Key Cellular Components and Interactive Histocompatibility Molecules Regulating Tolerance to the Fetal Allograft

American Journal of Reproductive Immunology

Volumn 68, Issue 2, 2012, Pages 95-99

  Spencer, Patrick S ^a   Hakam, Soukaina M ^a   Laissue, Phillipe P ^a   Jabeen, Asma ^a   Jain, Pallavi ^a   Hayrabedyan, Soren ^b   Todorova, Krassimira ^b   Blanch, Alyssa ^a   Mcelhinney, James M W R ^a   Muhandiram, Niwedhie ^a   Alkhatib, Shaza ^a   Dealtry, Gill B ^c   Miranda Sayago, Jose M ^a   Fernández, Nelson ^a  

^a UNIVERSITY OF ESSEX   (United Kingdom)

^b BULGARIAN ACADEMY OF SCIENCES   (Bulgaria)

^c NELSON MANDELA METROPOLITAN UNIVERSITY   (South Africa)

Author keywords

Fetal tolerance; HLA; Treg

Indexed keywords

ALLOANTIGEN; HISTOCOMPATIBILITY ANTIGEN; INTERLEUKIN 10; INTERLEUKIN 2; TRANSCRIPTION FACTOR FOXP3;

ALLOGRAFT; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CELL COMPONENT; FATHER; GRAFT REJECTION; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; LYMPHOCYTE FUNCTION; LYMPHOCYTE SUBPOPULATION; MOLECULE; MOTHER; NONHUMAN; PREGNANCY; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; T CELL DEPLETION; TROPHOBLAST;

ANIMALS; EMBRYO IMPLANTATION; FEMALE; FETAL DEVELOPMENT; FETUS; HISTOCOMPATIBILITY; HLA ANTIGENS; HUMANS; IMMUNE TOLERANCE; PREGNANCY; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY;

EID: 84863878191     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2012.01138.x     Document Type: Article

References (53)

