Susceptibility-associated genetic variation at IL12B enhances Th1 polarization in psoriasis

Human Molecular Genetics

Volumn 22, Issue 9, 2013, Pages 1807-1815

  Johnston, Andrew ^a   Xing, Xianying ^a   Swindell, William R ^a   Kochkodan, James ^a   Riblett, MaryBeth ^a   Nair, Rajan P ^a   Stuart, Philip E ^a   Ding, Jun ^b   Voorhees, John J ^a   Elder, James T ^a,c   Gudjonsson, Johann E ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

^b UNIVERSITY OF MICHIGAN SCHOOL OF PUBLIC HEALTH   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; GAMMA INTERFERON INDUCIBLE PROTEIN 10; INTERLEUKIN 12; INTERLEUKIN 12P40; INTERLEUKIN 12P70; INTERLEUKIN 17; INTERLEUKIN 22; INTERLEUKIN 23;

ARTICLE; CELL POLARITY; CONTROLLED STUDY; GENE EXPRESSION; GENETIC RISK; GENETIC VARIABILITY; HAPLOTYPE; HETEROZYGOTE; HUMAN; KERATINOCYTE; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECRETION; PSORIASIS; TH1 CELL; UPREGULATION;

ALLELES; CASE-CONTROL STUDIES; CELL LINE; CHEMOKINE CXCL10; GENETIC LOCI; GENETIC PREDISPOSITION TO DISEASE; GENETIC VARIATION; HAPLOTYPES; HUMANS; INTERFERON-GAMMA; INTERLEUKIN-12 SUBUNIT P40; INTERLEUKIN-17; INTERLEUKIN-23; KERATINOCYTES; MONOCYTES; PSORIASIS; RISK FACTORS; RNA, MESSENGER; TH1 CELLS; TH17 CELLS; UP-REGULATION;

EID: 84875915049     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddt034     Document Type: Article

References (49)

