An Essential Role for IFN-γ in Regulation of Alloreactive CD8 T Cells Following Allogeneic Hematopoietic Cell Transplantation

Biology of Blood and Marrow Transplantation

Volumn 13, Issue 1, 2007, Pages 46-55

  Asavaroengchai, Wannee ^a   Wang, Hui ^a   Wang, Shumei ^a   Wang, Lan ^a   Bronson, Roderick ^b   Sykes, Megan ^a   Yang, Yong Guang ^a  

^a MASSACHUSETTS GENERAL HOSPITAL   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

allogeneic hematopoietic cell transplantation; CD8 T cells; Graft versus host disease; interferon gamma

Indexed keywords

CD4 ANTIGEN; DIPEPTIDYL PEPTIDASE IV; GAMMA INTERFERON; HERMES ANTIGEN;

ALLOGENEIC HEMATOPOIETIC STEM CELL TRANSPLANTATION; ALLOIMMUNITY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CD25+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL DEATH; CELL DIVISION; CELL SURVIVAL; CELLULAR IMMUNITY; CONTROLLED STUDY; DISEASE SEVERITY; DONOR; EFFECTOR CELL; FEMALE; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HAPLOTYPE; IMMUNOREGULATION; IRRADIATION; KNOCKOUT GENE; LIVER INJURY; LUNG INJURY; LYMPHOCYTE ACTIVATION; LYMPHOCYTE DEPLETION; LYMPHOCYTE SUBPOPULATION; MITOSIS INHIBITION; MOUSE; NONHUMAN; SPLEEN CELL; WILD TYPE;

ANIMALS; APOPTOSIS; CD8-POSITIVE T-LYMPHOCYTES; CELL DIVISION; FEMALE; GRAFT VS HOST DISEASE; HEMATOPOIETIC STEM CELL TRANSPLANTATION; INTERFERON TYPE II; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MINOR HISTOCOMPATIBILITY ANTIGENS; MODELS, ANIMAL; TRANSPLANTATION, HOMOLOGOUS;

EID: 33846018568     PISSN: 10838791     EISSN: 15236536     Source Type: Journal    
DOI: 10.1016/j.bbmt.2006.09.014     Document Type: Article

References (60)

