Current understanding of the genetic basis of psoriasis

Expert Review of Clinical Immunology

Volumn 5, Issue 4, 2009, Pages 433-443

  Gudjonsson, Johann E ^a   Johnston, Andrew ^a  

^a UNIVERSITY OF MICHIGAN HEALTH SYSTEM   (United States)

Author keywords

IL 23 axis; Innate immunity; Psoriasis; Skin barrier; Th17

Indexed keywords

CYTOKINE; CYTOKINE RECEPTOR; GAMMA INTERFERON; INTERLEUKIN 12; INTERLEUKIN 22; INTERLEUKIN 23; INTERLEUKIN 23 RECEPTOR;

CHRONIC DISEASE; CLINICAL FEATURE; CYTOKINE PRODUCTION; DISEASE ASSOCIATION; DISEASE PREDISPOSITION; GENE LOCUS; GENETIC LINKAGE; GENETIC SUSCEPTIBILITY; GENOME; GENOME WIDE ASSOCIATION STUDIES; HLA SYSTEM; HUMAN; INFLAMMATION; INNATE IMMUNITY; NONHUMAN; PATHOGENESIS; PSORIASIS; PSORIATIC ARTHRITIS; REVIEW; RHEUMATOID ARTHRITIS; SKIN; SKIN DISEASE; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE; T LYMPHOCYTE SUBPOPULATION; TH17 CELL;

EID: 77649147195     PISSN: 1744666X     EISSN: None     Source Type: Journal    
DOI: 10.1586/eci.09.13     Document Type: Review

References (109)

