463–472 (2008).
   PubMedGoogle Scholar
• Segerer SE, Müller N, van den Brandt J et al. Impact of female sex hormones on the maturation and function of human dendritic cells. Am. J. Reprod. Immunol. 62(3), 165–173 (2009).
   PubMed Web of Science ®Google Scholar
• Koldehoff M, Katzorke T, Wisbrun NC et al. Modulating impact of human chorionic gonadotropin hormone on the maturation and function of hematopoietic cells. J. Leukoc. Biol. 90(5), 1017–1026 (2011).
   PubMedGoogle Scholar
• Kruse N, Greif M, Moriabadi NF, Marx L, Toyka KV, Rieckmann P. Variations in cytokine mRNA expression during normal human pregnancy. Clin. Exp. Immunol. 119(2), 317–322 (2000).
   PubMed Web of Science ®Google Scholar
• Inoue T, Kanzaki H, Imai K et al. Progesterone stimulates the induction of human endometrial CD56+ lymphocytes in an in vitro culture system. J. Clin. Endocrinol. Metab. 81(4), 1502–1507 (1996).
   PubMed Web of Science ®Google Scholar
• Mao G, Wang J, Kang Y et al. Progesterone increases systemic and local uterine proportions of CD4+CD25+ Treg cells during midterm pregnancy in mice. Endocrinology 151(11), 5477–5488 (2010).
   PubMed Web of Science ®Google Scholar
• Carbone F, Procaccini C, De Rosa V et al. Divergent immunomodulatory effects of recombinant and urinary-derived FSH, LH, and hCG on human CD4+ T cells. J. Reprod. Immunol. 85(2), 172–179 (2010).
   PubMed Web of Science ®Google Scholar
• Kane N, Kelly R, Saunders PT, Critchley HO. Proliferation of uterine natural killer cells is induced by human chorionic gonadotropin and mediated via the mannose receptor. Endocrinology 150(6), 2882–2888 (2009).
   PubMed Web of Science ®Google Scholar
• Nakashima A, Shima T, Inada K, Ito M, Saito S. The balance of the immune system between T cells and NK cells in miscarriage. Am. J. Reprod. Immunol. 67(4), 304–310 (2012).
   PubMed Web of Science ®Google Scholar
• Higuma-Myojo S, Sasaki Y, Miyazaki S et al. Cytokine profile of natural killer cells in early human pregnancy. Am. J. Reprod. Immunol. 54(1), 21–29 (2005).
   PubMed Web of Science ®Google Scholar
• Bansal AS, Bajardeen B, Shehata H, Thum MY. Recurrent miscarriage and autoimmunity. Expert Rev. Clin. Immunol. 7(1), 37–44 (2011).
   PubMed Web of Science ®Google Scholar
• Jasper MJ, Tremellen KP, Robertson SA. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol. Hum. Reprod. 12(5), 301–308 (2006).
   PubMed Web of Science ®Google Scholar
• Jin LP, Chen QY, Zhang T, Guo PF, Li DJ. The CD4+CD25 bright regulatory T cells and CTLA-4 expression in peripheral and decidual lymphocytes are down-regulated in human miscarriage. Clin. Immunol. 133(3), 402–410 (2009).
   PubMed Web of Science ®Google Scholar
• Schumacher A, Brachwitz N, Sohr S et al. Human chorionic gonadotropin attracts regulatory T cells into the fetal–maternal interface during early human pregnancy. J. Immunol. 182(9), 5488–5497 (2009).
   PubMed Web of Science ®Google Scholar
• Thum MY, Bhaskaran S, Abdalla HI et al. An increase in the absolute count of CD56dimCD16+CD69+ NK cells in the peripheral blood is associated with a poorer IVF treatment and pregnancy outcome. Hum. Reprod. 19(10), 2395–2400 (2004).
   PubMed Web of Science ®Google Scholar
• Toldi G, Svec P, Vásárhelyi B et al. Decreased number of FoxP3+ regulatory T cells in preeclampsia. Acta Obstet. Gynecol. Scand. 87(11), 1229–1233 (2008).
   PubMed Web of Science ®Google Scholar
• Singh O, Rao LV, Gaur A, Sharma NC, Alam A, Talwar GP. Antibody response and characteristics of antibodies in women immunized with three contraceptive vaccines inducing antibodies against human chorionic gonadotropin. Fertil. Steril. 52(5), 739–744 (1989).
   PubMedGoogle Scholar
• Talwar GP, Singh O, Pal R et al. A vaccine that prevents pregnancy in women. Proc. Natl Acad. Sci. USA 91(18), 8532–8536 (1994).
