44
Views
7
CrossRef citations to date
0
Altmetric
Review

Role of T-cell-mediated inflammation in psoriasis: pathogenesis and targeted therapy

&
Pages 1-10 | Published online: 27 Feb 2013

References

  • Mehta NN, Azfar RS, Shin DB, Neimann AL, Troxel AB, Gelfand JM. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database. Eur Heart J. 2010;31(8):1000–1006.
  • Gelfand JM, Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB. Risk of myocardial infarction in patients with psoriasis. JAMA. 2006;296(14):1735–1741.
  • Gisondi P, Tessari G, Conti A, et al. Prevalence of metabolic syndrome in patients with psoriasis: a hospital-based case-control study. Br J Dermatol. 2007;157(1):68–73.
  • Kurd SK, Troxel AB, Crits-Christoph P, Gelfand JM. The risk of depression, anxiety, and suicidality in patients with psoriasis: a population-based cohort study. Arch Dermatol. 2010;146(8):891–895.
  • Krueger G, Koo J, Lebwohl M, Menter A, Stern RS, Rolstad T. The impact of psoriasis on quality of life: results of a 1998 National Psoriasis Foundation patient-membership survey. Arch Dermatol. 2001;137(3): 280–284.
  • Wolf N, Quaranta M, Prescott NJ, et al. Psoriasis is associated with pleiotropic susceptibility loci identified in type II diabetes and Crohn disease. J Med Genet. 2008;45(2):114–116.
  • Nair RP, Henseler T, Jenisch S, et al. Evidence for two psoriasis susceptibility loci (HLA and 17q) and two novel candidate regions (16q and 20p) by genome-wide scan. Hum Mol Genet. 1997;6(8):1349–1356.
  • Mueller W, Herrmann B. Cyclosporin A for psoriasis. N Engl J Med. 1979;301(10):555.
  • Gottlieb SL, Gilleaudeau P, Johnson R, et al. Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune, but not keratinocyte, pathogenic basis. Nat Med. 1995;1(5):442–447.
  • Nicolas JF, Chamchick N, Thivolet J, Wijdenes J, Morel P, Revillard JP. CD4 antibody treatment of severe psoriasis. Lancet. 1991;338(8762):321.
  • Sano S, Chan KS, Carbajal S, et al. Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat Med. 2005;11(1):43–49.
  • Nestle FO, Conrad C, Tun-Kyi A, et al. Plasmacytoid predendritic cells initiate psoriasis through interferon-alpha production. J Exp Med. 2005;202(1):135–143.
  • Lande R, Gregorio J, Facchinetti V et al. Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature. 2007;449(7162):564–569.
  • Conrad C, Boyman O, Tonel G, et al. Alpha1beta1 integrin is crucial for accumulation of epidermal T cells and the development of psoriasis. Nat Med. 2007;13(7):836–842.
  • Ganguly D, Chamilos G, Lande R, et al. Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med. 2009;206(9):1983–1994.
  • Gilliet M, Cao W, Liu YJ. Plasmacytoid dendritic cells: sensing nucleic acids in viral infection and autoimmune diseases. Nat Rev Immunol. 2008;8(8):594–606.
  • Prinz JC, Vollmer S, Boehncke WH, Menssen A, Laisney I, Trommler P Selection of conserved TCR VDJ rearrangements in chronic psoriatic plaques indicates a common antigen in psoriasis vulgaris. Eur J Immunol. 1999;29(10):3360–3368.
  • Vollmer S, Menssen A, Prinz JC. Dominant lesional T cell receptor rearrangements persist in relapsing psoriasis but are absent from nonlesional skin: evidence for a stable antigen-specific pathogenic T cell response in psoriasis vulgaris. J Invest Dermatol. 2001;117(5):1296–1301.
  • Uyemura K, Yamamura M, Fivenson DF, Modlin RL, Nickoloff BJ. The cytokine network in lesional and lesion-free psoriatic skin is characterized by a T-helper type 1 cell-mediated response. J Invest Dermatol. 1993;101(5):701–705.
  • Lowes MA, Kikuchi T, Fuentes-Duculan J, et al. Psoriasis vulgaris lesions contain discrete populations of Th1 and Th17 T cells. J Invest Dermatol. 2008;128(5):1207–1211.
  • Kagami S, Rizzo HL, Lee JJ, Koguchi Y, Blauvelt A. Circulating Th17, Th22, and Th1 cells are increased in psoriasis. J Invest Dermatol. 2010;130(5):1373–1383.
  • Steinman L. A brief history of T(H)17, the first major revision in the T(H)1/T(H)2 hypothesis of T cell-mediated tissue damage. Nat Med. 2007;13(2):139–145.
