PD-1/PD-L1, PD-1/PD-L2, and other co-inhibitory signaling pathways in transplantation

Transplant International

Volumn 21, Issue 11, 2008, Pages 1015-1028

  Del Rio, Maria Luisa ^a   Buhler, Leo ^b   Gibbons, Carrie ^c   Tian, Jiong ^d   Rodriguez Barbosa, Jose Ignacio ^a  

^a UNIVERSITY OF LEÓN   (Spain)

^b GENEVA UNIVERSITY HOSPITALS   (Switzerland)

^c MASSACHUSETTS GENERAL HOSPITAL   (United States)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

Antigen presenting cells; BTLA; CD160; Co inhibition; Co stimulation; HVEM; PD 1; PD L1; PD L2; Peripheral tolerance; T cells; Transplantation

Indexed keywords

B AND T LYMPHOCYTE ATTENUATOR; CD 160; GLOBULIN; HERPESVIRUS ENTRY MEDIATOR; HYBRID PROTEIN; IMMUNOGLOBULIN; LIGAND; LIGHT PROTEIN; MONOCLONAL ANTIBODY; PD 1; PD L1; PD L2; UNCLASSIFIED DRUG;

CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL FUNCTION; DNA MODIFICATION; GRAFT REJECTION; HEART TRANSPLANTATION; HUMAN; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; REVIEW; SKIN TRANSPLANTATION; XENOTRANSPLANTATION;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGEN-PRESENTING CELLS; ANTIGENS, CD; ANTIGENS, CD80; APOPTOSIS REGULATORY PROTEINS; GRAFT REJECTION; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; RECEPTORS, IMMUNOLOGIC; RECEPTORS, TUMOR NECROSIS FACTOR, MEMBER 14; SIGNAL TRANSDUCTION; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION IMMUNOLOGY;

EID: 53749092575     PISSN: 09340874     EISSN: 14322277     Source Type: Journal    
DOI: 10.1111/j.1432-2277.2008.00726.x     Document Type: Review

References (106)

