Keratinocytes as targets for interleukin-10-related cytokines: A putative role in the pathogenesis of psoriasis

European Cytokine Network

Volumn 16, Issue 4, 2005, Pages 309-319

  Boniface, Katia ^a   Lecron, Jean Claude ^a   Bernard, François Xavier ^b   Dagregorio, Guy ^c   Guillet, Gérard ^c   Nau, François ^a   Morel, Franck ^a  

^a UNIVERSITÉ DE POITIERS   (France)

^b BIOalternatives   (France)

^c POITIERS UNIVERSITY HOSPITAL   (France)

Author keywords

Cytokines; Inflammation; Keratinocyte; Psoriasis; Skin

Indexed keywords

INTERLEUKIN 10; INTERLEUKIN 19; INTERLEUKIN 20; INTERLEUKIN 22; INTERLEUKIN 24; INTERLEUKIN 26;

DNA POLYMORPHISM; GENE EXPRESSION; HUMAN; IMMUNE RESPONSE; KERATINOCYTE; PATHOGENESIS; PROTEIN FUNCTION; PSORIASIS; REVIEW; SKIN INFLAMMATION;

ANIMALS; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-10; KERATINOCYTES; MULTIGENE FAMILY; PSORIASIS;

EID: 33750712522     PISSN: 11485493     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (128)

