Tracking of TCR-transgenic T cells reveals that multiple mechanisms maintain cardiac transplant tolerance in mice

American Journal of Transplantation

Volumn 16, Issue 10, 2016, Pages 2854-2864

  Miller, M L ^a   Daniels, M D ^a,b   Wang, T ^a,c   Wang, Y ^a   Xu, J ^a   Yin, D ^a   Chong, A S ^a   Alegre, Maria Luisa ^a  

^a UNIVERSITY OF CHICAGO   (United States)

^b CHICAGO STATE UNIVERSITY   (United States)

^c The First People's Hospital of Yunnan Province   (China)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; HERMES ANTIGEN; IONOMYCIN; PROGRAMMED DEATH 1 LIGAND 1; T LYMPHOCYTE RECEPTOR; CD274 PROTEIN, MOUSE; LYMPHOCYTE ANTIGEN RECEPTOR;

ADOPTIVE TRANSFER; ALLOREACTIVE T CELL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CD25+ T LYMPHOCYTE; CELL COUNT; CELL TRANSFER; COMPARATIVE STUDY; CONTROLLED STUDY; CYTOKINE PRODUCTION; GRAFT SURVIVAL; HEART GRAFT; IMMUNIZATION; MEDIAN SURVIVAL TIME; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TRANSPLANTATION TOLERANCE; ALLOGRAFT; ANIMAL; BAGG ALBINO MOUSE; C57BL MOUSE; GRAFT REJECTION; HEART TRANSPLANTATION; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; REGULATORY T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TRANSGENIC MOUSE;

ADOPTIVE TRANSFER; ALLOGRAFTS; ANIMALS; B7-H1 ANTIGEN; GRAFT REJECTION; HEART TRANSPLANTATION; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, TRANSGENIC; RECEPTORS, ANTIGEN, T-CELL; T-LYMPHOCYTE SUBSETS; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION TOLERANCE;

EID: 84965138769     PISSN: 16006135     EISSN: 16006143     Source Type: Journal    
DOI: 10.1111/ajt.13814     Document Type: Article

References (42)