  • Trifari S, Kaplan CD, Tran EH, Crellin NK, Spits H. Identification of a human helper T cell population that has abundant production of interleukin 22 and is distinct from T(H)-17, T(H)1 and T(H)2 cells. Nat Immunol. 2009;10(8):864–871.
  • Duhen T, Geiger R, Jarrossay D, Lanzavecchia A, Sallusto F. Production of interleukin 22 but not interleukin 17 by a subset of human skin-homing memory T cells. Nat Immunol. 2009;10(8):857–863.
  • Lee E, Trepicchio WL, Oestreicher JL, et al. Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med. 2004;199(1):125–130.
  • Chan JR, Blumenschein W, Murphy E, et al. IL-23 stimulates epidermal hyperplasia via TNF and IL-20R2-dependent mechanisms with implications for psoriasis pathogenesis. J Exp Med. 2006;203(12): 2577–2587.
  • Tonel G, Conrad C, Laggner U, et al. Cutting edge: a critical functional role for IL-23 in psoriasis. J Immunol. 2010;185(10):5688–5691.
  • McGeachy MJ, Chen Y, Tato CM, et al. The interleukin 23 receptor is essential for the terminal differentiation of interleukin 17-producing effector T helper cells in vivo. Nat Immunol. 2009;10(3):314–324.
  • Zheng Y, Danilenko DM, Valdez P, et al. Interleukin-22, a T(H)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature. 2007;445(7128):648–651.
  • Tonel G, Conrad C. Interplay between keratinocytes and immune cells: recent insights into psoriasis pathogenesis. Int J Biochem Cell Biol. 2009;41(5):963–968.
  • Liang SC, Tan XY, Luxenberg DP, et al. Interleukin (IL)-22 and IL-17 are coexpressed by Th17 cells and cooperatively enhance expression of antimicrobial peptides. J Exp Med. 2006;203(10):2271–2279.
  • Wolk K, Kunz S, Witte E, Friedrich M, Asadullah K, Sabat R. IL-22 increases the innate immunity of tissues. Immunity. 2004;21(2): 241–254.
  • Peric M, Koglin S, Kim SM, et al. IL-17A enhances vitamin D3-induced expression of cathelicidin antimicrobial peptide in human keratinocytes. J Immunol. 2008;181(12):8504–8512.
  • Conrad C, Meller S, Gilliet M. Plasmacytoid dendritic cells in the skin: to sense or not to sense nucleic acids. Semin Immunol. 2009;21(3): 101–109.
  • Gregorio J, Meller S, Conrad C, et al. Plasmacytoid dendritic cells sense skin injury and promote wound healing through type I interferons. J Exp Med. 2010;207(13):2921–2930.
  • Tohyama M, Yang L, Hanakawa Y, Dai X, Shirakata Y, Sayama K. IFN-a enhances IL-22 receptor expression in keratinocytes: a possible role in the development of psoriasis. J Invest Dermatol. 2012;132(7): 1933–1935.
  • Eyerich S, Eyerich K, Pennino D, et al. Th22 cells represent a distinct human T cell subset involved in epidermal immunity and remodeling. J Clin Invest. 2009;119(12):3573–3585.
  • Van Belle AB, de Heusch M, Lemaire MM, et al. IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice. J Immunol. 2012;188(1):462–469.
  • Lang KS, Recher M, Junt T, et al. Toll-like receptor engagement converts T-cell autoreactivity into overt autoimmune disease. Nat Med. 2005;11(2):138–145.
  • S�nchez FO, Linga Reddy MV, Mallbris L, Sakuraba K, St�hle M, Alarc�n-Riquelme ME. IFN-regulatory factor 5 gene variants interact with the class I MHC locus in the Swedish psoriasis population. J Invest Dermatol. 2008;128(7):1704–1709.
  • Nair RP, Stuart PE, Nistor I, et al. Sequence and haplotype analysis supports HLA-C as the psoriasis susceptibility 1 gene. Am J Hum Genet. 2006;78(5):827–851.
  • Cargill M, Schrodi SJ, Chang M, et al. A large-scale genetic association study confirms IL12B and leads to the identification of IL23R as psoriasis-risk genes. Am J Hum Genet. 2007;80(2):273–290.
  • Capon F, Di Meglio P, Szaub J, et al. Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum Genet. 2007;122(2):201–206.
  • Hollox EJ, Huffmeier U, Zeeuwen PL, et al. Psoriasis is associated with increased beta-defensin genomic copy number. Nat Genet. 2008;40(1): 23–25.
  • Sutton CE, Lalor SJ, Sweeney CM, Brereton CF, Lavelle EC, Mills KH. Interleukin-1 and IL-23 induce innate IL-17 production from gammadelta T cells, amplifying Th17 responses and autoimmunity. Immunity. 2009;31(2):331–341.
  • Cai Y, Shen X, Ding C, et al. Pivotal role of dermal IL-17-producing y8 T cells in skin inflammation. Immunity. 2011;35(4):596–610.