1. Laskarin G, Kammerer U, Rukavina D, Thomson AW, Fernandez N, Blois SM: Antigen-presenting cells and materno-fetal tolerance: an emerging role for dendritic cells. Am J Reprod Immunol 2007; 58:255-267.
2. Blois SM, Kammerer U, Alba Soto C, Tometten MC, Shaikly V, Barrientos G, Jurd R, Rukavina D, Thomson AW, Klapp BF, Fernandez N, Arck PC: Dendritic cells: key to fetal tolerance? Biol Reprod 2007; 77:590-598.
3. Lockwood CJ, Huang SJ, Krikun G, Caze R, Rahman M, Buchwalder LF, Schatz F: Decidual hemostasis, inflammation, and angiogenesis in pre-eclampsia. Semin Thromb Hemost 2011; 37:158-164.
4. Colonna M, Nakajima H, Cella M: Inhibitory and activating receptors involved in immune surveillance by human NK and myeloid cells. J Leukoc Biol 1999; 66:718-722.
5. Rajagopalan S, Long EO: A human histocompatibility leukocyte antigen (HLA)-G-specific receptor expressed on all natural killer cells. J Exp Med 1999; 189:1093-1100.
6. Shakhawat A, Shaikly V, Elzatma E, Mavrakos E, Jabeen A, Fernandez N: Interaction between HLA-G and monocyte/macrophages in human pregnancy. J Reprod Immunol 2010; 85:40-46.
7. Li C, Houser BL, Nicotra ML, Strominger JL: HLA-G homodimer-induced cytokine secretion through HLA-G receptors on human decidual macrophages and natural killer cells. Proc Natl Acad Sci U S A 2009; 106:5767-5772.
8. Shaikly VR, Morrison IE, Taranissi M, Noble CV, Withey AD, Cherry RJ, Blois SM, Fernandez N: Analysis of HLA-G in maternal plasma, follicular fluid, and preimplantation embryos reveal an asymmetric pattern of expression. J Immunol 2008; 180:4330-4337.
9. Shiroishi M, Tsumoto K, Amano K, Shirakihara Y, Colonna M, Braud VM, Allan DS, Makadzange A, Rowland-Jones S, Willcox B, Jones EY, van der Merwe PA, Kumagai I, Maenaka K: Human inhibitory receptors Ig-like transcript 2 (ILT2) and ILT4 compete with CD8 for MHC class I binding and bind preferentially to HLA-G. Proc Natl Acad Sci U S A 2003; 100:8856-8861.
10. Blois SM, Barrientos G, Garcia MG, Orsal AS, Tometten M, Cordo-Russo RI, Klapp BF, Santoni A, Fernandez N, Terness P, Arck PC: Interaction between dendritic cells and natural killer cells during pregnancy in mice. J Mol Med 2008; 86:837-852.
11. Dealtry GB, O'Farrell MK, Fernandez N: The Th2 cytokine environment of the placenta. Int Arch Allergy Immunol 2000; 123:107-119.
12. Apps R, Gardner L, Sharkey AM, Holmes N, Moffett A: A homodimeric complex of HLA-G on normal trophoblast cells modulates antigen-presenting cells via LILRB1. Eur J Immunol 2007; 37:1924-1937.
13. Rajagopalan S, Bryceson YT, Kuppusamy SP, Geraghty DE, van der Meer A, Joosten I, Long EO: Activation of NK cells by an endocytosed receptor for soluble HLA-G. PLoS Biol 2006; 4:e9.
14. Hanna J, Goldman-Wohl D, Hamani Y, Avraham I, Greenfield C, Natanson-Yaron S, Prus D, Cohen-Daniel L, Arnon TI, Manaster I, Gazit R, Yutkin V, Benharroch D, Porgador A, Keshet E, Yagel S, Mandelboim O: Decidual NK cells regulate key developmental processes at the human fetal-maternal interface. Nat Med 2006; 12:1065-1074.
15. van der Meer A, Lukassen HG, van Cranenbroek B, Weiss EH, Braat DD, van Lierop MJ, Joosten I: Soluble HLA-G promotes Th1-type cytokine production by cytokine-activated uterine and peripheral natural killer cells. Mol Hum Reprod 2007; 13:123-133.
16. Miah SM, Hughes TL, Campbell KS: KIR2DL4 differentially signals downstream functions in human NK cells through distinct structural modules. J Immunol 2008; 180:2922-2932.
17. Wu ZM, Yang H, Li M, Yeh CC, Schatz F, Lockwood CJ, Di W, Huang SJ: Pro-inflammatory cytokine-stimulated first trimester decidual cells enhance macrophage-induced apoptosis of extravillous trophoblasts. Placenta 2012; 33:188-194.
18. Sacks G, Sargent I, Redman C: An innate view of human pregnancy. Immunol Today 1999; 20:114-118.
19. Makrigiannakis A, Zoumakis E, Kalantaridou S, Coutifaris C, Margioris AN, Coukos G, Rice KC, Gravanis A, Chrousos GP: Corticotropin-releasing hormone promotes blastocyst implantation and early maternal tolerance. Nat Immunol 2001; 2:1018-1024.
20. 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.
21. Sakaguchi S: Regulatory T cells: key controllers of immunologic self-tolerance. Cell 2000; 101:455-458.
22. Shevach EM: CD4+ CD25+ suppressor T cells: more questions than answers. Nat Rev Immunol 2002; 2:389-400.
23. Read S, Powrie F: CD4(+) regulatory T cells. Curr Opin Immunol 2001; 13:644-649.
24. Fontenot JD, Gavin MA, Rudensky AY: Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat Immunol 2003; 4:330-336.
25. Hori S, Nomura T, Sakaguchi S: Control of regulatory T cell development by the transcription factor Foxp3. Science 2003; 299:1057-1061.