1. Hoede K. The problem of heredity of soriasis. Hautarzt. 8(10), 433-438 (1957).
2. Farber EM, Nall ML, Watson W. Natural history of psoriasis in 61 twin pairs. Arch. Dermatol. 109(2), 207-211 (1974).
3. Brandrup F, Holm N, Grunnet N, Henningsen K, Hansen HE. Psoriasis in monozygotic twins: variations in expression in individuals with identical genetic constitution. Acta Derm. Venereol. 62(3), 229-236 (1982).
4. Duffy DL, Spelman LS, Martin NG. Psoriasis in Australian twins. J. Am. Acad. Dermatol. 29(3), 428-434 (1993).
5. Gudjonsson JE, Elder JT. Psoriasis: epidemiology. Clin. Dermatol. 25(6), 535-546 (2007).
6. Andressen C, Henseler T. Inheritance of psoriasis. Analysis of 2035 family histories. Hautarzt. 33(4), 214-217 (1982).
7. Traupe H, van Gurp PJ, Happle R, Boezeman J, van de Kerkhof PC. Psoriasis vulgaris, fetal growth, and genomic imprinting. Am. J. Med. Genet. 42(5), 649-654 (1992).
8. Russell TJ, Schultes LM, Kuban DJ. Histocompatibility (HL-A) antigens associated with psoriasis. N. Engl. J. Med. 287(15), 738-740 (1972).
9. Brenner W, Gschnait F, Mayr WR. HLA B13, B17, B37 and Cw6 in psoriasis vulgaris: association with the age of onset. Arch. Dermatol. Res. 262(3), 337-339 (1978).
10. Tiilikainen A, Lassus A, Karvonen J, Vartiainen P, Julin M. Psoriasis and HLA-Cw6. Br. J. Dermatol. 102(2), 179-184 (1980).
11. Valdimarsson H. The genetic basis of psoriasis. Clin. Dermatol. 23(6), 563-567 (2007).
12. Baron M. The search for complex disease genes: fault by linkage or fault by association? Mol. Psychiatry 6(2), 143-149 (2001).
13. Trembath RC, Clough RL, Rosbotham JL et al. 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. 6(5), 813-820 (1997).
14. International HapMap Consortium. A haplotype map of the human genome. Nature 437(7063), 1299-1320 (2005).
15. Frazer KA, Ballinger DG, Cox DR et al. A second generation human haplotype map of over 3.1 million SNPs. Nature 449(7164), 851-861 (2007).
16. Wellcome Trust Case Control Consortium. Genome-wide association study of 14,000 cases of seven common diseases and 3,000 shared controls. Nature 447(7145), 661-678 (2007).
17. Ionita-Laza I, Rogers AJ, Lange C, Raby BA, Lee C. Genetic association analysis of copy-number variation (CNV) in human disease pathogenesis. Genomics 93(1), 22-26 (2009).
18. Cook EH Jr, Scherer SW. Copy-number variations associated with neuropsychiatric conditions. Nature 455(7215), 919-923 (2008).
19. Hollox EJ, Huffmeier U, Zeeuwen PLJM et al. Psoriasis is associated with increased -defensin genomic copy number. Nat. Genet. 40(1), 23-25 (2008).
20. Nair RP, Duffin KC, Helms C et al. Genome-wide scan reveals association of psoriasis with IL-23 and NF-B pathways. Nat. Genet. 41(2), 199-204 (2009).
21. 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. 78(5), 827-851 (2006).
22. Capon F, Bijlmakers MJ, Quaranta M et al. Characterization of ZNF313/RNF114 as a novel psoriasis susceptibility gene. Br. J. Dermatol. 159(6), 1436-1474 (2008) (Abstract FC01).
23. de Cid R, Riveira-Munoz E, Zeeuwen PL et al. Deletion of the late cornified envelope LCE3B and LCE3C genes as a susceptibility factor for psoriasis. Nat. Genet. 41(2), 211-215 (2009).
24. 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. 80(2), 273-290 (2007).
25. Trembath RC, Clough RL, Rosbotham JL et al. 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. 6(5), 813-820 (1997).
26. 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. 6(8), 1349-1356 (1997).
27. Horton R, Wilming L, Rand V et al. Gene map of the extended human MHC. Nat. Rev. Genet. 5(12), 889-899 (2004).
