Role of PD1/PDL1 pathway, and TH17 and treg cells in maternal tolerance to the fetus

Biomedical Journal

Volumn 38, Issue 1, 2015, Pages 25-31

  Tripathi, Sudipta ^a,b   Guleria, Indira ^a,b  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

feto maternal tolerance; PD1 PDL1; Th17

Indexed keywords

FETAL ANTIGEN; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; CD274 PROTEIN, HUMAN; PDCD1 PROTEIN, HUMAN;

FEMALE; FETUS; GESTATION PERIOD; HOMEOSTASIS; HUMAN; IMMUNOCOMPETENT CELL; IMMUNOLOGICAL TOLERANCE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LYMPHOCYTE PROLIFERATION; MOLECULAR INTERACTION; MOTHER FETUS RELATIONSHIP; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW; TH17 CELL; ANIMAL; CYTOLOGY; IMMUNOLOGY;

ANIMALS; ANTIGENS, CD274; FETUS; HUMANS; IMMUNE TOLERANCE; PROGRAMMED CELL DEATH 1 RECEPTOR; T-LYMPHOCYTES, REGULATORY; TH17 CELLS;

EID: 84923365870     PISSN: 23194170     EISSN: None     Source Type: Journal    
DOI: 10.4103/2319-4170.143511     Document Type: Review

References (83)

