Modulation of epidermal transcription circuits in psoriasis: New links between inflammation and hyperproliferation

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Swindell, William R ^a   Johnston, Andrew ^a   Xing, Xianying ^a   Voorhees, John J ^a   Elder, James T ^a   Gudjonsson, Johann E ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; STAT1 PROTEIN; TRANSCRIPTION FACTOR E2F; TRANSCRIPTION FACTOR RUNX1; TUMOR NECROSIS FACTOR ALPHA;

APOPTOSIS; ARTICLE; CELIAC DISEASE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CROHN DISEASE; DISEASE PREDISPOSITION; EPIDERMIS; GENE; GENE EXPRESSION; GENE LOCUS; GENE SILENCING; GENETIC ASSOCIATION; GRHL3 GENE; IFIH1 GENE; IL12B GENE; INFLAMMATORY BOWEL DISEASE; KERATINOCYTE; LCED GENE; METHYLATION; MITOSIS; NOS2 GENE; PRSS53 GENE; PSORIASIS; REL GENE; SDC4 GENE; STAT1 57 GENE;

COHORT STUDIES; EPIDERMIS; FEMALE; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENOME-WIDE ASSOCIATION STUDY; HUMANS; MALE; PSORIASIS; TRANSCRIPTION, GENETIC;

EID: 84896708817     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0079253     Document Type: Article

References (101)

