NF-κB-inducing kinase plays an essential T cell-intrinsic role in graft-versus-host disease and lethal autoimmunity in mice

Journal of Clinical Investigation

Volumn 121, Issue 12, 2011, Pages 4775-4786

  Murray, Susan E ^a   Polesso, Fanny ^a   Rowe, Alexander M ^a,c   Basak, Soumen ^b,d   Koguchi, Yoshinobu ^a   Toren, Katelynne Gardner ^a   Hoffmann, Alexander ^b   Parker, David C ^a  

^a OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF PITTSBURGH MEDICAL CENTER   (United States)

^d NATIONAL INSTITUTE OF IMMUNOLOGY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

CD134 ANTIGEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; LYMPHOCYTE ANTIGEN RECEPTOR; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; NF KAPPA B INDUCING KINASE; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOIMMUNITY; CELL TRANSFER; CONTROLLED STUDY; EFFECTOR CELL; GENE OVEREXPRESSION; GRAFT RECIPIENT; GRAFT VERSUS HOST REACTION; HLA MATCHING; IMMUNE RESPONSE; MOUSE; NONHUMAN; PRIORITY JOURNAL; T LYMPHOCYTE;

ADOPTIVE TRANSFER; ANIMALS; AUTOIMMUNE DISEASES; AUTOIMMUNITY; CD4-POSITIVE T-LYMPHOCYTES; FEMALE; GRAFT VS HOST DISEASE; ISOANTIGENS; MALE; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NF-KAPPA B; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RADIATION CHIMERA; RECEPTORS, ANTIGEN, T-CELL; RECEPTORS, OX40; SIGNAL TRANSDUCTION; T-LYMPHOCYTES; T-LYMPHOCYTES, REGULATORY;

EID: 84055193888     PISSN: 00219738     EISSN: 15588238     Source Type: Journal    
DOI: 10.1172/JCI44943     Document Type: Article

References (56)

