The persistence of paternal antigens in the maternal body is involved in regulatory T-cell expansion and fetal-maternal tolerance in murine pregnancy

American Journal of Reproductive Immunology

Volumn 63, Issue 3, 2010, Pages 200-208

  Zenclussen, Maria Laura ^a   Thuere, Catharina ^a   Ahmad, Nadja ^a   Wafula, Paul O ^a   Fest, Stefan ^b   Teles, Ana ^a,b   Leber, Anne ^a,b   Casalis, Pablo A ^a   Bechmann, Ingo ^c   Priller, Josef ^a   Volk, Hans Dieter ^a   Zenclussen, Ana Claudia ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c UNIVERSITY OF LEIPZIG   (Germany)

Author keywords

Fetal maternal interface; Male antigens; Reproductive immunology; Tolerance; Treg cells

Indexed keywords

ALLOANTIGEN; GREEN FLUORESCENT PROTEIN; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ANTIGEN DETECTION; ANTIGEN PRESENTATION; ARTICLE; BREEDING; CELL EXPANSION; CELL LINE; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; FEMALE; FOXP3+ T LYMPHOCYTE; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; LYMPH NODE; MALE; MOUSE; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ABORTION, SPONTANEOUS; ANIMALS; ANTIGENS; FEMALE; FETUS; HISTOCOMPATIBILITY, MATERNAL-FETAL; IMMUNE TOLERANCE; LYMPHOCYTE ACTIVATION; MALE; MATERNAL-FETAL EXCHANGE; MICE; MICE, INBRED C57BL; MICE, INBRED CBA; MICE, INBRED DBA; PREGNANCY; T-LYMPHOCYTES, REGULATORY;

EID: 76749147929     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2009.00793.x     Document Type: Article

References (30)