  • Sumaria N, Roediger B, Ng LG, et al. Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J Exp Med. 2011;208(3): 505–518.
  • Pantelyushin S, Haak S, Ingold B, et al. Roryt+ innate lymphocytes and 78 T cells initiate psoriasiform plaque formation in mice. J Clin Invest. 2012;122(6):2252–2256.
  • Laggner U, Di Meglio P, Perera GK, et al. Identification of a novel proinflammatory human skin-homing Vy9V82 T cell subset with a potential role in psoriasis. J Immunol. 2011;187(5):2783–2793.
  • Ghoreschi K, Bruck J, Kellerer C, et al. Fumarates improve psoriasis and multiple sclerosis by inducing type II dendritic cells. J Exp Med. 2011;208(11):2291–2303.
  • Ellis CN, Gorsulowsky DC, Hamilton TA, et al. Cyclosporine improves psoriasis in a double-blind study. JAMA. 1986;256(22):3110–3116.
  • Elias PM. Epidermal effects of retinoids: supramolecular observations and clinical implications. J Am Acad Dermatol. 1986;15(4 Pt 2):797–809.
  • Jeffes EW 3rd, McCullough JL, Pittelkow MR, et al. Methotrexate therapy of psoriasis: differential sensitivity of proliferating lymphoid and epithelial cells to the cytotoxic and growth-inhibitory effects of methotrexate. J Invest Dermatol. 1995;104(2):183–188.
  • Nijsten T, Margolis DJ, Feldman SR, Rolstad T, Stern RS. Traditional systemic treatments have not fully met the needs of psoriasis patients: results from a national survey. J Am Acad Dermatol. 2005;52(3 Pt 1): 434–444.
  • Baugh JA, Bucala R. Mechanisms for modulating TNF alpha in immune and inflammatory disease. Curr Opin Drug Discov Devel. 2001;4(5):635–650.
  • Oh CJ, Das KM, Gottlieb AB. Treatment with anti-tumor necrosis factor alpha (TNF-alpha) monoclonal antibody dramatically decreases the clinical activity of psoriasis lesions. J Am Acad Dermatol. 2000;42(5 Pt 1): 829–830.
  • Sterry W, van de Kerkhof P. Is �class effect� relevant when assessing the benefit/risk profile of a biologic agent? J Eur Acad Dermatol Venereol 2012;26 Suppl 5:9–16.
  • Leonardi CL, Kimball AB, Papp KA, et al; PHOENIX 1 study investigators. 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. 2008;371(9625):1665–1674.
  • Papp KA, Langley RG, Lebwohl M, et al; PHOENIX 2 study investigators. 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. 2008;371(9625):1675–1684.
  • Griffiths CE, Strober BE, van de Kerkhof P, et al. Comparison of ustekinumab and etanercept for moderate-to-severe psoriasis. N Engl J Med. 2010;362(2):118–128.
  • Reich K, Langley RG, Papp KA, et al. A 52-week trial comparing bri-akinumab with methotrexate in patients with psoriasis. N Engl J Med. 2011;365(17):1586–1596.
  • Strober BE, Crowley JJ, Yamauchi PS, Olds M, Williams DA. Efficacy and safety results from a phase III, randomized controlled trial comparing the safety and efficacy of briakinumab with etanercept and placebo in patients with moderate to severe chronic plaque psoriasis. Br J Dermatol. 2011;165(3):661–668.
  • Gordon KB, Langley RG, Gottlieb AB, et al. A phase III, randomized, controlled trial of the fully human IL-12/23 mAb briakinumab in moderate-to-severe psoriasis. J Invest Dermatol. 2012;132(2):304�314.
  • Ryan C, Leonardi CL, Krueger JG, et al. Association between biologic therapies for chronic plaque psoriasis and cardiovascular events: a metaanalysis of randomized controlled trials. JAMA. 2011;306(8):864�871.
  • Simon T, Taleb S, Danchin N, et al. Circulating levels of interleukin-17 and cardiovascular outcomes in patients with acute myocardial infarction. Eur Heart J. Epub September 6, 2012.
  • Langowski JL, Zhang X, Wu L, et al. IL-23 promotes tumour incidence and growth. Nature. 2006;442(7101):461–465.
  • Brunda MJ, Luistro L, Warrier RR, et al. Antitumor and antimetastatic activity of interleukin 12 against murine tumors. J Exp Med. 1993;178(4):1223�1230.
  • Cavallo F, Quaglino E, Cifaldi L, et al. Interleukin 12-activated lymphocytes influence tumor genetic programs. Cancer Res. 2001;61(8):3518�3523.
  • Hueber W, Patel DD, Dryja T, et al. Effects of AIN457, a fully human antibody to interleukin-17A, on psoriasis, rheumatoid arthritis, and uveitis. Sci Transl Med. 2010;2(52):52ra72.
