NK cells mediate reduction of GVHD by inhibiting activated, alloreactive T cells while retaining GVT effects

Blood

Volumn 115, Issue 21, 2010, Pages 4293-4301

  Olson, Janelle A ^a,c   Leveson Gower, Dennis B ^a   Gill, Saar ^a   Baker, Jeanette ^a   Beilhack, Andreas ^b   Negrin, Robert S ^a  

^a STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD69 ANTIGEN; FAS LIGAND; GAMMA INTERFERON; INTERLEUKIN 2; INTERLEUKIN 2 RECEPTOR ALPHA; PERFORIN; TRANSCRIPTION FACTOR FOXP3; AUTACOID; CYTOKINE; FASL PROTEIN, MOUSE; IL2RA PROTEIN, MOUSE; PERFORIN, MOUSE; PORE FORMING CYTOTOXIC PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; B CELL LYMPHOMA; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELL ACTIVATION; CELL LINE; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GRAFT SURVIVAL; GRAFT VERSUS HOST REACTION; GRAFT VERSUS LEUKEMIA EFFECT; INHIBITION KINETICS; MALE; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL; ALLOTRANSPLANTATION; ANIMAL; BAGG ALBINO MOUSE; BIOSYNTHESIS; BONE MARROW TRANSPLANTATION; C57BL MOUSE; CYTOLOGY; GENETICS; IMMUNOLOGY; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE MUTANT; REGULATORY T LYMPHOCYTE; TRANSGENIC MOUSE; TRANSPLANTATION;

ANIMALS; APOPTOSIS; BONE MARROW TRANSPLANTATION; CD4-POSITIVE T-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; CYTOKINES; FAS LIGAND PROTEIN; FEMALE; GRAFT VS HOST DISEASE; GRAFT VS TUMOR EFFECT; INFLAMMATION MEDIATORS; INTERFERON-GAMMA; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; KILLER CELLS, NATURAL; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PORE FORMING CYTOTOXIC PROTEINS; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY; TRANSPLANTATION, HOMOLOGOUS;

EID: 77953644448     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2009-05-222190     Document Type: Article

References (40)