1. Zourbas S, Dubanchet S, Martal J, Chaouat G. Localization of pro-inflammatory (IL-12, IL-15) and anti-inflammatory (IL-11, IL-13) cytokines at the foetomaternal interface during murine pregnancy. Clin Exp Immunol 2001;126:519-28
2. Blois SM, Joachim R, Kandil J, Margni R, Tometten M, Klapp BF, Arck PC. Depletion of CD8+ cells abolishes the pregnancy protective effect of progesterone substitution with dydrogesterone in mice by altering the Th1/Th2 cytokine profile. J Immunol 2004;172:5893-9
3. Lin H, Mosmann TR, Guilbert L, Tuntipopipat S, Wegmann TG. Synthesis of T helper 2-type cytokines at the maternal-fetal interface. J Immunol 1993;151:4562-73
4. Piccinni MP. T cell tolerance towards the fetal allograft. J Reprod Immunol 2010;85:71-5
5. Blois SM, Klapp BF, Barrientos G. Decidualization and angiogenesis in early pregnancy: Unravelling the functions of DC and NK cells. J Reprod Immunol 2011;88:86-92
6. Wilczynski JR. Th1/Th2 cytokines balance-yin and yang of reproductive immunology. Eur J Obstet Gynecol Reprod Biol 2005;122:136-43
7. Saito S, Nakashima A, Shima T, Ito M. Th1/Th2/Th17 and regulatory T-cell paradigm in pregnancy. Am J Reprod Immunol 2010;63:601-10
8. Guleria I, Sayegh MH. Maternal acceptance of the fetus: True human tolerance. J Immunol 2007;178:3345-51
9. Riley JK. Trophoblast immune receptors in maternal-fetal tolerance. Immunol Invest 2008;37:395-426
10. Clark DA, Chaouat G, Wong K, Gorczynski RM, Kinsky R. Tolerance mechanisms in pregnancy: A reappraisal of the role of class I paternal MHC antigens. Am J Reprod Immunol 2010;63:93-103
11. Leber A, Zenclussen ML, Teles A, Brachwitz N, Casalis P, El-Mousleh T, et al. Pregnancy: Tolerance and suppression of immune responses. Methods Mol Biol 2011;677:397-417
12. Oreshkova T, Dimitrov R, Mourdjeva M. A cross-talk of decidual stromal cells, trophoblast, and immune cells: A prerequisite for the success of pregnancy. Am J Reprod Immunol 2012;68:366-73
13. Raulet DH. Missing self recognition and self tolerance of natural killer (NK) cells. Semin Immunol 2006;18:145-50
14. Raulet DH, Held W, Correa I, Dorfman JR, Wu MF, Corral L. Specificity, tolerance and developmental regulation of natural killer cells defined by expression of class I-specific Ly49 receptors. Immunol Rev 1997;155:41-52
15. Apps R, Gardner L, Moffett A. A critical look at HLA-G. Trends Immunol 2008;29:313-21
16. Miwa N, Hayakawa S, Miyazaki S, Myojo S, Sasaki Y, Sakai M, et al. IDO expression on decidual and peripheral blood dendritic cells and monocytes/macrophages after treatment with CTLA-4 or interferon-gamma increase in normal pregnancy but decrease in spontaneous abortion. Mol Hum Reprod 2005;11:865-70
17. Alok A, Karande AA. The role of glycodelin as an immune-modulating agent at the feto-maternal interface. J Reprod Immunol 2009;83:124-7
18. Lee CL, Chiu PC, Lam KK, Siu SO, Chu IK, Koistinen R, et al. Differential actions of glycodelin-A on Th-1 and Th-2 cells: A paracrine mechanism that could produce the Th-2 dominant environment during pregnancy. Hum Reprod 2011;26:517-26
19. Scholz C, Toth B, Brunnhuber R, Rampf E, Weissenbacher T, Santoso L, et al. Glycodelin A induces a tolerogenic phenotype in monocyte-derived dendritic cells in vitro. Am J Reprod Immunol 2008;60:501-12
20. Kauma SW, Huff TF, Hayes N, Nilkaeo A. Placental Fas ligand expression is a mechanism for maternal immune tolerance to the fetus. J Clin Endocrinol Metab 1999;84:2188-94
21. Uckan D, Steele A, Cherry, Wang BY, Chamizo W, Koutsonikolis A, et al. Trophoblasts express Fas ligand: A proposed mechanism for immune privilege in placenta and maternal invasion. Mol Hum Reprod 1997;3:655-62
22. Jiang SP, Vacchio MS. Multiple mechanisms of peripheral T cell tolerance to the fetal allograft. J Immunol 1998;160:3086-90
23. Hammer A, Blaschitz A, Daxbock C, Walcher W, Dohr G. Fas and Fas-ligand are expressed in the uteroplacental unit of first-trimester pregnancy. Am J Reprod Immunol 1999;41:41-51
24. Eide IP, Isaksen CV, Salvesen KA, Langaas M, Gunther CC, Iversen AC, et al. Fetal growth restriction is associated with reduced FasL expression by decidual cells. J Reprod Immunol 2007;74:7-14
25. Hunt JS, Vassmer D, Ferguson TA, Miller L. Fas ligand is positioned in mouse uterus and placenta to prevent trafficking of activated leukocytes between the mother and the conceptus. J Immunol 1997;158:4122-8
26. Vacchio MS, Hodes RJ. Fetal expression of Fas ligand is necessary and sufficient for induction of CD8 T cell tolerance to the fetal antigen H-Y during pregnancy. J Immunol 2005;174:4657-61
27. Sacks G, Sargent I, Redman C. An innate view of human pregnancy. Immunol Today 1999;20:114-8
