A single intradermal injection of IFN-γ induces an inflammatory state in both non-lesional psoriatic and healthy skin

Journal of Investigative Dermatology

Volumn 132, Issue 4, 2012, Pages 1177-1187

  Johnson Huang, Leanne M ^a   Suárez Fariñas, Mayte ^a   Pierson, Katherine C ^a   Fuentes Duculan, Judilyn ^a   Cueto, Inna ^a   Lentini, Tim ^a   Sullivan Whalen, Mary ^a   Gilleaudeau, Patricia ^a   Krueger, James G ^a   Haider, Asifa S ^a   Lowes, Michelle A ^a  

^a ROCKEFELLER UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; GAMMA INTERFERON; INTERLEUKIN 23; NITRIC OXIDE SYNTHASE; TUMOR NECROSIS FACTOR;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; GENE EXPRESSION; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; MICROARRAY ANALYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PSORIASIS; SKIN BIOPSY; T LYMPHOCYTE;

EID: 84858283022     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2011.458     Document Type: Article

References (52)

1. Ackermann L, Harvima IT, Pelkonen J et al. (1999) Mast cells in psoriatic skin are strongly positive for interferon-gamma. Br J Dermatol 140: 624-33
2. Aggarwal S, Ghilardi N, Xie MH et al. (2003) Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J Biol Chem 278:1910-4
3. Aloisi F, Pujol-Borrell R (2006) Lymphoid neogenesis in chronic inflammatory diseases. Nat Rev Immunol 6:205-17
4. Annunziato F, Cosmi L, Santarlasci V et al. (2007) Phenotypic and functional features of human Th17 cells. J Exp Med 204:1849-61
5. Austin LM, Ozawa M, Kikuchi T et al. (1999) The majority of epidermal T cells in Psoriasis vulgaris lesions can produce type 1 cytokines, interferon-gamma, interleukin-2, and tumor necrosis factor-Alpha, defining TC1 (cytotoxic T lymphocyte) and TH1 effector populations: A type 1 differentiation bias is also measured in circulating blood T cells in psoriatic patients. J Invest Dermatol 113:752-9
6. Baker BS, Swain AF, Fry L et al. (1984) Epidermal T lymphocytes and HLA-DR expression in psoriasis. Br J Dermatol 110:555-64
7. Banks TA, Rouse BT, Kerley MK et al. (1995) Lymphotoxin-Alpha-deficient mice. Effects on secondary lymphoid organ development and humoral immune responsiveness. J Immunol 155:1685-93
8. Barker JN, Allen MH, MacDonald DM (1989) The effect of in vivo interferongamma on the distribution of LFA-1 and ICAM-1 in normal human skin. J Invest Dermatol 93:439-42
9. Barker JN, Allen MH, MacDonald DM (1990) Alterations induced in normal human skin by in vivo interferon-gamma. Br J Dermatol 122: 451-8
10. Bending D, De La Pena H, Veldhoen M et al. (2009) Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J Clin Invest 119:565-72
11. Bonish B, Jullien D, Dutronc Y et al. (2000) Overexpression of CD1d by keratinocytes in psoriasis and CD1d-dependent IFN-gamma production by NK-T cells. J Immunol 165:4076-85
12. Bos JD, Hulsebosch HJ, Krieg SR et al. (1983) Immunocompetent cells in psoriasis. In situ immunophenotyping by monoclonal antibodies. Arch Dermatol Res 275:181-9
13. Cannon GW, Pincus SH, Emkey RD et al. (1989) Double-blind trial of recombinant gamma-interferon versus placebo in the treatment of rheumatoid arthritis. Arthritis Rheum 32:964-73
14. Chamian F, Lowes MA, Lin SL et al. (2005) Alefacept reduces infiltrating T cells, activated dendritic cells, and inflammatory genes in psoriasis vulgaris. Proc Natl Acad Sci USA 102:2075-80
15. Dardalhon V, Korn T, Kuchroo VK et al. (2008) Role of Th1 and Th17 cells in organ-specific autoimmunity. J Autoimmun 31:252-5
16. De Togni P, Goellner J, Ruddle NH et al. (1994) Abnormal development of peripheral lymphoid organs in mice deficient in lymphotoxin. Science 264:703-7
17. Elder JT (2009) Genome-wide association scan yields new insights into the immunopathogenesis of psoriasis. Genes Immun 10:201-9
18. Ethuin F, Gerard B, Benna JE et al. (2004) Human neutrophils produce interferon gamma upon stimulation by interleukin-12. Lab Invest 84:1363-71
19. Fierlbeck G, Rassner G (1990) Treatment of psoriasis and psoriatic arthritis with interferon gamma. J Invest Dermatol 95:138S-41S
20. Fierlbeck G, Rassner G, Muller C (1990) Psoriasis induced at the injection site of recombinant interferon gamma. Results of immunohistologic investigations. Arch Dermatol 126:351-5
21. Fuentes-Duculan J, Suarez-Farinas M, Zaba LC et al. (2010) A subpopulation of CD163-positive macrophages is classically activated in psoriasis. J Invest Dermatol 130:2412-22
22. Fukuyama S, Nagatake T, Kim DY et al. (2006) Cutting edge: Uniqueness of lymphoid chemokine requirement for the initiation and maturation of nasopharynx-Associated lymphoid tissue organogenesis. J Immunol 177:4276-80
23. Futterer A, Mink K, Luz A et al. (1998) The lymphotoxin beta receptor controls organogenesis and affinity maturation in peripheral lymphoid tissues. Immunity 9:59-70