1. Alarcon-Zurita A, Ladefoged J. Treatment of acute allograft rejection with high doses of corticosteroids. Kidney Int 1976 9 : 351.
2. Cohen DJ, Loertscher R, Rubin MF, Tilney NL, Carpenter CB, Strom TB. Cyclosporine: a new immunosuppressive agent for organ transplantation. Ann Intern Med 1984 101 : 667.
3. Starzl TE, Todo S, Fung J, Demetris AJ, Venkataramman R, Jain A. FK 506 for liver, kidney, and pancreas transplantation. Lancet 1989 2 : 1000.
4. Chiba K. FTY720, a new class of immunomodulator, inhibits lymphocyte egress from secondary lymphoid tissues and thymus by agonistic activity at sphingosine 1-phosphate receptors. Pharmacol Ther 2005 108 : 308.
5. Calne R, Friend P, Moffatt S, et al. Prope tolerance, perioperative campath 1H, and low-dose cyclosporin monotherapy in renal allograft recipients. Lancet 1998 351 : 1701.
6. Nashan B, Moore R, Amlot P, Schmidt AG, Abeywickrama K, Soulillou JP. Randomised trial of basiliximab versus placebo for control of acute cellular rejection in renal allograft recipients. CHIB 201 International Study Group. Lancet 1997 350 : 1193.
7. Buhaescu I, Segall L, Goldsmith D, Covic A. New immunosuppressive therapies in renal transplantation: monoclonal antibodies. J Nephrol 2005 18 : 529.
8. Vincenti F, Larsen C, Durrbach A, et al. Costimulation blockade with belatacept in renal transplantation. N Engl J Med 2005 353 : 770.
9. Calne RY. The future of organ transplantation: from the laboratory to the clinic. Philos Trans R Soc Lond B Biol Sci 2001 356 : 767.
10. Starzl TE, Murase N, Abu-Elmagd K, et al. Tolerogenic immunosuppression for organ transplantation. Lancet 2003 361 : 1502.
11. Gould DS, Auchincloss H, Jr., Direct and indirect recognition: the role of MHC antigens in graft rejection. Immunol Today 1999 20 : 77.
12. Shoskes DA, Wood KJ. Indirect presentation of MHC antigens in transplantation. Immunol Today 1994 15 : 32.
13. Bluestone JA. Costimulation and its role in organ transplantation. Clin Transplant 1996 10 : 104.
14. Adams AB, Larsen CP, Pearson TC, Newell KA. The role of TNF receptor and TNF superfamily molecules in organ transplantation. Am J Transplant 2002 2 : 12.
15. 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.
16. Rietz C, Chen L. New B7 family members with positive and negative costimulatory function. Am J Transplant 2004 4 : 8.
17. Lenschow DJ, Walunas TL, Bluestone JA. CD28/B7 system of T cell costimulation. Annu Rev Immunol 1996 14 : 233.
18. Williams AF, Barclay AN. The immunoglobulin superfamily - domains for cell surface recognition. Annu Rev Immunol 1988 6 : 381.
19. June CH, Ledbetter JA, Linsley PS, Thompson CB. Role of the CD28 receptor in T-cell activation. Immunol Today 1990 11 : 211.
20. Riley JL, June CH. The CD28 family: a T-cell rheostat for therapeutic control of T-cell activation. Blood 2005 105 : 13.
21. Chambers CA, Kuhns MS, Egen JG, Allison JP. CTLA-4-mediated inhibition in regulation of T cell responses: mechanisms and manipulation in tumor immunotherapy. Annu Rev Immunol 2001 19 : 565.
22. Pentcheva-Hoang T, Egen JG, Wojnoonski K, Allison JP. B7-1 and B7-2 selectively recruit CTLA-4 and CD28 to the immunological synapse. Immunity 2004 21 : 401.
23. Brunner MC, Chambers CA, Chan FK, Hanke J, Winoto A, Allison JP. CTLA-4-Mediated inhibition of early events of T cell proliferation. J Immunol 1999 162 : 5813.
24. Wekerle T, Kurtz J, Ito H, et al. Allogeneic bone marrow transplantation with co-stimulatory blockade induces macrochimerism and tolerance without cytoreductive host treatment. Nat Med 2000 6 : 464.
25. Salomon B, Bluestone JA. Complexities of CD28/B7: CTLA-4 costimulatory pathways in autoimmunity and transplantation. Annu Rev Immunol 2001 19 : 225.
26. Ishida Y, Agata Y, Shibahara K, Honjo T. Induced expression of PD-1, a novel member of the immunoglobulin gene superfamily, upon programmed cell death. EMBO J 1992 11 : 3887.
27. Okazaki T, Honjo T. The PD-1-PD-L pathway in immunological tolerance. Trends Immunol 2006 27 : 195.
28. Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity 1999 11 : 141.
29. Nishimura H, Okazaki T, Tanaka Y, et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science 2001 291 : 319.