1. Fiorentino DF, Bond MW, Mosmann TR. Two types of mouse T helper cell. IV. Th2 clones secrete a factor that inhibits cytokine production by Th1 clones. J Exp Med 1989; 170: 2081.
2. Moore KW, de Waal Malefyt R, Coffman RL, O'Garra A. Interleukin-10 and the interleukin-10 receptor. Annu Rev Immunol 2001; 19: 683.
3. Gallagher G, Dickensheets H, Eskdale J, Izotova LS, Mirochnitchenko OV, Peat JD, Vazquez N, Pestka S, Donnelly RP, Kotenko SV. Cloning, expression and initial characterization of interleukin-19 (IL-19), a novel homologue of human interleukin-10 (IL-10). Genes Immun 2000; 1: 442.
4. Blumberg H, Conklin D, Xu WF, Grossmann A, Brender T, Carollo S, Eagan M, Foster D, Haldeman BA, Hammond A, Haugen H, Jelinek L, Kelly JD, Madden K, Maurer MF, Parrish-Novak J, Prunkard D, Sexson S, Sprecher C, Waggie K, West J, Whitmore TE, Yao L, Kuechle MK, Dale BA, Chandrasekher YA. Interleukin 20: discovery, receptor identification, and role in epidermal function. Cell 2001; 104: 9.
5. Xie MH, Aggarwal S, Ho WH, Foster J, Zhang Z, Stinson J, Wood WI, Goddard AD, Gurney AL. Interleukin (IL)-22, a novel human cytokine that signals through the interferon receptor-related proteins CRF2-4 and IL-22R. J Biol Chem 2000; 275: 31335.
6. Dumoutier L, Louahed J, Renauld JC. Cloning and characterization of IL-10-related T cell-derived inducible factor (IL-TIF), a novel cytokine structurally related to IL-10 and inducible by IL-9. J Immunol 2000; 164: 1814.
7. Jiang H, Lin JJ, Su ZZ, Goldstein NI, Fisher PB. Subtraction hybridization identifies a novel melanoma differentiation associated gene, mda-7, modulated during human melanoma differentiation, growth and progression. Oncogene 1995; 11: 2477.
8. Wang M, Tan Z, Zhang R, Kotenko SV, Liang P. Interleukin 24 (MDA-7/MOB-5) signals through two heterodimeric receptors, IL-22R1/IL-20R2 and IL-20R1/IL-20R2. J Biol Chem 2002; 277: 7341.
9. Knappe A, Hor S, Wittmann S, Fickenscher H. Induction of a novel cellular homolog of interleukin-10, AK155, by transformation of T lymphocytes with herpes virus saimiri. J Virol 2000; 74: 3881.
10. Liu Y, Wei SH, Ho AS, de Waal Malefyt R, Moore KW. Expression cloning and characterization of a human IL-10 receptor. J Immunol 1994; 152: 1821.
11. Kotenko SV, Krause CD, Izotova LS, Pollack BP, Wu W, Pestka S. Identification and functional characterization of a second chain of the interleukin-10 receptor complex. EMBO J 1997; 16: 5894.
12. Spencer SD, Di Marco F, Hooley J, Pitts-Meek S, Bauer M, Ryan AM, Sordat B, Gibbs VC, Aguet M. The orphan receptor CRF2-4 is an essential subunit of the interleukin 10 receptor. J Exp Med 1998; 187: 571.
13. Kotenko SV, Izotova LS, Mirochnitchenko OV, Esterova E, Dickensheets H, Donnelly RP, Pestka S. Identification of the functional interleukin-22 (IL-22) receptor complex: the IL-10R2 chain (IL-10R beta) is a common chain of both the IL-10 and IL-22 (IL-10-related T cell-derived inducible factor, IL-TIF) receptor complexes. J Biol Chem 2001; 276: 2725.
14. Sheikh F, Baurin VV, Lewis-Antes A, Shah NK, Smirnov SV, Anantha S, Dickensheets H, Dumoutier L, Renauld JC, Zdanov A, Donnelly RP, Kotenko SV. Cutting edge: IL-26 signals through a novel receptor complex composed of IL-20 receptor 1 and IL-10 receptor 2. J Immunol 2004; 172: 2006.
15. Wolk K, Kunz S, Asadullah K, Sabat R. Cutting edge: immune cells as sources and targets of the IL-10 family members? J Immunol 2002; 168: 5397.
16. Gurney AL. IL-22, a Th1 cytokine that targets the pancreas and select other peripheral tissues. Int Immunopharmacol 2004; 4: 669.
17. Boniface K, Bernard FX, Garcia M, Gurney AL, Lecron JC, Morel F. IL-22 inhibits epidermal differentiation and induces proinflammatory gene expression and migration of human keratinocytes. J Immunol 2005; 174: 3695.
18. Lecart S, Morel F, Noraz N, Pene J, Garcia M, Boniface K, Lecron JC, Yssel H. IL-22, in contrast to IL-10, does not induce Ig production, due to absence of a functional IL-22 receptor on activated human B cells. Int Immunol 2002; 14: 1351.
