Psoriasis (Ps) is a chronic, immune-mediated, skin inflammatory disease affecting up to 3% of the population worldwide. Different environmental triggers initiate this complex multifactorial syndrome. Many individuals affected by Ps (6-26%) develop inflammatory disease in other organs, often in the joints as in psoriasis arthritis (PsA). Animal models that reflect the typical Ps syndrome, including both skin and joint pathology as in Ps and PsA, are valuable tools for dissecting disease pathways leading to clinical manifestations. In this context, we developed a new acute Ps and PsA-like disease model that appears after exposure to Saccharomyces cerevisiae mannan in certain mouse strains. The disease was found to be triggered by mannan-activated macrophages, leading to the activation of a pathogenic interleukin-17 pathway involving innate lymphocytes. Interestingly, the production of reactive oxygen species protected the mice from the triggering of this pathway and ameliorated Ps and PsA development.

Keywords:
Psoriasis, Inflammation, Keratinocytes, Mouse models, Reactive oxygen species
1.
Stern RS, Nijsten T, Feldman SR, Margolis DJ, Rolstad T: Psoriasis is common, carries a substantial burden even when not extensive, and is associated with widespread treatment dissatisfaction. J Investig Dermatol Symp Proc 2004;9:136-139.
2.
Fry L, Baker BS: Triggering psoriasis: the role of infections and medications. Clin Dermatol 2007;25:606-615.
3.
Morar N, Willis-Owen SA, Maurer T, Bunker CB: HIV-associated psoriasis: pathogenesis, clinical features, and management. Lancet Infect Dis 2010;10:470-478.
4.
Tsankov N, Angelova I, Kazandjieva J: Drug-induced psoriasis. Recognition and management. Am J Clin Dermatol 2000;1:159-165.
5.
Raychaudhuri SP, Jiang WY, Raychaudhuri SK: Revisiting the Koebner phenomenon: role of NGF and its receptor system in the pathogenesis of psoriasis. Am J Pathol 2008;172:961-971.
6.
Neimann AL, Shin DB, Wang X, Margolis DJ, Troxel AB, Gelfand JM: Prevalence of cardiovascular risk factors in patients with psoriasis. J Am Acad Dermatol 2006;55:829-835.
7.
Picardi A, Abeni D: Stressful life events and skin diseases: disentangling evidence from myth. Psychother Psychosom 2001;70:118-136.
8.
Ni C, Chiu MW: Psoriasis and comorbidities: links and risks. Clin Cosmet Invest Dermatol 2014;7:119-132.
9.
Scarpa R, Soscia E, Peluso R, Atteno M, Manguso F, Del Puente A, Spano A, Sirignano C, Oriente A, Di Minno MN, Iervolino S, Salvatore M: Nail and distal interphalangeal joint in psoriatic arthritis. J Rheumatol 2006;33:1315-1319.
10.
Ritchlin C: Psoriatic disease - from skin to bone. Nat Clin Pract Rheumatol 2007;3:698-706.
11.
Nestle FO, Kaplan DH, Barker J: Psoriasis. N Engl J Med 2009;361:496-509.
12.
Lowes MA, Bowcock AM, Krueger JG: Pathogenesis and therapy of psoriasis. Nature 2007;445:866-873.
13.
Farber EM, Nall ML: The natural history of psoriasis in 5,600 patients. Dermatologica 1974;148:1-18.
14.
Johnson-Huang LM, Lowes MA, Krueger JG: Putting together the psoriasis puzzle: an update on developing targeted therapies. Dis Model Mech 2012;5:423-433.
15.
Trembath RC, Clough RL, Rosbotham JL, Jones AB, Camp RD, Frodsham A, Browne J, Barber R, Terwilliger J, Lathrop GM, Barker JN: Identification of a major susceptibility locus on chromosome 6p and evidence for further disease loci revealed by a two-stage genome-wide search in psoriasis. Hum Mol Genet 1997;6:813-820.
16.
Capon F, Munro M, Barker J, Trembath R: Searching for the major histocompatibility complex psoriasis susceptibility gene. J Invest Dermatol 2002;118:745-751.
17.
Nair RP, Stuart PE, Nistor I, Hiremagalore R, Chia NV, Jenisch S, Weichenthal M, Abecasis GR, Lim HW, Christophers E, Voorhees JJ, Elder JT: Sequence and haplotype analysis supports HLA-C as the psoriasis susceptibility 1 gene. Am J Hum Genet 2006;78:827-851.
18.
Henseler T, Christophers E: Psoriasis of early and late onset: characterization of two types of psoriasis vulgaris. J Am Acad Dermatol 1985;13:450-456.
19.
Patel RV, Lebwohl M: In the clinic. Psoriasis. Ann Intern Med 2011;155:ITC2-1−ICT2-15; quiz ITC12-16.
20.
Henseler T: The genetics of psoriasis. J Am Acad Dermatol 1997;37:S1-S11.
