Blocking IL-21 signaling ameliorates xenogeneic GVHD induced by human lymphocytes

Blood

Volumn 119, Issue 2, 2012, Pages 619-628

  Hippen, Keli L ^a   Bucher, Christoph ^b   Schirm, Dawn K ^a   Bearl, Amanda M ^a   Brender, Ty ^c   Mink, Kathy A ^c   Waggie, Kimberly S ^c   De Latour, Regis Peffault ^d,e   Janin, Anne ^e   Curtsinger, Julie M ^a   Dillon, Stacey R ^c   Miller, Jeffrey S ^a   Socie, Gerard ^d,e   Blazar, Bruce R ^a  

^a UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^b UNIVERSITY HOSPITAL BASEL   (Switzerland)

^c ZYMOGENETICS INC   (United States)

^d ASSISTANCE PUBLIQUE HÔPITAUX DE PARIS   (France)

^e INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GRANZYME B; INTERLEUKIN 12; INTERLEUKIN 12 ANTIBODY; INTERLEUKIN 17; INTERLEUKIN 21; INTERLEUKIN 4;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CLINICAL ARTICLE; COLON; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; GRAFT VERSUS HOST REACTION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; LYMPHOCYTE; MALE; MORTALITY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY T LYMPHOCYTE; SIGNAL TRANSDUCTION; SKIN; WEIGHT REDUCTION; XENOGRAFT;

EID: 84862909139     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2011-07-368027     Document Type: Article

References (50)