19. Nagalakshmi ML, Rascle A, Zurawski S, Menon S, de Waal Malefyt R. Interleukin-22 activates STAT3 and induces IL-10 by colon epithelial cells. Int Immunopharmacol 2004; 4: 679.
20. Dumoutier L, Leemans C, Lejeune D, Renauld JC. Cutting edge: STAT activation by IL-19, IL-20 and mda-7 through IL-20 receptor complexes of two types. J Immunol 2001; 167: 3545.
21. Parrish-Novak J, Xu W, Brender T, Yao L, Jones C, West J, Brandt C, Jelinek L, Madden K, McKernan PA, Foster DC, Jaspers S, Chandrasekher YA. Interleukins 19, 20, and 24 signal through two distinct receptor complexes. Differences in receptor-ligand interactions mediate unique biological functions. J Biol Chan 2002; 277: 47517.
22. Nagalakshmi ML, Murphy E, McClanahan T, de Waal Malefyt R. Expression patterns of IL-10 ligand and receptor gene families provide leads for biological characterization. Int Immunopharmacol 2004; 4: 577.
23. Finbloom DS, Winestock KD. IL-10 induces the tyrosine phosphorylation of tyk2 and Jak1 and the differential assembly of STAT1 alpha and STAT3 complexes in human T cells and monocytes. J Immunol 1995; 155: 1079.
24. Hor S, Pirzer H, Dumoutier L, Bauer F, Wittmann S, Sticht H, Renauld JC, de Waal Malefyt R, Fickenscher H. The T-cell lymphokine interleukin-26 targets epithelial cells through the interleukin-20 receptor 1 and interleukin-10 receptor 2 chains. J Biol Chem 2004; 279: 33343.
25. Donnelly RP, Sheikh F, Kotenko SV, Dickensheets H. The expanded family of class II cytokines that share the IL-10 receptor-2 (IL-10R2) chain. J Leukoc Biol 2004; 76: 314.
26. Lejeune D, Dumoutier L, Constantinescu S, Kruijer W, Schuringa JJ, Renauld JC. Interleukin-22 (IL-22) activates the JAK/STAT, ERK, JNK, and p38 MAP kinase pathways in a rat hepatoma cell line. Pathways that are shared with and distinct from IL-10. J Biol Chem 2002; 277: 33676.
27. Sarkar D, Su ZZ, Lebedeva IV, Sauane M, Gopalkrishnan RV, Valerie K, Dent P, Fisher PB. mda-7 (IL-24) mediates selective apoptosis in human melanoma cells by inducing the coordinated overexpression of the GADD family of genes by means of p38 MAPK. Proc Natl Acad Sci USA 2002; 99: 10054.
28. Yacoub A, Mitchell C, Lebedeva IV, Sarkar D, Su ZZ, McKinstry R, Gopalkrishnan RV, Grant S, Fisher PB, Dent P. mda-7 (IL-24) Inhibits growth and enhances radiosensitivity of glioma cells in vitro via JNK signaling. Cancer Biol Ther 2003; 2: 347.
29. Ding L, Shevach EM. IL-10 inhibits mitogen-induced T cell proliferation by selectively inhibiting macrophage costimulatory function. J Immunol 1992; 148: 3133.
30. Macatonia SE, Doherty TM, Knight SC, O'Garra A. Differential effect of IL-10 on dendritic cell-induced T cell proliferation and IFN-gamma production. J Immunol 1993; 150: 3755.
31. Enk AH, Angeloni VL, Udey MC, Katz SI. Inhibition of Langerhans cell antigen-presenting function by IL-10. A role for IL-10 in induction of tolerance. J Immunol 1993; 151: 2390.
32. Peguet-Navarro J, Moulon C, Caux C, Dalbiez-Gauthier C, Banchereau J, Schmitt D. Interleukin-10 inhibits the primary allogeneic T cell response to human epidermal Langerhans cells. Eur J Immunol 1994; 24: 884.
33. de Waal Malefyt R, Haanen J, Spits H, Roncarolo MG, te Velde A, Figdor C, Johnson K, Kastelein R, Yssel H, de Vries JE. Interleukin 10 (IL-10) and viral IL-10 strongly reduce antigen-specific human T cell proliferation by diminishing the antigen-presenting capacity of monocytes via downregulation of class II major histocompatibility complex expression. J Exp Med 1991; 174: 915.
34. Fiorentino DF, Zlotnik A, Vieira P, Mosmann TR, Howard M, Moore KW, O'Garra A. IL-10 acts on the antigen-presenting cell to inhibit cytokine production by Th1 cells. J Immunol 1991; 146: 3444.
35. de Waal Malefyt R, Yssel H, de Vries JE. Direct effects of IL-10 on subsets of human CD4+ T cell clones and resting T cells. Specific inhibition of IL-2 production and proliferation. J Immunol 1993; 150: 4754.