30. Okazaki T, Tanaka Y, Nishio R, et al. Autoantibodies against cardiac troponin I are responsible for dilated cardiomyopathy in PD-1-deficient mice. Nat Med 2003 9 : 1477.
31. Dong H, Zhu G, Tamada K, Chen L. B7-H1, a third member of the B7 family, co-stimulates T-cell proliferation and interleukin-10 secretion. Nat Med 1999 5 : 1365.
32. Yamazaki T, Akiba H, Iwai H, et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol 2002 169 : 5538.
33. Nakazawa A, Dotan I, Brimnes J, et al. The expression and function of costimulatory molecules B7H and B7-H1 on colonic epithelial cells. Gastroenterology 2004 126 : 1347.
34. Loke P, Allison JP. PD-L1 and PD-L2 are differentially regulated by Th1 and Th2 cells. Proc Natl Acad Sci U S A 2003 100 : 5336.
35. Latchman Y, Wood CR, Chernova T, et al. PD-L2 is a second ligand for PD-1 and inhibits T cell activation. Nat Immunol 2001 2 : 261.
36. Tseng SY, Otsuji M, Gorski K, et al. B7-DC, a new dendritic cell molecule with potent costimulatory properties for T cells. J Exp Med 2001 193 : 839.
37. Freeman GJ, Long AJ, Iwai Y, et al. Engagement of the PD-1 immunoinhibitory receptor by a novel B7 family member leads to negative regulation of lymphocyte activation. J Exp Med 2000 192 : 1027.
38. Carter L, Fouser L, Jussif J, et al. PD-1:PD-L inhibitory pathway affects both CD4(+) and CD8(+) T cells and is overcome by IL-2. Eur J Immunol 2002 32 : 634.
39. Ozkaynak E, Wang L, Goodearl A, et al. Programmed death-1 targeting can promote allograft survival. J Immunol 2002 169 : 6546.
40. Gao W, Demirci G, Strom TB, Li XC. Stimulating PD-1-negative signals concurrent with blocking CD154 co-stimulation induces long-term islet allograft survival. Transplantation 2003 76 : 994.
41. Wang L, Han R, Hancock WW. Programmed cell death 1 (PD-1) and its ligand PD-L1 are required for allograft tolerance. Eur J Immunol 2007 37 : 2983.
42. Cai G, Karni A, Oliveira EM, Weiner HL, Hafler DA, Freeman GJ. PD-1 ligands, negative regulators for activation of naive, memory, and recently activated human CD4+ T cells. Cell Immunol 2004 230 : 89.
43. Corry RJ, Winn HJ, Russell PS. Primarily vascularized allografts of hearts in mice. The role of H-2D, H-2K, and non-H-2 antigens in rejection. Transplantation 1973 16 : 343.
44. Auchincloss H, Jr., Mayer T, Ghobrial R, Winn HJ. T-cell subsets, bm mutants, and the mechanisms of allogeneic skin graft rejection. Immunol Res 1989 8 : 149.
45. Ito T, Ueno T, Clarkson MR, et al. 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.
46. Tao R, Wang L, Han R, et al. Differential effects of B and T lymphocyte attenuator and programmed death-1 on acceptance of partially versus fully MHC-mismatched cardiac allografts. J Immunol 2005 175 : 5774.
47. Yang J, Popoola J, Khandwala S, et al. Critical role of donor tissue expression of programmed death ligand-1 in regulating cardiac allograft rejection and vasculopathy. Circulation 2008 117 : 660.
48. Sandner SE, Clarkson MR, Salama AD, et al. Role of the programmed death-1 pathway in regulation of alloimmune responses in vivo. J Immunol 2005 174 : 3408.
49. Butte MJ, Keir ME, Phamduy TB, Sharpe AH, Freeman GJ. Programmed death-1 ligand 1 interacts specifically with the B7-1 costimulatory molecule to inhibit T cell responses. Immunity 2007 27 : 111.
50. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol 2008 26 : 677.
51. Wang S, Bajorath J, Flies DB, Dong H, Honjo T, Chen L. Molecular modeling and functional mapping of B7-H1 and B7-DC uncouple costimulatory function from PD-1 interaction. J Exp Med 2003 197 : 1083.
52. Kawai K, Shahinian A, Mak TW, Ohashi PS. Skin allograft rejection in CD28-deficient mice. Transplantation 1996 61 : 352.
53. Habicht A, Kewalaramani R, Vu MD, et al. Striking dichotomy of PD-L1 and PD-L2 pathways in regulating alloreactive CD4(+) and CD8(+) T cells in vivo. Am J Transplant 2007 7 : 2683.
54. Zheng XX, Sanchez-Fueyo A, Sho M, Domenig C, Sayegh MH, Strom TB. Favorably tipping the balance between cytopathic and regulatory T cells to create transplantation tolerance. Immunity 2003 19 : 503.
55. Lin H, Bolling SF, Linsley PS, et al. Long-term acceptance of major histocompatibility complex mismatched cardiac allografts induced by CTLA4Ig plus donor-specific transfusion. J Exp Med 1993 178 : 1801.