1. Huang S., Hendriks W., Althage A., et al. Immune response in mice that lack the interferon-gamma receptor. Science 259 (1993) 1742-1745
2. Dalton D.K., Pitts-Meek S., Keshav S., Figari I.S., Bradley A., and Stewart T.A. Multiple defects of immune cell function in mice with disrupted interferon-gamma genes. Science 259 (1993) 1739-1742
3. Whitmire J.K., Tan J.T., and Whitton J.L. Interferon-{gamma} acts directly on CD8+ T cells to increase their abundance during virus infection. J Exp Med 201 (2005) 1053-1059
4. Refaeli Y., Van Parijs L., Alexander S.I., and Abbas A.K. Interferon {gamma} is required for activation-induced death of T lymphocytes. J Exp Med 196 (2002) 999-1005
5. Chu C.Q., Wittmer S., and Dalton D.K. Failure to suppress the expansion of the activated CD4 T cell population in interferon gamma-deficient mice leads to exacerbation of experimental autoimmune encephalomyelitis. J Exp Med 192 (2000) 123-128
6. Dalton D.K., Haynes L., Chu C.Q., Swain S.L., and Wittmer S. Interferon gamma eliminates responding CD4 T cells during mycobacterial infection by inducing apoptosis of activated CD4 T cells. J Exp Med 192 (2000) 117-122
7. Xu H., Wipasa J., Yan H., et al. The mechanism and significance of deletion of parasite-specific CD4+ T cells in malaria infection. J Exp Med 195 (2002) 881-892
8. Seder R.A., and Ahmed R. Similarities and differences in CD4+ and CD8+ effector and memory T cell generation. Nat Immunol 4 (2003) 835-842
9. Badovinac V.P., Tvinnereim A.R., and Harty J.T. Regulation of antigen-specific CD8(+) T cell homeostasis by perforin and interferon-gamma. Science 290 (2000) 1354-1358
10. Badovinac V.P., and Harty J.T. Adaptive immunity and enhanced CD8+ T cell response to Listeria monocytogenes in the absence of perforin and IFN-gamma. J Immunol 164 (2000) 6444-6452
11. Liu Y., and Janeway C.A. Interferon-gamma plays a critical role in induced cell death of effector T cell: a possible third mechanism of self-tolerance. J Exp Med 172 (1990) 1735-1739
12. Novelli F., D'Elios M.M., Bernabei P., et al. Expression and role in apoptosis of the alpha- and beta-chains of the IFN-gamma receptor on human Th1 and Th2 clones. J Immunol 159 (1997) 206-213
13. Oyaizu N., McCloskey T.W., Than S., Hu R., Kalyanaraman V.S., and Pahwa S. Cross-linking of CD4 molecules upregulates Fas antigen expression in lymphocytes by inducing interferon-γ and tumor necrosis factor-α secretion. Blood 84 (1994) 2622-2631
14. Badovinac V.P., Tvinnereim A.R., and Harty J.T. Regulation of antigen-specific CD8(+) T cell homeostasis by perforin and interferon-gamma [In Process Citation]. Science 290 (2000) 1354-1358
15. Konieczny B.T., Dai Z., Elwood E.T., et al. IFN-γ is critical for long-term allograft survival induced by blocking the CD28 and CD40 ligand T cell costimulation pathways. J Immunol 160 (1998) 2059-2064
16. Sawitzki B., Kingsley C.I., Oliveira V., Karim M., Herber M., and Wood K.J. IFN-{gamma} production by alloantigen-reactive regulatory T cells is important for their regulatory function in vivo. J Exp Med 201 (2005) 1925-1935
17. Badovinac V.P., Messingham K.A.N., Jabbari A., Haring J.S., and Harty J.T. Accelerated CD8+ T-cell memory and prime-boost response after dendritic-cell vaccination. Nat Med 11 (2005) 748-756
18. Niederwieser D., Herold M., Woloszczuk W., et al. Endogenous IFN-gamma during human bone marrow transplantation. Analysis of serum levels of interferon and interferon-dependent secondary messages. Transplantation 50 (1990) 620-625
19. Dickinson A.M., Sviland L., Hamilton P.J., et al. Cytokine involvement in predicting clinical graft-versus-host disease in allogeneic bone marrow transplant recipients. Bone Marrow Transplant 13 (1994) 65-70
20. Tanaka J., Imamura M., Kasai M., Sakurada K., and Miyazaki T. Cytokine gene expression after allogeneic bone marrow transplantation. Leuk Lymphoma 16 (1995) 413-418