1. Copelan EA. Hematopoietic stem-cell transplantation. N Engl J Med. 2006;354(17):1813-1826.
2. Ferrara JL, Deeg HJ. Graft-versus-host disease. N Engl J Med. 1991;324(10):667-674.
3. Yokoyama WM, Kim S, French AR. The dynamic life of natural killer cells. Annu Rev Immunol. 2004;22:405-429. (Pubitemid 38680428)
4. Asai O, Longo DL, Tian ZG, et al. Suppression of graft-versus-host disease and amplification of graft-versus-tumor effects by activated natural killer cells after allogeneic bone marrow transplantation. J Clin Invest. 1998;101(9):1835-1842.
5. Ruggeri L, Capanni M, Urbani E, et al. Effectiveness of donor natural killer cell alloreactivity in mismatched hematopoietic transplants. Science. 2002;295(5562):2097-2100.
6. Shlomchik WD, Couzens MS, Tang CB, et al. Prevention of graft versus host disease by inactivation of host antigen-presenting cells. Science. 1999;285(5426):412-415. (Pubitemid 29343964)
7. Beilhack A, Schulz S, Baker J, et al. In vivo analyses of early events in acute graft-versus-host disease reveal sequential infiltration of T-cell subsets. Blood. 2005;106(3):1113-1122.
8. Panoskaltsis-Mortari A, Price A, Hermanson JR, et al. In vivo imaging of graft-versus-host-disease in mice. Blood. 2004;103(9):3590-3598.
9. Reddy P. Pathophysiology of acute graft-versus-host disease. Hematol Oncol. 2003;21(4):149-161.
10. Olson JA, Zeiser R, Beilhack A, Goldman JJ, Negrin RS. Tissue-specific homing and expansion of donor NK cells in allogeneic bone marrow transplantation. J Immunol. 2009;183(5):3219-3228.
11. Rabinovich BA, Li J, Shannon J, et al. Activated, but not resting, T cells can be recognized and killed by syngeneic NK cells. J Immunol. 2003;170(7):3572-3576.
12. Cerboni C, Zingoni A, Cippitelli M, Piccoli M, Frati L, Santoni A. Antigen-activated human T lymphocytes express cell-surface NKG2D ligands via an ATM/ATR-dependent mechanism and become susceptible to autologous NK-cell lysis. Blood. 2007;110(2):606-615. (Pubitemid 47105399)
13. Diefenbach A, Jamieson AM, Liu SD, Shastri N, Raulet DH. Ligands for the murine NKG2D receptor: expression by tumor cells and activation of NK cells and macrophages. Nat Immunol. 2000;1(2):119-126.
14. Carayannopoulos LN, Naidenko OV, Fremont DH, Yokoyama WM. Cutting edge: murine UL16-binding protein-like transcript 1: a newly described transcript encoding a high-affinity ligand for murine NKG2D. J Immunol. 2002;169(8):4079-4083.
15. Diefenbach A, Hsia JK, Hsiung MY, Raulet DH. A novel ligand for the NKG2D receptor activates NK cells and macrophages and induces tumor immunity. Eur J Immunol. 2003;33(2):381-391.
16. Cerwenka A, Bakker AB, McClanahan T, et al. Retinoic acid early inducible genes define a ligand family for the activating NKG2D receptor in mice. Immunity. 2000;12(6):721-727.
17. Kägi D, Ledermann B, Burki K, et al. Cytotoxicity mediated by T cells and natural killer cells is greatly impaired in perforin-deficient mice. Nature. 1994;369(6475):31-37.
18. Arase H, Arase N, Saito T. Fas-mediated cytotoxicity by freshly isolated natural killer cells. J Exp Med. 1995;181(3):1235-1238.
19. Kayagaki N, Yamaguchi N, Nakayama M, et al. Expression and function of TNF-related apoptosis-inducing ligand on murine activated NK cells. J Immunol. 1999;163(4):1906-1913.
20. Cao YA, Wagers AJ, Beilhack A, et al. Shifting foci of hematopoiesis during reconstitution from single stem cells. Proc Natl Acad Sci U S A. 2004;101(1):221-226. (Pubitemid 38084231)
21. Zeiser R, Leveson-Gower DB, Zambricki EA, et al. Differential impact of mammalian target of rapamycin inhibition on CD4+CD25+Foxp3+ regulatory T cells compared with conventional CD4+ T cells. Blood. 2008;111(1):453-462.
22. Edinger M, Cao YA, Verneris MR, Bachmann MH, Contag CH, Negrin RS. Revealing lymphoma growth and the efficacy of immune cell therapies using in vivo bioluminescence imaging. Blood. 2003;101(2):640-648.
23. Verneris MR, Karami M, Baker J, Jayaswal A, Negrin RS. Role of NKG2D signaling in the cytotoxicity of activated and expanded CD8+ T cells. Blood. 2004;103(8):3065-3072.
24. Kim YM, Sachs T, Asavaroengchai W, Bronson R, Sykes M. Graft-versus-host disease can be separated from graft-versus-lymphoma effects by control of lymphocyte trafficking with FTY720. J Clin Invest. 2003;111(5):659-669. (Pubitemid 36278584)
25. Tanaka J, Imamura M, Kasai M, et al. The important balance between cytokines derived from type 1 and type 2 helper T cells in the control of graft-versus-host disease. Bone Marrow Transplant. 1997;19(6):571-576.
26. Via CS, Finkelman FD. Critical role of interleukin-2 in the development of acute graft-versus-host disease. Int Immunol. 1993;5(6):565-572.
27. Goker H, Haznedaroglu IC, Chao NJ. Acute graft-vs-host disease: pathobiology and management. Exp Hematol. 2001;29(3):259-277.
28. Mowat AM. Antibodies to IFN-gamma prevent immunologically mediated intestinal damage in murine graft-versus-host reaction. Immunology. 1989;68(1):18-23.
29. Dickinson AM, Sviland L, Dunn J, Carey P, Proctor SJ. Demonstration of direct involvement of cytokines in graft-versus-host reactions using an in vitro human skin explant model. Bone Marrow Transplant. 1991;7(3):209-216.
30. Hallett WH, Murphy WJ. Natural killer cells: biology and clinical use in cancer therapy. Cell Mol Immunol. 2004;1(1):12-21.
31. Fort MM, Leach MW, Rennick DM. A role for NK cells as regulators of CD4+ T cells in a transfer model of colitis. J Immunol. 1998;161(7):3256-3261. (Pubitemid 128470617)
32. Zhang B, Yamamura T, Kondo T, Fujiwara M, Tabira T. Regulation of experimental autoimmune encephalomyelitis by natural killer (NK) cells. J Exp Med. 1997;186(10):1677-1687.
33. Xu W, Fazekas G, Hara H, Tabira T. Mechanism of natural killer (NK) cell regulatory role in experimental autoimmune encephalomyelitis. J Neuroimmunol. 2005;163(1-2):24-30.
34. Yang YG, Dey BR, Sergio JJ, Pearson DA, Sykes M. Donor-derived interferon gamma is required for inhibition of acute graft-versus-host disease by interleukin 12. J Clin Invest. 1998;102(12):2126-2135. (Pubitemid 29018819)
35. Nishimura R, Baker J, Beilhack A, et al. In vivo trafficking and survival of cytokine-induced killer cells resulting in minimal GVHD with retention of antitumor activity. Blood. 2008;112(6):2563-2574.
36. Trivedi PP, Roberts PC, Wolf NA, Swanborg RH. NK cells inhibit T cell proliferation via p21-mediated cell cycle arrest. J Immunol. 2005;174(8):4590-4597. (Pubitemid 40504539)
37. Edinger M, Hoffmann P, Ermann J, et al. CD4+CD25+ regulatory T cells preserve graft-versus-tumor activity while inhibiting graft-versus-host disease after bone marrow transplantation. Nat Med. 2003;9(9):1144-1150.
38. Su HC, Nguyen KB, Salazar-Mather TP, Ruzek MC, Dalod MY, Biron CA. NK cell functions restrain T cell responses during viral infections. Eur J Immunol. 2001;31(10):3048-3055.
39. Regunathan J, Chen Y, Wang D, Malarkannan S. NKG2D receptor-mediated NK cell function is regulated by inhibitory Ly49 receptors. Blood. 2005;105(1):233-240. (Pubitemid 40053088)
40. Ruggeri L, Capanni M, Casucci M, et al. Role of natural killer cell alloreactivity in HLA-mismatched hematopoietic stem cell transplantation. Blood. 1999;94(1):333-339.