PD-1 but not CTLA-4 blockage abrogates the protective effect of regulatory T cells in a pregnancy murine model

American Journal of Reproductive Immunology

Volumn 62, Issue 5, 2009, Pages 283-292

  Wafula, Paul Ojiambo ^a   Teles, Ana ^b   Schumacher, Anne ^b   Pohl, Kerstin ^a   Yagita, Hideo ^c   Volk, Hans Dieter ^a   Zenclussen, Ana Claudia ^a,b  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b OTTO VON GUERICKE UNIVERSITY   (Germany)

^c JUNTENDO UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

CTLA 4; Fetal protection; PD 1; Treg

Indexed keywords

CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; IMMUNOGLOBULIN G; MEMBRANE RECEPTOR; PROGRAMMED CELL DEATH 1; TRANSCRIPTION FACTOR FOXP3; UNCLASSIFIED DRUG; VASCULOTROPIN A;

ABORTION; ADOPTIVE TRANSFER; ANIMAL EXPERIMENT; ARTICLE; CBA MOUSE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; DBA 2 MOUSE; EXTRAVASATION; FEMALE; MOUSE; NONHUMAN; PREGNANCY; PREMATURE LABOR; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ABORTION, SPONTANEOUS; ADOPTIVE TRANSFER; ANIMALS; ANTIBODIES, BLOCKING; ANTIGENS, CD; ANTIGENS, DIFFERENTIATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DISEASE SUSCEPTIBILITY; FEMALE; IMMUNE TOLERANCE; MICE; MICE, INBRED BALB C; MICE, INBRED CBA; MICE, INBRED DBA; PREGNANCY; T-LYMPHOCYTES, REGULATORY; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 70350431248     PISSN: 10467408     EISSN: 16000897     Source Type: Journal    
DOI: 10.1111/j.1600-0897.2009.00737.x     Document Type: Article

References (43)

