IL-4 abrogates TH17 cell-mediated inflammation by selective silencing of IL-23 in antigen-presenting cells

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 7, 2015, Pages 2163-2168

  Guenova, Emmanuella ^a,b,c   Skabytska, Yuliya ^a   Hoetzenecker, Wolfram ^a,b,c   Weindl, Günther ^a,d   Sauer, Karin ^a   Tham, Manuela ^a   Kim, Kyu Won ^e   Park, Ji Hyeon ^e   Seo, Ji Hae ^e,f   Ignatova, Desislava ^c   Cozzio, Antonio ^c   Levesque, Mitchell P ^c   Volz, Thomas ^a,g   Köberle, Martin ^a,g   Kaesler, Susanne ^a   Thomas, Peter ^h   Mailhammer, Reinhard ^g   Ghoreschi, Kamran ^a   Schäkel, Knut ⁱ   Amarov, Boyko ^d   Eichner, Martin ^a   Schaller, Martin ^a   Clark, Rachael A ^b   Röcken, Martin ^a   Biedermann, Tilo ^a,g   more..

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b BRIGHAM AND WOMEN S HOSPITAL   (United States)

^c UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^d FREIE UNIVERSITÄT BERLIN   (Germany)

^e Seoul National University   (South Korea)

^f Seoul National University   (South Korea)

^g TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^h UNIVERSITY OF MUNICH   (Germany)

ⁱ UNIVERSITY HOSPITAL HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; INTERLEUKIN 12; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 4; STAT6 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANTIGEN PRESENTING CELL; ARTICLE; BONE MARROW; CELL POLARITY; CHIMERA; CONTROLLED STUDY; CYTOKINE RELEASE; DELAYED HYPERSENSITIVITY; DENDRITIC CELL; HUMAN; HUMAN CELL; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PSORIASIS; TH17 CELL; GENE SILENCING; GENETICS; IMMUNOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY;

MUS;

ANTIGEN-PRESENTING CELLS; GENE SILENCING; HUMANS; INFLAMMATION; INTERLEUKIN-23; INTERLEUKIN-4; TH17 CELLS;

EID: 84923172388     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1416922112     Document Type: Article

References (51)

