Alloantigen expression on non-hematopoietic cells reduces graft-versus-leukemia effects in mice

Journal of Clinical Investigation

Volumn 120, Issue 7, 2010, Pages 2370-2378

  Asakura, Shoji ^a   Hashimoto, Daigo ^a,b   Takashima, Shuichiro ^b   Sugiyama, Haruko ^a   Maeda, Yoshinobu ^a   Akashi, Koichi ^b   Tanimoto, Mitsune ^a   Teshima, Takanori ^b  

^a OKAYAMA UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOANTIGEN; PROGRAMMED DEATH 1 LIGAND 1; PROGRAMMED DEATH 1 RECEPTOR; MINOR HISTOCOMPATIBILITY ANTIGEN;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ANTIGEN PRESENTING CELL; APOPTOSIS; ARTICLE; BONE MARROW TRANSPLANTATION; CONTROLLED STUDY; FEMALE; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; HEMATOLOGIC MALIGNANCY; LEUKEMIA CELL; MAJOR HISTOCOMPATIBILITY COMPLEX; MOUSE; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; T LYMPHOCYTE; ANIMAL; BAGG ALBINO MOUSE; C3H MOUSE; C57BL MOUSE; DBA MOUSE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; IMMUNOLOGY; LEUKEMIA; MOUSE MUTANT; PATHOLOGY; TRANSPLANTATION;

ANIMALS; ANTIGEN-PRESENTING CELLS; BONE MARROW TRANSPLANTATION; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; ISOANTIGENS; LEUKEMIA; MICE; MICE, INBRED BALB C; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, INBRED DBA; MICE, KNOCKOUT; MINOR HISTOCOMPATIBILITY ANTIGENS; T-LYMPHOCYTES;

EID: 77954987288     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI39165     Document Type: Article

References (62)