26. Khattri R, Cox T, Yasayko SA, Ramsdell F: An essential role for Scurfin in CD4+CD25+ T regulatory cells. Nat Immunol 2003; 4:337-342.
27. Terness P, Kallikourdis M, Betz AG, Rabinovich GA, Saito S, Clark DA: Tolerance signaling molecules and pregnancy: IDO, galectins, and the renaissance of regulatory T cells. Am J Reprod Immunol 2007; 58:238-254.
28. Thorstenson KM, Khoruts A: Generation of anergic and potentially immunoregulatory CD25+CD4 T cells in vivo after induction of peripheral tolerance with intravenous or oral antigen. J Immunol 2001; 167:188-195.
29. Bach JF: Regulatory T cells under scrutiny. Nat Rev Immunol 2003; 3:189-198.
30. Thellin O, Coumans B, Zorzi W, Igout A, Heinen E: Tolerance to the foeto-placental 'graft': ten ways to support a child for nine months. Curr Opin Immunol 2000; 12:731-737.
31. Maloy KJ, Salaun L, Cahill R, Dougan G, Saunders NJ, Powrie F: CD4+CD25+ T(R) cells suppress innate immune pathology through cytokine-dependent mechanisms. J Exp Med 2003; 197:111-119.
32. Finger EB, Bluestone JA: When ligand becomes receptor-tolerance via B7 signaling on DCs. Nat Immunol 2002; 3:1056-1057.
33. 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.
34. Aluvihare VR, Kallikourdis M, Betz AG: Regulatory T cells mediate maternal tolerance to the fetus. Nat Immunol 2004; 5:266-271.
35. Taylor PA, Noelle RJ, Blazar BR: CD4(+)CD25(+) immune regulatory cells are required for induction of tolerance to alloantigen via costimulatory blockade. J Exp Med 2001; 193:1311-1318.
36. Cohen JL, Trenado A, Vasey D, Klatzmann D, Salomon BL: CD4(+)CD25(+) immunoregulatory T Cells: new therapeutics for graft-versus-host disease. J Exp Med 2002; 196:401-406.
37. Hoffmann P, Ermann J, Edinger M, Fathman CG, Strober S: Donor-type CD4(+)CD25(+) regulatory T cells suppress lethal acute graft-versus-host disease after allogeneic bone marrow transplantation. J Exp Med 2002; 196:389-399.
38. Jonuleit H, Schmitt E, Stassen M, Tuettenberg A, Knop J, Enk AH: Identification and functional characterization of human CD4(+)CD25(+) T cells with regulatory properties isolated from peripheral blood. J Exp Med 2001; 193:1285-1294.
39. Levings MK, Sangregorio R, Roncarolo MG: Human cd25(+)cd4(+) t regulatory cells suppress naive and memory T cell proliferation and can be expanded in vitro without loss of function. J Exp Med 2001; 193:1295-1302.
40. Ng WF, Duggan PJ, Ponchel F, Matarese G, Lombardi G, Edwards AD, Isaacs JD, Lechler RI: Human CD4(+)CD25(+) cells: a naturally occurring population of regulatory T cells. Blood 2001; 98:2736-2744.
41. Stephens LA, Mottet C, Mason D, Powrie F: Human CD4(+)CD25(+) thymocytes and peripheral T cells have immune suppressive activity in vitro. Eur J Immunol 2001; 31:1247-1254.
42. 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.
43. 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; 102:106-109.
44. Heikkinen J, Mottonen M, Alanen A, Lassila O: Phenotypic characterization of regulatory T cells in the human decidua. Clin Exp Immunol 2004; 136:373-378.
45. James E, Chai JG, Dewchand H, Macchiarulo E, Dazzi F, Simpson E: Multiparity induces priming to male-specific minor histocompatibility antigen, HY, in mice and humans. Blood 2003; 102:388-393.
46. Aluvihare VR, Betz AG: The role of regulatory T cells in alloantigen tolerance. Immunol Rev 2006; 212:330-343.
47. Wood KJ, Sakaguchi S: Regulatory T cells in transplantation tolerance. Nat Rev Immunol 2003; 3:199-210.
48. Cosmi L, Liotta F, Angeli R, Mazzinghi B, Santarlasci V, Manetti R, Lasagni L, Vanini V, Romagnani P, Maggi E, Annunziato F, Romagnani S: Th2 cells are less susceptible than Th1 cells to the suppressive activity of CD25+ regulatory thymocytes because of their responsiveness to different cytokines. Blood 2004; 103:3117-3121.
49. Smith RN, Powell AE: The adoptive transfer of pregnancy-induced unresponsiveness to male skin grafts with thymus-dependent cells. J Exp Med 1977; 146:899-904.
50. Hara M, Kingsley CI, Niimi M, Read S, Turvey SE, Bushell AR, Morris PJ, Powrie F, Wood KJ: IL-10 is required for regulatory T cells to mediate tolerance to alloantigens in vivo. J Immunol 2001; 166:3789-3796.
51. Kupiec-Weglinski JW, Onodera K, Volk HD: The "infectious" tolerance pathway in organ allograft recipients. Transpl Proc 1998; 30:1595-1597.
52. Waldmann H, Adams E, Fairchild P, Cobbold S: Infectious tolerance and the long-term acceptance of transplanted tissue. Immunol Rev 2006; 212:301-313.
53. 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.