36. de Waal Malefyt R, Abrams J, Bennett B, Figdor CG, de Vries JE. Interleukin 10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J Exp Med 1991; 174: 1209.
37. Fiorentino DF, Zlotnik A, Mosmann TR, Howard M, O'Garra A. IL-10 inhibits cytokine production by activated macrophages. J Immunol 1991; 147: 3815.
38. D'Andrea A, Aste-Amezaga M, Valiante NM, Ma X, Kubin M, Trinchieri G. Interleukin 10 (IL-10) inhibits human lymphocyte interferon gamma-production by suppressing natural killer cell stimulatory factor/IL-12 synthesis in accessory cells. J Exp Med 1993; 178: 1041.
39. Liao YC, Liang WG, Chen RV, Hsu JH, Yang JJ, Chang MS. IL-19 induces production of IL-6 and TNF-alpha and results in cell apoptosis through TNF-alpha. J Immunol 2002; 169: 4288.
40. Gallagher G, Eskdale J, Jordan W, Peat J, Campbell J, Boniotto M, Lennon GP, Dickensheets H, Donnelly RP. Human interleukin-19 and its receptor: a potential role in the induction of Th2 responses. Int Immunopharmacol 2004; 4: 615.
41. Jordan WJ, Eskdale J, Boniotto M, Lennon GP, Peat J, Campbell JD, Gallagher G. Human IL-19 regulates immunity through auto-induction of IL-19 and production of IL-10. Eur J Immunol 2005; 35: 1576.
42. Liao SC, Cheng YC, Wang YC, Wang CW, Yang SM, Yu CK, Shieh CC, Cheng KC, Lee MF, Chiang SR, Shieh JM, Chang MS. IL-19 induced Th2 cytokines and was up-regulated in asthma patients. J Immunol 2004; 173: 6712.
43. Li HH, Lin YC, Chen PJ, Hsiao CH, Lee JY, Chen WC, Tzung TY, Wu JC, Chang MS. Interleukin-19 upregulates keratinocyte growth factor and is associated with psoriasis. Br J Dermatol 2005; 153: 591.
44. Hosoi T, Wada S, Suzuki S, et al. Bacterial endotoxin induces IL-20 expression in the glial cells. Brain Res Mol Brain Res 2004; 130: 23.
45. Wei CC, Chen WY, Wang YC, et al. Detection of IL-20 and its receptors on psoriatic skin. Clin Immunol 2005; 117: 65.
46. Liu L, Ding C, Zeng W, et al. Selective enhancement of multipotential hematopoietic progenitors in vitro and in vivo by IL-20. Blood 2003; 102: 3206.
47. Heuze-Vourc'h N, Liu M, Dalwadi H, et al. IL-20, an antiangiogenic cytokine that inhibits COX-2 expression. Biochem Biophys Res Commun 2005; 333: 470.
48. Wolk K, Kunz S, Witte E, et al. IL-22 increases the innate immunity of tissues. Immunity 2004; 21: 241.
49. Dumoutier L, Van Roost E, Colau D, et al. Human interleukin-10-related T cell-derived inducible factor: molecular cloning and functional characterization as an hepatocyte-stimulating factor. Proc Natl Acad Sci USA 2000; 97: 10144.
50. Aggarwal S, Xie MH, Maruoka M, et al. Acinar cells of the pancreas are a target of interleukin-22. J Interferon Cytokine Res 2001; 21: 1047.
51. Ikeuchi H, Kuroiwa T, Hiramatsu N, et al. Expression of interleukin-22 in rheumatoid arthritis: potential role as a proinflammatory cytokine. Arthritis Rheum 2005; 52: 1037.
52. Radaeva S, Sun R, Pan HN, et al. Interleukin 22 (IL-22) plays a protective role in T cell-mediated murine hepatitis: IL-22 is a survival factor for hepatocytes via STAT3 activation. Hepatology 2004; 39: 1332.
53. Dumoutier L, Lejeune D, Colau D, et al. Cloning and characterization of IL-22 binding protein, a natural antagonist of IL-10-related T cell-derived inducible factor/IL-22. J Immunol 2001; 166: 7090.
54. Kotenko SV, Izotova LS, Mirochnitchenko OV, et al. Identification, cloning, and characterization of a novel soluble receptor that binds IL-22 and neutralizes its activity. J Immunol 2001; 166: 7096.
55. Xu W, Presnell SR, Parrish-Novak J, et al. A soluble class II cytokine receptor, IL-22RA2, is a naturally occurring IL-22 antagonist. Proc Natl Acad Sci USA 2001; 98: 9511.
56. Caudell EG, Mumm JB, Poindexter N, et al. The protein product of the tumor suppressor gene, melanoma differentiation-associated gene 7, exhibits immunostimulatory activity and is designated IL-24. J Immunol 2002; 168: 6041.
57. Garn H, Schmidt A, Grau V, et al. IL-24 is expressed by rat and human macrophages. Immunobiology 2002; 205: 321.