1. Sakaguchi S, Sakaguchi N, Asano M, Itoh M, Toda M. Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self tolerance causes various autoimmune diseases. J Immunol 1995, 15:1151-1164.
2. Aluvihare VR, Kallikourdis M, Betz AG. Regulatory T cells mediate maternal tolerance to the fetus. Nat Immun 2004, 5:266-271.
3. 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.
4. Zenclussen AC, Gerlof K, Zenclussen ML, Sollwedel A, Bertoja AZ, Ritter T, Kotsch K, Leber J, Volk H-D. Abnormal T-cell reactivity against paternal antigens in spontaneous abortion: adoptive transfer of pregnancy-induced CD4+CD25+ T regulatory cells prevent fetal rejection in a murine abortion model. Am J Pathol 2005, 166:811-822.
5. Somerset DA, Zheng Y, Kilby MD, Samson DM, Drayson MT. Normal human pregnancy is associated with an elevation in the immune suppressive CD4+CD25+ regulatory T-cell subset. Immunology 2004, 112:38-43.
6. Freeman GJ, Long AJ, Iwai Y, Bourque K, Chernova T, Nishimura H, Fitz LJ, Malenkovich N, Okazaki T, Byrne MC, Horton MF, Fouser L, Carter L, Ling V, Bowman MR, Carreno BM, Collins M, Wood CR, Honjo T. Engagement of the PD-1 immunohibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000, 192:1027-1034.
7. Carreno BM, Collins M. The B7 family of ligands and its receptors: new pathways for costimulation and inhibition of immune responses. Annu Rev Immunol 2002, 20:29-53.
8. Alegre ML, Frauwirth KA, Thomson CB. T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 2001, 1:220-228.
9. Gajewski TF, Fallarino F, Fields PE, Rivas F, Alegre ML. Absence of CTLA-4 lowers the activation threshold of primed CD8+ TCR-transgenic T cells: lack of correlation with Scr homology domain 2-containing protein tyrosine phosphatase. J Immunol 2001, 166:3900-3907.
10. Krummel MF, Allison JP. CD28 and CTLA-4 have opposing effects on the response of T cells to stimulation. J Exp Med 1995, 182:459-465.
11. Walunas TL, Lenshow DJ, Bakker CY, Linsley PS, Freeman GJ, Green JM, Thompson CB, Bluestone JA. CTLA-4 can function as a negative regulator of T cell activation. Immunity 1994, 1:405-413.
12. Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science 1996, 271:1734-1736.
13. McCoy K, Camberis M, Gros GL. Protective immunity to nematode infection is induced by CTLA-4 blockade. J Exp Med 1997, 186:183-187.
14. Martins GA, Tadokoro CE, Silva RB, Silva JS, Risso LV. CTLA-4 blockage increases resistance to infection with the intracellular protozoan Trypanosoma cruzi. J Immunol 2004, 172:4893-4901.
15. Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Scarpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity 1995, 3:541-547.
16. Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, Thompson CB, Griesser H, Mak TW. Lymphoproliferative disorders with early lethality in mice deficient in CTLA-4. Science 1995, 270:985-988.
17. Bennette CL, Christie J, Ramsdell F, Brunkow ME, Ferguson PJ, Whitesell L, Kelly TE, Saulsbury FT, Chance PF, Ochs HD. The immune dysregulation, polyendocrinopathy, entropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001, 27:20-21.
18. Rothstein DM, Sayegh MH. T-cell costimulatory pathways in allograft rejection and tolerance. Immunol Rev 2003, 196:85-108.
19. Khoury SJ, Sayegh MH. The roles of the new negative T cell costimulatory pathways in regulating autoimmunity. Immunity 2004, 20:529-538.
20. Okazaki T, Honjo T. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol 2006, 27:195-201.
21. Petroff MG, Chen L, Philips TA, Azzola D, Sedlmayr P, Hunt JS. B7 family molecules are favourably positioned at the human maternal-fetal interface. Biol Reprod 2003, 68:1496-1504.
22. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003, 9:669-676.
23. Aramaki O, Inoue F, Takayama T, Shimazu M, Kitajima M, Ikeda Y, Okumura K, Yagita H, Shirasugi N, Niimi M. Interleukin-10 but not transforming growth factor-beta is essential for generation and suppressor function of regulatory cells induced by intratracheal delivery of alloantigen. Transplantation 2005, 79:568-576.
24. Clark DA, McDermott MR, Szewczuk MR. Impairment of the host-versus-graft reaction in pregnant mice II. Selective suppression of cytotoxic cell generation correlates with soluble suppressor activity and with successful allogeneic pregnancy. Cell Immunol 1980, 52:106-118.
25. Saint-Marie G. A paraffin embedding technique for studies employing immunofluorescence. J Histochem Cytochem 1962, 10:250-256.
26. Akiyama Y, Shirasugi N, Uchida N, Matsumoto K, Kitajima M, Bashuda H, Yagita H, Okumura K, Aramaki O, Niimi M. B7/CTLA4 pathway is essential for generating regulatory cells after intratracheal delivery of alloantigen in mice. Transplantation 2002, 74:732-738.
27. Aramaki O, Shirasugi N, Takayama T, Shimazu M, Kitajima M, Ikeda Y, Azuma M, Okumura K, Yagita H, Niimi M. Programmed death-1-programmed death-L1 interaction is essential for induction of regulatory cells by intratracheal delivery of alloantigen. Transplantation 2004, 77:6-12.
28. Yamazaki T, Akiba H, Koyanagi A, Azuma M, Yagita H, Okumura K. Blockade of B7-H1 on macrophages suppresses CD4+ T cell proliferation by augmenting IFN-gamma-induced nitric oxide production. J Immunol 2005, 175:1586-1592.
29. Ferrara N, Carver-moore K, Chen H, Dowd M, Lu L, O′shea KS, Powell-Braxton L, Hillan KJ, Moore MW. Heterozygous embryonic lethality induced by target inactivation of the VEGF gene. Nature 1996, 380:439-442.
30. Christiaens I, Zaragoza DB, Guilbert L, Robertson SA, Mitchell BF, Olson DM. Inflammatory processes in preterm and term parturition. J Reprod Immunol 2008, 79:50-57.
31. Birebent B, Lorho R, Lechartier H, de Guibert S, Alizadeh M, Vu N, Beauplet A, Robillard N, Semana G. Suppressive properties of human CD4+CD25+ regulatory T cells are dependent on CTLA-4 expression. Eur J Immunol 2004, 34:3485-3496.
32. Guleria I, Khosroshahi A, Ansari MJ, Habitch A, Azuma M, Yagita H, Noelle RJ, Coyle A, Mellor AL, Khoury SJ, Sayegh MH. A critical role for programmed death ligand 1 in fetal maternal tolerance. J Exp Med 2005, 202:231-237.
33. Habicht A, Dada S, Jurewicz M, Fife B, Yagita H, Azuma M, Sayegh M, Guleria I. A link between PDL1 and T regulatory cells in the fetomaternal tolerance. J Immunol 2007, 179:5211-5219.
34. 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.
35. Taglauer ES, Trikhacheva AS, Slusser JG, Petroff MG. Expression and function of PCD1 at the human maternal-fetal interface. Biol Reprod 2008, 79:562-569.
36. Ozkaynak E, Wang L, Goodearl A, McDonald K, Qin S, O′Keefe T, Duong T, Smith T, Gutierrez-Ramos JC, Rottman JB, Coyle AJ, Hancock WW. Programmed death-1 targeting can promote allograft survival. J Immunol 2002, 169:6546-6553.
37. Itoh T, Ueno T, Clarkson MR, Yuan X, Jurewicz MM, Yagita H, Azuma M, Sharpe AH, Auchincloss H, Sayegh M, Najafian N. Analysis of the role of negative T cell costimulatory pathways in CD4 and CD8 T cell-mediated alloimmune responses in vivo. J Immunol 2005, 174:6648-6656.
38. Li W, Li B, Fan W, Geng L, Li X, Li L, Huang Z, Li S. CTLA4Ig gene transfer alleviates abortion in mice by expanding CD4+CD25+ regulatory T cells and inducing indoleamine 2,3-dioxygenase. J Reprod Immunol 2009, 80:1-11.
39. Sansom DM, Walker LS. The role of CD28 and cytotoxic T-lymphocyte antigen-4 (CTLA-4) in regulatory T-cell biology. Immunol Rev 2006, 212:131-148.
40. Tang Q, Boden EK, Henriksen BJ, Bour-jourdan H, Bi M, Bluestone JA. Distinct roles of CTLA-4 and TGF-beta in CD4+CD25+ regulatory T cell function. Eur J Immunol 2004, 34:2996-3005.
41. Marson A, Kretschmer K, Frampton GM, Jacobsen ES, Polansky JK, MacIsaac KD, Levine SS, Fraenkel E, von Boehmer H, Young RA. Foxp3 occupancy and regulation of key target genes during T-cell stimulation. Nature 2007, 445:931-935.
42. Marvin KW, Keelan JA, Eykholt RL, Sato TA, Mitchell MD. Expression of angiogenic and neurotrophic factors in the human amnion and choriodecidua. Am J Obstet Gynecol 2002, 187:728-734.
43. Lee HH, Hong SH, Shin SJ, Ko JJ, Oh D, Kim NK. Association study of vascular endothelial growth factor polymorphisms with the risk of recurrent spontaneous abortion. Fertil Steril 2009, doi, [Epub ahead of print]