   PubMed Web of Science ®Google Scholar
• Wass M, McCann K, Bagshawe KD. Isolation of antibodies to HCG/LH from human sera. Nature 274(5669), 369–370 (1978).
   PubMedGoogle Scholar
• Housseau F, Rouas-Freiss N, Benifla JL et al. Reaction of peripheral-blood lymphocytes to the human chorionic gonadotropin β sub-unit in patients with productive tumors. Int. J. Cancer 63(5), 633–638 (1995).
   PubMedGoogle Scholar
• Amato F, Warnes GM, Kirby CA, Norman RJ. Infertility caused by HCG autoantibody. J. Clin. Endocrinol. Metab. 87(3), 993–997 (2002).
   PubMedGoogle Scholar
• Wang WJ, Hao CF, Yi-Lin et al. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J. Reprod. Immunol. 84(2), 164–170 (2010).
   PubMed Web of Science ®Google Scholar
• Zou SH, Yang ZZ, Zhang P et al. [Autoimmune disorders affect the in vitro fertilization outcome in infertile women]. Zhonghua Nan Ke Xue 14(4), 343–346 (2008).
   PubMedGoogle Scholar
• Nakamura H, Usa T, Motomura M et al. Prevalence of interrelated autoantibodies in thyroid diseases and autoimmune disorders. J. Endocrinol. Invest. 31(10), 861–865 (2008).
   PubMed Web of Science ®Google Scholar
• Dittmar M, Kahaly GJ. Genetics of the autoimmune polyglandular syndrome type 3 variant. Thyroid 20(7), 737–743 (2010).
   PubMed Web of Science ®Google Scholar
• Mintziori G, Anagnostis P, Toulis KA, Goulis DG. Thyroid diseases and female reproduction. Minerva Med. 103(1), 47–62 (2012).
   PubMed Web of Science ®Google Scholar
• Bruysters M, Verhoef-Post M, Themmen AP. Asp330 and Tyr331 in the C-terminal cysteine-rich region of the luteinizing hormone receptor are key residues in hormone-induced receptor activation. J. Biol. Chem. 283(38), 25821–25828 (2008).
   PubMedGoogle Scholar
• Zhang YM, Rao ChV, Lei ZM. Macrophages in human reproductive tissues contain luteinizing hormone/chorionic gonadotropin receptors. Am. J. Reprod. Immunol. 49(2), 93–100 (2003).
   PubMedGoogle Scholar
• Walkington L, Webster J, Hancock BW, Everard J, Coleman RE. Hyperthyroidism and human chorionic gonadotrophin production in gestational trophoblastic disease. Br. J. Cancer 104(11), 1665–1669 (2011).
   PubMed Web of Science ®Google Scholar
• Toulis KA, Goulis DG, Venetis CA, Kolibianakis EM, Tarlatzis BC, Papadimas I. Thyroid autoimmunity and miscarriages: the corpus luteum hypothesis. Med. Hypotheses 73(6), 1060–1062 (2009).
   PubMed Web of Science ®Google Scholar
• Moncayo H, Moncayo R, Benz R, Wolf A, Lauritzen C. Ovarian failure and autoimmunity. Detection of autoantibodies directed against both the unoccupied luteinizing hormone/human chorionic gonadotropin receptor and the hormone-receptor complex of bovine corpus luteum. J. Clin. Invest. 84(6), 1857–1865 (1989).
   PubMedGoogle Scholar
• Checa MA, Espinós JJ, Requena A. Efficacy and safety of human chorionic gonadotropin for follicular phase stimulation in assisted reproduction: a systematic review and meta-analysis. Fertil. Steril. 97(6), 1343–50.e1 (2012).
   PubMedGoogle Scholar
• van der Linden M, Buckingham K, Farquhar C, Kremer JA, Metwally M. Luteal phase support for assisted reproduction cycles. Cochrane Database Syst. Rev. 10, CD009154 (2011).
   Google Scholar
• Chambers AE, Nayini KP, Mills WE, Lockwood GM, Banerjee S. Circulating LH/hCG receptor (LHCGR) may identify pre-treatment IVF patients at risk of OHSS and poor implantation. Reprod. Biol. Endocrinol. 9, 161 (2011).
   PubMedGoogle Scholar
• Bansal AS, Bajardeen B, Thum MY. The basis and value of currently used immunomodulatory therapies in recurrent miscarriage. J. Reprod. Immunol. 93(1), 41–51 (2012).
   PubMed Web of Science ®Google Scholar