58. Huang EY, Madireddi MT, Gopalkrishnan RV, et al. Genomic structure, chromosomal localization and expression profile of a novel melanoma differentiation associated (mda-7) gene with cancer specific growth suppressing and apoptosis inducing properties. Oncogene 2001; 20: 7051.
59. Jiang H, Su ZZ, Lin JJ, et al. The melanoma differentiation associated gene mda-7 suppresses cancer cell growth. Proc Natl Acad Sci USA 1996; 93: 9160.
60. Saeki T, Mhashilkar A, Chada S, et al. Tumor-suppressive effects by adenovirus-mediated mda-7 gene transfer in non-small cell lung cancer cell in vitro. Gene Ther 2000; 7: 2051.
61. Mhashilkar AM, Schrock RD, Hindi M, et al. Melanoma differentiation associated gene-7 (mda-7): a novel anti-tumor gene for cancer gene therapy. Mol Med 2001; 7: 271.
62. Lebedeva IV, Su ZZ, Chang Y, et al. The cancer growth suppressing gene mda-7 induces apoptosis selectively in human melanoma cells. Oncogene 2002; 21: 708.
63. Saeki T, Mhashilkar A, Swanson X, et al. Inhibition of human lung cancer growth following adenovirus-mediated mda-7 gene expression in vivo. Oncogene 2002; 21: 4558.
64. Cao XX, Mohuiddin I, Chada S, et al. Adenoviral transfer of mda-7 leads to BAX up-regulation and apoptosis in mesothelioma cells, and is abrogated by over-expression of BCL-XL. Mol Med 2002; 8: 869.
65. Sauane M, Gopalkrishnan RV, Sarkar D, et al. MDA-7/IL-24: novel cancer growth suppressing and apoptosis inducing cytokine. Cytokine Growth Factor Rev 2003; 14: 35.
66. Ramesh R, Mhashilkar AM, Tanaka F, et al. Melanoma differentiation-associated gene 7/interleukin (IL)-24 is a novel ligand that regulates angiogenesis via the IL-22 receptor. Cancer Res 2003; 63: 5105.
67. Ellerhorst JA, Prieto VG, Ekmekcioglu S, et al. Loss of MDA-7 expression with progression of melanoma. J Clin Oncol 2002; 20: 1069.
68. Cunningham CC, Chada S, Merritt JA, et al. Clinical and local biological effects of an intratumoral injection of mda-7 (IL24; INGN 241) in patients with advanced carcinoma: a phase I study. Mol Ther 2005; 11: 149.
69. Tong AW, Nemunaitis J, Su D, et al. Intratumoral injection of INGN 241, a nonreplicating adenovector expressing the melanoma-differentiation associated gene-7 (mda-7/IL24): biologic outcome in advanced cancer patients. Mol Titer 2005; 11: 160.
70. Ohshima T, Sato Y. Time-dependent expression of interleukin-10 (IL-10) mRNA during the early phase of skin wound healing as a possible indicator of wound vitality. Int J Legal Med 1998; 111: 251.
71. Sato Y, Ohshima T, Kondo T. Regulatory role of endogenous interleukin-10 in cutaneous inflammatory response of murine wound healing. Biochem Biophys Res Commun 1999; 265: 194.
72. Seifert M, Sterry W, Effenberger E, et al. The antipsoriatic activity of IL-10 is rather caused by effects on peripheral blood cells than by a direct effect on human keratinocytes. Arch Dermatol Res 2000; 292: 164.
73. Seifert M, Gruenberg BH, Sabat R, et al. Keratinocyte unresponsiveness towards interleukin-10: lack of specific binding due to deficient IL-10 receptor 1 expression. Exp Dermatol 2003; 12: 137.
74. Becherel PA, Le Goff L, Ktorza S, et al. Interleukin-10 inhibits IgE-mediated nitric oxide synthase induction and cytokine synthesis in normal human keratinocytes. Eur J Immunol 1995; 25: 2992.
75. Michel G, Gailis A, Jarzebska-Deussen B, et al. 1,25- (OH)2-vitamin D3 and calcipotriol induce IL-10 receptor gene expression in human epidermal cells. Inflamm Res 1997; 46: 32.
76. Grewe M, Gyufko K, Krutmann J. Interleukin-10 production by cultured human keratinocytes: regulation by ultraviolet B and ultraviolet A1 radiation. J Invest Dermatol 1995; 104: 3.
77. Rivas JM, Ullrich SE. Systemic suppression of delayed-type hypersensitivity by supernatants from UV-irradiated keratinocytes. An essential role for keratinocyte-derived IL-10. J Immunol 1992; 149: 3865.
78. Brink N, Szamel M, Young AR, et al. Comparative quantification of IL-1beta, IL-10, IL-10r, TNFalpha and IL-7 mRNA levels in UV-irradiated human skin in vivo. Inflamm Res 2000; 49: 290.