1. Weiden P, et al. Antileukemic effect of graft-versus-host disease in human recipients of allogeneic-marrow grafts. N Engl J Med. 1979;300(19):1068- 1073.
2. Weiden PL, Sullivan KM, Flournoy N, Storb R, Thomas ED. Antileukemic effect of chronic graft-versus-host disease: contribution to improved survival after allogeneic marrow transplantation. N Engl J Med. 1981;304(25):1529-1533.
3. Korngold R, Sprent J. Lethal graft-versus-host disease after bone marrow transplantation across minor histocompatibility barriers in mice. Prevention by removing mature T-cells from marrow. J Exp Med. 1978;148(6):1687-1698.
4. Apperley JF, Jones L, Hale G, Goldman JM. Bone marrow transplantation for chronic myeloid leukemia: T-cell depletion with Campath-1 reduces the incidence of acute graft-versus-host disease but may increase the risk of leukemia relapse. Bone Marrow Transplant. 1986;1(1):53-66.
5. Atkinson K, et al. Risk factors for chronic graft-versus-host disease after HLA-identical sibling bone marrow transplantation. Blood. 1990;75(12):2459-2464.
6. Shlomchik WD, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285(5426):412-415.
7. Reddy P, Maeda Y, Liu C, Krijanovski OI, Korngold R, Ferrara JL. A crucial role for antigen-presenting cells and alloantigen expression in graft-versus-leukemia responses. Nat Med. 2005;11(11):1244-1249.
8. Bleakley M, Riddell SR. Molecules and mechanisms of the graft-versus-leukaemia effect. Nat Rev Cancer. 2004;4(5):371-380.
9. Teshima T, et al. Acute graft-versus-host disease does not require alloantigen expression on host epithelium. Nat Med. 2002;8(6):575-581.
10. Jones SC, Murphy GF, Friedman TM, Korngold R. Importance of minor histocompatibility antigen expression by nonhematopoietic tissues in a CD4+ T cell-mediated graft-versus-host disease model. J Clin Invest. 2003;112(12):1880-1886.
11. Ruggeri L, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097-2100.
12. Matte CC, et al. Donor APCs are required for maximal GVHD but not for GVL. Nat Med. 2004; 10(9):987-992.
13. Cooke KR, et al. An experimental model of idiopathic pneumonia syndrome after bone marrow transplantation. I. The roles of minor H antigens and endotoxin. Blood. 1996;88(8):3230-3239.
14. Korngold R, Sprent J. Features of T cells causing H-2-restricted lethal graft-vs.-host disease across minor histocompatibility barriers. J Exp Med. 1982;155(3):872-883.
15. Zhang Y, Joe G, Hexner E, Zhu J, Emerson SG. Alloreactive memory T cells are responsible for the persistence of graft-versus-host disease. J Immunol. 2005;174(5):3051-3058. (Pubitemid 40279726)
16. Stefanova I, Dorfman JR, Germain RN. Self-recognition promotes the foreign antigen sensitivity of naive T lymphocytes. Nature. 2002;420(6914):429- 434.
17. Zhang Y, Louboutin JP, Zhu J, Rivera AJ, Emerson SG. Preterminal host dendritic cells in irradiated mice prime CD8+ T cell-mediated acute graft-versushost disease. J Clin Invest. 2002;109(10):1335-1344.
18. Zajac AJ, et al. Viral immune evasion due to persistence of activated T cells without effector function. J Exp Med. 1998;188(12):2205-2213.
19. Barber DL, et al. Restoring function in exhausted CD8 T cells during chronic viral infection. Nature. 2006; 439(7077):682-687.
20. Shin H, Wherry EJ. CD8 T cell dysfunction during chronic viral infection. Curr Opin Immunol. 2007; 19(4):408-415.
21. Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008;26:677-704.
22. Dong H, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8(8):793-800.
23. Ahmadzadeh M, et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009; 114(8):1537-1544.
24. Zhang L, Gajewski TF, Kline J. PD-1/PD-L1 interactions inhibit anti-tumor immune responses in a murine acute myeloid leukemia model. Blood. 2009; 114(8):1545-1552.
25. Mumprecht S, Schurch C, Schwaller J, Solenthaler M, Ochsenbein AF. PD-1 signaling on chronic myeloid leukemia-specific T cells results in T cell exhaustion and disease progression. Blood. 2009; 114(8):1528-1536.
26. Iwai Y, Terawaki S, Ikegawa M, Okazaki T, Honjo T. PD-1 inhibits antiviral immunity at the effector phase in the liver. J Exp Med. 2003;198(1):39-50.
27. Horowitz MM, et al. Graft-versus-leukemia reactions after bone marrow transplantation. Blood. 1990;75(3):555-562.
28. Gallimore A, et al. Induction and exhaustion of lymphocytic choriomeningitis virus-specific cytotoxic T lymphocytes visualized using soluble tetrameric major histocompatibility complex class I-peptide complexes. J Exp Med. 1998;187(9):1383-1393.
29. Welsh RM. Assessing CD8 T cell number and dysfunction in the presence of antigen. J Exp Med. 2001; 193(5):F19-F22.
30. Moskophidis D, Lechner F, Pircher H, Zinkernagel RM. Virus persistence in acutely infected immuno-competent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 1993;362(6422):758-761.
31. Appay V, et al. HIV-specific CD8(+) T cells produce antiviral cytokines but are impaired in cytolytic function. J Exp Med. 2000;192(1):63-75.
32. Xiong Y, et al. Simian immunodeficiency virus (SIV) infection of a rhesus macaque induces SIV-specific CD8(+) T cells with a defect in effector function that is reversible on extended interleukin-2 incubation. J Virol. 2001;75(6):3028-3033.