1. Gudjonsson, J.E. and Elder, J.T. (2007) Psoriasis: epidemiology. Clin. Dermatol., 25, 535-546.
2. Nestle, F.O., Kaplan, D.H. and Barker, J. (2009) Psoriasis. N. Engl. J. Med., 361, 496-509.
3. Elder, J.T., Bruce, A.T., Gudjonsson, J.E., Johnston, A., Stuart, P.E., Tejasvi, T., Voorhees, J.J., Abecasis, G.R. and Nair, R.P. (2010) Molecular dissection of psoriasis: integrating genetics and biology. J. Invest. Dermatol., 130, 1213-1226.
4. Capon, F., Burden, A.D., Trembath, R.C. and Barker, J.N. (2012) Psoriasis and other complex trait dermatoses: from Loci to functional pathways. J. Invest. Dermatol., 132, 915-922.
5. Cargill, M., Schrodi, S.J., Chang, M., Garcia, V.E., Brandon, R., Callis, K.P., Matsunami, N., Ardlie, K.G., Civello, D., Catanese, J.J. et al. (2007) A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am. J. Hum. Genet., 80, 273-290.
6. Gubler, U., Chua, A.O., Schoenhaut, D.S., Dwyer, C.M., McComas, W., Motyka, R., Nabavi, N., Wolitzky, A.G., Quinn, P.M., Familletti, P.C. et al. (1991) Coexpression of two distinct genes is required to generate secreted bioactive cytotoxic lymphocyte maturation factor. Proc. Natl. Acad. Sci. USA, 88, 4143-4147.
7. Oppmann, B., Lesley, R., Blom, B., Timans, J.C., Xu, Y., Hunte, B., Vega, F., Yu, N., Wang, J., Singh, K. et al. (2000) Novel p19 protein engages IL-12p40 to form a cytokine, IL-23, with biological activities similar as well as distinct from IL-12. Immunity, 13, 715-725.
8. Boniface, K., Blom, B., Liu, Y.J. and de Waal Malefyt, R. (2008) From interleukin-23 to T-helper 17 cells: human T-helper cell differentiation revisited. Immunol. Rev., 226, 132-146.
9. Leonardi, C.L., Kimball, A.B., Papp, K.A., Yeilding, N., Guzzo, C., Wang, Y., Li, S., Dooley, L.T. and Gordon, K.B. (2008) Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 1). Lancet, 371, 1665- 1674.
10. Papp, K.A., Langley, R.G., Lebwohl, M., Krueger, G.G., Szapary, P., Yeilding, N., Guzzo, C., Hsu, M.C., Wang, Y., Li, S. et al. (2008) Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 52-week results from a randomised, double-blind, placebo-controlled trial (PHOENIX 2). Lancet, 371, 1675-1684.
11. Morahan, G., Huang, D., Ymer, S.I., Cancilla, M.R., Stephen, K., Dabadghao, P., Werther, G., Tait, B.D., Harrison, L.C. and Colman, P.G. (2001) Linkage disequilibrium of a type 1 diabetes susceptibility locus with a regulatory IL12B allele. Nat. Genet., 27, 218-221.
12. Stanilova, S. and Miteva, L. (2005) Taq-I polymorphism in 3'UTR of the IL-12B and association with IL-12p40 production from human PBMC. Genes Immun., 6, 364-366.
13. Seegers, D., Zwiers, A., Strober, W., Pena, A.S. and Bouma, G. (2002) A TaqI polymorphism in the 3'UTR of the IL-12 p40 gene correlates with increased IL-12 secretion. Genes Immun., 3, 419-423.
14. Yilmaz, V., Yentur, S.P. and Saruhan-Direskeneli, G. (2005) IL-12 and IL-10 polymorphisms and their effects on cytokine production. Cytokine, 30, 188-194.
15. Nair, R.P., Ruether, A., Stuart, P.E., Jenisch, S., Tejasvi, T., Hiremagalore, R., Schreiber, S., Kabelitz, D., Lim, H.W., Voorhees, J.J. et al. (2008) Polymorphisms of the IL12B and IL23R genes are associated with psoriasis. J. Invest. Dermatol., 128, 1653-1661.
16. Lee, E., Trepicchio, W.L., Oestreicher, J.L., Pittman, D., Wang, F., Chamian, F., Dhodapkar, M. and Krueger, J.G. (2004) Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J. Exp. Med., 199, 125-130.
17. Kryczek, I., Bruce, A.T., Gudjonsson, J.E., Johnston, A., Aphale, A., Vatan, L., Szeliga, W., Wang, Y., Liu, Y., Welling, T.H. et al. (2008) Induction of IL-17+ T cell trafficking and development by IFN-gamma: mechanism and pathological relevance in psoriasis. J. Immunol., 181, 4733-4741.
18. Gudjonsson, J.E., Aphale, A., Grachtchouk, M., Ding, J., Nair, R.P., Wang, T., Voorhees, J.J., Dlugosz, A.A. and Elder, J.T. (2009) Lack of evidence for activation of the hedgehog pathway in psoriasis. J. Invest. Dermatol., 129, 635-640.
19. Bjerke, J.R., Livden, J.K., Degre, M. and Matre, R. (1983) Interferon in suction blister fluid from psoriatic lesions. Br. J. Dermatol., 108, 295-299.
20. Schlaak, J.F., Buslau, M., Jochum, W., Hermann, E., Girndt, M., Gallati, H., Meyer zum Buschenfelde, K.H. and Fleischer, B. (1994) T cells involved in psoriasis vulgaris belong to the Th1 subset. J. Invest. Dermatol., 102, 145-149.
21. Livden, J.K., Bjerke, J.R., Degre, M. and Matre, R. (1986) The effect of Goeckerman therapy on interferon in serum and suction blister fluid from patients with psoriasis. Br. J. Dermatol., 114, 217-225.
22. Austin, L.M., Ozawa, M., Kikuchi, T., Walters, I.B. and Krueger, J.G. (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, 752-759.
23. Trepicchio, W.L., Ozawa, M., Walters, I.B., Kikuchi, T., Gilleaudeau, P., Bliss, J.L., Schwertschlag, U., Dorner, A.J. and Krueger, J.G. (1999) Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions. J. Clin. Invest., 104, 1527-1537.
24. Murphy, K.M. and Reiner, S.L. (2002) The lineage decisions of helper T cells. Nat. Rev. Immunol., 2, 933-944.
25. Aggarwal, S., Ghilardi, N., Xie, M.H., de Sauvage, F.J. and Gurney, A.L. (2003) Interleukin-23 promotes a distinct CD4 T cell activation state characterized by the production of interleukin-17. J. Biol. Chem., 278, 1910-1914.
