Elsevier Trophoblast Research Award Lecture: Unique Properties of Decidual T Cells and their Role in Immune Regulation during Human Pregnancy

Placenta

Volumn 31, Issue SUPPL., 2010, Pages

  Tilburgs, T ^a,b   Claas, F H J ^b   Scherjon, S A ^b  

^a HARVARD UNIVERSITY   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

CD4+CD25bright; Decidua; HLA C; Human; T cells

Indexed keywords

CD103 ANTIGEN; CD28 ANTIGEN; CD45 ANTIGEN; CD56 ANTIGEN; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; FAS LIGAND; HLA C ANTIGEN; HLA E ANTIGEN; HLA G ANTIGEN; INDOLEAMINE 2,3 DIOXYGENASE; MAJOR HISTOCOMPATIBILITY ANTIGEN; T LYMPHOCYTE RECEPTOR ALPHA CHAIN; T LYMPHOCYTE RECEPTOR BETA CHAIN; T LYMPHOCYTE RECEPTOR DELTA CHAIN; T LYMPHOCYTE RECEPTOR GAMMA CHAIN; TRANSCRIPTION FACTOR FOXP3;

ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; ANTIGEN RECOGNITION; APOPTOSIS; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL CONTACT; CELL EXPANSION; CELL INTERACTION; CELL PROLIFERATION; CELL SPECIFICITY; CYTOLYSIS; CYTOTOXIC T LYMPHOCYTE; DECIDUA; ENDOMETRIUM; FETOPLACENTAL UNIT; FETUS GROWTH; GENETIC POLYMORPHISM; HLA MATCHING; HUMAN; IMMUNOMODULATION; IMMUNOREGULATION; LYMPHOCYTE DIFFERENTIATION; LYMPHOCYTE PROLIFERATION; NATURAL KILLER CELL; PHENOTYPE; PREGNANCY; PREGNANCY COMPLICATION; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SPONTANEOUS ABORTION; SUPPRESSOR CELL; T CELL DEPLETION; T LYMPHOCYTE; T LYMPHOCYTE ACTIVATION; T LYMPHOCYTE SUBPOPULATION; TROPHOBLAST;

DECIDUA; FEMALE; HLA-C ANTIGENS; HUMANS; MATERNAL-FETAL EXCHANGE; PREGNANCY; T-LYMPHOCYTES;

EID: 76749106973     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2010.01.007     Document Type: Article

References (46)