56. Sho M, Kishimoto K, Harada H, et al. Requirements for induction and maintenance of peripheral tolerance in stringent allograft models. Proc Natl Acad Sci U S A 2005 102 : 13230.
57. Parker DC, Greiner DL, Phillips NE, et al. Survival of mouse pancreatic islet allografts in recipients treated with allogeneic small lymphocytes and antibody to CD40 ligand. Proc Natl Acad Sci U S A 1995 92 : 9560.
58. Tanaka K, Albin MJ, Yuan X, et al. PDL1 is required for peripheral transplantation tolerance and protection from chronic allograft rejection. J Immunol 2007 179 : 5204.
59. Jones ND, van Maurik A, Hara M, et al. CD40-CD40 ligand-independent activation of CD8+ T cells can trigger allograft rejection. J Immunol 2000 165 : 1111.
60. Mai G, Bucher P, Morel P, et al. Anti-CD154 mAb treatment but not recipient CD154 deficiency leads to long-term survival of xenogeneic islet grafts. Am J Transplant 2005 5 : 1021.
61. Lehnert AM, Yi S, Burgess JS, O'Connell PJ. Pancreatic islet xenograft tolerance after short-term costimulation blockade is associated with increased CD4+ T cell apoptosis but not immune deviation. Transplantation 2000 69 : 1176.
62. Mai G, Del Rio ML, Tian J, Ramirez P, Buhler L, Rodriguez-Barbosa JI. Blockade of the PD-1/PD-1L pathway reverses the protective effect of anti-CD40L therapy in a rat to mouse concordant islet xenotransplantation model. Xenotransplantation 2007 14 : 243.
63. Raimondi G, Shufesky WJ, Tokita D, Morelli AE, Thomson AW. Regulated compartmentalization of programmed cell death-1 discriminates CD4+CD25+ resting regulatory T cells from activated T cells. J Immunol 2006 176 : 2808.
64. Gavin MA, Clarke SR, Negrou E, Gallegos A, Rudensky A. Homeostasis and anergy of CD4(+)CD25(+) suppressor T cells in vivo. Nat Immunol 2002 3 : 33.
65. Kitazawa Y, Fujino M, Wang Q, et al. Involvement of the programmed death-1/programmed death-1 ligand pathway in CD4+CD25+ regulatory T-cell activity to suppress alloimmune responses. Transplantation 2007 83 : 774.
66. Izawa A, Yamaura K, Albin MJ, et al. A novel alloantigen-specific CD8+PD1+ regulatory T cell induced by ICOS-B7h blockade in vivo. J Immunol 2007 179 : 786.
67. Tamura H, Dong H, Zhu G, et al. B7-H1 costimulation preferentially enhances CD28-independent T-helper cell function. Blood 2001 97 : 1809.
68. Shin T, Yoshimura K, Shin T, et al. In vivo costimulatory role of B7-DC in tuning T helper cell 1 and cytotoxic T lymphocyte responses. J Exp Med 2005 201 : 1531.
69. Watanabe N, Gavrieli M, Sedy JR, et al. BTLA is a lymphocyte inhibitory receptor with similarities to CTLA-4 and PD-1. Nat Immunol 2003 4 : 670.
70. Han P, Goularte OD, Rufner K, Wilkinson B, Kaye J. An inhibitory Ig superfamily protein expressed by lymphocytes and APCs is also an early marker of thymocyte positive selection. J Immunol 2004 172 : 5931.
71. Sedy JR, Gavrieli M, Potter KG, et al. B and T lymphocyte attenuator regulates T cell activation through interaction with herpesvirus entry mediator. Nat Immunol 2005 6 : 90.
72. Zeng C, Wu T, Zhen Y, Xia XP, Zhao Y. BTLA, a new inhibitory B7 family receptor with a TNFR family ligand. Cell Mol Immunol 2005 2 : 427.
73. Gonzalez LC, Loyet KM, Calemine-Fenaux J, et al. A coreceptor interaction between the CD28 and TNF receptor family members B and T lymphocyte attenuator and herpesvirus entry mediator. Proc Natl Acad Sci U S A 2005 102 : 1116.
74. Hurchla MA, Sedy JR, Gavrieli M, Drake CG, Murphy TL, Murphy KM. B and T lymphocyte attenuator exhibits structural and expression polymorphisms and is highly Induced in anergic CD4+ T cells. J Immunol 2005 174 : 3377.
75. Zeng C, Zhen Y, Shu SA, et al. The influence of cyclosporin A on lymphocyte attenuator expression. J Autoimmun 2007 28 : 234.
76. Nelson CA, Fremont MD, Sedy JR, et al. Structural determinants of herpesvirus entry mediator recognition by murine B and T lymphocyte attenuator. J Immunol 2008 180 : 940.
77. Zang X, Loke P, Kim J, Murphy K, Waitz R, Allison JP. B7x: a widely expressed B7 family member that inhibits T cell activation. Proc Natl Acad Sci U S A 2003 100 : 10388.
78. Mauri DN, Ebner R, Montgomery RI, et al. LIGHT, a new member of the TNF superfamily, and lymphotoxin alpha are ligands for herpesvirus entry mediator. Immunity 1998 8 : 21.
