Noncanonical NF-κB signaling in dendritic cells is required for indoleamine 2,3-dioxygenase (IDO) induction and immune regulation

Blood

Volumn 110, Issue 5, 2007, Pages 1540-1549

  Tas, Sander W ^a   Vervoordeldonk, Margriet J ^a   Hajji, Najat ^a   Schuitemaker, Joost H N ^a   Van Der Sluijs, Koen F ^a   May, Michael J ^b   Ghosh, Sankar ^c   Kapsenberg, Martien L ^a   Tak, Paul P ^a   De Jong, Esther C ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF PENNSYLVANIA SCHOOL OF VETERINARY MEDICINE   (United States)

^c YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD40 LIGAND; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDOLEAMINE; INDOLEAMINE 2,3 DIOXYGENASE; SMALL INTERFERING RNA; CYTOKINE; I KAPPA B KINASE; IKBKG PROTEIN, HUMAN; PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOKINE PRODUCTION; DENDRITIC CELL; DOWN REGULATION; ENZYME INDUCTION; ENZYME INHIBITION; HUMAN; HUMAN CELL; IMMUNITY; IMMUNOFLUORESCENCE; IMMUNOREGULATION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; T LYMPHOCYTE ACTIVATION; WESTERN BLOTTING; ANIMAL; BIOSYNTHESIS; CELL CULTURE; DRUG ANTAGONISM; DRUG EFFECT; ENZYMOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; INFLAMMATION; LYMPHOCYTE ACTIVATION; METABOLISM; MOUSE; T LYMPHOCYTE;

ANIMALS; CELLS, CULTURED; CYTOKINES; DENDRITIC CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; I-KAPPA B KINASE; INDOLEAMINE-PYRROLE 2,3,-DIOXYGENASE; INFLAMMATION; LYMPHOCYTE ACTIVATION; MICE; NF-KAPPA B; PEPTIDES; PROTEIN BINDING; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; T-LYMPHOCYTES;

EID: 34548863106     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-11-056010     Document Type: Article

References (57)