21.
Levine D, Gottlieb A: Evaluation and management of psoriasis: an internist's guide. Med Clin North Am 2009;93:1291-1303.
22.
Gudjonsson JE, Karason A, Antonsdottir AA, Runarsdottir EH, Gulcher JR, Stefansson K, Valdimarsson H: HLA-Cw6-positive and HLA-Cw6-negative patients with psoriasis vulgaris have distinct clinical features. J Invest Dermatol 2002;118:362-365.
23.
Mallon E, Bunce M, Savoie H, Rowe A, Newson R, Gotch F, Bunker CB: HLA-C and guttate psoriasis. Br J Dermatol 2000;143:1177-1182.
24.
Marrakchi S, Guigue P, Renshaw BR, Puel A, Pei XY, Fraitag S, Zribi J, Bal E, Cluzeau C, Chrabieh M, Towne JE, Douangpanya J, Pons C, Mansour S, Serre V, Makni H, Mahfoudh N, Fakhfakh F, Bodemer C, Feingold J, Hadj-Rabia S, Favre M, Genin E, Sahbatou M, Munnich A, Casanova JL, Sims JE, Turki H, Bachelez H, Smahi A: Interleukin-36-receptor antagonist deficiency and generalized pustular psoriasis. New Engl J Med 2011;365:620-628.
25.
Capon F, Di Meglio P, Szaub J, Prescott NJ, Dunster C, Baumber L, Timms K, Gutin A, Abkevic V, Burden AD, Lanchbury J, Barker JN, Trembath RC, Nestle FO: Sequence variants in the genes for the interleukin-23 receptor (IL23R) and its ligand (IL12B) confer protection against psoriasis. Hum Genet 2007;122:201-206.
26.
Sonkoly E, Wei T, Janson PC, Saaf A, Lundeberg L, Tengvall-Linder M, Norstedt G, Alenius H, Homey B, Scheynius A, Stahle M, Pivarcsi A: MicroRNAs: novel regulators involved in the pathogenesis of psoriasis? PLoS One 2007;2:e610.
27.
Xu N, Brodin P, Wei T, Meisgen F, Eidsmo L, Nagy N, Kemeny L, Stahle M, Sonkoly E, Pivarcsi A: MiR-125b, a microRNA downregulated in psoriasis, modulates keratinocyte proliferation by targeting FGFR2. J Invest Dermatol 2011;131:1521-1529.
28.
Ichihara A, Jinnin M, Yamane K, Fujisawa A, Sakai K, Masuguchi S, Fukushima S, Maruo K, Ihn H: MicroRNA-mediated keratinocyte hyperproliferation in psoriasis vulgaris. Br J Dermatol 2011;165:1003-1010.
29.
Lerman G, Avivi C, Mardoukh C, Barzilai A, Tessone A, Gradus B, Pavlotsky F, Barshack I, Polak-Charcon S, Orenstein A, Hornstein E, Sidi Y, Avni D: MiRNA expression in psoriatic skin: reciprocal regulation of hsa-miR-99a and IGF-1R. PLoS One 2011;6:e20916.
30.
Meisgen F, Xu N, Wei T, Janson PC, Obad S, Broom O, Nagy N, Kauppinen S, Kemeny L, Stahle M, Pivarcsi A, Sonkoly E: MiR-21 is up-regulated in psoriasis and suppresses T cell apoptosis. Exp Dermatol 2012;21:312-314.
31.
Xu N, Meisgen F, Butler LM, Han G, Wang XJ, Soderberg-Naucler C, Stahle M, Pivarcsi A, Sonkoly E: MicroRNA-31 is overexpressed in psoriasis and modulates inflammatory cytokine and chemokine production in keratinocytes via targeting serine/threonine kinase 40. J Immunol 2013;190:678-688.
32.
Prey S, Paul C, Bronsard V, Puzenat E, Gourraud PA, Aractingi S, Aubin F, Bagot M, Cribier B, Joly P, Jullien D, Maitre ML, Richard-Lallemand MA, Ortonne JP: Assessment of risk of psoriatic arthritis in patients with plaque psoriasis: a systematic review of the literature. J Eur Acad Dermatol Venereol 2010;24(suppl 2):31-35.
33.
Coates LC, Conaghan PG, Emery P, Green MJ, Ibrahim G, MacIver H, Helliwell PS: Sensitivity and specificity of the classification of psoriatic arthritis criteria in early psoriatic arthritis. Arthritis Rheum 2012;64:3150-3155.
34.
Moll JM, Wright V: Psoriatic arthritis. Semin Arthritis Rheum 1973;3:55-78.
35.
Eder L, Chandran V, Pellett F, Shanmugarajah S, Rosen CF, Bull SB, Gladman DD: Differential human leucocyte allele association between psoriasis and psoriatic arthritis: a family-based association study. Ann Rheum Dis 2012;71:1361-1365.
36.