1. Welniak LA, Blazar BR, Murphy WJ. Immunobiology of allogeneic hematopoietic stem cell transplantation. Annu Rev Immunol. 2007;25:139-170. (Pubitemid 46697905)
2. Burman AC, Banovic T, Kuns RD, et al. IFNgamma differentially controls the development of idiopathic pneumonia syndrome and GVHD of the gastrointestinal tract. Blood. 2007;110(3):1064-1072. (Pubitemid 47267449)
3. Nikolic B, Lee S, Bronson RT, Grusby MJ, Sykes M. Th1 and Th2 mediate acute graft-versus-host disease, each with distinct endorgan targets. J Clin Invest. 2000;105(9):1289-1298. (Pubitemid 30266082)
4. Murphy WJ, Welniak LA, Taub DD, et al. Differential effects of the absence of interferon-gamma and IL-4 in acute graft-versus-host disease after allogeneic bone marrow transplantation in mice. J Clin Invest. 1998;102(9):1742-1748. (Pubitemid 28516259)
5. Tawara I, Maeda Y, Sun Y, et al. Combined Th2 cytokine deficiency in donor T cells aggravates experimental acute graft-vs-host disease. Exp Hematol. 2008;36(8):988-996.
6. Fowler DH, Kurasawa K, Husebekk A, Cohen PA, Gress RE. Cells of Th2 cytokine phenotype prevent LPS-induced lethality during murine graft-versus-host reaction: regulation of cytokines and CD8+ lymphoid engraftment. J Immunol. 1994;152(3):1004-1013.
7. Fowler DH, Kurasawa K, Smith R, Eckhaus MA, Gress RE. Donor CD4-enriched cells of Th2 cytokine phenotype regulate graft-versus-host disease without impairing allogeneic engraftment in sublethally irradiated mice. Blood. 1994;84(10):3540-3549. (Pubitemid 24352920)
8. Carlson MJ, West ML, Coghill JM, Panoskaltsis-Mortari A, Blazar BR, Serody JS. In vitro-differentiated TH17 cells mediate lethal acute graft-versus-host disease with severe cutaneous and pulmonary pathologic manifestations. Blood. 2009;113(6):1365-1374.
9. Iclozan C, Yu Y, Liu C, et al. T helper17 cells are sufficient but not necessary to induce acute graft-versus-host disease: biology of blood and marrow transplantation. Transplantation. 2010;16(2):170-178.
10. Kappel LW, Goldberg GL, King CG, et al. IL-17 contributes to CD4-mediated graft-versus-host disease. Blood. 2009;113(4):945-952.
11. Yi T, Chen Y, Wang L, et al. Reciprocal differentiation and tissue-specific pathogenesis of Th1, Th2, and Th17 cells in graft-versus-host disease. Blood. 2009;114(14):3101-3112.
12. Yi T, Zhao D, Lin CL, et al. Absence of donor Th17 leads to augmented Th1 differentiation and exacerbated acute graft-versus-host disease. Blood. 2008;112(5):2101-2110.
13. Coghill JM, Sarantopoulos S, Moran TP, Murphy WJ, Blazar BR, Serody JS. Effector CD4+ T cells, the cytokines they generate, and GVHD: something old and something new. Blood. 2011;117(12):3268-3276.
14. Parrish-Novak J, Dillon SR, Nelson A, et al. Interleukin 21 and its receptor are involved in NK cell expansion and regulation of lymphocyte function. Nature. 2000;408(6808):57-63.
15. Leonard WJ, Zeng R, Spolski R. Interleukin 21: a cytokine/cytokine receptor system that has come of age. J Leukoc Biol. 2008;84(2):348-356.
16. Monteleone G, Pallone F, MacDonald TT. Interleukin-21: a critical regulator of the balance between effector and regulatory T-cell responses. Trends Immunol. 2008;29(6):290-294.
17. Spolski R, Kashyap M, Robinson C, Yu Z, Leonard WJ. IL-21 signaling is critical for the development of type I diabetes in the NOD mouse. Proc Natl Acad Sci U S A. 2008;105(37):14028-14033.
18. Liu R, Bai Y, Vollmer TL, et al. IL-21 receptor expression determines the temporal phases of experimental autoimmune encephalomyelitis. Exp Neurol. 2008;211(1):14-24.
19. Korn T, Bettelli E, Gao W, et al. IL-21 initiates an alternative pathway to induce proinflammatory T(H)17 cells. Nature. 2007;448(7152):484-487. (Pubitemid 47123515)
20. Coquet JM, Chakravarti S, Smyth MJ, Godfrey DI. Cutting edge: IL-21 is not essential for Th17 differentiation or experimental autoimmune encephalomyelitis. J Immunol. 2008;180(11):7097-7101.
21. Sonderegger I, Kisielow J, Meier R, King C, Kopf M. IL-21 and IL-21R are not required for development of Th17 cells and autoimmunity in vivo. Eur J Immunol. 2008;38(7):1833-1838.
22. Bucher C, Koch L, Vogtenhuber C, et al. IL-21 blockade reduces graft-versus-host disease mortality by supporting inducible T regulatory cell generation. Blood. 2009;114(26):5375-5384.
23. Hanash AM, Kappel LW, Yim NL, et al. Abrogation of donor T cell IL-21 signaling leads to tissue-specific modulation of immunity and separation of GVHD from GVL. Blood. 2011;118(2):446-455.
24. Meguro A, Ozaki K, Hatanaka K, et al. Lack of IL-21 signal attenuates graft-versus-leukemia effect in the absence of CD8 T-cells. Bone Marrow Transplant. 2011 Jan 24 [Epub ahead of print].