1. Steinman RM, Hawiger D, Liu K, et al. Dendritic cell function in vivo during the steady state: a role in peripheral tolerance. Ann N Y Acad Sci. 2003;987:15-25.
2. Mellor AL, Munn DH. IDO expression by dendritic cells: tolerance and tryptophan catabolism. Nat Rev Immunol. 2004;4:762-774.
3. Hwu P, Du MX, Lapointe R, et al. Indoleamine 2,3-dioxygenase production by human dendritic cells results in the inhibition of T cell proliferation. J Immunol. 2000;164:3596-3599.
4. Mellor AL, Baban B, Chandler P, et al. Cutting edge: induced indoleamine 2,3 dioxygenase expression in dendritic cell subsets suppresses T cell clonal expansion. J Immunol. 2003;171:1652-1655.
5. Mellor AL, Keskin DB, Johnson T, Chandler P, Munn DH. Cells expressing indoleamine 2,3-dioxygenase inhibit T cell responses. J Immunol. 2002;168:3771-3776.
6. Fallarino F, Grohmann U, Vacca C, et al. T cell apoptosis by tryptophan catabolism. Cell Death Differ. 2002;9:1069-1077.
7. Munn DH, Zhou M, Attwood JT, et al. Prevention of allogeneic fetal rejection by tryptophan catabolism. Science. 1998;281:1191-1193.
8. Mellor AL, Sivakumar J, Chandler P, et al. Prevention of T cell-driven complement activation and inflammation by tryptophan catabolism during pregnancy. Nat Immunol. 2001;2:64-68.
9. Hwang SL, Chung NP, Chan JK, Lin CL. Indoleamine 2, 3-dioxygenase (IDO) is essential for dendritic cell activation and chemotactic responsiveness to chemokines. Cell Res. 2005;15:167-175.
10. Munn DH, Sharma MD, Lee JR, et al. Potential regulatory function of human dendritic cells expressing indoleamine 2,3-dioxygenase. Science. 2002;297:1867-1870.
11. Fallarino F, Grohmann U, Hwang KW, et al. Modulation of tryptophan catabolism by regulatory T cells. Nat Immunol. 2003;4:1206-1212.
12. Munn DH, Sharma MD, Mellor AL. Ligation of B7-1/B7-2 by human CD4+ T cells triggers indoleamine 2,3-dioxygenase activity in dendritic cells. J Immunol. 2004;172:4100-4110.
13. Braun D, Longman RS, Albert ML. A two-step induction of indoleamine 2,3 dioxygenase (IDO) activity during dendritic-cell maturation. Blood. 2005;106:2375-2381.
14. Ouaaz F, Arron J, Zheng Y, Choi Y, Beg AA. Dendritic cell development and survival require distinct NF-kappaB subunits. Immunity. 2002;16:257-270.
15. Du MX, Sotero-Esteva WD, Taylor MW. Analysis of transcription factors regulating induction of indoleamine 2,3-dioxygenase by IFN-gamma. J Interferon Cytokine Res. 2000;20:133-142.
16. Li ZW, Chu W, Hu Y, et al. The IKKbeta subunit of IkappaB kinase (IKK) is essential for nuclear factor kappaB activation and prevention of apoptosis. J Exp Med. 1999;189:1839-1845.
17. Senftleben U, Li ZW, Baud V, Karin M. IKKbeta is essential for protecting T cells from TNFalpha-induced apoptosis. Immunity. 2001;14:217-230.
18. Li Q, Van Antwerp D, Mercurio F, Lee KF, Verma IM. Severe liver degeneration in mice lacking the IkappaB kinase 2 gene. Science. 1999;284:321-325.
19. Delhase M, Hayakawa M, Chen Y, Karin M. Positive and negative regulation of IkappaB kinase activity through IKKbeta subunit phosphorylation. Science. 1999;284:309-313.
20. Chu WM, Ostertag D, Li ZW, et al. JNK2 and IKKbeta are required for activating the innate response to viral infection. Immunity. 1999;11:721-731.
21. Hu Y, Baud V, Delhase M, et al. Abnormal morphogenesis but intact IKK activation in mice lacking the IKKalpha subunit of IkappaB kinase. Science. 1999;284:316-320.
22. Senftleben U, Cao Y, Xiao G, et al. Activation by IKKalpha of a second, evolutionary conserved, NF-kappa B signaling pathway. Science. 2001;293:1495-1499.
23. Dejardin E, Droin NM, Delhase M, et al. The lymphotoxin-beta receptor induces different patterns of gene expression via two NF-kappaB pathways. Immunity. 2002;17:525-535.
24. Hayden MS, Ghosh S. Signaling to NF-kappaB. Genes Dev. 2004;18:2195-2224.
25. Bonizzi G, Karin M. The two NF-kappaB activation pathways and their role in innate and adaptive immunity. Trends Immunol. 2004;25:280-288.
26. Lawrence T, Bebien M, Liu GY, Nizet V, Karin M. IKKalpha limits macrophage NF-kappaB activation and contributes to the resolution of inflammation. Nature. 2005;434:1138-1143.
27. Li Q, Lu Q, Bottero V, et al. Enhanced NF-{kappa}B activation and cellular function in macrophages lacking I{kappa}B kinase 1 (IKK1). Proc Natl Acad Sci U S A. 2005;102:12425-12430.
28. 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 glucocorticoid-induced TNF receptor family-related gene stimulation. J Immunol. 2005;175:1651-1657.
29. Kinoshita D, Hirota F, Kaisho T, et al. Essential role of IkappaB kinase alpha in thymic organo-genesis required for the establishment of selftolerance. J Immunol. 2006;176:3995-4002.
30. Fallarino F, Grohmann U, You S, et al. The combined effects of tryptophan starvation and tryptophan catabolites down-regulate T cell receptor {zeta}-chain and induce a regulatory phenotype in naive T cells. J Immunol. 2006;176:6752-6761.