21. Das H., Imoto S., Murayama T., et al. Kinetic analysis of cytokine gene expression in patients with GVHD after donor lymphocyte infusion. Bone Marrow Transplant 27 (2001) 373-380
22. Guy-Grand D., and Vassalli P. Gut injury in mouse graft-vs-host reaction: study of its occurrence and mechanism. J Clin Invest 77 (1986) 1584-1595
23. Mowat A.M. Antibodies to IFN-gamma prevent immunologically mediated intestinal damage in murine graft-versus-host reaction. Immunology 68 (1989) 18-23
24. Klimpel G.R., Annable C.R., Cleveland M.G., Jerrells T.R., and Patterson J.C. Immunosuppression and lymphoid hypoplasia associated with chronic graft versus host disease is dependent upon IFN-gamma production. J Immunol 144 (1990) 84-93
25. Parfrey N.A., El Sheikh A., Monckton E.A., Cockfield S.M., Halloran P.F., and Linetsky E. Interferon-gamma gene expression during acute graft-versus-host disease: relationship to MHC induction and tissue injury. J Pathol 189 (1999) 99-104
26. Yang Y.G., Dey B., Sergio J.J., Pearson D.A., and Sykes M. Donor-derived interferon γ is required for inhibition of acute graft-versus-host disease by interleukin 12. J Clin Invest 102 (1998) 2126-2135
27. Dey B., Yang Y.G., Szot G.L., Pearson D.A., and Sykes M. IL-12 inhibits GVHD through a Fas-mediated mechanism associated with alterations in donor T cell activation and expansion. Blood 91 (1998) 3315-3322
28. Murphy W.J., Welniak L.A., Taub D.D., et al. Differential effects of the absence of interferon-γ and IL-4 in acute graft-versus-host disease after allogeneic bone marrow transplantation in mice. J Clin Invest 102 (1998) 1742-1748
29. Reddy P., Teshima T., Kukuruga M., et al. Interleukin-18 regulates acute graft-versus-host disease by enhancing Fas-mediated donor T cell apoptosis. J Exp Med 194 (2001) 1433-1440
30. Yang Y.G., Qi J., Wang M.G., and Sykes M. Donor-derived interferon gamma separates graft-versus-leukemia effects and graft-versus-host disease induced by donor CD8 T cells. Blood 99 (2002) 4207-4215
31. Sha W.C., Nelson C.A., Newberry R.D., Kranz D.M., Russell R.D., and Loh D.Y. Selective expression of an antigen receptor on CD8-bearing T lymphocytes in transgenic mice. Nature 335 (1988) 271-274
32. Rubio M.T., Kim Y.M., Sachs T., Mapara M., Zhao G., and Sykes M. Antitumor effect of donor marrow graft rejection induced by recipient leukocyte infusions in mixed chimeras prepared with nonmyeloablative conditioning: critical role for recipient-derived IFN-{gamma}. Blood 102 (2003) 2300-2307
33. Ferrara J.L., Cooke K.R., Pan L., and Krenger W. The immunopathophysiology of acute graft-versus-host-disease. Stem Cells 14 (1996) 473-489
34. Butcher E.C., and Picker L.J. Lymphocyte homing and homeostasis. Science 272 (1996) 60-66
35. Kranz D.M., Sherman D.H., Sitkowsky M.V., Pasternack M.S., and Eisen H.N. Immunoprecipitation of cell surface structures of cloned cytotoxic T lymphocytes by clone-specific antisera. Proc Natl Acad Sci USA 81 (1984) 573-577
36. Anderson B.E., McNiff J., Yan J., et al. Memory CD4+ T cells do not induce graft-versus-host disease. J Clin Invest 112 (2003) 101-108
37. Foster A.E., Marangolo M., Sartor M.M., et al. Human CD62L- memory T cells are less responsive to alloantigen stimulation than CD62L+ naive T cells: potential for adoptive immunotherapy and allodepletion. Blood 104 (2004) 2403-2409
38. Zhang Y., Joe G., Zhu J., et al. Dendritic cell-activated CD44hiCD8+ T cells are defective in mediating acute graft-versus-host disease but retain graft-versus-leukemia activity. Blood 103 (2004) 3970-3978
39. Chen B.J., Cui X., Sempowski G.D., Liu C., and Chao N.J. Transfer of allogeneic CD62L- memory T cells without graft-versus-host disease. Blood 103 (2004) 1534-1541
40. Sherr C.J. Cancer cell cycles. Science 274 (1996) 1672-1677