1. 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.
2. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immun 2004, 5:266-271.
3. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk HD. 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.
4. Thuere C, Zenclussen ML, Schumacher A, Langwisch S, Schulte-Wrede U, Teles A, Paeschke S, Volk HD, Zenclussen ML. Kinetics of regulatory T cells during murine pregnancy. Am J Reprod Immunol 2007, 58:514-523.
5. Schumacher A, Wafula PO, Bertoja AZ, Sollwedel A, Thuere C, Wollenberg I, Yagita H, Volk HD, Zenclussen AC. Mechanisms of action of regulatory T cells specific for paternal antigens during pregnancy. Obstet Gynecol 2007, 110:1137-1145.
6. Wafula PO, Teles A, Schumacher A, Pohl K, Yagita H, Volk HD, Zenclussen AC. PD-1 but not CTLA-4 blockage abrogates the protective effect of regulatory T cells in a pregnancy murine model. Am J Reprod Immunol 2009, 62(5):283-292.
7. Okabe M, Ikawa M, Kominami K, Nakanishi T, Nishimune Y. Green mice as a source of ubiquitous green cells. FEBS Lett 1997, 407:313-319.
8. Blois S, Zenclussen AC, Roux ME, Olmos O, di Conza J, Arck PC, Margni RA. Asymmetric antibodies (AAb) in the female reproductive tract. J Reprod Immunol 2004, 64:31-43.
9. Kirby DR, Billington WD, Bradbury S, Goldstein DJ. Antigen barrier of the mouse placenta. Nature 1964, 204:548-549.
10. Billington WD. The normal fetomaternal immune relationship. Baillieres Clin Obstet Gynaecol 1992, 6:417-438.
11. Andrassy J, Kusaka S, Jankowska-Gan E, Torrealba JR, Haynes LD, Marthaler BR, Tam RC, Illigens BM, Anosova N, Benichou G, Burlingham WJ. Tolerance to noninherited maternal MHC antigens in mice. J Immunol 2003, 171:5554-5561.
12. Yan Z, Lambert NC, Guthrie KA, Porter AJ, Loubiere LS, Loubiere LS, Madeleine MM, Stevens AM, Hermes HM, Nelson JL. Male microchimerism in women without sons: quantitative assessment and correlation with pregnancy history. Am J Med 2005, 118:899-906.
13. Khosrotehrani K, Johnson KL, Guégan S, Stroh H, Bianchi DW. Natural history of fetal cell microchimerism during and following murine pregnancy. J Reprod Immunol 2005, 66:1-12.
14. Tan XW, Liao H, Sun L, Okabe M, Xiao ZC, Dawe GS. Fetal microchimerism in the maternal mouse brain: a novel population of fetal progenitor or stem cells able to cross the blood-brain barrier? Stem Cells 2005, 23:1443-1452.
15. Root-Bernstein RS, DeWitt SH. Semen alloantigens and lymphocytotoxic antibodies in AIDS and ICL. Genetica 1995, 95:133-156.
16. Robertson SA. Seminal plasma and male factor signalling in the female reproductive tract. Cell Tissue Res 2005, 322:43-52.
17. Sargent IL, Borzychowski AM, Redman CW. Immunoregulation in normal pregnancy and pre-eclampsia: an overview. Reprod Biomed Online 2006, 13:680-686.
18. Tilburgs T, Roelen DL, van der Mast BJ, de Groot-Swings GM, Kleijburg C, Scherjon SA, Claas FH. Evidence for a selective migration of fetus-specific CD4+ CD25bright regulatory T cells from the peripheral blood to the decidua in human pregnancy. J Immunol 2008, 180:5737-5745.
19. Bulmer JN, Johnson PM. The T-lymphocyte population in first-trimester human decidua does not express the interleukin-2 receptor. Immunology 1986, 58:685-687.
20. Athanassakis I, Iconomidou B. Cytokine production in the serum and spleen of mice from day 6 to 14 of gestation: cytokines/placenta/spleen/serum. Dev Immunol 1996, 4:247-255.
21. Tezabwala BU, Johnson PM, Rees RC. Inhibition of pregnancy viability in mice following IL-2 administration. Immunology 1989, 67:115-119.
22. Bischof RJ, Lee CS, Brandon MR, Meusen E. Inflammatory response in the pig uterus induced by seminal plasma. J Reprod Immunol 1994, 26:131-146.
23. Autiero M, Abrescia P, Guardiola J. Interaction of seminal plasma proteins with cell surface antigens: presence of a CD4-binding glycoprotein in human seminal plasma. Exp Cell Res 1991, 197:268-271.
24. Robertson SA, Guerin LR, Bromfield JJ, Branson KM, Ahlström AC, Care AS. Seminal fluid drives expansion of the CD4+ CD25+ T regulatory cell pool and induces tolerance to paternal alloantigens in mice. Biol Reprod 2009, 80:1036-1045.
25. Onodera K, Lehmann M, Akalin E, Volk HD, Sayegh MH, Kupiec-Weglinski JW. Induction of " infectious" tolerance to MHC-incompatible cardiac allografts in CD4 monoclonal antibody-treated sensitized rat recipients. J Immunol 1996, 157:1944-1950.
26. Scully R, Qin S, Cobbold S, Waldmann H. Mechanisms in CD4 antibody-mediated transplantation tolerance: kinetics of induction, antigen dependency and role of regulatory T cells. Eur J Immunol 1994, 24:2383-2392.
27. Waldmann H, Graca L, Cobbold S, Adamas E, Tone M, Tone Y. Regulatory T cells and organ transplantation. Semin Immunol 2004, 16:119-126.
28. Zenclussen AC, Gerlof K, Zenclussen ML, Ritschel S, Zambon Bertoja A, Fest S, Hontsu S, Ueha S, Matsushima K, Leber J, Volk HD. Regulatory T cells induce a privileged tolerant microenvironment at the fetal-maternal interface. Eur J Immunol 2006, 36:82-94.
29. Goswami D, Tannetta DS, Magee LA, Fuchisawa A, Redman CW, Sargent IL, von Dadelszen P. Excess syncytiotrophoblast microparticle shedding is a feature of early-onset pre-eclampsia, but not normotensive intrauterine growth restriction. Placenta 2006, 27:56-61.
30. Tafuri A, Alferink J, Möller P, Hämmerling GJ, Arnold B. T cell awareness of paternal alloantigens during pregnancy. Science 1995, 270:630-633.