1. Miniszewska J, Juczyński Z, Ograczyk A, Zalewska A (2013) Health-related Quality of Life in Psoriasis: Important Role of Personal Resources. Acta Derm Venereol, In Press.
2. Armstrong AW, Harskamp CT, Armstrong EJ (2012) The association between psoriasis and obesity: a systematic review and meta-analysis of observational studies. Nutr Diabetes 2: e54.
3. Armstrong AW, Harskamp CT, Armstrong EJ (2013) Psoriasis and metabolic syndrome: A systematic review and meta-analysis of observational studies. J Am Acad Dermatol 68: 654-662.
4. Armstrong AW, Harskamp CT, Armstrong EJ (2012) The association between psoriasis and hypertension: a systematic review and meta-analysis of observational studies. J Hypertens 31: 442-443.
5. Dowlatshahi EA, Wakkee M, Herings RM, Hollestein LM, Nijsten T (2013) Increased Antidepressant Drug Exposure in Psoriasis Patients: A Longitudinal Population-based Cohort Study. Acta Derm Venereol, In Press.
6. Tsoi LC, Spain SL, Knight J, Ellinghaus E, Stuart PE, et al. (2012) Identification of 15 new psoriasis susceptibility loci highlights the role of innate immunity. Nat Genet 44: 1341-1348.
7. Gudjonsson JE, Ding J, Li X, Nair RP, Tejasvi T, et al. (2009) Global gene expression analysis reveals evidence for decreased lipid biosynthesis and increased innate immunity in uninvolved psoriatic skin. J Invest Dermatol 129: 2795-2804.
8. Gudjonsson JE, Ding J, Johnston A, Tejasvi T, Guzman AM, et al. (2010) Assessment of the psoriatic transcriptome in a large sample: additional regulated genes and comparisons with in vitro models. J Invest Dermatol 130: 1829-1840.
9. Swindell WR, Xing X, Stuart PE, Chen CS, Aphale A, et al. (2012) Heterogeneity of inflammatory and cytokine networks in chronic plaque psoriasis. PLoS ONE 7: e34594.
10. Ainali C, Valeyev N, Perera G, Williams A, Gudjonsson JE, et al. (2012) Transcriptome classification reveals molecular subtypes in psoriasis. BMC Genomics 13: 472.
11. Suárez-Fariñas M, Li K, Fuentes-Duculan J, Hayden K, Brodmerkel C, et al. (2012) Expanding the Psoriasis Disease Profile: Interrogation of the Skin and Serum of Patients with Moderate-to-Severe Psoriasis. J Invest Dermatol 132: 2552-2564.
12. Kulski JK, Kenworthy W, Bellgard M, Taplin R, Okamoto K, et al. (2005) Gene expression profiling of Japanese psoriatic skin reveals an increased activity in molecular stress and immune response signals. J Mol Med (Berl) 83: 964-975. (Pubitemid 41745755)
13. Reischl J, Schwenke S, Beekman JM, Mrowietz U, Stürzebecher S, et al. (2007) Increased expression of Wnt5a in psoriatic plaques. J Invest Dermatol 127: 163-169. (Pubitemid 46005674)
14. Lu X, Du J, Liang J, Zhu X, Yang Y, et al. (2013) Transcriptional regulatory network for psoriasis. J Dermatol 40: 48-53.
15. Swindell WR, Johnston A, Voorhees JJ, Elder JT, Gudjonsson JE (2013) Dissecting the psoriasis transcriptome: inflammatory- and cytokine-driven gene expression in lesions from 163 patients. BMC Genomics 14: 527.
16. Xia J, Joyce CE, Bowcock AM, Zhang W (2013) Noncanonical microRNAs and endogenous siRNAs in normal and psoriatic human skin. Hum Mol Genet 22: 737-748.
17. Roberson ED, Liu Y, Ryan C, Joyce CE, Duan S, et al. (2012) A subset of methylated CpG sites differentiate psoriatic from normal skin. J Invest Dermatol 132: 583-592.
18. Gudjonsson JE, Elder JT (2007) Psoriasis. In: Wolff K, Goldsmith LA, Katz SI, Gilchrest BA, Paller AM, editors. Fitzpatrick's Dermatology in General Medicine. New York: McGraw-Hill. 169-194.
19. Nestle FO, Kaplan DH, Barker J (2009) Psoriasis. N Engl J Med 361: 496-509.
20. Samarasekera EJ, Sawyer L, Wonderling D, Tucker R, Smith CH (2013) Topical therapies for the treatment of plaque psoriasis: systematic review and network meta-analyses. Br J Dermatol 168: 954-967.
21. Man XY, Li W, Chen JQ, Zhou J, Landeck L, et al. (2013) Impaired nuclear translocation of glucocorticoid receptors: novel findings from psoriatic epidermal keratinocytes. Cell Mol Life Sci 70: 2205-2220.
22. Ishimaru M, Tsukimoto M, Harada H, Kojima S (2013) Involvement of P2Y11 receptor in IFN-γ-induced IL-6 production in human keratinocytes. Eur J Pharmacol 703: 67-73.
23. Johnston A, Gudjonsson JE, Aphale A, Guzman AM, Stoll SW, et al. (2011) EGFR and IL-1 signaling synergistically promote keratinocyte antimicrobial defenses in a differentiation-dependent manner. J Invest Dermatol 131: 329-337.