Winchester R, Minevich G, Steshenko V, Kirby B, Kane D, Greenberg DA, FitzGerald O: HLA associations reveal genetic heterogeneity in psoriatic arthritis and in the psoriasis phenotype. Arthritis Rheum 2012;64:1134-1144.
37.
Pollock R, Chandran V, Barrett J, Eder L, Pellett F, Yao C, Lino M, Shanmugarajah S, Farewell VT, Gladman DD: Differential major histocompatibility complex class I chain-related A allele associations with skin and joint manifestations of psoriatic disease. Tissue Antigens 2011;77:554-561.
38.
Chandran V: Time to event and progressive multi-state analyses confirm the association between human leukocyte antigen alleles and the development of arthritis mutilans in patients with psoriatic arthritis. Proceedings of the 3rd World Congress of Psoriasis and Psoriatic Arthritis, Stockholm, June 2012.
39.
Murdaca G, Gulli R, Spano F, Lantieri F, Burlando M, Parodi A, Mandich P, Puppo F: TNF-alpha gene polymorphisms: association with disease susceptibility and response to anti-TNF-alpha treatment in psoriatic arthritis. J Invest Dermatol 2014;134:2503-2509.
40.
Pollock RA, Abji F, Liang K, Chandran V, Pellett FJ, Virtanen C, Gladman DD: Gene expression differences between psoriasis patients with and without inflammatory arthritis. J Invest Dermatol 2015;135:620-623.
41.
Holmdahl R, Jansson L, Andersson M, Jonsson R: Genetic, hormonal and behavioural influence on spontaneously developing arthritis in normal mice. Clin Exp Immunol 1992;88:467-472.
42.
Corthay A, Hansson AS, Holmdahl R: T lymphocytes are not required for the spontaneous development of entheseal ossification leading to marginal ankylosis in the DBA/1 mouse. Arthritis Rheum 2000;43:844-851.
43.
Sundberg JP, Beamer WG, Shultz LD, Dunstan RW: Inherited mouse mutations as models of human adnexal, cornification, and papulosquamous dermatoses. J Invest Dermatol 1990;95:62S-63S.
44.
Sundberg JP, France M, Boggess D, Sundberg BA, Jenson AB, Beamer WG, Shultz LD: Development and progression of psoriasiform dermatitis and systemic lesions in the flaky skin (FSN) mouse mutant. Pathobiology 1997;65:271-286.
45.
HogenEsch H, Gijbels MJ, Offerman E, van Hooft J, van Bekkum DW, Zurcher C: A spontaneous mutation characterized by chronic proliferative dermatitis in C57BL mice. Am J Pathol 1993;143:972-982.
46.
Kauffman CL, Aria N, Toichi E, McCormick TS, Cooper KD, Gottlieb AB, Everitt DE, Frederick B, Zhu Y, Graham MA, Pendley CE, Mascelli MA: A phase I study evaluating the safety, pharmacokinetics, and clinical response of a human IL-12 p40 antibody in subjects with plaque psoriasis. J Invest Dermatol 2004;123:1037-1044.
47.
Sano S, Chan KS, Carbajal S, Clifford J, Peavey M, Kiguchi K, Itami S, Nickoloff BJ, DiGiovanni J: Stat3 links activated keratinocytes and immunocytes required for development of psoriasis in a novel transgenic mouse model. Nat Med 2005;11:43-49.
48.
Wang H, Peters T, Sindrilaru A, Kess D, Oreshkova T, Yu XZ, Seier AM, Schreiber H, Wlaschek M, Blakytny R, Rohrbein J, Schulz G, Weiss JM, Scharffetter-Kochanek K: TGF-beta-dependent suppressive function of Tregs requires wild-type levels of CD18 in a mouse model of psoriasis. J Clin Invest 2008;118:2629-2639.
49.
Bullard DC, Scharffetter-Kochanek K, McArthur MJ, Chosay JG, McBride ME, Montgomery CA, Beaudet AL: A polygenic mouse model of psoriasiform skin disease in CD18-deficient mice. Proc Nat Acad Sci USA 1996;93:2116-2121.
50.
Kess D, Peters T, Zamek J, Wickenhauser C, Tawadros S, Loser K, Varga G, Grabbe S, Nischt R, Sunderkotter C, Muller W, Krieg T, Scharffetter-Kochanek K: CD4+ T cell-associated pathophysiology critically depends on CD18 gene dose effects in a murine model of psoriasis. J Immunol 2003;171:5697-5706.
51.
Zenz R, Eferl R, Kenner L, Florin L, Hummerich L, Mehic D, Scheuch H, Angel P, Tschachler E, Wagner EF: Psoriasis-like skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 2005;437:369-375.
52.
Bardos T, Zhang J, Mikecz K, David CS, Glant TT: Mice lacking endogenous major histocompatibility complex class II develop arthritis resembling psoriatic arthritis at an advanced age. Arthritis Rheum 2002;46:2465-2475.
53.