25. Meguro A, Ozaki K, Oh I, et al. IL-21 is critical for GVHD in a mouse model. Bone Marrow Transplant. 2010;45(4):723-729.
26. Oh I, Ozaki K, Meguro A, et al. Altered effector CD4+ T-cell function in IL-21R-/- CD4+ T cell-mediated graft-versus-host disease. J Immunol. 2010;185(3):1920-1926.
27. Yang L, Anderson DE, Baecher-Allan C, et al. IL-21 and TGF-beta are required for differentiation of human T(H)17 cells. Nature. 2008;454(7202):350- 352.
28. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006;441(7090):235-238.
29. Veldhoen M, Hocking RJ, Atkins CJ, Locksley RM, Stockinger B. TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity. 2006;24(2):179-189. (Pubitemid 43214587)
30. Socie G, Mary JY, Lemann M, et al. Prognostic value of apoptotic cells and infiltrating neutrophils in graft-versus-host disease of the gastrointestinal tract in humans: TNF and Fas expression. Blood. 2004;103(1):50-57. (Pubitemid 38029917)
31. Baker MB, Altman NH, Podack ER, Levy RB. The role of cell-mediated cytotoxicity in acute GVHD after MHC-matched allogeneic bone marrow transplantation in mice. J Exp Med. 1996;183(6):2645-2656. (Pubitemid 26192373)
32. Graubert TA, DiPersio JF, Russell JH, Ley TJ. Perforin/granzyme-dependent and independent mechanisms are both important for the development of graft-versus-host disease after murine bone marrow transplantation. J Clin Invest. 1997;100(4):904-911. (Pubitemid 27371709)
33. Graubert TA, Russell JH, Ley TJ. The role of granzyme B in murine models of acute graft-versus-host disease and graft rejection. Blood. 1996;87(4):1232-1237. (Pubitemid 26060539)
34. Socie G, Blazar BR. Acute graft-versus-host disease: from the bench to the bedside. Blood. 2009;114(20):4327-4336.
35. Ratajczak P, Janin A, Peffault de Latour R, et al. Th17/Treg ratio in human graft-versus-host disease. Blood. 2010;116(7):1165-1171.
36. Glucksberg H, Storb R, Fefer A, et al. Clinical manifestations of graft-versus-host disease in human recipients of marrow from HL-A-matched sibling donors. Transplantation. 1974;18(4):295-304.
37. Afonina IS, Cullen SP, Martin SJ. Cytotoxic and non-cytotoxic roles of the CTL/NK protease granzyme B. Immunol Rev. 2010;235(1):105-116.
38. Broady R, Yu J, Chow V, et al. Cutaneous GVHD is associated with the expansion of tissue-localized Th1 and not Th17 cells. Blood. 2010;116(25):5748-5751.
39. Zanin-Zhorov A, Ding Y, Kumari S, et al. Protein kinase C-theta mediates negative feedback on regulatory T-cell function. Science. 2010;328(5976):372- 376.
40. Hippen KL, Harker-Murray P, Porter SB, et al. Umbilical cord blood regulatory T-cell expansion and functional effects of tumor necrosis factor receptor family members OX40 and 4-1BB expressed on artificial antigen-presenting cells. Blood. 2008;112(7):2847-2857.
41. Hippen KL, Merkel SC, Schirm DK, et al. Generation and large-scale expansion of human inducible regulatory T cells that suppress graft-versus-host disease. Am J Transplant. 2011;11(6):1148-1157.
42. Taylor PA, Panoskaltsis-Mortari A, Swedin JM, et al. L-Selectin(hi) but not the L-selectin(lo) CD49+25+ T-regulatory cells are potent inhibitors of GVHD and BM graft rejection. Blood. 2004;104(12):3804-3812. (Pubitemid 39564461)
43. Hippen KL, Merkel SC, Schirm DK, et al. Massive ex vivo expansion of human natural regulatory T cells (Tregs) with minimal loss of in vivo functional activity. Sci Transl Med. 2011;3(78):78ra33.
44. Taylor PA, Lees CJ, Blazar BR. The infusion of ex vivo activated and expanded CD4(+)CD25(+) immune regulatory cells inhibits graft-versus-host disease lethality. Blood. 2002;99(10):3493-3499. (Pubitemid 34534513)
45. Brunstein CG, Miller JS, Cao Q, et al. Infusion of ex vivo expanded T regulatory cells in adults transplanted with umbilical cord blood: safety profile and detection kinetics. Blood. 2011;117(3):1061-1070.
46. Belkaid Y. Regulatory T cells and infection: a dangerous necessity. Nat Rev Immunol. 2007;7(11):875-888. (Pubitemid 350006238)
47. ZouW. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006;6(4):295-307.
48. Belkaid Y, Rouse BT. Natural regulatory T cells in infectious disease. Nat Immunol. 2005;6(4):353-360. (Pubitemid 41716772)
49. Krenger W, Blazar BR, Hollander GA. Thymic T-cell development in allogeneic stem cell transplantation. Blood. 2011;117(25):6768-6776.
50. Publicover J, Goodsell A, Nishimura S, et al. IL-21 is pivotal in determining age-dependent effectiveness of immune responses in a mouse model of human hepatitis B. J Clin Invest. 2011;121(3):1154-1162.