33. Pantaleo G, Harari A. Functional signatures in antiviral T-cell immunity for monitoring virus-associated diseases. Nat Rev Immunol. 2006;6(5):417-423.
34. Tham EL, Mescher MF. Signaling alterations in activation-induced nonresponsive CD8 T cells. J Immunol. 2001;167(4):2040-2048.
35. Tham EL, Shrikant P, Mescher MF. Activation-induced nonresponsiveness: a Th-dependent regulatory checkpoint in the CTL response. J Immunol. 2002;168(3):1190-1197.
36. Boissonnas A, et al. Antigen distribution drives programmed antitumor CD8 cell migration and determines its efficiency. J Immunol. 2004;173(1):222-229.
37. Saito T, Dworacki G, Gooding W, Lotze MT, Whiteside TL. Spontaneous apoptosis of CD8+ T lymphocytes in peripheral blood of patients with advanced melanoma. Clin Cancer Res. 2000;6(4):1351-1364.
38. Fontaine P, Roy-Proulx G, Knafo L, Baron C, Roy DC, Perreault C. Adoptive transfer of minor histocompatibility antigen-specific T lymphocytes eradicates leukemia cells without causing graft-versus-host disease. Nat Med. 2001;7(7):789-794.
39. Meunier MC, Roy-Proulx G, Labrecque N, Perreault C. Tissue distribution of target antigen has a decisive influence on the outcome of adoptive cancer immunotherapy. Blood. 2003;101(2):766-770.
40. Dickinson AM, et al. In situ dissection of the graftversus- host activities of cytotoxic T cells specific for minor histocompatibility antigens. Nat Med. 2002; 8(4):410-414.
41. Ding ZC, Blazar BR, Mellor AL, Munn DH, Zhou G. Chemotherapy rescues tumor-driven aberrant CD4+ T-cell differentiation and restores an activated polyfunctional helper phenotype. Blood. 2010; 115(12):2397-2406.
42. Tanaka K, et al. PDL1 is required for peripheral transplantation tolerance and protection from chronic allograft rejection. J Immunol. 2007; 179(8):5204-5210.
43. Haspot F, 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(5):2149-2155.
44. Yamazaki T, et al. Expression of programmed death 1 ligands by murine T cells and APC. J Immunol. 2002;169(10):5538-5545.
45. Keir ME, et al. Tissue expression of PD-L1 mediates peripheral T cell tolerance. J Exp Med. 2006; 203(4):883-895.
46. Crawford A, Wherry EJ. The diversity of costimulatory and inhibitory receptor pathways and the regulation of antiviral T cell responses. Curr Opin Immunol. 2009;21(2):179-186.
47. Blackburn SD, et al. Coregulation of CD8+ T cell exhaustion by multiple inhibitory receptors during chronic viral infection. Nat Immunol. 2009; 10(1):29-37.
48. Petrovas C, et al. PD-1 is a regulator of virus-specific CD8+ T cell survival in HIV infection. J Exp Med. 2006;203(10):2281-2292.
49. Brooks DG, Trifilo MJ, Edelmann KH, Teyton L, McGavern DB, Oldstone MB. Interleukin-10 determines viral clearance or persistence in vivo. Nat Med. 2006;12(11):1301-1309.
50. Blackburn SD, Shin H, Freeman GJ, Wherry EJ. Selective expansion of a subset of exhausted CD8 T cells by alphaPD-L1 blockade. Proc Natl Acad Sci U S A. 2008;105(39):15016-15021.
51. Kaufmann DE, et al. Upregulation of CTLA-4 by HIV-specific CD4+ T cells correlates with disease progression and defines a reversible immune dysfunction. Nat Immunol. 2007;8(11):1246-1254.
52. Franceschini D, et al. PD-L1 negatively regulates CD4+CD25+Foxp3+ Tregs by limiting STAT-5 phosphorylation in patients chronically infected with HCV. J Clin Invest. 2009;119(3):551-564.
53. Socie G, Blazar BR. Acute graft-versus-host disease: from the bench to the bedside. Blood. 2009; 114(20):4327-4336.
54. Blazar BR, et al. Blockade of programmed death-1 engagement accelerates graft-versus-host disease lethality by an IFN-gamma-dependent mechanism. J Immunol. 2003;171(3):1272-1277.
55. Brochu S, Rioux-Masse B, Roy J, Roy DC, Perreault C. Massive activation-induced cell death of alloreactive T cells with apoptosis of bystander postthymic T cells prevents immune reconstitution in mice with graft-versus-host disease. Blood. 1999;94(2):390-400.
56. Dey B, et al. The fate of donor T-cell receptor transgenic T cells with known host antigen specificity in a graft-versus-host disease model. Transplantation. 1999;68(1):141-149.
57. Choi EY, et al. Real-time T-cell profiling identifies H60 as a major minor histocompatibility antigen in murine graft-versus-host disease. Blood. 2002; 100(13):4259-4265.
58. Michalek J, Collins RH, Hill BJ, Brenchley JM, Douek DC. Identification and monitoring of graft-versus-host specific T-cell clone in stem cell transplantation. Lancet. 2003;361(9364):1183-1185.
59. Hirano F, et al. Blockade of B7-H1 and PD-1 by monoclonal antibodies potentiates cancer therapeutic immunity. Cancer Res. 2005;65(3):1089-1096.
60. Ando K, et al. Perforin, Fas/Fas ligand, and TNFalpha pathways as specific and bystander killing mechanisms of hepatitis C virus-specific human CTL. J Immunol. 1997;158(11):5283-5291.
61. Tsushima F, et al. Preferential contribution of B7-H1 to programmed death-1-mediated regulation of hapten-specific allergic inflammatory responses. Eur J Immunol. 2003;33(10):2773-2782.
62. Teshima T, et al. IL-11 separates graft-versus-leukemia effects from graft-versus-host disease after bone marrow transplantation. J Clin Invest. 1999;104(3):317-325.