Detmar M, Brown LF, Schon MP, Elicker BM, Velasco P, Richard L, Fukumura D, Monsky W, Claffey KP, Jain RK: Increased microvascular density and enhanced leukocyte rolling and adhesion in the skin of VEGF transgenic mice. J Invest Dermatol 1998;111:1-6.
54.
Pasparakis M, Courtois G, Hafner M, Schmidt-Supprian M, Nenci A, Toksoy A, Krampert M, Goebeler M, Gillitzer R, Israel A, Krieg T, Rajewsky K, Haase I: TNF-mediated inflammatory skin disease in mice with epidermis-specific deletion of IKK2. Nature 2002;417:861-866.
55.
Danilenko DM: Review paper: preclinical models of psoriasis. Vet Pathol 2008;45:563-575.
56.
Cook PW, Piepkorn M, Clegg CH, Plowman GD, DeMay JM, Brown JR, Pittelkow MR: Transgenic expression of the human amphiregulin gene induces a psoriasis-like phenotype. J Clin Invest 1997;100:2286-2294.
57.
Croxford AL, Karbach S, Kurschus FC, Wortge S, Nikolaev A, Yogev N, Klebow S, Schuler R, Reissig S, Piotrowski C, Brylla E, Bechmann I, Scheller J, Rose-John S, Wunderlich FT, Munzel T, von Stebut E, Waisman A: IL-6 regulates neutrophil microabscess formation in IL-17A-driven psoriasiform lesions. J Invest Dermatol 2014;134:728-735.
58.
Cook PW, Brown JR, Cornell KA, Pittelkow MR: Suprabasal expression of human amphiregulin in the epidermis of transgenic mice induces a severe, early-onset, psoriasis-like skin pathology: expression of amphiregulin in the basal epidermis is also associated with synovitis. Exp Dermatol 2004;13:347-356.
59.
van der Fits L, Mourits S, Voerman JS, Kant M, Boon L, Laman JD, Cornelissen F, Mus AM, Florencia E, Prens EP, Lubberts E: Imiquimod-induced psoriasis-like skin inflammation in mice is mediated via the IL-23/IL-17 axis. J Immunol 2009;182:5836-5845.
60.
El Malki K, Karbach SH, Huppert J, Zayoud M, Reissig S, Schuler R, Nikolaev A, Karram K, Munzel T, Kuhlmann CR, Luhmann HJ, von Stebut E, Wortge S, Kurschus FC, Waisman A: An alternative pathway of imiquimod-induced psoriasis-like skin inflammation in the absence of interleukin-17 receptor A signaling. J Invest Dermatol 2013;133:441-451.
61.
Shibata S, Tada Y, Asano Y, Yanaba K, Sugaya M, Kadono T, Kanda N, Watanabe S, Sato S: IL-27 activates Th1-mediated responses in imiquimod-induced psoriasis-like skin lesions. J Invest Dermatol 2013;133:479-488.
62.
Yoshiki R, Kabashima K, Honda T, Nakamizo S, Sawada Y, Sugita K, Yoshioka H, Ohmori S, Malissen B, Tokura Y, Nakamura M: IL-23 from Langerhans cells is required for the development of imiquimod-induced psoriasis-like dermatitis by induction of IL-17A-producing gammadelta T cells. J Invest Dermatol 2014;134:1912-1921.
63.
Khmaladze I, Kelkka T, Guerard S, Wing K, Pizzolla A, Saxena A, Lundqvist K, Holmdahl M, Nandakumar KS, Holmdahl R: Mannan induces ROS-regulated, IL-17A-dependent psoriasis arthritis-like disease in mice. Proc Nat Acad Sci USA 2014;111:E3669-E3678.
64.
Gudjonsson JE, Johnston A, Dyson M, Valdimarsson H, Elder JT: Mouse models of psoriasis. J Invest Dermatol 2007;127:1292-1308.
65.
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;199:731-736.
66.
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;174:3695-3702.
67.
van den Bogaard EH, Tjabringa GS, Joosten I, Vonk-Bergers M, van Rijssen E, Tijssen HJ, Erkens M, Schalkwijk J, Koenen HJ: Crosstalk between keratinocytes and T cells in a 3D microenvironment: a model to study inflammatory skin diseases. J Invest Dermatol 2014;134:719-727.
68.
Taniguchi K, Arima K, Masuoka M, Ohta S, Shiraishi H, Ontsuka K, Suzuki S, Inamitsu M, Yamamoto K, Simmons O, Toda S, Conway SJ, Hamasaki Y, Izuhara K: Periostin controls keratinocyte proliferation and differentiation by interacting with the paracrine IL-1alpha/IL-6 loop. J Invest Dermatol 2014;134:1295-1304.
69.
Miller LS, Modlin RL: Human keratinocyte Toll-like receptors promote distinct immune responses. J Invest Dermatol 2007;127:262-263.
70.