31. May MJ, D'Acquisto F, Madge LA, et al. Selective inhibition of NF-kappaB activation by a peptide that blocks the interaction of NEMO with the IkappaB kinase complex. Science. 2000;289:1550-1554.
32. Vieira PL, Kalinski P, Wierenga EA, Kapsenberg ML, de Jong EC. Glucocorticoids inhibit bioactive IL-12p70 production by in vitro-generated human dendritic cells without affecting their T cell stimulatory potential. J Immunol. 1998;161:5245-5251.
33. Tas SW, de Jong EC, Hajji N, et al. Selective inhibition of NF-kappaB in dendritic cells by the NEMO-binding domain peptide blocks maturation and prevents T cell proliferation and polarization. Eur J Immunol. 2005;35:1164-1174.
34. Feng GS, Taylor MW. Interferon gamma-resistant mutants are defective in the induction of indoleamine 2,3-dioxygenase. Proc Natl Acad Sci U S A. 1989;86:7144-7148.
35. Terness P, Bauer TM, Rose L, et al. Inhibition of allogeneic T cell proliferation by indoleamine 2,3-dioxygenase-expressing dendritic cells: mediation of suppression by tryptophan metabolites. J Exp Med. 2002;196:447-457.
36. Karin M, Yamamoto Y, Wang QM. The IKK NF-kappa B system: a treasure trove for drug development. Nat Rev Drug Discov. 2004;3:17-26.
37. Kalinski P, Schuitemaker JH, Hilkens CM, Kapsenberg ML. Prostaglandin E2 induces the final maturation of IL-12-deficient CD1a+CD83+ dendritic cells: the levels of IL-12 are determined during the final dendritic cell maturation and are resistant to further modulation. J Immunol. 1998;161:2804-2809.
38. Smits HH, Engering A, Van der KD, et al. Selective probiotic bacteria induce IL-10-producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell-specific intercellular adhesion molecule 3-grabbing nonintegrin. J Allergy Clin Immunol. 2005;115:1260-1267.
39. Munn DH, Shafizadeh E, Attwood JT, et al. Inhibition of T cell proliferation by macrophage tryptophan catabolism. J Exp Med. 1999;189:1363-1372.
40. Munn DH, Mellor AL, Rossi M, Young JW. Dendritic cells have the option to express IDO-mediated suppression or not. Blood. 2005;105:2618.
41. Fehervari Z, Sakaguchi S. CD4+ Tregs and immune control. J Clin Invest. 2004;114:1209-1217.
42. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol. 2005;6:338-344.
43. Vacca C, Fallarino F, Perruccio K, et al. CD40 ligation prevents onset of tolerogenic properties in human dendritic cells treated with CTLA-4-Ig. Microbes Infect. 2005;7:1040-1048.
44. Trinchieri G. Interleukin-12 and the regulation of innate resistance and adaptive immunity. Nat Rev Immunol. 2003;3:133-146.
45. Agaugue S, Perrin-Cocon L, Coutant F, Andre P, Lotteau V. 1-Methyl-tryptophan can interfere with TLR signaling in dendritic cells independently of IDO activity. J Immunol. 2006;177:2061-2071.
46. Kelsen J, Agnholt J, Hoffmann HJ, et al. FoxP3CD4CD25 T cells with regulatory properties can be cultured from colonic mucosa of patients with Crohn's disease. Clin Exp Immunol. 2005;141:549-557.
47. Maerten P, Shen C, Bullens DM, et al. Effects of interleukin 4 on CD25(+)CD4(+) regulatory T cell function. J Autoimmun. 2005;25:112-120.
48. Tan PH, Sagoo P, Chan C, et al. Inhibition of NF-kappaB and oxidative pathways in human dendritic cells by antioxidative vitamins generates regulatory T cells. J Immunol. 2005;174:7633-7644.
49. Davies JD, Martin G, Phillips J, et al. T cell regulation in adult transplantation tolerance. J Immunol. 1996;157:529-533.
50. Akbari O, Freeman GJ, Meyer EH, et al. Antigenspecific regulatory T cells develop via the ICOSICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med. 2002;8:1024-1032.
51. Vasu C, Prabhakar BS, Holterman MJ. Targeted CTLA-4 engagement induces CD4+CD25+CTLA-4high T regulatory cells with target (allo)antigen specificity. J Immunol. 2004;173:2866-2876.
52. Wildbaum G, Netzer N, Karin N. Tr1 cell-dependent active tolerance blunts the pathogenic effects of determinant spreading. J Clin Invest. 2002;110:701-710.
53. Watanabe T, Yoshida M, Shirai Y, et al. Administration of an antigen at a high dose generates regulatory CD4+ T cells expressing CD95 ligand and secreting IL-4 in the liver. J Immunol. 2002;168:2188-2199.
54. Seddon B, Mason D. Regulatory T cells in the control of autoimmunity: the essential role of transforming growth factor beta and interleukin 4 in the prevention of autoimmune thyroiditis in rats by peripheral CD4(+)CD. J Exp Med. 1999;189:279-288.
55. Orabona C, Grohmann U, Belladonna ML, et al. CD28 induces immunostimulatory signals in dendritic cells via CD80 and CD86. Nat Immunol. 2004;5:1134-1142.
56. Yang J, Bernier SM, Ichim TE, et al. LF15-0195 generates tolerogenic dendritic cells by suppression of NF-kappaB signaling through inhibition of IKK activity. J Leukoc Biol. 2003;74:438-447.
57. Tomasoni S, Aiello S, Cassis L, et al. Dendritic cells genetically engineered with adenoviral vector encoding dnIKK2 induce the formation of potent CD4+ T-regulatory cells. Transplantation. 2005;79:1056-1061.