26. Bettelli, E., Carrier, Y., Gao, W., Korn, T., Strom, T.B., Oukka, M., Weiner, H.L. and Kuchroo, V.K. (2006) Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature, 441, 235-238.
27. Langrish, C.L., Chen, Y., Blumenschein, W.M., Mattson, J., Basham, B., Sedgwick, J.D., McClanahan, T., Kastelein, R.A. and Cua, D.J. (2005) IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med., 201, 233-240.
28. Zaba, L.C., Suarez-Farinas, M., Fuentes-Duculan, J., Nograles, K.E., Guttman-Yassky, E., Cardinale, I., Lowes, M.A. and Krueger, J.G. (2009) Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J. Allergy Clin. Immunol., 124, 1022-1010 e1021-1395.
29. Zaba, L.C., Cardinale, I., Gilleaudeau, P., Sullivan-Whalen, M., Suarez-Farinas, M., Fuentes-Duculan, J., Novitskaya, I., Khatcherian, A., Bluth, M.J., Lowes, M.A. et al. (2007) Amelioration of epidermal hyperplasia by TNF inhibition is associated with reduced Th17 responses. J. Exp. Med., 204, 3183-3194.
30. Nair, R.P., Duffin, K.C., Helms, C., Ding, J., Stuart, P.E., Goldgar, D., Gudjonsson, J.E., Li, Y., Tejasvi, T., Feng, B.J. et al. (2009) Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat. Genet., 41, 199-204.
31. Tonel, G., Conrad, C., Laggner, U., Di Meglio, P., Grys, K., McClanahan, T.K., Blumenschein, W.M., Qin, J.Z., Xin, H., Oldham, E. et al. (2010) Cutting edge: a critical functional role for IL-23 in psoriasis. J. Immunol., 185, 5688-5691.
32. Di Cesare, A., Di Meglio, P. and Nestle, F.O. (2009) The IL-23/Th17 axis in the immunopathogenesis of psoriasis. J. Invest. Dermatol., 129, 1339-1350.
33. Annunziato, F., Cosmi, L., Santarlasci, V., Maggi, L., Liotta, F., Mazzinghi, B., Parente, E., Fili, L., Ferri, S., Frosali, F. et al. (2007) Phenotypic and functional features of human Th17 cells. J. Exp. Med., 204, 1849-1861.
34. Lowes, M.A., Kikuchi, T., Fuentes-Duculan, J., Cardinale, I., Zaba, L.C., Haider, A.S., Bowman, E.P. and Krueger, J.G. (2008) Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J. Invest. Dermatol., 128, 1207-1211.
35. Veldhoen, M., Hocking, R.J., Atkins, C.J., Locksley, R.M. and Stockinger, B. (2006) TGFbeta in the context of an inflammatory cytokine milieu supports de novo differentiation of IL-17-producing T cells. Immunity, 24, 179-189.
36. Mangan, P.R., Harrington, L.E., O'Quinn, D.B., Helms, W.S., Bullard, D.C., Elson, C.O., Hatton, R.D., Wahl, S.M., Schoeb, T.R. and Weaver, C.T. (2006) Transforming growth factor-beta induces development of the T(H)17 lineage. Nature, 441, 231-234.
37. Lexberg, M.H., Taubner, A., Albrecht, I., Lepenies, I., Richter, A., Kamradt, T., Radbruch, A. and Chang, H.D. (2010) IFN-gamma and IL-12 synergize to convert in vivo generated Th17 into Th1/Th17 cells. Eur. J. Immunol., 40, 3017-3027.
38. Bending, D., De la Pena, H., Veldhoen, M., Phillips, J.M., Uyttenhove, C., Stockinger, B. and Cooke, A. (2009) Highly purified Th17 cells from BDC2.5NOD mice convert into Th1-like cells in NOD/SCID recipient mice. J. Clin. Invest., 119, 565-572.
39. Annunziato, F. and Romagnani, S. (2010) The transient nature of the Th17 phenotype. Eur. J. Immunol., 40, 3312-3316.
40. Zaba, L.C., Fuentes-Duculan, J., Eungdamrong, N.J., Abello, M.V., Novitskaya, I., Pierson, K.C., Gonzalez, J., Krueger, J.G. and Lowes, M.A. (2009) Psoriasis is characterized by accumulation of immunostimulatory and Th1/Th17 cell-polarizing myeloid dendritic cells. J. Invest. Dermatol., 129, 79-88.
41. Johnson-Huang, L.M., Suarez-Farinas, M., Pierson, K.C., Fuentes-Duculan, J., Cueto, I., Lentini, T., Sullivan-Whalen, M., Gilleaudeau, P., Krueger, J.G., Haider, A.S. et al. (2012) A single intradermal injection of IFN-gamma induces an inflammatory state in both non-lesional psoriatic and healthy skin. J. Invest. Dermatol., 132, 1177-1187.
42. Uyemura, K., Yamamura, M., Fivenson, D.F., Modlin, R.L. and Nickoloff, B.J. (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, 701-705.
43. Leonardi, C., Matheson, R., Zachariae, C., Cameron, G., Li, L., Edson-Heredia, E., Braun, D. and Banerjee, S. (2012) Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N. Engl. J. Med., 366, 1190-1199.
44. Papp, K.A., Leonardi, C., Menter, A., Ortonne, J.P., Krueger, J.G., Kricorian, G., Aras, G., Li, J., Russell, C.B., Thompson, E.H. et al. (2012) Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N. Engl. J. Med., 366, 1181-1189.
45. Gudjonsson, J.E., Ding, J., Johnston, A., Tejasvi, T., Guzman, A.M., Nair, R.P., Voorhees, J.J., Abecasis, G.R. and Elder, J.T. (2010) Assessment of the psoriatic transcriptome in a large sample: additional regulated genes and comparisons with in vitro models. J. Invest. Dermatol., 130, 1829-1840.
46. Irizarry, R.A., Hobbs, B., Collin, F., Beazer-Barclay, Y.D., Antonellis, K.J., Scherf, U. and Speed, T.P. (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics, 4, 249-264.
47. Elder, J.T., Fisher, G.J., Zhang, Q.Y., Eisen, D., Krust, A., Kastner, P., Chambon, P. and Voorhees, J.J. (1991) Retinoic acid receptor gene expression in human skin. J. Invest. Dermatol., 96, 425-433.
48. Lottaz, C., Yang, X., Scheid, S. and Spang, R. (2006) OrderedList-a bioconductor package for detecting similarity in ordered gene lists. Bioinformatics, 22, 2315-2316.
49. Smyth, G.K. (2004) Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat. Appl. Genet. Mol. Biol., 3, Article 3.