1. Kearney ER, Pape KA, Loh DY, Jenkins MK. Visualization of peptide-specific T-cell immunity and peripheral tolerance in vivo. Immunity. 1994;1(4):327-339.
2. Watts T. TNF/TNFR family members in costimulation of T cell responses. Annu Rev Immunol. 2005; 23:23-68. (Pubitemid 40563164)
3. Croft M. Control of immunity by the TNFR-related molecule OX40 (CD134). Annu Rev Immunol. 2010;28:57-78.
4. Beinke S, Ley SC. Functions of NF-kappaB1 and NF-kappaB2 in immune cell biology. Biochem J. 2004;382(pt 2):393-409. (Pubitemid 39243905)
5. Shinkura R, et al. Alymphoplasia is caused by a point mutation in the mouse gene encoding Nf-kappa binducing kinase. Nat Genet. 1999;22(1):74-77. (Pubitemid 29214808)
6. Miyawaki S, et al. A new mutation, aly, that induces a generalized lack of lymph nodes accompanied by immunodeficiency in mice. Eur J Immunol. 1994; 24(2):429-434. (Pubitemid 24041135)
7. Akiyama T, et al. The tumor necrosis factor family receptors RANK and CD40 cooperatively establish the thymic medullary microenvironment and selftolerance. Immunity. 2008;29(3):423-437.
8. Claudio E, Brown K, Park S, Wang H, Siebenlist U. BAFF-induced NEMO-independent processing of NF-kappa B2 in maturing B cells. Nat Immunol. 2002;3(10):958-965. (Pubitemid 35154010)
9. Yin L, et al. Defective lymphotoxin-beta receptorinduced NF-kappaB transcriptional activity in NIKdeficient mice. Science. 2001;291(5511):2162- 2165. (Pubitemid 32224449)
10. Lind EF, et al. Dendritic cells require the NF-kappaB2 pathway for cross-presentation of soluble antigens. J Immunol. 2008;181(1):354-363.
11. Coope HJ, et al. CD40 regulates the processing of NF-kappaB2 p100 to p52. Embo J. 2002; 21(20):5375-5385. (Pubitemid 35231017)
12. Tsubata R, et al. Autoimmune disease of exocrine organs in immunodeficient alymphoplasia mice: a spontaneous model for Sjogren's syndrome. Eur J Immunol. 1996;26(11):2742-2748. (Pubitemid 26364854)
13. Kajiura F, et al. NF-kappa B-inducing kinase establishes self-tolerance in a thymic stroma-dependent manner. J Immunol. 2004;172(4):2067-2075. (Pubitemid 38182352)
14. Lakkis FG, Arakelov A, Konieczny BT, Inoue Y. Immunologic 'ignorance' of vascularized organ transplants in the absence of secondary lymphoid tissue. Nat Med. 2000;6(6):686-688. (Pubitemid 30398793)
15. Matsumoto M, et al. Essential role of NF-kappa Binducing kinase in T cell activation through the TCR/ CD3 pathway. J Immunol. 2002;169(3):1151-1158. (Pubitemid 34809154)
16. Ishimaru N, Kishimoto H, Hayashi Y, Sprent J. Regulation of naive T cell function by the NF-kappaB2 pathway. Nat Immunol. 2006;7(7):763-772. (Pubitemid 43905876)
17. Aya K, Alhawagri M, Hagen-Stapleton A, Kitaura H, Kanagawa O, Novack DV. NF-(kappa)B-inducing kinase controls lymphocyte and osteoclast activities in inflammatory arthritis. J Clin Invest. 2005; 115(7):1848-1854. (Pubitemid 40979723)
18. Hofmann J, Mair F, Greter M, Schmidt-Supprian M, Becher B. NIK signaling in dendritic cells but not in T cells is required for the development of effector T cells and cell-mediated immune responses. J Exp Med. 2011;208(9):1917-1929.
19. Jin W, Zhou XF, Yu J, Cheng X, Sun SC. Regulation of Th17 cell differentiation and EAE induction by MAP3K NIK. Blood. 2009;113(26):6603-6610.
20. Zarnegar BJ, et al. Noncanonical NF-kappaB activation requires coordinated assembly of a regulatory complex of the adaptors cIAP1, cIAP2, TRAF2 and TRAF3 and the kinase NIK. Nat Immunol. 2008; 9(12):1371-1378.
21. Vallabhapurapu S, et al. Nonredundant and complementary functions of TRAF2 and TRAF3 in a ubiquitination cascade that activates NIK-dependent alternative NF-kappaB signaling. Nat Immunol. 2008;9(12):1364-1370.
22. Socie G, Blazar BR. Acute graft-versus-host disease: from the bench to the bedside. Blood. 2009; 114(20):4327-4336.
23. Blazar BR, et al. Ligation of OX40 (CD134) regulates graft-versus-host disease (GVHD) and graft rejection in allogenic bone marrow transplant (BMT) recipients. Blood. 2003;101(9):3741-3748. (Pubitemid 36857967)
24. Huddleston CA, Weinberg AD, Parker DC. OX40 (CD134) engagement drives differentiation of CD4+ T cells to effector cells. Eur J Immunol. 2006; 36(5):1093-1103.
25. Piconese S, Valzasina B, Colombo MP. OX40 triggering blocks suppression by regulatory T cells and facilitates tumor rejection. J Exp Med. 2008; 205(4):825-839. (Pubitemid 351549881)
26. Valzasina B, Guiducci C, Dislich H, Killeen N, Weinberg AD, Colombo MP. Triggering of OX40 (CD134) on CD4(+)CD25+ T cells blocks their inhibitory activity: a novel regulatory role for OX40 and its comparison with GITR. Blood. 2005;105(7):2845-2851. (Pubitemid 40446278)
27. Vu MD, et al. OX40 costimulation turns off Foxp3+ Tregs. Blood. 2007;110(7):2501-2510. (Pubitemid 47523172)
28. Song J, So T, Croft M. Activation of NF-kappaB1 by OX40 contributes to antigen-driven T cell expansion and survival. J Immunol. 2008;180(11):7240-7248.
29. Sasaki Y, et al. NIK overexpression amplifies, whereas ablation of its TRAF3-binding domain replaces BAFF:BAFF-R-mediated survival signals in B cells. Proc Natl Acad Sci U S A. 2008;105(31):10883-10888.
30. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4(+)CD25(+) regulatory T cells. Nat Immunol. 2003;4(4):330-336. (Pubitemid 36432314)
31. Liu T, Soong L, Liu G, Konig R, Chopra AK. CD44 expression positively correlates with Foxp3 expression and suppressive function of CD4+ Treg cells. Biol Direct. 2009;4:40.
32. Komatsu N, Hori S. Full restoration of peripheral Foxp3+ regulatory T cell pool by radioresistant host cells in scurfy bone marrow chimeras. Proc Natl Acad Sci U S A. 2007;104(21):8959-8964. (Pubitemid 47175419)
33. Hauer J, et al. TNF receptor (TNFR)-associated factor (TRAF) 3 serves as an inhibitor of TRAF2/5- mediated activation of the noncanonical NF-kappaB pathway by TRAF-binding TNFRs. Proc Natl Acad Sci U S A. 2005;102(8):2874-2879. (Pubitemid 40299884)
34. Takaori-Kondo A, Hori T, Fukunaga K, Morita R, Kawamata S, Uchiyama T. Both amino- and carboxyl- terminal domains of TRAF3 negatively regulate NF-kappaB activation induced by OX40 signaling. Biochem Biophys Res Commun. 2000;272(3):856-863. (Pubitemid 30420726)
35. Rauert H, et al. Membrane tumor necrosis factor (TNF) induces p100 processing via TNF receptor-2 (TNFR2). J Biol Chem. 2010;285(10):7394-7404.
36. Dejardin E, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity. 2002;17(4):525.
37. Basak S, et al. A fourth IkappaB protein within the NF-kappaB signaling module. Cell. 2007; 128(2):369-381. (Pubitemid 46123518)
38. Legarda-Addison D, Ting AT. Negative regulation of TCR signaling by NF-kappaB2/p100. J Immunol. 2007;178(12):7767-7778. (Pubitemid 46898048)
39. Wang Z, Zhang B, Yang L, Ding J, Ding HF. Constitutive production of NF-kappaB2 p52 is not tumorigenic but predisposes mice to inflammatory autoimmune disease by repressing Bim expression. J Biol Chem. 2008;283(16):10698-10706.
40. Ishikawa H, Carrasco D, Claudio E, Ryseck RP, Bravo R. Gastric hyperplasia and increased proliferative responses of lymphocytes in mice lacking the COOH-terminal ankyrin domain of NF-kappaB2. J Exp Med. 1997;186(7):999- 1014. (Pubitemid 27441145)
41. Yang L, et al. Loss of negative feedback control of nuclear factor-kappaB2 activity in lymphocytes leads to fatal lung inflammation. Am J Pathol. 2010; 176(6):2646-2657.
42. Murata K, Nose M, Ndhlovu LC, Sato T, Sugamura K, Ishii N. Constitutive OX40/OX40 ligand interaction induces autoimmune-like diseases. J Immunol. 2002;169(8):4628-4636. (Pubitemid 35178243)
43. Griseri T, Asquith M, Thompson C, Powrie F. OX40 is required for regulatory T cell-mediated control of colitis. J Exp Med. 2010;207(4):699-709.
44. Ruby CE, et al. Cutting Edge: OX40 agonists can drive regulatory T cell expansion if the cytokine milieu is right. J Immunol. 2009;183(8):4853-4857.
45. Ji HB, et al. Cutting edge: the natural ligand for glucocorticoid- induced TNF receptor-related protein abrogates regulatory T cell suppression. J Immunol. 2004;172(10):5823-5827.
46. Nagar M, et al. TNF activates a NF-kappaB-regulated cellular program in human CD45RA- regulatory T cells that modulates their suppressive function. J Immunol. 2010;184(7):3570-3581.
47. Lu LF, Gondek DC, Scott ZA, Noelle RJ. NF kappa B-inducing kinase deficiency results in the development of a subset of regulatory T cells, which shows a hyperproliferative activity upon glucocorticoidinduced TNF receptor family-related gene stimulation. J Immunol. 2005;175(3):1651-1657. (Pubitemid 41023068)
48. Liston A, Lu LF, O'Carroll D, Tarakhovsky A, Rudensky AY. Dicer-dependent microRNA pathway safeguards regulatory T cell function. J Exp Med. 2008;205(9):1993-2004.
49. MacDonald KP, et al. Effector and regulatory T-cell function is differentially regulated by RelB within antigen-presenting cells during GVHD. Blood. 2007; 109(11):5049-5057. (Pubitemid 46827805)
50. Andreakos E, Williams RO, Wales J, Foxwell BM, Feldmann M. Activation of NF-kappaB by the intracellular expression of NF-kappaB-inducing kinase acts as a powerful vaccine adjuvant. Proc Natl Acad Sci U S A. 2006;103(39):14459-14464. (Pubitemid 44484772)
51. Gardam S, Beyaert R. The kinase NIK as a therapeutic target in multiple myeloma. Expert Opin Ther Targets. 2011;15(2):207-218.
52. Sun SC. Non-canonical NF-kappaB signaling pathway. Cell Res. 2011;21(1):71-85.
53. Lee PP, et al. A critical role for dnmt1 and DNA methylation in T cell development, function, and survival. Immunity. 2001;15(5):763-774. (Pubitemid 34008504)
54. Lathrop SK, Huddleston CA, Dullforce PA, Montfort MJ, Weinberg AD, Parker DC. A signal through OX40 (CD134) allows anergic, autoreactive T cells to acquire effector cell functions. J Immunol. 2004; 172(11):6735-6743. (Pubitemid 38669110)
55. Karasuyama H, Melchers F. Establishment of mouse cell lines which constitutively secrete large quantities of interleukin 2, 3, 4 or 5, using modified cDNA expression vectors. Eur J Immunol. 1988;18(1):97-104. (Pubitemid 18072702)
56. Peitz M, Pfannkuche K, Rajewsky K, Edenhofer F. Ability of the hydrophobic FGF and basic TAT peptides to promote cellular uptake of recombinant Cre recombinase: a tool for efficient genetic engineering of mammalian genomes. Proc Natl Acad Sci U S A. 2002;99(7):4489-4494. (Pubitemid 34286012)