79. Jackson M, Thomson KE, Laker R, et al. Lack of induction of IL-10 expression in human keratinocytes. J Invest Dermatol 1996; 106: 1329.
80. Teunissen MB, Koomen CW, Jansen J, et al. In contrast to their murine counterparts, normal human keratinocytes and human epidermoid cell lines A431 and HaCaT fail to express IL-10 mRNA and protein. Clin Exp Immunol 1997; 107: 213.
81. Ohmen JD, Hanifin JM, Nickoloff BJ, et al. Overexpression of IL-10 in atopic dermatitis. Contrasting cytokine patterns with delayed-type hypersensitivity reactions. J Immunol 1995; 154: 1956.
82. Kruger-Krasagakes S, Krasagakis K, Garbe C, et al. Expression of interleukin 10 in human melanoma. Br J Cancer 1994; 70: 1182.
83. Asadullah K, Docke WD, Haeussler A, et al. Progression of mycosis fungoides is associated with increasing cutaneous expression of interleukin-10 mRNA. J Invest Dermatol 1996; 107: 833.
84. Asadullah K, Sterry W, Stephanek K, et al. IL-10 is a key cytokine in psoriasis. Proof of principle by IL-10 therapy: a new therapeutic approach. J Clin Invest 1998; 101: 783.
85. Broome AM, Ryan D, Eckert RL. S100 protein subcellular localization during epidermal differentiation and psoriasis. J Histochem Cytochem 2003; 51: 675.
86. Glaser R, Harder J, Lange H, et al. Antimicrobial psoriasin (S100A7) protects human skin from Escherichia coli infection. Nat Immunol 2005; 6: 57.
87. Chada S, Mhashilkar AM, Ramesh R, et al. Bystander activity of Ad-mda7: human MDA-7 protein kills melanoma cells via an IL-20 receptor-dependent but STAT3-independent mechanism. Mol Ther 2004; 10: 1085.
88. Soo C, Shaw WW, Freymiller E, et al. Cutaneous rat wounds express c49a, a novel gene with homology to the human melanoma differentiation associated gene, mda-7. J Cell Biochem 1999; 74: 1.
89. Sano S, Itami S, Takeda K, et al. Keratinocyte-specific ablation of Stat3 exhibits impaired skin remodeling, but does not affect skin morphogenesis. EMBO J 1999; 18: 4657.
90. 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: 43.
91. Lebwohl M. Psoriasis. Lancet 2003; 361: 1197.
92. Lew W, Bowcock AM, Krueger JG. Psoriasis vulgaris: cutaneous lymphoid tissue supports T-cell activation and 'Type 1' inflammatory gene expression. Trends Immunol 2004; 25: 295.
93. Gearing AJ, Fincham NJ, Bird CR, et al. Cytokines in skin lesions of psoriasis. Cytokine 1990; 2: 68.
94. Nestle FO, Conrad C. Mechanisms of psoriasis. Drug Discovery Today. Disease Mechanisms 2004; 1: 315.
95. Fierlbeck G, Rassner G, Muller C. Psoriasis induced at the injection site of recombinant interferon gamma. Results of immunohistologic investigations. Arch Dermatol 1990; 126: 351.
96. Grone A. Keratinocytes and cytokines. Vet Immunol Immunopathol 2002; 88: 1.
97. Yawalkar N, Karlen S, Hunger R, et al. Expression of interleukin-12 is increased in psoriatic skin. J Invest Dermatol 1998; 111: 1053.
98. Villadsen LS, Schuurman J, Beurskens F, et al. Resolution of psoriasis upon blockade of IL-15 biological activity in a xenograft mouse model. J Clin Invest 2003; 112: 1571.
99. 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: 125.
100. Nestle FO, Conrad C. The IL-12 family member p40 chain as a master switch and novel therapeutic target in psoriasis. J Invest Dermatol 2004; 123: 14.
101. Ohta Y, Hamada Y, Katsuoka K. Expression of IL-18 in psoriasis. Arch Dermatol Res 2001; 293: 334.
102. Uyemura K, Yamamura M, Fivenson DF, et al. 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: 701.
103. Schlaak JF, Buslau M, Jochum W, et al. T cells involved in psoriasis vulgaris belong to the Th1 subset. J Invest Dermatol 1994; 102: 145.
104. Homey B, Alenius H, Muller A, et al. CCL27-CCR10 interactions regulate T cell-mediated skin inflammation. Nat Med 2002; 8: 157.
105. Homey B. Chemokines and chemokine receptors as targets in the therapy of psoriasis. Curr Drug Targets Inflamm Allergy 2004; 3: 169.
106. Nickoloff BJ, Nestle FO. Recent insights into the immunopathogenesis of psoriasis provide new therapeutic opportunities. J Clin Invest 2004; 113: 1664.