28. Beck S, Trowsdale J. The human major histocompatability complex: lessons from the DNA sequence. Annu. Rev. Genomics Hum. Genet. 1, 117-137 (2000).
29. Walsh EC, Mather KA, Schaffner SF et al. An integrated haplotype map of the human major histocompatibility complex. Am. J. Hum. Genet. 73(3), 580-590 (2003).
30. Fan X, Yang S, Huang W et al. Fine mapping of the psoriasis susceptibility locus PSORS1 supports HLA-C as the susceptibility gene in the Han Chinese population. PLoS Genet. 4(3), e1000038 (2008).
31. Gudjonsson JE, Johnston A, Sigmundsdottir H, Valdimarsson H. Immunopathogenic mechanisms in psoriasis. Clin. Exp. Immunol. 135(1), 1-8 (2004).
32. Ahlenstiel G, Martin MP, Gao X, Carrington M, Rehermann B. Distinct KIR/HLA compound genotypes affect the kinetics of human antiviral natural killer cell responses. J. Clin. Invest. 118(3), 1017-1026 (2008).
33. Lin WJ, Norris DA, Achziger M, Kotzin BL, Tomkinson B. Oligoclonal expansion of intraepidermal T cells in psoriasis skin lesions. J. Invest. Dermatol. 117(6), 1546-1553 (2001).
34. Johnston A, Gudjonsson JE, Sigmundsdottir H, Love TJ, Valdimarsson H. Peripheral blood T cell responses to keratin peptides that share sequences with streptococcal M proteins are largely restricted to skinhoming CD8 T cells. Clin. Exp. Immunol. 138(7), 83-93 (2004).
35. 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. 101(5), 701-705 (1993).
36. Steinman L. A brief history of TH17, the first major revision in the TH1/TH2 hypothesis of T cell-mediated tissue damage. Nat. Med. 13(2), 139-145 (2007).
37. Langrish CL, Chen Y, Blumenschein WM et al. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. J. Exp. Med. 201(2), 233-240 (2005).
38. Yen D, Cheung J, Scheerens H et al. IL-23 is essential for T cell-mediated colitis and promotes inflammation via IL-17 and IL-6. J. Clin. Invest. 116(5), 1310-1316 (2006).
39. Oppmann B, Lesley R, Blom B et al. 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(5), 715-725 (2000).
40. Stritesky GL, Yeh N, Kaplan MH. IL-23 promotes maintenance but not commitment to the Th17 lineage. J. Immunol. 181(9), 5948-5955 (2008).
41. 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. 199(1), 125-130 (2004).
42. Leonardi CL, Kimball AB, Papp KA et al. Efficacy and safety of ustekinumab, a human interleukin-12/23 monoclonal antibody, in patients with psoriasis: 76-week results from a randomised, doubleblind, placebo-controlled trial (PHOENIX 1). Lancet 371(9625), 1665-1674 (2008).
43. Papp KA, Langley RG, Lebwohl M et al. 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(9625), 1675-1684 (2008).
44. Nair RP, Ruether A, Stuart PE et al. Polymorphisms of the IL12B and IL23R genes are associated with psoriasis. J. Invest. Dermatol. 128(7), 1653-1661 (2008).
45. Smith RL, Warren RB, Eyre S et al. Polymorphisms in the IL-12βand IL-23R genes are associated with psoriasis of early onset in a UK cohort. J. Invest. Dermatol. 128(5), 1325-1327 (2008).
46. 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. 80(2), 273-390 (2007).
47. Kryczek I, Bruce AT, Gudjonsson JE et al. Induction of IL-17+ T cell trafficking and development by IFN-γ: mechanism and pathological relevance in psoriasis. J. Immunol. 181(7), 4733-4741 (2008).
48. Rogan DF, Cousins DJ, Santangelo S et al. Analysis of intergenic transcription in the human IL-4/IL-13 gene cluster. Proc. Natl Acad. Sci. USA 101(8), 2446-2451 (2004).
49. Mills KH. Induction, function and regulation of IL-17-producing T cells. Eur. J. Immunol. 38(10), 2636-2649 (2008).
50. Lee EG, Boone DL, Chai S et al. Failure to regulate TNF-induced NF-κB and cell death responses in A20-deficient mice. Science 289(5488), 2350-2354 (2000).