  • Leonardi C, Matheson R, Zachariae C, et al. Anti-interleukin-17 monoclonal antibody ixekizumab in chronic plaque psoriasis. N Engl J Med. 2012;366(13):1190�1199.
  • Papp KA, Leonardi C, Menter A, et al. Brodalumab, an anti-interleukin-17-receptor antibody for psoriasis. N Engl J Med. 2012;366(13): 1181�1189.
  • Wilson NJ, Boniface K, Chan JR, et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells. Nat Immunol. 2007;8(9):950�957.
  • Goris A, Marrosu MG, Vandenbroeck K. Novel polymorphisms in the IL-10 related AK155 gene (chromosome 12q15). Genes Immun. 2001;2(5):284�286.
  • Vandenbroeck K, Cunningham S, Goris A, et al. Polymorphisms in the interferon-gamma/interleukin-26 gene region contribute to sex bias in susceptibility to rheumatoid arthritis. Arthritis Rheum. 2003;48(10): 2773�2778.
  • Silverberg MS, Cho JH, Rioux JD, et al. Ulcerative colitis-risk loci on chromosomes 1p36 and 12q15 found by genome-wide association study. Nat Genet. 2009;41(2):216�220.
  • Milner JD, Brenchley JM, Laurence A, et al. Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature. 2008;452(7188):773�776.
  • Acosta-Rodriguez EV, Napolitani G, Lanzavecchia A, Sallusto F. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells. Nat Immunol. 2007;8(9):942�949.
  • Chamilos G, Ganguly D, Lande R, et al. Generation of IL-23 producing dendritic cells (DCs) by airborne fungi regulates fungal pathogenicity via the induction of T(H)-17 responses. P LoS One. 2010;5(9):e12955.
  • Lebwohl M, Tyring SK, Hamilton TK, et al. A novel targeted T-cell modulator, efalizumab, for plaque psoriasis. N Engl J Med. 2003;349(21):2004�2013.
  • Ellis CN, Krueger GG. Treatment of chronic plaque psoriasis by selective targeting of memory effector T lymphocytes. N Engl J Med. 2001;345(4):248�255.
  • Bissonnette R, Langley RG, Papp K, et al. Humanized anti-CD2 monoclonal antibody treatment of plaque psoriasis: efficacy and pharmacodynamic results of two randomized, double-blind, placebo-controlled studies of intravenous and subcutaneous siplizumab. Arch Dermatol Res. 2009;301(6):429�442.
  • Gottlieb AB, Lebwohl M, Shirin S, et al. Anti-CD4 monoclonal antibody treatment of moderate to severe psoriasis vulgaris: results of a pilot, multicenter, multiple-dose, placebo-controlled study. J Am Acad Dermatol. 2000;43(4):595�604.
  • Mandala S, Hajdu R, Bergstrom J, et al. Alteration of lymphocyte trafficking by sphingosine-1-phosphate receptor agonists. Science. 2002;296(5566):346�349.
  • Matloubian M, Lo CG, Cinamon G, et al. Lymphocyte egress from thymus and peripheral lymphoid organs is dependent on S1P receptor 1. Nature. 2004;427(6972):355�360.
  • Boyman O, Hefti HP, Conrad C, Nickoloff BJ, Suter M, Nestle FO. Spontaneous development of psoriasis in a new animal model shows an essential role for resident T cells and tumor necrosis factor-alpha. J Exp Med. 2004;199(5):731�736.
  • Boyman O, Conrad C, Tonel G, Gilliet M, Nestle FO. The pathogenic role of tissue-resident immune cells in psoriasis. Trends Immunol. 2007;28(2):51�57.
  • Evenou JP, Wagner J, Zenke G, et al. The potent protein kinase C-selective inhibitor AEB071 (sotrastaurin) represents a new class of immunosuppressive agents affecting early T-cell activation. J Pharmacol Exp Ther. 2009;330(3):792�801.
  • Skvara H, Dawid M, Kleyn E, et al. The PKC inhibitor AEB071 may be a therapeutic option for psoriasis. J Clin Invest. 2008;118(9): 3151�3159.
  • Seavey MM, Dobrzanski P. The many faces of Janus kinase. Biochem Pharmacol. 2012;83(9):1136�1145.
  • Ghoreschi K, Laurence A, O�Shea JJ. Selectivity and therapeutic inhibition of kinases: to be or not to be? Nat Immunol. 2009;10(4): 356�360.
  • Gottlieb AB, Strober B, Krueger JG, et al. An open-label, single-arm pilot study in patients with severe plaque-type psoriasis treated with an oral anti-inflammatory agent, apremilast. Curr Med Res Opin. 2008;24(5):1529�1538.