107. Piskin G, Sylva-Steenland RM, Bos JD, et al. T cells in psoriatic lesional skin that survive conventional therapy with NB-UVB radiation display reduced IFN-gamma expression. Arch Dermatol Res 2004; 295: 509.
108. Asadullah K, Docke WD, Ebeling M, et al. Interleukin 10 treatment of psoriasis: clinical results of a phase 2 trial. Arch Dermatol 1999; 135: 187.
109. Reich K, Garbe C, Blaschke V, et al. Response of psoriasis to interleukin-10 is associated with suppression of cutaneous type 1 inflammation, downregulation of the epidermal interleukin-8/CXCR2 pathway and normalization of keratinocyte maturation. J Invest Dermatol 2001; 116: 319.
110. Kimball AB, Kawamura T, Tejura K, et al. Clinical and immunologic assessment of patients with psoriasis in a randomized, double-blind, placebo-controlled trial using recombinant human interleukin 10. Arch Dermatol 2002; 138: 1341.
111. Friedrich M, Docke WD, Klein A, et al. Immunomodulation by interleukin-10 therapy decreases the incidence of relapse and prolongs the relapse-free interval in Psoriasis. J Invest Dermatol 2002; 118: 672.
112. Romer J, Hasselager E, Norby PL, et al. Epidermal overexpression of interleukin-19 and -20 mRNA in psoriatic skin disappears after short-term treatment with cyclosporine a or calcipotriol. J Invest Dermatol 2003; 121: 1306.
113. Ghoreschi K, Thomas P, Breit S, et al. Interleukin-4 therapy of psoriasis induces Th2 responses and improves human autoimmune disease. Nat Med 2003; 9: 40.
114. Kingo K, Koks S, Silm H, et al. IL-10 promoter polymorphisms influence disease severity and course in psoriasis. Genes Immun 2003; 4: 455.
115. Hensen P, Asadullah K, Windemuth C, et al. Interleukin-10 promoter polymorphism IL10.G and familial early onset psoriasis. Br J Dermatol 2003; 149: 381.
116. Crawley E, Isenberg D, Woo P, et al. Interleukin-10 promoter polymorphism and lupus nephritis: comment on the article by Mok et al. Arthritis Rheum 1999; 42: 590.
117. Kingo K, Koks S, Nikopensius T, et al. Polymorphisms in the interleukin-20 gene: relationships to plaque-type psoriasis. Genes Immun 2004; 5: 117.
118. Koks S, Kingo K, Ratsep R, et al. Combined haplotype analysis of the interleukin-19 and -20 genes: relationship to plaque-type psoriasis. Genes Immun 2004; 5: 662.
119. Koks S, Kingo K, Vabrit K, et al. Possible relations between the polymorphisms of the cytokines IL-19, IL-20 and IL-24 and plaque-type psoriasis. Genes Immun 2005; 6: 407.
120. Gottlieb AB. Therapeutic options in the treatment of psoriasis and atopic dermatitis. J Am Acad Dermatol 2005; 53: S3.
121. Chamian F, Lowes MA, Lin S-L, et al. Alefacept reduces infiltrating T cells, activated dendritic cells, and inflammatory genes in psoriasis vulgaris. Proc Natl Acad Sci 2005; USA 102: 2075.
122. Abrams JR, Lebwohl MG, Guzzo CA, et al. CTLA4Ig-mediated blockade of T-cell costimulation in patients with psoriasis vulgaris. J Clin Invest 1999; 103: 1243.
123. Abrams JR, Kelley SL, Hayes E, et al. Blockade of T Lymphocyte Costimulation with Cytotoxic T Lymphocyte-associated Antigen 4-ImmunogIobulin (CTLA4Ig) Reverses the Cellular Pathology of Psoriatic Plaques, Including the Activation of Keratinocytes, Dendritic Cells, and Endothelial Cells. J Exp Med 2000; 192: 681.
124. 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: 595.
125. Chaudhari U, Romano P, Mulcahy LD, et al. Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial. Lancet 2001; 357: 1842.
126. Papp KA, Tyring S, Lahfa M, et al. A global phase III randomized controlled trial of etanercept in psoriasis: safety, efficacy, and effect of dose reduction. Br J Dermatol 2005; 152: 1304.
127. Asadullah K, Friedrich M, Hanneken S, et al. Effects of Systemic Interleukin-10 Therapy on Psoriatic Skin Lesions: Histologic, Immunohistologic, and Molecular Biology Findings. J Invest Dermatol 2001; 116: 721.
128. Trepicchio WL, Ozawa M, Walters IB, et al. Interleukin-11 therapy selectively downregulates type I cytokine proinflammatory pathways in psoriasis lesions. J Clin Invest 1999; 104: 1527.