41. Kiyokawa H., Kineman R.D., Manova-Todorova K.O., et al. Enhanced growth of mice lacking the cyclin-dependent kinase inhibitor function of p27(Kip1). Cell 85 (1996) 721-732
42. Nakayama K., Ishida N., Shirane M., et al. Mice lacking p27(Kip1) display increased body size, multiple organ hyperplasia, retinal dysplasia, and pituitary tumors. Cell 85 (1996) 707-720
43. Veiga-Fernandes H., and Rocha B. High expression of active CDK6 in the cytoplasm of CD8 memory cells favors rapid division. Nat Immunol 5 (2004) 31-37
44. Takami K., Takuwa N., Okazaki H., et al. Interferon-gamma inhibits hepatocyte growth factor-stimulated cell proliferation of human bronchial epithelial cells. Upregulation of p27kip1 cyclin-dependent kinase inhibitor. Am J Respir Cell Mol Biol 26 (2002) 231-238
45. Pernis A., Gupta S., Gollob K.J., et al. Lack of interferon gamma receptor beta chain and the prevention of interferon gamma signaling in TH1 cells. Science 269 (1995) 245-247
46. Bach E.A., Szabo S.J., Dighe A.S., et al. Ligand-induced autoregulation of IFN-gamma receptor β chain expression in T helper cell subsets. Science 270 (1995) 1215-1221
47. Sercan O., Hammerling G.J., Arnold B., and Schuler T. Cutting edge: innate immune cells contribute to the IFN-{gamma}-dependent regulation of antigen-specific CD8+ T cell homeostasis. J Immunol 176 (2006) 735-739
48. Cohen J.L., Trenado A., Vasey D., Klatzmann D., and Salomon B.L. CD4+CD25+ immunoregulatory T cells: new therapeutics for graft-versus-host disease. J Exp Med 196 (2002) 401-406
49. Ermann J., Hoffmann P., Edinger M., et al. Only the CD62L+ subpopulation of CD4+CD25+ regulatory T cells protects from lethal acute GVHD. Blood 105 (2005) 2220-2226
50. Seino K., Fukao K., Muramoto K., et al. Requirement for natural killer T (NKT) cells in the induction of allograft tolerance. Proc Natl Acad Sci USA 98 (2001) 2577-2581
51. Lan F., Zeng D., Higuchi M., Huie P., Higgins J.P., and Strober S. Predominance of NK1.1+TCR{alpha}{beta}+ or DX5+TCR{alpha}{beta}+ T cells in mice conditioned with fractionated lymphoid irradiation protects against graft-versus-host disease: "natural suppressor" cells. J Immunol 167 (2001) 2087-2096
52. Haraguchi K., Takahashi T., Matsumoto A., et al. Host-residual invariant NK T cells attenuate graft-versus-host immunity. J Immunol 175 (2005) 1320-1328
53. Farrar M.A., and Schreiber R.D. The molecular cell biology of interferon-gamma and its receptor. Annu Rev Immunol 11 (1993) 571-611
54. Peritt D., Robertson S., Gri G., Showe L., Aste-Amezaga M., and Trinchieri G. Cutting edge: differentiation of human NK cells into NK1 and NK2 subsets. J Immunol 161 (1998) 5821-5824
55. Fricke I., Mitchell D., Mittelstadt J., et al. Mycobacteria induce IFN-{gamma} production in human dendritic cells via triggering of TLR2. J Immunol 176 (2006) 5173-5182
56. Fukao T., Matsuda S., and Koyasu S. Synergistic Effects of IL-4 and IL-18 on IL-12-dependent IFN-{gamma} production by dendritic cells. J Immunol 164 (2000) 64-71
57. Chan C.W., Crafton E., Fan H.N., et al. Interferon-producing killer dendritic cells provide a link between innate and adaptive immunity. Nat Med 12 (2006) 207-213
58. Taieb J., Chaput N., Menard C., et al. A novel dendritic cell subset involved in tumor immunosurveillance. Nat Med 12 (2006) 214-219
59. Pelot M.R., Pearson D.A., Swenson K., et al. Lymphohematopoietic graft-vs-host reactions can be induced without graft-vs-host disease in murine mixed chimeras established with a cyclophosphamide-based non-myeloablative conditioning regimen. Biol Blood Marrow Transplant 5 (1999) 133-143
60. Kim Y.M., Sachs T., Asavaroengchai W., Bronson R., and Sykes M. Graft-versus-host disease can be separated from graft-versus-lymphoma effects by control of lymphocyte trafficking with FTY720. J Clin Invest 111 (2003) 659