28. Tafuri A, Alferink J, Moller P, Hammerling GJ, Arnold B. T cell awareness of paternal alloantigens during pregnancy. Science 1995;270:630-3
29. Clark DA, Slapsys R, Croy BA, Krcek J, Rossant J. Local active suppression by suppressor cells in the decidua: A review. Am J Reprod Immunol 1984;5:78-83
30. 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;10:347-53
31. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004;5:266-71
32. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, 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 2005;166:811-22
33. 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
34. Wegienka G, Havstad S, Bobbitt KR, Woodcroft KJ, Zoratti EM, Ownby DR, et al. Within-woman change in regulatory T cells from pregnancy to the postpartum period. J Reprod Immunol 2010;88:58-65
35. Ait-Azzouzene D, Gendron MC, Houdayer M, Langkopf A, Burki K, Nemazee D, et al. Maternal B lymphocytes specific for paternal histocompatibility antigens are partially deleted during pregnancy. J Immunol 1998;161:2677-83
36. Ait-Azzouzene D, Caucheteux S, Tchang F, Wantyghem J, Moutier R, Langkopf A, et al. Transgenic major histocompatibility complex class I antigen expressed in mouse trophoblast affects maternal immature B cells. Biol Reprod 2001;65:337-44
37. Samsami Dehaghani A, Doroudchi M, Kalantari T, Pezeshki AM, Ghaderi A. Heterozygosity in CTLA-4 gene and severe preeclampsia. Int J Gynaecol Obstet 2005;88:19-24
38. Ruter J, Hoffmann T, Heiser U, Demuth HU, Arck PC, Klapp BF, et al. The expression of T-cell surface antigens CTLA-4, CD26, and CD28 is modulated by inhibition of dipeptidylpeptidase IV (DPP IV, CD26) activity in murine stress-induced abortions. Cell Immunol 2002;220:150-6
39. 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 2009;133:402-10
40. Wang X, Ma Z, Hong Y, Lu P, Lin Q. Expression of CD28 and cytotoxic T lymphocyte antigen 4 at the maternal-fetal interface in women with unexplained pregnancy loss. Int J Gynaecol Obstet 2006;93:123-9
41. Jin LP, Zhou YH, Wang MY, Zhu XY, Li DJ. Blockade of CD80 and CD86 at the time of implantation inhibits maternal rejection to the allogeneic fetus in abortion-prone matings. J Reprod Immunol 2005;65:133-46
42. Wafula PO, Teles A, Schumacher A, Pohl K, Yagita H, Volk HD, et al. 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;62:283-92
43. Guleria I, Khosroshahi A, Ansari MJ, Habicht A, Azuma M, Yagita H, et al. A critical role for the programmed death ligand 1 in fetomaternal tolerance. J Exp Med 2005;202:231-7
44. Jin LP, Fan DX, Li DJ. Regulation of costimulatory signal in maternal-fetal immune tolerance. Am J Reprod Immunol 2011;66:76-83
45. Okazaki T, Honjo T. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol 2006;27:195-201
46. Habicht A, Dada S, Jurewicz M, Fife BT, Yagita H, Azuma M, et al. A link between PDL1 and T regulatory cells in fetomaternal tolerance. J Immunol 2007;179:5211-9
47. Riella LV, Dada S, Chabtini L, Smith B, Huang L, Dakle P, et al. B7h (ICOS-L) maintains tolerance at the fetomaternal interface. Am J Pathol 2013;182:2204-13
48. Petroff MG, Perchellet A. B7 family molecules as regulators of the maternal immune system in pregnancy. Am J Reprod Immunol 2010;63:506-19
49. Krey G, Frank P, Shaikly V, Barrientos G, Cordo-Russo R, Ringel F, et al. In vivo dendritic cell depletion reduces breeding efficiency, affecting implantation and early placental development in mice. J Mol Med (Berl) 2008;86:999-1011
50. Plaks V, Birnberg T, Berkutzki T, Sela S, BenYashar A, Kalchenko V, et al. Uterine DCs are crucial for decidua formation during embryo implantation in mice. J Clin Invest 2008;118:3954-65
51. Nagamatsu T, Schust DJ. The contribution of macrophages to normal and pathological pregnancies. Am J Reprod Immunol 2010;63:460-71
52. Vacca P, Mingari MC, Moretta L. Natural killer cells in human pregnancy. J Reprod Immunol 2013;97:14-9
53. Heikkinen J, Mottonen M, Alanen A, Lassila O. Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol 2004;136:373-8
54. Saito S, Sasaki Y, Sakai M. CD4(+) CD25high regulatory T cells in human pregnancy. J Reprod Immunol 2005;65:111-20
55. Zhao JX, Zeng YY, Liu Y. Fetal alloantigen is responsible for the expansion of the CD4(+) CD25(+) regulatory T cell pool during pregnancy. J Reprod Immunol 2007;75:71-81
56. Kahn DA, Baltimore D. Pregnancy induces a fetal antigen-specific maternal T regulatory cell response that contributes to tolerance. Proc Natl Acad Sci U S A 2010;107:9299-304
57. Shima T, Sasaki Y, Itoh M, Nakashima A, Ishii N, Sugamura K, et al. Regulatory T cells are necessary for implantation and maintenance of early pregnancy but not late pregnancy in allogeneic mice. J Reprod Immunol 2010;85:121-9