1. Billinham R.E., Brent L., and Medawar P.B. Actively acquired tolerance of foreign cells. Nature 172 (1953) 603-606
2. van Kampen C.A., Versteeg-vd Voort Maarschalk M.F., Langerak-Langerak J., Roelen D.L., and Claas F.H. Kinetics of the pregnancy-induced humoral and cellular immune response against the paternal HLA class I antigens of the child. Hum Immunol 63 (2002) 452-458
3. Verdijk R.M., Kloosterman A., Pool J., van de K.M., Naipal A.M., van Halteren A.G., et al. Pregnancy induces minor histocompatibility antigen-specific cytotoxic T cells: implications for stem cell transplantation and immunotherapy. Blood 103 (2004) 1961-1964
4. van Kampen C.A., Versteeg-van der Voort Maarschalk M.F., Langerak-Langerak J., van Beelen E., Roelen D.L., and Claas F.H. Pregnancy can induce long-persisting primed CTLs specific for inherited paternal HLA antigens. Hum Immunol 62 (2001) 201-207
5. Munn D.H., Zhou M., Attwood J.T., Bondarev I., Conway S.J., Marshall B., et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science 281 (1998) 1191-1193
6. Makrigiannakis A., Zoumakis E., Kalantaridou S., Coutifaris C., Margioris A.N., Coukos G., et al. Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nat Immunol 2 (2001) 1018-1024
7. Xu C., Mao D., Holers V.M., Palanca B., Cheng A.M., and Molina H. A critical role for murine complement regulator crry in fetomaternal tolerance. Science 287 (2000) 498-501
8. Aluvihare V.R., Kallikourdis M., and Betz A.G. Tolerance, suppression and the fetal allograft. J Mol Med 83 (2005) 88-96
9. Moffett-King A. Natural killer cells and pregnancy. Nat Rev Immunol 2 (2002) 656-663
10. LeMaoult J., Krawice-Radanne I., Dausset J., and Carosella E.D. HLA-G1-expressing antigen-presenting cells induce immunosuppressive CD4+ T cells. Proc Natl Acad Sci U S A 101 (2004) 7064-7069
11. Heemskerk M.B., Roelen D.L., Dankers M.K., van Rood J.J., Claas F.H., Doxiadis II, et al. Allogeneic MHC class I molecules with numerous sequence differences do not elicit a CTL response. Hum Immunol 66 (2005) 969-976
12. Romagnani C., Pietra G., Falco M., Millo E., Mazzarino P., Biassoni R., et al. Identification of HLA-E-specific alloreactive T lymphocytes: a cell subset that undergoes preferential expansion in mixed lymphocyte culture and displays a broad cytolytic activity against allogeneic cells. Proc Natl Acad Sci U S A 99 (2002) 11328-11333
13. Szekeres-Bartho J. Regulation of NK cell cytotoxicity during pregnancy. Reprod Biomed Online 16 (2008) 211-217
14. Manaster I., Mizrahi S., Goldman-Wohl D., Sela H.Y., Stern-Ginossar N., Lankry D., et al. Endometrial NK cells are special immature cells that await pregnancy. J Immunol 181 (2008) 1869-1876
15. Vassiliadou N., and Bulmer J.N. Quantitative analysis of T lymphocyte subsets in pregnant and nonpregnant human endometrium. Biol Reprod 55 (1996) 1017-1022
16. Tilburgs T., van der Mast B.J., Nagtzaam N.M., Roelen D.L., Scherjon S.A., and Claas F.H. Expression of NK cell receptors on decidual T cells in human pregnancy. J Reprod Immunol 80 (2009) 22-32
17. Mincheva-Nilsson L. Pregnancy and gamma/delta T cells: taking on the hard questions. Reprod Biol Endocrinol 1 (2003) 120
18. Mincheva-Nilsson L., Nagaeva O., Sundqvist K.G., Hammarstrom M.L., Hammarstrom S., and Baranov V. Gammadelta T cells of human early pregnancy decidua: evidence for cytotoxic potency. Int Immunol 12 (2000) 585-596
19. Boyson J.E., Rybalov B., Koopman L.A., Exley M., Balk S.P., Racke F.K., et al. CD1d and invariant NKT cells at the human maternal-fetal interface. Proc Natl Acad Sci U S A 99 (2002) 13741-13746
20. Tilburgs T., Roelen D.L., van der Mast B.J., de Groot-Swings G.M., Kleijburg C., Scherjon S.A., et al. 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 180 (2008) 5737-5745
21. Sasaki Y., Sakai M., Miyazaki S., Higuma S., Shiozaki A., and Saito S. Decidual and peripheral blood CD4+CD25+ regulatory T cells in early pregnancy subjects and spontaneous abortion cases. Mol Hum Reprod 10 (2004) 347-353
22. Tilburgs T., Roelen D.L., van der Mast B.J., van Schip J.J., Kleijburg C., Groot-Swings G.M., et al. Differential distribution of CD4(+)CD25(bright) and CD8(+)CD28(-) T-cells in decidua and maternal blood during human pregnancy. Placenta 27 Suppl. A (2006) S47-S53