51. Boone DL, Turer EE, Lee EG et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 5(10), 1052-1060 (2004).
52. Turer EE, Tavares RM, Mortier E et al. Homeostatic MyD88-dependent signals cause lethal inflammation in the absence of A20. J. Exp. Med. 205(2), 451-464 (2008).
53. Plenge RM, Cotsapas C, Davies L et al. Two independent alleles at 6q23 associated with risk of rheumatoid arthritis. Nat. Genet. 39(12), 1477-1482 (2007).
54. Graham RR, Cotsapas C, Davies L et al. Genetic variants near TNFAIP3 on 6q23 are associated with systemic lupus erythematosus. Nat. Genet. 40(9), 1059-1061 (2008).
55. Idel S, Dansky HM, Breslow JL. A20, a regulator of NFκB, maps to an atherosclerosis locus and differs between parental sensitive C57BL/6J and resistant FVB/N strains. Proc. Natl Acad. Sci. USA 100(24), 14235-14240 (2003).
56. Mease PJ, Goffe BS, Metz J, VanderStoep A, Finck B, Burge DJ. Etanercept in the treatment of psoriatic arthritis and psoriasis: a randomised trial. Lancet 356(9227), 385-390 (2000).
57. Chaudhari U, Romano P, Mulcahy LD, Dooley LT, Baker DG, Gottlieb AB. Efficacy and safety of infliximab monotherapy for plaque-type psoriasis: a randomised trial. Lancet 357(9271), 1842-1847 (2001).
58. Chew AL, Bennett A, Smith CH, Barker J, Kirkham B. Successful treatment of severe psoriasis and psoriatic arthritis with adalimumab. Br. J. Dermatol. 151(2), 492-496 (2004).
59. Werner SL, Kearns JD, Zadorozhnaya V et al. Encoding NF-κB temporal control in response to TNF: distinct roles for the negative regulators IκBand A20. Genes Dev. 22(15), 2093-2101 (2008).
60. Shembade N, Harhaj NS, Parvatiyar K et al. The E3 ligase Itch negatively regulates inflammatory signaling pathways by controlling the function of the ubiquitinediting enzyme A20. Nat. Immunol. 9(3), 254-262 (2008).
61. Heyninck K, Beyaert R. The cytokineinducible zinc finger protein A20 inhibits IL-1-induced NF-κB activation at the level of TRAF6. FEBS Lett. 442(2-3), 147-150 (1999).
62. Mauro C, Pacifico F, Lavorgna A et al. ABIN-1 binds to NEMO/IKKκand co-operates with A20 in inhibiting NF-κB. J. Biol. Chem. 281(27), 18482-18488 (2006).
63. Capon F, Bijlmakers MJ, Wolf N et al. Identification of ZNF313/RNF114 as a novel psoriasis susceptibility gene. Hum. Mol. Genet. 17(13), 1938-1945 (2008).
64. Ma YX, Zhang SZ, Hou YP, Huang XL, Wu QQ, Sun Y. Identification of a novel human zinc finger protein gene ZNF313. ACTA Biochimica et Bophysica Sinica 35(3), 230-237 (2003).
65. Zhao XP, Elder JT. Positional cloning of novel skin-specific genes from the human epidermal differentiation complex. Genomics 45(2), 250-258 (1997).
66. Capon F, Semprini S, Dallapiccola B, Novelli G. Evidence for interaction between psoriasis-susceptibility loci on chromosomes 6p21 and 1q21. Am. J. Hum. Genet. 65(6), 1798 - 1800 (1999).
67. Elias PM. The skin barrier as an innate immune element. Semin. Immunopathol. 29(1), 3-14 (2007).
68. Elias PM, Hatano Y, Williams ML. Basis for the barrier abnormality in atopic dermatitis: outside-inside-outside pathogenic mechanisms. J. Allergy. Clin. Immunol. 121(6), 1337-1343 (2008).
69. Zanetti M. Cathelicidins, multifunctional peptides of the innate immunity. J. Leukoc. Biol. 75(1), 39-48 (2004).
70. Lehrer RI, Ganz T. Defensins of vertebrate animals. Curr. Opin. Immunol. 14(1), 96-102 (2002).
71. Mee JB, Johnson CM, Morar N, Burslem F, Groves RW. The psoriatic transcriptome closely resembles that induced by interleukin-1 in cultured keratinocytes: dominance of innate immune responses in psoriasis. Am. J. Pathol. 171(1), 32-42 (2007).