Buchau AS, Gallo RL: Innate immunity and antimicrobial defense systems in psoriasis. Clin Dermatol 2007;25:616-624.
71.
Nestle FO, Di Meglio P, Qin JZ, Nickoloff BJ: Skin immune sentinels in health and disease. Nat Rev Immunol 2009;9:679-691.
72.
Witte E, Kokolakis G, Witte K, Philipp S, Doecke WD, Babel N, Wittig BM, Warszawska K, Kurek A, Erdmann-Keding M, Kunz S, Asadullah K, Kadin ME, Volk HD, Sterry W, Wolk K, Sabat R: IL-19 is a component of the pathogenetic IL-23/IL-17 cascade in psoriasis. J Invest Dermatol 2014;134:2757-2767.
73.
Johnston A, Fritz Y, Dawes SM, Diaconu D, Al-Attar PM, Guzman AM, Chen CS, Fu W, Gudjonsson JE, McCormick TS, Ward NL: Keratinocyte overexpression of IL-17C promotes psoriasiform skin inflammation. J Immun 2013;190:2252-2262.
74.
Kemeny L, Ruzicka T, Dobozy A, Michel G: Role of interleukin-8 receptor in skin. Int Arch Allergy Immunol 1994;104:317-322.
75.
Skoglund C, Scheynius A, Holmdahl R, Van der Meide PH: Enhancement of DTH reaction and inhibition of the expression of class II transplantation antigens by in vivo treatment with antibodies against gamma-interferon. Clin Exp Immunol 1988;71:428-432.
76.
Mosser DM, Edwards JP: Exploring the full spectrum of macrophage activation. Nat Rev Immunol 2008;8:958-969.
77.
Wang CQ, Suarez-Farinas M, Nograles KE, Mimoso CA, Shrom D, Dow ER, Heffernan MP, Hoffman RW, Krueger JG: IL-17 induces inflammation-associated gene products in blood monocytes, and treatment with ixekizumab reduces their expression in psoriasis patient blood. J Invest Dermatol 2014;134:2990-2993.
78.
Wang H, Peters T, Kess D, Sindrilaru A, Oreshkova T, Van Rooijen N, Stratis A, Renkl AC, Sunderkotter C, Wlaschek M, Haase I, Scharffetter-Kochanek K: Activated macrophages are essential in a murine model for T cell-mediated chronic psoriasiform skin inflammation. J Clin Invest 2006;116:2105-2114.
79.
Stratis A, Pasparakis M, Rupec RA, Markur D, Hartmann K, Scharffetter-Kochanek K, Peters T, van Rooijen N, Krieg T, Haase I: Pathogenic role for skin macrophages in a mouse model of keratinocyte-induced psoriasis-like skin inflammation. J Clin Invest 2006;116:2094-2104.
80.
Yawalkar N, Tscharner GG, Hunger RE, Hassan AS: Increased expression of IL-12p70 and IL-23 by multiple dendritic cell and macrophage subsets in plaque psoriasis. J Dermatol Sci 2009;54:99-105.
81.
Sabat R, Philipp S, Hoflich C, Kreutzer S, Wallace E, Asadullah K, Volk HD, Sterry W, Wolk K: Immunopathogenesis of psoriasis. Exp Dermatol 2007;16:779-798.
82.
Lin AM, Rubin CJ, Khandpur R, Wang JY, Riblett M, Yalavarthi S, Villanueva EC, Shah P, Kaplan MJ, Bruce AT: Mast cells and neutrophils release IL-17 through extracellular trap formation in psoriasis. J Immunol 2011;187:490-500.
83.
Zaba LC, Krueger JG, Lowes MA: Resident and ‘inflammatory' dendritic cells in human skin. J Invest Dermatol 2009;129:302-308.
84.
Lande R, Gregorio J, Facchinetti V, Chatterjee B, Wang YH, Homey B, Cao W, Wang YH, Su B, Nestle FO, Zal T, Mellman I, Schroder JM, Liu YJ, Gilliet M: Plasmacytoid dendritic cells sense self-DNA coupled with antimicrobial peptide. Nature 2007;449:564-569.
85.
Ganguly D, Chamilos G, Lande R, Gregorio J, Meller S, Facchinetti V, Homey B, Barrat FJ, Zal T, Gilliet M: Self-RNA-antimicrobial peptide complexes activate human dendritic cells through TLR7 and TLR8. J Exp Med 2009;206:1983-1994.
86.
Chamian F, Lowes MA, Lin SL, Lee E, Kikuchi T, Gilleaudeau P, Sullivan-Whalen M, Cardinale I, Khatcherian A, Novitskaya I, Wittkowski KM, Krueger JG: Alefacept reduces infiltrating T cells, activated dendritic cells, and inflammatory genes in psoriasis vulgaris. Proc Nat Acad Sci USA 2005;102:2075-2080.
87.