79. Murphy KM, Nelson CA, Sedy JR. Balancing co-stimulation and inhibition with BTLA and HVEM. Nat Rev Immunol 2006 6 : 671.
80. Croft M. The evolving crosstalk between co-stimulatory and co-inhibitory receptors: HVEM-BTLA. Trends Immunol 2005 26 : 292.
81. Force WR, Walter BN, Hession C, et al. Mouse lymphotoxin-beta receptor. Molecular genetics, ligand binding, and expression. J Immunol 1995 155 : 5280.
82. Wang Y, Subudhi SK, Anders RA, et al. The role of herpesvirus entry mediator as a negative regulator of T cell-mediated responses. J Clin Invest 2005 115 : 711.
83. Cai G, Anumanthan A, Brown JA, Greenfield EA, Zhu B, Freeman GJ. CD160 inhibits activation of human CD4+ T cells through interaction with herpesvirus entry mediator. Nat Immunol 2008 9 : 176.
84. Kaye J. CD160 and BTLA: LIGHTs out for CD4+ T cells. Nat Immunol 2008 9 : 122.
85. Hurchla MA, Sedy JR, Murphy KM. Unexpected role of B and T lymphocyte attenuator in sustaining cell survival during chronic allostimulation. J Immunol 2007 178 : 6073.
86. Wang Y, Pontesilli O, Gill RG, La Rosa FG, Lafferty KJ. The role of CD4+ and CD8+ T cells in the destruction of islet grafts by spontaneously diabetic mice. Proc Natl Acad Sci U S A 1991 88 : 527.
87. Prowse SJ, Lafferty KJ, Simeonovic CJ, Agostino M, Bowen KM, Steele EJ. The reversal of diabetes by pancreatic islet transplantation. Diabetes 1982 31 (Suppl. 4 30.
88. Benhamou PY. Immunomodulation with CTLA4-Ig in islet transplantation. Transplantation 2002 73 : S40.
89. Truong W, Hancock WW, Anderson CC, Merani S, Shapiro AM. Coinhibitory T-cell signaling in islet allograft rejection and tolerance. Cell Transplant 2006 15 : 105.
90. Truong W, Plester JC, Hancock WW, et al. Combined coinhibitory and costimulatory modulation with anti-BTLA and CTLA4Ig facilitates tolerance in murine islet allografts. Am J Transplant 2007 7 : 2663.
91. Scheu S, Alferink J, Potzel T, Barchet W, Kalinke U, Pfeffer K. Targeted disruption of LIGHT causes defects in costimulatory T cell activation and reveals cooperation with lymphotoxin beta in mesenteric lymph node genesis. J Exp Med 2002 195 : 1613.
92. Ye Q, Fraser CC, Gao W, et al. Modulation of LIGHT-HVEM costimulation prolongs cardiac allograft survival. J Exp Med 2002 195 : 795.
93. Chapoval AI, Ni J, Lau JS, et al. B7-H3: a costimulatory molecule for T cell activation and IFN-gamma production. Nat Immunol 2001 2 : 269.
94. Sun M, Richards S, Prasad DV, Mai XM, Rudensky A, Dong C. Characterization of mouse and human B7-H3 genes. J Immunol 2002 168 : 6294.
95. Suh WK, Gajewska BU, Okada H, et al. The B7 family member B7-H3 preferentially down-regulates T helper type 1-mediated immune responses. Nat Immunol 2003 4 : 899.
96. Prasad DV, Richards S, Mai XM, Dong C. B7S1, a novel B7 family member that negatively regulates T cell activation. Immunity 2003 18 : 863.
97. Prasad DV, Nguyen T, Li Z, et al. Murine B7-H3 is a negative regulator of T cells. J Immunol 2004 173 : 2500.
98. Wang L, Fraser CC, Kikly K, et al. B7-H3 promotes acute and chronic allograft rejection. Eur J Immunol 2005 35 : 428.
99. Sica GL, Choi IH, Zhu G, et al. B7-H4, a molecule of the B7 family, negatively regulates T cell immunity. Immunity 2003 18 : 849.
100. Agata Y, Kawasaki A, Nishimura H, et al. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int Immunol 1996 8 : 765.
101. 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.
102. Del Rio ML, Penuelas-Rivas G, Dominguez-Perles R, Ramirez P, Parrilla P, Rodriguez-Barbosa JI. Antibody-mediated signaling through PD-1 costimulates T cells and enhances CD28-dependent proliferation. Eur J Immunol 2005 35 : 3545.
103. Liang SC, Latchman YE, Buhlmann JE, et al. Regulation of PD-1, PD-L1, and PD-L2 expression during normal and autoimmune responses. Eur J Immunol 2003 33 : 2706.
104. Matsumoto K, Inoue H, Nakano T, et al. B7-DC regulates asthmatic response by an IFN-gamma-dependent mechanism. J Immunol 2004 172 : 2530.
105. Ishida M, Iwai Y, Tanaka Y, et al. Differential expression of PD-L1 and PD-L2, ligands for an inhibitory receptor PD-1, in the cells of lymphohematopoietic tissues. Immunol Lett 2002 84 : 57.
106. Xu Y, Flies AS, Flies DB, et al. Selective targeting of the LIGHT-HVEM costimulatory system for the treatment of graft-versus-host disease. Blood 2007 109 : 4097.