72. Fulton C, Anderson GM, Zasloff M, Bull R, Quinn AG. Expression of natural peptide antibiotics in human skin. Lancet 350(9093), 1750-1751 (1997).
73. Sorensen OE, Thapa DR, Rosenthal A, Liu L, Roberts AA, Ganz T. Differential regulation of β-defensin expression in human skin by microbial stimuli. J. Immunol. 174(8), 4870-4879 (2005).
74. Harder J, Bartels J, Christophers E, Schroder JM. A peptide antibiotic from human skin. Nature 387(6636), 861 (1997).
75. Huh WK, Oono T, Shirafuji Y et al. Dynamic alteration of human β-defensin 2 localization from cytoplasm to intercellular space in psoriatic skin. J. Mol. Med. 80(10), 678-684 (2002).
76. Liu L, Wang L, Jia HP et al. Structure and mapping of the human β-defensin HBD-2 gene and its expression at sites of inflammation. Gene 222(2), 237-244 (1998).
77. Duits LA, Ravensbergen B, Rademaker M, Hiemstra PS, Nibbering PH. Expression of β-defensin 1 and 2 mRNA by human monocytes, macrophages and dendritic cells. Immunology 106(4), 517-525 (2002).
78. Harder J, Bartels J, Christophers E, Schroder JM. Isolation and characterization of human β-defensin-3, a novel human inducible peptide antibiotic. J. Biol. Chem. 276(8), 5707-5713 (2001).
79. Garcia JR, Jaumann F, Schulz S et al. Identification of a novel, multifunctional β-defensin (human β-defensin 3) with specific antimicrobial activity. Its interaction with plasma membranes of Xenopus oocytes and the induction of macrophage chemoattraction. Cell Tissue Res. 306(2), 257-264 (2001).
80. Garcia JR, Krause A, Schulz S et al. Human β-defensin 4: a novel inducible peptide with a specific salt-sensitive spectrum of antimicrobial activity. FASEB J. 15(10), 1819-1821 (2001).
81. Harder J, Meyer-Hoffert U, Wehkamp K, Schwichtenberg L, Schroder JM. Differential gene induction of human β-defensins (hBD-1, -2, -3, and -4) in keratinocytes is inhibited by retinoic acid. J. Invest. Dermatol. 123(3), 522-529 (2004).
82. Niyonsaba F, Ushio H, Nakano N et al. Antimicrobial peptides human β-defensins stimulate epidermal keratinocyte migration, proliferation and production of proinflammatory cytokines and chemokines. J. Invest. Dermatol. 127(3), 594-604 (2007).
83. Chen X, Niyonsaba F, Ushio H et al. Synergistic effect of antibacterial agents human β-defensins, cathelicidin LL-37 and lysozyme against Staphylococcus aureus and Escherichia coli. J. Dermatol. Sci. 40(2), 123-132 (2005).
84. Niyonsaba F, Ushio H, Nagaoka I, Okumura K, Ogawa H. The human β-defensins (-1, -2, -3, -4) and cathelicidin LL-37 induce IL-18 secretion through p38 and ERK MAPK activation in primary human keratinocytes. J. Immunol. 175(3), 1776-1784 (2005).
85. Niyonsaba F, Iwabuchi K, Matsuda H, Ogawa H, Nagaoka I. Epithelial cellderived human β-defensin-2 acts as a chemotaxin for mast cells through a pertussis toxin-sensitive and phospholipase C-dependent pathway. Int. Immunol. 14(4), 421-426 (2002).
86. Niyonsaba F, Ogawa H, Nagaoka I. Human β-defensin-2 functions as a chemotactic agent for tumour necrosis factor-α-treated human neutrophils. Immunology 111(3), 273-281 (2004).
87. Yang D, Chertov O, Bykovskaia SN et al. β-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286(5439), 525-528 (1999).
88. Soruri A, Grigat J, Forssmann U, Riggert J, Zwirner J. β-defensins chemoattract macrophages and mast cells but not lymphocytes and dendritic cells: CCR6 is not involved. Eur J. Immunol. 37(9), 2474-2486 (2007).
89. Funderburg N, Lederman MM, Feng Z et al. Human-defensin-3 activates professional antigen-presenting cells via Toll-like receptors 1 and 2. Proc. Natl Acad. Sci. USA 104(47), 18631-18635 (2007).
90. Hollox EJ, Armour JA, Barber JC. Extensive normal copy number variation of a β-defensin antimicrobial-gene cluster. Am. J. Hum. Genet. 73(3), 591-600 (2003).