1. Zhu J, Yamane H, Paul WE (2010) Differentiation of effector CD4 T cell populations (∗). Annu Rev Immunol 28:445-489.
2. Lebman DA, Coffman RL (1988) Interleukin 4 causes isotype switching to IgE in T cellstimulated clonal B cell cultures. J Exp Med 168(3):853-862.
3. Min B, et al. (2004) Basophils produce IL-4 and accumulate in tissues after infection with a Th2-inducing parasite. J Exp Med 200(4):507-517.
4. Liang HE, et al. (2012) Divergent expression patterns of IL-4 and IL-13 define unique functions in allergic immunity. Nat Immunol 13(1):58-66.
5. Guenova E, et al. (2013) TH2 cytokines from malignant cells suppress TH1 responses and enforce a global TH2 bias in leukemic cutaneous T-cell lymphoma. Clin Cancer Res 19(14):3755-3763.
6. Lee E, et al. (2004) Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med 199(1):125-130.
7. McFarland HF, Martin R (2007) Multiple sclerosis: A complicated picture of autoimmunity. Nat Immunol 8(9):913-919.
8. Nair RP, et al.; Collaborative Association Study of Psoriasis (2009) Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet 41(2): 199-204.
9. Tonel G, et al. (2010) Cutting edge: A critical functional role for IL-23 in psoriasis. J Immunol 185(10):5688-5691.
10. Uhlig HH, et al. (2006) Differential activity of IL-12 and IL-23 in mucosal and systemic innate immune pathology. Immunity 25(2):309-318.
11. Racke MK, et al. (1994) Cytokine-induced immune deviation as a therapy for inflammatory autoimmune disease. J Exp Med 180(5):1961-1966.
12. Sheikh SZ, et al. (2011) An anti-inflammatory role for carbon monoxide and heme oxygenase-1 in chronic Th2-mediated murine colitis. J Immunol 186(9):5506-5513.
13. Mueller R, Krahl T, Sarvetnick N (1996) Pancreatic expression of interleukin-4 abrogates insulitis and autoimmune diabetes in nonobese diabetic (NOD) mice. J Exp Med 184(3):1093-1099.
14. Tarner IH, et al. (2002) Retroviral gene therapy of collagen-induced arthritis by local delivery of IL-4. Clin Immunol 105(3):304-314.
15. Biedermann T, et al. (2001) Reversal of established delayed type hypersensitivity reactions following therapy with IL-4 or antigen-specific Th2 cells. Eur J Immunol 31(5): 1582-1591.
16. Ghoreschi K, et al. (2003) Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease. Nat Med 9(1):40-46.
17. Milner JD, et al. (2010) Sustained IL-4 exposure leads to a novel pathway for hemophagocytosis, inflammation, and tissue macrophage accumulation. Blood 116(14):2476-2483.
18. Tepper RI, et al. (1990) IL-4 induces allergic-like inflammatory disease and alters T cell development in transgenic mice. Cell 62(3):457-467.
19. Biedermann T, et al. (2001) IL-4 instructs TH1 responses and resistance to Leishmania major in susceptible BALB/c mice. Nat Immunol 2(11):1054-1060.
20. Hurdayal R, Brombacher F (2014) The role of IL-4 and IL-13 in cutaneous Leishmaniasis. Immunol Lett 161(2):179-183.
21. Cua DJ, et al. (2003) Interleukin-23 rather than interleukin-12 is the critical cytokine for autoimmune inflammation of the brain. Nature 421(6924):744-748.
22. Murphy CA, et al. (2003) Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198(12):1951-1957.
23. Zhang GX, et al. (2003) Induction of experimental autoimmune encephalomyelitis in IL-12 receptor-beta 2-deficient mice: IL-12 responsiveness is not required in the pathogenesis of inflammatory demyelination in the central nervous system. J Immunol 170(4): 2153-2160.
24. Chen Y, et al. (2006) Anti-IL-23 therapy inhibits multiple inflammatory pathways and ameliorates autoimmune encephalomyelitis. J Clin Invest 116(5):1317-1326.
25. Elder JT (2009) Genome-wide association scan yields new insights into the immunopathogenesis of psoriasis. Genes Immun 10(3):201-209.
26. Braumüller H, et al. (2013) T-helper-1-cell cytokines drive cancer into senescence. Nature 494(7437):361-365.
27. Acosta-Rodriguez EV, et al. (2007) Surface phenotype and antigenic specificity of human interleukin 17-producing T helper memory cells. Nat Immunol 8(6):639-646.
28. Manel N, Unutmaz D, Littman DR (2008) The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat. Nat Immunol 9(6):641-649.
29. Gilchrist M, et al. (2006) Systems biology approaches identify ATF3 as a negative regulator of Toll-like receptor 4. Nature 441(7090):173-178.
30. Hoetzenecker W, et al. (2012) ROS-induced ATF3 causes susceptibility to secondary infections during sepsis-associated immunosuppression. Nat Med 18(1):128-134.
31. Whitmore MM, et al. (2007) Negative regulation of TLR-signaling pathways by activating transcription factor-3. J Immunol 179(6):3622-3630.
32. Hertz AL, et al. (2009) Elevated cyclic AMP and PDE4 inhibition induce chemokine expression in human monocyte-derived macrophages. Proc Natl Acad Sci USA 106(51): 21978-21983.
33. Oliveira CJ, et al. (2011) Deconstructing tick saliva: Non-protein molecules with potent immunomodulatory properties. J Biol Chem 286(13):10960-10969.
34. Wang J, Cao Y, Steiner DF (2003) Regulation of proglucagon transcription by activated transcription factor (ATF) 3 and a novel isoform, ATF3b, through the cAMPresponse element/ATF site of the proglucagon gene promoter. J Biol Chem 278(35): 32899-32904.
35. Perera GK, Di Meglio P, Nestle FO (2012) Psoriasis. Annu Rev Pathol 7:385-422.
36. Lowes MA, et al. (2008) Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 128(5):1207-1211.
37. Gomez MR, et al. (2014) Basophils control T-cell responses and limit disease activity in experimental murine colitis. Mucosal Immunol 7(1):188-199.
38. Coffman RL (2010) The origin of Th2 responses. Science 328(5982):1116-1117.
39. Guenova E, et al. (2008) IL-4-mediated fine tuning of IL-12p70 production by human DC. Eur J Immunol 38(11):3138-3149.
40. Hochrein H, et al. (2000) Interleukin (IL)-4 is a major regulatory cytokine governing bioactive IL-12 production by mouse and human dendritic cells. J Exp Med 192(6): 823-833.
41. Yao Y, Li W, Kaplan MH, Chang CH (2005) Interleukin (IL)-4 inhibits IL-10 to promote IL-12 production by dendritic cells. J Exp Med 201(12):1899-1903.
42. Morita Y, Gupta R, Seidl KM, McDonagh KT, Fox DA (2005) Cytokine production by dendritic cells genetically engineered to express IL-4: Induction of Th2 responses and differential regulation of IL-12 and IL-23 synthesis. J Gene Med 7(7):869-877.
43. Uemura Y, et al. (2009) Cytokine-dependent modification of IL-12p70 and IL-23 balance in dendritic cells by ligand activation of Valpha24 invariant NKT cells. J Immunol 183(1):201-208.
44. Bullens DM, Kasran A, Thielemans K, Bakkus M, Ceuppens JL (2001) CD40L-induced IL-12 production is further enhanced by the Th2 cytokines IL-4 and IL-13. Scand J Immunol 53(5):455-463.
45. Sarkar S, Tesmer LA, Hindnavis V, Endres JL, Fox DA (2007) Interleukin-17 as a molecular target in immune-mediated arthritis: Immunoregulatory properties of genetically modified murine dendritic cells that secrete interleukin-4. Arthritis Rheum 56(1):89-100.
46. Cooney LA, Towery K, Endres J, Fox DA (2011) Sensitivity and resistance to regulation by IL-4 during Th17 maturation. J Immunol 187(9):4440-4450.
47. Ghoreschi K, et al. (2011) Fumarates improve psoriasis and multiple sclerosis by inducing type II dendritic cells. J Exp Med 208(11):2291-2303.
48. Chan JR, et al. (2006) IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med 203(12):2577-2587.
49. Fallon PG, et al. (2002) IL-4 induces characteristic Th2 responses even in the combined absence of IL-5, IL-9, and IL-13. Immunity 17(1):7-17.
50. Krueger GG, et al.; CNTO 1275 Psoriasis Study Group (2007) A human interleukin-12/23 monoclonal antibody for the treatment of psoriasis. N Engl J Med 356(6):580-592.
51. Junttila IS, et al. (2012) Redirecting cell-type specific cytokine responses with engineered interleukin-4 superkines. Nat Chem Biol 8(12):990-998.