Luteinizing hormone contributes to fetal tolerance by regulating adaptive immune responses

American Journal of Reproductive Immunology

Volumn 71, Issue 5, 2014, Pages 434-440

  Schumacher, Anne ^a   Poloski, Eileen ^a   Spörke, Dominique ^a   Zenclussen, Ana C ^a  

^a OTTO VON GUERICKE UNIVERSITY   (Germany)

Author keywords

Dendritic cell; Luteinizing hormone; Pregnancy; Treg

Indexed keywords

LUTEINIZING HORMONE;

ABORTION, SPONTANEOUS; ADAPTIVE IMMUNITY; ANIMAL; CBA MOUSE; CROSS BREEDING; CYTOLOGY; DBA MOUSE; DENDRITIC CELL; DRUG EFFECTS; FEMALE; FETUS; GESTATIONAL AGE; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; LYMPHOCYTE COUNT; MOUSE; PATHOLOGY; PREGNANCY; REGULATORY T LYMPHOCYTE;

ABORTION, SPONTANEOUS; ADAPTIVE IMMUNITY; ANIMALS; CROSSES, GENETIC; DENDRITIC CELLS; FEMALE; FETUS; GESTATIONAL AGE; HUMANS; IMMUNE TOLERANCE; LUTEINIZING HORMONE; LYMPHOCYTE COUNT; MICE; MICE, INBRED CBA; MICE, INBRED DBA; PREGNANCY; T-LYMPHOCYTES, REGULATORY;

EID: 84898789808     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/aji.12215     Document Type: Article

References (26)

1. Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, Alexander T, Taran A, Malfertheiner SF, Costa S, Zimmermann G, Nitschke C, Volk H, Alexander H, Gunzer M, Zenclussen AC: Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol 2009; 182:5488-5497.
2. Schumacher A, Heinze K, Witte J, Poloski E, Linzke N, Woidacki K, Zenclussen AC: Human chorionic gonadotropin as a central regulator of pregnancy immune tolerance. J Immunol 2013; 190:2650-2658.
3. Ueno A, Cho S, Cheng L, Wang J, Hou S, Nakano H, Santamaria P, Yang Y: Transient upregulation of indoleamine 2, 3-dioxygenase in dendritic cells by human chorionic gonadotropin downregulates autoimmune diabetes. Diabetes 2007; 56:1686-1693.
4. Wan H, Versnel MA, Leijten LME, van Helden-Meeuwsen CG, Fekkes D, Leenen PJM, Khan NA, Benner R, Kiekens RCM: Chorionic gonadotropin induces dendritic cells to express a tolerogenic phenotype. J Leukoc Biol 2008; 83:894-901.
5. Segerer SE, Müller N, van Den Brandt J, Kapp M, Dietl J, Reichardt HM, Rieger L, Kämmerer U: Impact of female sex hormones on the maturation and function of human dendritic cells. Am J Reprod Immunol 2009; 62:165-173.
6. Sharma MD, Baban B, Chandler P, Hou D, Singh N, Yagita H, Azuma M, Blazar BR, Mellor AL, Munn DH: Plasmacytoid dendritic cells from mouse tumor-draining lymph nodes directly activate mature Tregs via indoleamine 2, 3-dioxygenase. J Clin Invest 2007; 117:2570-2582.
7. Chen W, Liang X, Peterson AJ, Munn DH, Blazar BR: The indoleamine 2, 3-dioxygenase pathway is essential for human plasmacytoid dendritic cell-induced adaptive T regulatory cell generation. J Immunol 2008; 181:5396-5404.
8. Schumacher A, Wafula PO, Teles A, El-Mousleh T, Linzke N, Zenclussen ML, Langwisch S, Heinze K, Wollenberg I, Casalis PA, Volk H, Fest S, Zenclussen AC, Kassiotis G: Blockage of heme oxygenase-1 abrogates the protective effect of regulatory T cells on murine pregnancy and promotes the maturation of dendritic cells. PLoS ONE 2012; 7:e42301.
9. Tepper MA, Roberts JL: Evidence for only one beta-luteinizing hormone and no beta-chorionic gonadotropin gene in the rat. Endocrinology 1984; 115:385-391.
10. Salesse R, Genty N, Garnier J: Lutropin is processed much more rapidly than human choriogonadotropin by porcine Leydig cells in primary culture. Biol Cell 1983; 49:187-190.
11. Ascoli M, Fanelli F, SegaloffDL: The lutropin/choriogonadotropin receptor, a 2002 perspective. Endocr Rev 2002; 23:141-174.
12. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk H: Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevents fetal rejection in a murine abortion model. Am J Pathol 2005; 166:811-822.
13. 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 2004; 112:38-43.
14. Sasaki Y, Sakai M, Miyazaki S, Higuma S, Shiozaki A, Saito S: Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 2004; 10:347-353.
15. Thuere C, Zenclussen ML, Schumacher A, Langwisch S, Schulte-Wrede U, Teles A, Paeschke S, Volk H, Zenclussen AC: Kinetics of regulatory T cells during murine pregnancy. Am J Reprod Immunol 2007; 58:514-523.
16. Toldi G, Saito S, Shima T, Halmos A, Veresh Z, Vásárhelyi B, Rigó J, Molvarec A: The frequency of peripheral blood CD4+ CD25high FoxP3+ and CD4+ CD25-FoxP3+ regulatory T cells in normal pregnancy and pre-eclampsia. Am J Reprod Immunol 2012; 68:175-180.
17. Schumacher A, Wafula PO, Bertoja AZ, Sollwedel A, Thuere C, Wollenberg I, Yagita H, Volk H, Zenclussen AC: Mechanisms of action of regulatory T cells specific for paternal antigens during pregnancy. Obstet Gynecol 2007; 110:1137-1145.
18. Yin Y, Han X, Shi Q, Zhao Y, He Y: Adoptive transfer of CD4+CD25+ regulatory T cells for prevention and treatment of spontaneous abortion. Eur J Obstet Gynecol Reprod Biol 2012; 161:177-181.
19. Hsu P, Santner-Nanan B, Dahlstrom JE, Fadia M, Chandra A, Peek M, Nanan R: Altered decidual DC-SIGN(+) antigen-presenting cells and impaired regulatory T-cell induction in preeclampsia. Am J Pathol 2012; 181:2149-2160.
20. Blois SM, Alba Soto CD, Tometten M, Klapp BF, Margni RA, Arck PC: Lineage, maturity, and phenotype of uterine murine dendritic cells throughout gestation indicate a protective role in maintaining pregnancy. Biol Reprod 2004; 70:1018-1023.
21. Gridelet V, Tsampalas M, Berndt S, Hagelstein M, Charlet-Renard C, Conrath V, Ectors F, Hugé F, Munaut C, Foidart J, Geenen V, Perrier d'Hauterive S: Evidence for cross-talk between the LH receptor and LH during implantation in mice. Reprod Fertil Dev 2013; 25:511.
22. Hill MJ, Levens ED, Levy G, Ryan ME, Csokmay JM, DeCherney AH, Whitcomb BW: The use of recombinant luteinizing hormone in patients undergoing assisted reproductive techniques with advanced reproductive age: a systematic review and meta-analysis. Fertil Steril 2012; 97:1108-1114.e1.
23. Zenclussen AC, Gerlof K, Zenclussen ML, Ritschel S, Zambon Bertoja A, Fest S, Hontsu S, Ueha S, Matsushima K, Leber J, Volk H: Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur J Immunol 2006; 36:82-94.
24. Arruvito L, Sanz M, Banham AH, Fainboim L: Expansion of CD4+CD25+ and FOXP3+ regulatory T cells during the follicular phase of the menstrual cycle: implications for human reproduction. J Immunol 2007; 178:2572-2578.
25. Weinberg A, Enomoto L, Marcus R, CanniffJ: Effect of menstrual cycle variation in female sex hormones on cellular immunity and regulation. J Reprod Immunol 2011; 89:70-77.
26. Teles A, Schumacher A, Kühnle M, Linzke N, Thuere C, Reichardt P, Tadokoro CE, Hämmerling GJ, Zenclussen AC: Control of uterine microenvironment by Foxp3+ cells facilitates embryo implantation. Front Immunol 2013; 4:158.