91. Fellermann K, Stange DE, Schaeffeler E et al. A chromosome 8 gene-cluster polymorphism with low human β-defensin 2 gene copy number predisposes to Crohn disease of the colon. Am. J. Hum. Genet. 79(3), 439-448 (2006).
92. Ong PY, Ohtake T, Brandt C et al. Endogenous antimicrobial peptides and skin infections in atopic dermatitis. N. Engl. J. Med. 347(15), 1151-1160 (2002).
93. Nomura I, Goleva E, Howell MD et al. Cytokine milieu of atopic dermatitis, as compared to psoriasis, skin prevents induction of innate immune response genes. J. Immunol. 171(6), 3262-3269 (2003).
94. Jansen PA, Rodijk-Olthuis D, Hollox EJ et al. β-defensin-2 protein is a serum biomarker for disease activity in psoriasis and reaches biologically relevant concentrations in lesional skin. PLoS ONE 4(3), e4725 (2009).
95. Pauls K, Schon M, Kubitza RC et al. Role of integrin αE(CD103) β7 for tissuespecific epidermal localization of CD8+ T lymphocytes. J. Invest. Dermatol. 117(3), 569-575 (2001).
96. Conrad C, Boyman O, Tonel G et al. α1β1 integrin is crucial for accumulation of epidermal T cells and the development of psoriasis. Nat. Med. 13(7), 836-842 (2007).
97. Lowes MA, Bowcock AM, Krueger JG. Pathogenesis and therapy of psoriasis. Nature 445(7130), 866-873 (2007).
98. Barrett JC, Hansoul S, Nicolae DL et al. Genome-wide association defines more than 30 distinct susceptibility loci for Crohn's disease. Nat. Genet. 40(8), 955-962 (2008).
99. Tomfohrde J, Silverman A, Barnes R et al. Gene for familial psoriasis susceptibility mapped to the distal end of human chromosome 17q. Science 264(5162), 1141-1145 (1994).
100. Helms C, Cao L, Krueger JG et al. A putative RUNX1 binding site variant between SLC9A3R1 and NAT9 is associated with susceptibility to psoriasis. Nat. Genet. 35(4), 345-356 (2003).
101. Matthews D, Fry L, Powles A et al. Evidence that a locus for familial psoriasis maps to chromosome 4q. Nat. Genet. 14(2), 231-233 (1996).
102. Hewett D, Samuelsson L, Polding J et al. Identification of a psoriasis susceptibility candidate gene by linkage disequilibrium mapping with a localized single nucleotide polymorphism map. Genomics 79(3), 305-314 (2002).
103. Enlund F, Samuelsson L, Enerback C et al. Psoriasis susceptibility locus in chromosome region 3q21 identified in patients from southwest Sweden. Eur. J. Hum. Genet. 7(7), 783-790 (1999).
104. Zenz R, Eferl R, Kenner L et al. Psoriasislike skin disease and arthritis caused by inducible epidermal deletion of Jun proteins. Nature 437(7057), 369-375 (2005).
105. Lee YA, Ruschendorf F, Windemuth C et al. Genomewide scan in german families reveals evidence for a novel psoriasissusceptibility locus on chromosome 19p13. Am. J. Hum. Genet. 67(4), 1020-1024 (2000).
106. Veal CD, Clough RL, Barber RC et al. Identification of a novel psoriasis susceptibility locus at 1p and evidence of epistasis between PSORS1 and candidate loci. J. Med. Genet. 38(1), 7-13 (2001).
107. Zhang XJ, Yan KL, Wang ZM et al. Polymorphisms in interleukin-15 gene on chromosome 4q31.2 are associated with psoriasis vulgaris in Chinese population. J. Invest. Dermatol. 127(11), 2544-2551 (2007).
108. Zhang XJ, He PP, Wang ZX et al. Evidence for a major psoriasis susceptibility locus at 6p21(PSORS1) and a novel candidate region at 4q31 by genome-wide scan in Chinese hans. J. Invest. Dermatol. 119(6), 1361-1366 (2002).
109. Asumalahti K, Laitinen T, Lahermo P et al. Psoriasis susceptibility locus on 18p revealed by genome scan in Finnish families not associated with PSORS1. J. Invest. Dermatol. 121(4), 735-740 (2003).