Sumaria N, Roediger B, Ng LG, Qin J, Pinto R, Cavanagh LL, Shklovskaya E, Fazekas de St Groth B, Triccas JA, Weninger W: Cutaneous immunosurveillance by self-renewing dermal gammadelta T cells. J Exp Med 2011;208:505-518.
88.
Gray EE, Suzuki K, Cyster JG: Cutting edge: Identification of a motile IL-17-producing gammadelta T cell population in the dermis. J Immunol 2011;186:6091-6095.
89.
Cai Y, Shen X, Ding C, Qi C, Li K, Li X, Jala VR, Zhang HG, Wang T, Zheng J, Yan J: Pivotal role of dermal IL-17-producing gammadelta T cells in skin inflammation. Immunity 2011;35:596-610.
90.
Bouchaud G, Gehrke S, Krieg C, Kolios A, Hafner J, Navarini AA, French LE, Boyman O: Epidermal IL-15Ralpha acts as an endogenous antagonist of psoriasiform inflammation in mouse and man. J Exp Med 2013;210:2105-2117.
91.
Mabuchi T, Singh TP, Takekoshi T, Jia GF, Wu X, Kao MC, Weiss I, Farber JM, Hwang ST: CCR6 is required for epidermal trafficking of gammadelta-T cells in an IL-23-induced model of psoriasiform dermatitis. J Invest Dermatol 2013;133:164-171.
92.
Christophers E: The immunopathology of psoriasis. Int Arch Allergy Immunol 1996;110:199-206.
93.
Gottlieb SL, Gilleaudeau P, Johnson R, Estes L, Woodworth TG, Gottlieb AB, Krueger JG: Response of psoriasis to a lymphocyte-selective toxin (DAB389IL-2) suggests a primary immune, but not keratinocyte, pathogenic basis. Nat Med 1995;1:442-447.
94.
Ellis CN, Gorsulowsky DC, Hamilton TA, Billings JK, Brown MD, Headington JT, Cooper KD, Baadsgaard O, Duell EA, Annesley TM, et al: Cyclosporine improves psoriasis in a double-blind study. JAMA 1986;256:3110-3116.
95.
Lee E, Trepicchio WL, Oestreicher JL, Pittman D, Wang F, Chamian F, Dhodapkar M, Krueger JG: Increased expression of interleukin 23 p19 and p40 in lesional skin of patients with psoriasis vulgaris. J Exp Med 2004;199:125-130.
96.
Narita M, Nishizawa Y, Iwaya S, Oiwa E, Iwabuchi M, Uchiyama T, Matsuyama A, Masuko M, Takahashi M: Ustekinumab improves psoriasis without suppressing tumor antigen-specific cytotoxic T lymphocytes. Int Arch Allergy Immunol 2014;165:52-60.
97.
Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C: A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol 2005;6:1133-1141.
98.
Volpe E, Servant N, Zollinger R, Bogiatzi SI, Hupe P, Barillot E, Soumelis V: A critical function for transforming growth factor-beta, interleukin 23 and proinflammatory cytokines in driving and modulating human T(h)-17 responses. Nat Immunol 2008;9:650-657.
99.
Rizzo HL, Kagami S, Phillips KG, Kurtz SE, Jacques SL, Blauvelt A: IL-23-mediated psoriasis-like epidermal hyperplasia is dependent on IL-17A. J Immunol 2011;186:1495-1502.
100.
Cosmi L, Liotta F, Maggi E, Romagnani S, Annunziato F: Th17 and non-classic Th1 cells in chronic inflammatory disorders: two sides of the same coin. Int Arch Allergy Immunol 2014;164:171-177.
101.
Wolk K, Haugen HS, Xu W, Witte E, Waggie K, Anderson M, Vom Baur E, Witte K, Warszawska K, Philipp S, Johnson-Leger C, Volk HD, Sterry W, Sabat R: IL-22 and IL-20 are key mediators of the epidermal alterations in psoriasis while IL-17 and IFN-gamma are not. J Mol Med (Berl) 2009;87:523-536.
102.
Zheng Y, Danilenko DM, Valdez P, Kasman I, Eastham-Anderson J, Wu J, Ouyang W: Interleukin-22, a T(h)17 cytokine, mediates IL-23-induced dermal inflammation and acanthosis. Nature 2007;445:648-651.
103.
Van Belle AB, de Heusch M, Lemaire MM, Hendrickx E, Warnier G, Dunussi-Joannopoulos K, Fouser LA, Renauld JC, Dumoutier L: IL-22 is required for imiquimod-induced psoriasiform skin inflammation in mice. J Immunol 2012;188:462-469.
104.
Krueger JG: Hiding under the skin: a welcome surprise in psoriasis. Nat Med 2012;18:1750-1751.
105.
Schlapbach C, Gehad A, Yang C, Watanabe R, Guenova E, Teague JE, Campbell L, Yawalkar N, Kupper TS, Clark RA: Human Th9 cells are skin-tropic and have autocrine and paracrine proinflammatory capacity. Sci Transl Med 2014;6:219ra218.