23. Sakaguchi S., Sakaguchi N., Shimizu J., Yamazaki S., Sakihama T., Itoh M., et al. Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol Rev 182 (2001) 18-32
24. Aluvihare V.R., Kallikourdis M., and Betz A.G. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 5 (2004) 266-271
25. Zenclussen A.C., Gerlof K., Zenclussen M.L., Sollwedel A., Bertoja A.Z., Ritter T., et al. 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 166 (2005) 811-822
26. Moldenhauer L.M., Diener K.R., Thring D.M., Brown M.P., Hayball J.D., and Robertson S.A. Cross-presentation of male seminal fluid antigens elicits T cell activation to initiate the female immune response to pregnancy. J Immunol 182 (2009) 8080-8093
27. Arruvito L., Sanz M., Banham A.H., and 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 178 (2007) 2572-2578
28. Polanczyk M.J., Carson B.D., Subramanian S., Afentoulis M., Vandenbark A.A., Ziegler S.F., et al. Cutting edge: estrogen drives expansion of the CD4+CD25+ regulatory T cell compartment. J Immunol 173 (2004) 2227-2230
29. Prieto G.A., and Rosenstein Y. Oestradiol potentiates the suppressive function of human CD4 CD25 regulatory T cells by promoting their proliferation. Immunology 118 (2006) 58-65
30. Somerset D.A., Zheng Y., Kilby M.D., Sansom D.M., and Drayson M.T. Normal human pregnancy is associated with an elevation in the immune suppressive CD25+ CD4+ regulatory T-cell subset. Immunology 112 (2004) 38-43
31. Heikkinen J., Mottonen M., Alanen A., and Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol 136 (2004) 373-378
32. Mjosberg J., Svensson J., Johansson E., Hellstrom L., Casas R., Jenmalm M.C., et al. Systemic reduction of functionally suppressive CD4dimCD25highFoxp3+ Tregs in human second trimester pregnancy is induced by progesterone and 17beta-estradiol. J Immunol 183 (2009) 759-769
33. van Lier R.A., ten Berge I.J., and Gamadia L.E. Human CD8(+) T-cell differentiation in response to viruses. Nat Rev Immunol 3 (2003) 931-939
34. Chang C.C., Ciubotariu R., Manavalan J.S., Yuan J., Colovai A.I., Piazza F., et al. Tolerization of dendritic cells by T(S) cells: the crucial role of inhibitory receptors ILT3 and ILT4. Nat Immunol 3 (2002) 237-243
35. Tilburgs T., Scherjon S.A., Roelen D.L., and Claas F.H. Decidual CD8+CD28- T cells express CD103 but not perforin. Hum Immunol 70 (2009) 96-100
36. Scaife P.J., Bulmer J.N., Robson S.C., Innes B.A., and Searle R.F. Effector activity of decidual CD8+ T lymphocytes in early human pregnancy. Biol Reprod 75 (2006) 562-567
37. Shao L., Jacobs A.R., Johnson V.V., and Mayer L. Activation of CD8+ regulatory T cells by human placental trophoblasts. J Immunol 174 (2005) 7539-7547
38. Tilburgs T., Scherjon S.A., van der Mast B.J., Haasnoot G.W., Versteeg V., Roelen D.L., et al. Fetal-maternal HLA-C mismatch is associated with decidual T cell activation and induction of functional T regulatory cells. J Reprod Immunol 82 (2009) 148-157
39. Game D.S., and Lechler R.I. Pathways of allorecognition: implications for transplantation tolerance. Transpl Immunol 10 (2002) 101-108
40. Johnson K.L., and Bianchi D.W. Fetal cells in maternal tissue following pregnancy: what are the consequences?. Hum Reprod Update 10 (2004) 497-502
41. Kallikourdis M., Andersen K.G., Welch K.A., and Betz A.G. Alloantigen-enhanced accumulation of CCR5+ 'effector' regulatory T cells in the gravid uterus. Proc Natl Acad Sci U S A 104 (2007) 594-599
42. Sasaki Y., Darmochwal-Kolarz D., Suzuki D., Sakai M., Ito M., Shima T., et al. Proportion of peripheral blood and decidual CD4(+) CD25(bright) regulatory T cells in pre-eclampsia. Clin Exp Immunol 149 (2007) 139-145
43. Jasper M.J., Tremellen K.P., and Robertson S.A. Primary unexplained infertility is associated with reduced expression of the T-regulatory cell transcription factor Foxp3 in endometrial tissue. Mol Hum Reprod 12 (2006) 301-308
44. Matzinger P. Friendly and dangerous signals: is the tissue in control?. Nat Immunol 8 (2007) 11-13
45. Williams P.J., Searle R.F., Robson S.C., Innes B.A., and Bulmer J.N. Decidual leucocyte populations in early to late gestation normal human pregnancy. J Reprod Immunol 82 (2009) 24-31
46. Miko E., Szereday L., Barakonyi A., Jarkovich A., Varga P., and Szekeres-Bartho J. The role of invariant NKT cells in pre-eclampsia. Am J Reprod Immunol 60 (2008) 118-126