24. Gudjonsson JE, Ding J, Li X et al. (2009) Global gene expression analysis reveals evidence for decreased lipid biosynthesis and increased innate immunity in uninvolved psoriatic skin. J Invest Dermatol 129:2795-804
25. Guttman-Yassky E, Lowes MA, Fuentes-Duculan J et al. (2008) Low expression of the IL-23/Th17 pathway in atopic dermatitis compared to psoriasis. J Immunol 181:7420-7
26. Harrington LE, Hatton RD, Mangan PR et al. (2005) Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nat Immunol 6:1123-32
27. Hsu HC, Yang P, Wang J et al. (2008) Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice. Nat Immunol 9:166-75
28. Johnson-Huang LM, Suarez-Farinas M, Sullivan-Whalen M et al. (2010) Effective narrow-band UVB radiation therapy suppresses the IL-23/IL-17 axis in normalized psoriasis plaques. J Invest Dermatol 130:2654-63
29. Krueger JG (2002) The immunologic basis for the treatment of psoriasis with new biologic agents. J Am Acad Dermatol 46:1-23; quiz -5
30. Kryczek I, Bruce AT, Gudjonsson JE et al. (2008) Induction of IL-17+ T cell trafficking and development by IFN-gamma: Mechanism and pathological relevance in psoriasis. J Immunol 181:4733-41
31. Langrish CL, Chen Y, Blumenschein WM et al. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J Exp Med 201:233-40
32. Lebwohl M (2003) Psoriasis. Lancet 361:1197-204
33. Lew W, Bowcock AM, Krueger JG (2004) Psoriasis vulgaris: Cutaneous lymphoid tissue supports T-cell activation and 'Type 10 inflammatory gene expression. Trends Immunol 25:295-305
34. Lowes M, Bowcock AM, Krueger J (2007) Pathogenesis and therapy of psoriasis. Nature 445:866-73
35. Lowes MA, Chamian F, Abello MV et al. (2005) Increase in TNF-Alpha and inducible nitric oxide synthase-expressing dendritic cells in psoriasis and reduction with efalizumab (anti-CD11a). Proc Natl Acad Sci USA 102:19057-62
36. Lowes MA, Kikuchi T, Fuentes-Duculan J et al. (2008) Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol 128:1207-11
37. Martin-Orozco N, Chung Y, Chang SH et al. (2009) Th17 cells promote pancreatic inflammation but only induce diabetes efficiently in lymphopenic hosts after conversion into Th1 cells. Eur J Immunol 39:216-24
38. Morhenn VB, Pregerson-Rodan K, Mullen RH et al. (1987) Use of recombinant interferon gamma administered intramuscularly for the treatment of psoriasis. Arch Dermatol 123:1633-7
39. Murphy CA, Langrish CL, Chen Y et al. (2003) Divergent pro- and antiinflammatory roles for IL-23 and IL-12 in joint autoimmune inflammation. J Exp Med 198:1951-7
40. Nathan C, Squires K, Griffo W et al. (1990) Widespread intradermal accumulation of mononuclear leukocytes in lepromatous leprosy patients treated systemically with recombinant interferon gamma. J Exp Med 172:1509-12
41. Nathan CF, Kaplan G, Levis WR et al. (1986) Local and systemic effects of intradermal recombinant interferon-gamma in patients with lepromatous leprosy. N Engl J Med 315:6-15
42. Nograles KE, Davidovici B, Krueger JG (2010) New insights in the immunologic basis of psoriasis. Semin Cutan Med Surg 29:3-9
43. Park H, Li Z, Yang XO et al. (2005) A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 6:1133-41
44. Placek W, Haftek M, Thivolet J (1988) Sequence of changes in psoriatic epidermis. Immunocompetent cell redistribution precedes altered expression of keratinocyte differentiation markers. Acta Derm Venereol 68:369-77
45. Suarez-Farinas M, Lowes MA, Zaba LC et al. (2010) Evaluation of the psoriasis transcriptome across different studies by gene set enrichment analysis (GSEA). PLoS One 5:e10247
46. Uyemura K, Yamamura M, Fivenson DF et al. (1993) The cytokine network in lesional and lesion-free psoriatic skin is characterized by a T-helper type 1 cell-mediated response. J Invest Dermatol 101:701-5
47. Veys EM, Menkes CJ, Emery P (1997) A randomized, double-blind study comparing twenty-four-week treatment with recombinant interferongamma versus placebo in the treatment of rheumatoid arthritis. Arthritis Rheum 40:62-8
48. Wei L, Debets R, Hegmans JJ et al. (1999) IL-1 beta and IFN-gamma induce the regenerative epidermal phenotype of psoriasis in the transwell skin organ culture system. IFN-gamma up-regulates the expression of keratin 17 and keratinocyte transglutaminase via endogenous IL-1 production. J Pathol 187:358-64
49. Zaba L, Cardinale I, Gilleaudeau P et al. (2007) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J Exp Med 204:3183-94
50. Zaba LC, Fuentes-Duculan J, Eungdamrong NJ et al. (2009a) Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J Invest Dermatol 129:79-88
51. Zaba LC, Fuentes-Duculan J, Eungdamrong NJ et al. (2010) Identification of TNF-related apoptosis-inducing ligand and other molecules that distinguish inflammatory from resident dendritic cells in patients with psoriasis. J Allergy Clin Immunol 125:1261-8 e9
52. Zaba LC, Suarez-Farinas M, Fuentes-Duculan J et al. (2009b) Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J Allergy Clin Immunol 124:1022-10 e1-395