58. 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;161:177-81
59. Darrasse-Jeze G, Klatzmann D, Charlotte F, Salomon BL, Cohen JL. CD4+CD25+ regulatory/suppressor T cells prevent allogeneic fetus rejection in mice. Immunol Lett 2006;102:106-9
60. Robertson SA, Guerin LR, Bromfield JJ, Branson KM, Ahlstrom 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;80:1036-45
61. Shima T. Paternal antigen-specific regulatory T cells proliferate in the draining lymph nodes before the implantation and proliferate in the uterus after the implantation, and are necessary for maintenance of allogeneic pregnancy. 2010 ASRI Annual Meeting Abstract 2010
62. Schumacher A, Brachwitz N, Sohr S, Engeland K, Langwisch S, Dolaptchieva M, et al. Human chorionic gonadotropin attracts regulatory T cells into the fetal-maternal interface during early human pregnancy. J Immunol 2009;182:5488-97
63. 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 2006;12:301-8
64. Yang H, Qiu L, Chen G, Ye Z, Lu C, Lin Q. Proportional change of CD4+CD25+ regulatory T cells in decidua and peripheral blood in unexplained recurrent spontaneous abortion patients. Fertil Steril 2008;89:656-61
65. Mei S, Tan J, Chen H, Chen Y, Zhang J. Changes of CD4 + CD25high regulatory T cells and FOXP3 expression in unexplained recurrent spontaneous abortion patients. Fertil Steril 2010;94:2244-7
66. Hao K, Zhou Q, Chen W, Jia W, Zheng J, Kang J, et al. Possible role of the IDO-AhR axis in maternal-foetal tolerance. Cell Biol Int 2013;37:105-8
67. Teles A, Zenclussen AC, Schumacher A. Regulatory T cells are baby's best friends. Am J Reprod Immunol 2013;69:331-9
68. Rowe JH, Ertelt JM, Xin L, Way SS. Pregnancy imprints regulatory memory that sustains anergy to fetal antigen. Nature 2012;490:102-6
69. Rowe JH, Ertelt JM, Xin L, Way SS. Listeria monocytogenes cytoplasmic entry induces fetal wastage by disrupting maternal Foxp3+ regulatory T cell-sustained fetal tolerance. PLoS Pathog 2012;8:e1002873
70. Mjosberg J, Berg G, Jenmalm MC, Ernerudh J. FOXP3+ regulatory T cells and T helper 1, T helper 2, and T helper 17 cells in human early pregnancy decidua. Biol Reprod 2009;82:698-705
71. Wang WJ, Hao CF, Qu QL, Wang X, Qiu LH, Lin QD. The deregulation of regulatory T cells on interleukin-17-producing T helper cells in patients with unexplained early recurrent miscarriage. Hum Reprod 2010;25:2591-6
72. Wang WJ, Hao CF, Yi-Lin, Yin GJ, Bao SH, Qiu LH, et al. Increased prevalence of T helper 17 (Th17) cells in peripheral blood and decidua in unexplained recurrent spontaneous abortion patients. J Reprod Immunol 2010;84:164-70
73. Liu F, Guo J, Tian T, Wang H, Dong F, Huang H, et al. Placental trophoblasts shifted Th1/Th2 balance toward Th2 and inhibited Th17 immunity at fetomaternal interface. APMIS 2011;119:597-604
74. Wang WJ, Liu FJ, Xin-Liu, Hao CF, Bao HC, Qu QL, et al. Adoptive transfer of pregnancy-induced CD4+CD25+ regulatory T cells reverses the increase in abortion rate caused by interleukin 17 in the CBA/JxBALB/c mouse model. Hum Reprod 2014;29:946-52
75. Leung S, Liu X, Fang L, Chen X, Guo T, Zhang J. The cytokine milieu in the interplay of pathogenic Th1/Th17 cells and regulatory T cells in autoimmune disease. Cell Mol Immunol 2010;7:182-9
76. Kimura A, Kishimoto T. IL-6: Regulator of Treg/Th17 balance. Eur J Immunol 2010;40:1830-5
77. Cooney LA, Fox DA. Regulation of Th17 maturation by interleukin 4. Crit Rev Immunol 2013;33:379-87
78. Amarnath S, Mangus CW, Wang JC, Wei F, He A, Kapoor V, et al. The PDL1-PD1 axis converts human TH1 cells into regulatory T cells. Sci Transl Med 2011;3:111ra20
79. DAddio F, Riella LV, Mfarrej BG, Chabtini L, Adams LT, Yeung M, et al. The link between the PDL1 costimulatory pathway and Th17 in fetomaternal tolerance. J Immunol 2011;187:4530-41
80. Taglauer ES, Yankee TM, Petroff MG. Maternal PD-1 regulates accumulation of fetal antigen-specific CD8+ T cells in pregnancy. J Reprod Immunol 2009;80:12-21
81. Shepard MT, Bonney EA. PD-1 regulates T cell proliferation in a tissue and subset-specific manner during normal mouse pregnancy. Immunol Invest 2013;42:385-408
82. Dulos J, Carven GJ, Van Boxtel SJ, Evers S, Driessen-Engels LJ, Hobo W, et al. PD-1 blockade augments Th1 and Th17 and suppresses Th2 responses in peripheral blood from patients with prostate and advanced melanoma cancer. J Immunother 2012;35:169-78
83. Rui Y, Honjo T, Chikuma S. Programmed cell death 1 inhibits inflammatory helper T-cell development through controlling the innate immune response. Proc Natl Acad Sci U S A 2013;110:16073-8