1. Waldmann H, Adams E, Cobbold S. Reprogramming the immune system: Co-receptor blockade as a paradigm for harnessing tolerance mechanisms. Immunol Rev 2008; 223: 361–370.
2. Welsh RM, Markees TG, Woda BA, et al. Virus-induced abrogation of transplantation tolerance induced by donor-specific transfusion and anti-CD154 antibody. J Virol 2000; 74: 2210–2218.
3. Ahmed EB, Wang T, Daniels M, Alegre M-L, Chong AS. IL-6 induced by Staphylococcus aureus infection prevents the induction of skin allograft acceptance in mice. Am J Transplant 2011; 11: 936–946.
4. Wang T, Chen L, Ahmed E, et al. Prevention of allograft tolerance by bacterial infection with Listeria monocytogenes. J Immunol 2008; 180: 5991–5999.
5. Pantenburg B, Heinzel F, Das L, Heeger PS, Valujskikh A. T cells primed by Leishmania major infection cross-react with alloantigens and alter the course of allograft rejection. J Immunol 2002; 169: 3686–3693.
6. Chen L, Wang T, Zhou P, et al. TLR engagement prevents transplantation tolerance. Am J Transplant 2006; 6: 2282–2291.
7. Ford ML, Koehn BH, Wagener ME, et al. Antigen-specific precursor frequency impacts T cell proliferation, differentiation, and requirement for costimulation. J Exp Med 2007; 204: 299–309.
8. Wu Z, Bensinger SJ, Zhang J, et al. Homeostatic proliferation is a barrier to transplantation tolerance. Nat Med 2004; 10: 87–92.
9. Wells AD, Li XC, Li Y, et al. Requirement for T-cell apoptosis in the induction of peripheral transplantation tolerance. Nat Med 1999; 5: 1303–1307.
10. Schroeder G, Risch K, Kotsch K, et al. FTY720 prevents anti-CD4 mAb-induced tolerance but cannot reverse established tolerance in a rat kidney transplantation model. Am J Transplant 2004; 4: 863–871.
11. Lee I, Wang L, Wells AD, Dorf ME, Ozkaynak E, Hancock WW. Recruitment of Foxp3+ T regulatory cells mediating allograft tolerance depends on the CCR4 chemokine receptor. J Exp Med 2005; 201: 1037–1044.
12. Jiang X, Sun W, Guo D, et al. Cardiac allograft acceptance induced by blockade of CD40-CD40L costimulation is dependent on CD4+CD25+ regulatory T cells. Surgery 2011; 149: 336–346.
13. Lal G, Nakayama Y, Sethi A, et al. Interleukin-10 from marginal zone precursor B-cell subset is required for costimulatory blockade-induced transplantation tolerance. Transplantation 2015; 99: 1817–1828.
14. Lu L-F, Lind EF, Gondek DC, et al. Mast cells are essential intermediaries in regulatory T-cell tolerance. Nature 2006; 442: 997–1002.
15. 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: 6648–6656.
16. Haspot F, Fehr T, Gibbons C, et al. Peripheral deletional tolerance of alloreactive CD8 but not CD4 T cells is dependent on the PD-1/PD-L1 pathway. Blood 2008; 112: 2149–2155.
17. de Vries VC, Wasiuk A, Bennett KA, et al. Mast cell degranulation breaks peripheral tolerance. Am J Transplant 2009; 9: 2270–2280.
18. Miller ML, Daniels MD, Wang T, et al. Spontaneous restoration of transplantation tolerance after acute rejection. Nat Commun 2015; 6: 7566.
19. Wang T, Ahmed EB, Chen L, et al. Infection with the intracellular bacterium, Listeria monocytogenes, overrides established tolerance in a mouse cardiac allograft model. Am J Transplant 2010; 10: 1524–1533.
20. 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: 343–350.
21. Qin S, Cobbold SP, Pope H, et al. “Infectious” transplantation tolerance. Science 1993; 259: 974–977.
22. Quezada SA, Bennett K, Blazar BR, Rudensky AY, Sakaguchi S, Noelle RJ. Analysis of the underlying cellular mechanisms of anti-CD154-induced graft tolerance: The interplay of clonal anergy and immune regulation. J Immunol 2005; 175: 771–779.
23. Chai J-G, Ratnasothy K, Bucy RP, Noelle RJ, Lechler R, Lombardi G. Allospecific CD4(+) T cells retain effector function and are actively regulated by Treg cells in the context of transplantation tolerance. Eur J Immunol 2015; 45: 2017–2027.
24. 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: 5204–5210.
25. 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: 2983–2990.
26. Koehn BH, Ford ML, Ferrer IR, et al. PD-1-dependent mechanisms maintain peripheral tolerance of donor-reactive CD8+ T cells to transplanted tissue. J Immunol 2008; 181: 5313–5322.
27. Brouard S, Pallier A, Renaudin K, et al. The natural history of clinical operational tolerance after kidney transplantation through twenty-seven cases. Am J Transplant 2012; 12: 3296–3307.
28. Iwakoshi NN, Markees TG, Turgeon N, et al. Skin allograft maintenance in a new synchimeric model system of tolerance. J Immunol 2001; 167: 6623–6630.
29. Iwakoshi NN, Mordes JP, Markees TG, Phillips NE, Rossini AA, Greiner DL. Treatment of allograft recipients with donor-specific transfusion and anti-CD154 antibody leads to deletion of alloreactive CD8+ T cells and prolonged graft survival in a CTLA4-dependent manner. J Immunol 2000; 164: 512–521.
30. Adams AB, Williams MA, Jones TR, et al. Heterologous immunity provides a potent barrier to transplantation tolerance. J Clin Invest 2003; 111: 1887–1895.
31. Adler AJ, Huang CT, Yochum GS, Marsh DW, Pardoll DM. In vivo CD4+ T cell tolerance induction versus priming is independent of the rate and number of cell divisions. J Immunol 2000; 164: 649–655.
32. Lin C-Y, Graca L, Cobbold SP, Waldmann H. Dominant transplantation tolerance impairs CD8+ T cell function but not expansion. Nat Immunol 2002; 3: 1208–1213.
33. Bennett F, Luxenberg D, Ling V, et al. Program death-1 engagement upon TCR activation has distinct effects on costimulation and cytokine-driven proliferation: Attenuation of ICOS, IL-4, and IL-21, but not CD28, IL-7, and IL-15 responses. J Immunol 2003; 170: 711–718.
34. Ali J, Harper I, Bolton E, Bradley JA, Pettigrew G. Recipient natural killer cell allorecognition of passenger donor lymphocytes and its effect on adaptive alloimmunity after transplantation. Lancet 2015; 385(Suppl 1): S18.
35. Walch JM, Zeng Q, Li Q, et al. Cognate antigen directs CD8+ T cell migration to vascularized transplants. J Clin Invest 2013; 123: 2663–2671.
36. Yang J, Brook MO, Carvalho-Gaspar M, et al. Allograft rejection mediated by memory T cells is resistant to regulation. PNAS 2007; 104: 19954–19959.
37. Kendal AR, Chen Y, Regateiro FS, et al. Sustained suppression by Foxp3+ regulatory T cells is vital for infectious transplantation tolerance. J Exp Med 2011; 208: 2043–2053.
38. Baas M, Besançon A, Goncalves T, et al. TGFß-dependent expression of PD-1 and PD-L1 controls CD8(+) T cell anergy in transplant tolerance. Elife 2016; 5: e08133.
39. Miyajima M, Chase CM, Alessandrini A, et al. Early acceptance of renal allografts in mice is dependent on foxp3(+) cells. Am J Pathol 2011; 178: 1635–1645.
40. Yamada Y, Nadazdin O, Boskovic S, et al. Repeated injections of IL-2 break renal allograft tolerance induced via mixed hematopoietic chimerism in monkeys. Am J Transplant 2015; 15: 3055–3066.
41. Iida S, Suzuki T, Tanabe K, Valujskikh A, Fairchild RL, Abe R. Transient lymphopenia breaks costimulatory blockade-based peripheral tolerance and initiates cardiac allograft rejection. Am J Transplant 2013; 13: 2268–2279.
42. Okumi M, Fishbein JM, Griesemer AD, et al. Role of persistence of antigen and indirect recognition in the maintenance of tolerance to renal allografts. Transplantation 2008; 85: 270–280.