106.
Bedard K, Krause KH: The NOX family of ROS-generating NADPH oxidases: physiology and pathophysiology. Physiol Rev 2007;87:245-313.
107.
Hancock JT, Desikan R, Neill SJ: Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 2001;29:345-350.
108.
Zhou Q, Mrowietz U, Rostami-Yazdi M: Oxidative stress in the pathogenesis of psoriasis. Free Radic Biol Med 2009;47:891-905.
109.
Berendes H, Bridges RA, Good RA: A fatal granulomatosus of childhood: the clinical study of a new syndrome. Minn Med 1957;40:309-312.
110.
Quie PG, White JG, Holmes B, Good RA: In vitro bactericidal capacity of human polymorphonuclear leukocytes: diminished activity in chronic granulomatous disease of childhood. J Clin Invest 1967;46:668-679.
111.
Baehner RL, Nathan DG: Leukocyte oxidase: defective activity in chronic granulomatous disease. Science 1967;155:835-836.
112.
van den Berg JM, van Koppen E, Ahlin A, Belohradsky BH, Bernatowska E, Corbeel L, Espanol T, Fischer A, Kurenko-Deptuch M, Mouy R, Petropoulou T, Roesler J, Seger R, Stasia MJ, Valerius NH, Weening RS, Wolach B, Roos D, Kuijpers TW: Chronic granulomatous disease: the European experience. PLoS One 2009;4:e5234.
113.
Matute JD, Arias AA, Wright NA, Wrobel I, Waterhouse CC, Li XJ, Marchal CC, Stull ND, Lewis DB, Steele M, Kellner JD, Yu W, Meroueh SO, Nauseef WM, Dinauer MC: A new genetic subgroup of chronic granulomatous disease with autosomal recessive mutations in p40 phox and selective defects in neutrophil NADPH oxidase activity. Blood 2009;114:3309-3315.
114.
Wagener FA, Carels CE, Lundvig DM: Targeting the redox balance in inflammatory skin conditions. Int J Mol Sci 2013;14:9126-9167.
115.
Ortonne JP: Aetiology and pathogenesis of psoriasis. Br J Dermatol 1996;135(suppl 49):1-5.
116.
Raynaud F, Evain-Brion D, Gerbaud P, Marciano D, Gorin I, Liapi C, Anderson WB: Oxidative modulation of cyclic AMP-dependent protein kinase in human fibroblasts: possible role in psoriasis. Free Radic Biol Med 1997;22:623-632.
117.
Turner CP, Toye AM, Jones OT: Keratinocyte superoxide generation. Free Radic Biol Med 1998;24:401-407.
118.
Vignais PV: The superoxide-generating NADPH oxidase: structural aspects and activation mechanism. Cell Mol Life Sci: CMLS 2002;59:1428-1459.
119.
Babior BM, Lambeth JD, Nauseef W: The neutrophil NADPH oxidase. Arch Biochem Biophys 2002;397:342-344.
120.
Nauseef WM: Biological roles for the NOX family NADPH oxidases. J Biol Chem 2008;283:16961-16965.
121.
McCann SK, Roulston CL: NADPH oxidase as a therapeutic target for neuroprotection against ischaemic stroke: future perspectives. Brain Sci 2013;3:561-598.
122.
Therond P, Gerbaud P, Dimon S, Anderson WB, Evain-Broin D, Raynaud F: antioxidant enzymes in psoriatic fibroblasts and erythrocytes. J Invest Dermatol 1996;106:1325-1328.
123.
Yildirim M, Inaloz HS, Baysal V, Delibas N: The role of oxidants and antioxidants in psoriasis. J Eur Acad Dermatol Venereol 2003;17:34-36.
124.
Dogan P, Soyuer U, Tanrikulu G: Superoxide dismutase and myeloperoxidase activity in polymorphonuclear leukocytes and serum ceruloplasmin and copper levels in psoriasis. Br J Dermatol 1989;120:239-244.
125.
Utas S, Kose K, Yazici C, Akdas A, Kelestimur F: Antioxidant potential of propylthiouracil in patients with psoriasis. Clin Biochem 2002;35:241-246.
126.
Lee YS, Cheon IS, Kim BH, Kwon MJ, Lee HW, Kim TY: Loss of extracellular superoxide dismutase induces severe IL-23-mediated skin inflammation in mice. J Invest Dermatol 2013;133:732-741.
127.
Baek JO, Byamba D, Wu WH, Kim TG, Lee MG: Assessment of an imiquimod-induced psoriatic mouse model in relation to oxidative stress. Arch Dermatol Res 2012;304:699-706.
128.
Pastore S, Mariani V, Lulli D, Gubinelli E, Raskovic D, Mariani S, Stancato A, de Luca C, Pecorelli A, Valacchi G, Potapovich AI, Kostyuk VA, Korkina LG: Glutathione peroxidase activity in the blood cells of psoriatic patients correlates with their responsiveness to efalizumab. Free Radic Res 2011;45:585-599.
129.
Seifert O, Holmberg J, Linnarsson BM: Decreased activity of neutrophil glutathione peroxidase in chronic plaque-type psoriasis. J Am Acad Dermatol 2007;57:528-529.
130.
Polkanov VS, Bochkarev IuM, Shmeleva LT, Kipper SN: Lipid peroxidation and the blood antioxidant activity in psoriasis (in Russian). Vestn Dermatol Venerol 1987;7:42-46.
131.
Kim H-R: Attenuation of experimental colitis in glutathione peroxidase 1 and catalase double knockout mice through enhancing regulatory T cell function. PLoS One 2014;17:e95332.
132.
Won HY, Sohn JH, Min HJ, Lee K, Woo HA, Ho YS, Park JW, Rhee SG, Hwang ES: Glutathione peroxidase 1 deficiency attenuates allergen-induced airway inflammation by suppressing Th2 and Th17 cell development. Antioxid Redox Signal 2010;13:575-587.
133.
Won HY, Jang EJ, Lee K, Oh S, Kim HK, Woo HA, Kang SW, Yu DY, Rhee SG, Hwang ES: Ablation of peroxiredoxin II attenuates experimental colitis by increasing FoxO1-induced Foxp3+ regulatory T cells. J Immunol 2013;191:4029-4037.
134.
Rodrigues-Sousa T, Ladeirinha AF, Santiago AR, Carvalheiro H, Raposo B, Alarcao A, Cabrita A, Holmdahl R, Carvalho L, Souto-Carneiro MM: Deficient production of reactive oxygen species leads to severe chronic DSS-induced colitis in Ncf1/p47phox-mutant mice. PLoS One 2014;9:e97532.
135.
Hultqvist M, Olofsson P, Holmberg J, Backstrom BT, Tordsson J, Holmdahl R: Enhanced autoimmunity, arthritis, and encephalomyelitis in mice with a reduced oxidative burst due to a mutation in the Ncf1 gene. Proc Nat Acad Sci USA 2004;101:12646-12651.
136.
Olofsson P, Holmberg J, Tordsson J, Lu S, Akerstrom B, Holmdahl R: Positional identification of Ncf1 as a gene that regulates arthritis severity in rats. Nat Genet 2003;33:25-32.
137.
Gelderman KA, Hultqvist M, Holmberg J, Olofsson P, Holmdahl R: T cell surface redox levels determine T cell reactivity and arthritis susceptibility. Proc Nat Acad Sci USA 2006;103:12831-12836.
138.
Gelderman KA, Hultqvist M, Pizzolla A, Zhao M, Nandakumar KS, Mattsson R, Holmdahl R: Macrophages suppress T cell responses and arthritis development in mice by producing reactive oxygen species. J Clin Invest 2007;117:3020-3028.
139.
Efimova O, Szankasi P, Kelley TW: Ncf1 (p47phox) is essential for direct regulatory T cell mediated suppression of CD4+ effector T cells. PLoS One 2011;6:e16013.
140.
Kim H-R: Reactive oxygen species prevent imiquimod-induced psoriatic dermatitis through enhancing regulatory T cell function. PLoS One 2014;9:e91146.
141.
Thom SR: Experimental use of hyperbaric oxygen therapy. J Emerg Med 1985;3:65.
142.
Butler G, Michaels JC, Al-Waili N, Finkelstein M, Allen M, Petrillo R, Carrey Z, Kolanuvada B, Lee BY, Riera AG, Michaels CC, Urteaga G: Therapeutic effect of hyperbaric oxygen in psoriasis vulgaris: two case reports and a review of the literature. J Med Case Rep 2009;3:7023.
143.
Furuhashi T, Saito C, Torii K, Nishida E, Yamazaki S, Morita A: Photo(chemo)therapy reduces circulating Th17 cells and restores circulating regulatory T cells in psoriasis. PLoS One 2013;8:e54895.
144.
Briganti S, Wlaschek M, Hinrichs C, Bellei B, Flori E, Treiber N, Iben S, Picardo M, Scharffetter-Kochanek K: Small molecular antioxidants effectively protect from PUVA-induced oxidative stress responses underlying fibroblast senescence and photoaging. Free Radic Biol Med 2008;45:636-644.
145.
Deffert C, Carnesecchi S, Yuan H, Rougemont AL, Kelkka T, Holmdahl R, Krause KH, Schappi MG: Hyperinflammation of chronic granulomatous disease is abolished by NOX2 reconstitution in macrophages and dendritic cells. J Pathol 2012;228:341-350.
146.
Foerster J, Storch A, Fleischanderl S, Wittstock S, Pfeiffer S, Riemekasten G, Worm M: Neutrophil respiratory burst is decreased in scleroderma and normalized by near-infrared mediated hyperthermia. Clin Exp Dermatol 2006;31:799-806.
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2015
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