24. Johansen C, Kragballe K, Westergaard M, Henningsen J, Kristiansen K, et al. (2005) The mitogen-activated protein kinases p38 and ERK1/2 are increased in lesional psoriatic skin. Br J Dermatol 152: 37-42.
25. Zhang W, Dang E, Shi X, Jin L, Feng Z, et al. (2012) The pro-inflammatory cytokine IL-22 up-regulates keratin 17 expression in keratinocytes via STAT3 and ERK1/2. PLoS ONE 7: e40797.
26. Goldminz AM, Au SC, Kim N, Gottlieb AB, Lizzul PF (2013) NF-κB: an essential transcription factor in psoriasis. J Dermatol Sci 69: 89-94.
27. Sen GL, Boxer LD, Webster DE, Bussat RT, Qu K, et al. (2012) ZNF750 is a p63 target gene that induces KLF4 to drive terminal epidermal differentiation. Dev Cell 22: 669-677.
28. Cohen I, Birnbaum RY, Leibson K, Taube R, Sivan S, et al. (2012) ZNF750 is expressed in differentiated keratinocytes and regulates epidermal late differentiation genes. PLoS ONE 7: e42628.
29. Zarnegar BJ, Webster DE, Lopez-Pajares V, Vander Stoep Hunt B, Qu K, et al. (2012) Genomic profiling of a human organotypic model of AEC syndrome reveals ZNF750 as an essential downstream target of mutant TP63. Am J Hum Genet 91: 435-443.
30. Tian S, Krueger JG, Li K, Jabbari A, Brodmerkel C, et al. (2012) Meta-analysis derived (MAD) transcriptome of psoriasis defines the "core" pathogenesis of disease. PLoS ONE 7: e44274.
31. Bigler J, Rand HA, Kerkof K, Timour M, Russell CB (2013) Cross-study homogeneity of psoriasis gene expression in skin across a large expression range. PLoS ONE 8: e52242.
32. Kennedy-Crispin M, Billick E, Mitsui H, Gulati N, Fujita H, et al. (2012) Human keratinocytes' response to injury upregulates CCL20 and other genes linking innate and adaptive immunity. J Invest Dermatol 132: 105-113.
33. Nair RP, Duffin KC, Helms C, Ding J, Stuart PE, et al. (2009) Genome-wide scan reveals association of psoriasis with IL-23 and NF-kappaB pathways. Nat Genet 41: 199-204.
34. Yao Y, Richman L, Morehouse C, de los Reyes M, Higgs BW, et al. (2008) Type I interferon: potential therapeutic target for psoriasis? PLoS ONE 3: e2737.
35. Stuart JM, Segal E, Koller D, Kim SK (2003) A gene-coexpression network for global discovery of conserved genetic modules. Science 302: 249-255. (Pubitemid 37248749)
36. Wolfe CJ, Kohane IS, Butte AJ (2005) Systematic survey reveals general applicability of "guilt-by-association" within gene coexpression networks. BMC Bioinformatics 6: 227.
37. Childs KL, Davidson RM, Buell CR (2011) Gene coexpression network analysis as a source of functional annotation for rice genes. PLoS ONE 6: e22196.
38. Mitsui H, Suárez-Fariñas M, Belkin DA, Levenkova N, Fuentes-Duculan J, et al. (2012) Combined use of laser capture microdissection and cDNA microarray analysis identifies locally expressed disease-related genes in focal regions of psoriasis vulgaris skin lesions. J Invest Dermatol 132: 1615-1626.
39. Nickoloff BJ, Xin H, Nestle FO, Qin JZ (2007) The cytokine and chemokine network in psoriasis. Clin Dermatol 25: 568-573. (Pubitemid 350103656)
40. Tomic-Canic M, Komine M, Freedberg IM, Blumenberg M (1998) Epidermal signal transduction and transcription factor activation in activated keratinocytes. J Dermatol Sci 17: 167-181. (Pubitemid 28341660)
41. Eckert RL, Welter JF (1996) Transcription factor regulation of epidermal keratinocyte gene expression. Mol Biol Rep 23: 59-70. (Pubitemid 27015469)
42. Ivanova IA, D'Souza SJ, Dagnino L (2005) Signalling in the epidermis: the E2F cell cycle regulatory pathway in epidermal morphogenesis, regeneration and transformation. Int J Biol Sci 1: 87-95.
43. Frye M, Benitah SA (2012) Chromatin regulators in mammalian epidermis. Semin Cell Dev Biol 23: 897-905.
44. Spivakov M, Akhtar J, Kheradpour P, Beal K, Girardot C, et al. (2012) Analysis of variation at transcription factor binding sites in Drosophila and humans. Genome Biol 13: R49.
45. Suomela S, Cao L, Bowcock A, Saarialho-Kere U (2004) Interferon alpha-inducible protein 27 (IFI27) is upregulated in psoriatic skin and certain epithelial cancers. J Invest Dermatol 122: 717-721. (Pubitemid 38471341)
46. Satoh J, Tabunoki H (2013) A Comprehensive Profile of ChIP-Seq-Based STAT1 Target Genes Suggests the Complexity of STAT1-Mediated Gene Regulatory Mechanisms. Gene Regul Syst Bio 7: 41-56.
47. Bogunovic D, Boisson-Dupuis S, Casanova JL (2013) ISG15: leading a double life as a secreted molecule. Exp Mol Med 45: e18.
48. D'Cunha J, Knight E Jr, Haas AL, Truitt RL, Borden EC (1996) Immunoregulatory properties of ISG15, an interferon-induced cytokine. Proc Natl Acad Sci U S A 93: 211-215. (Pubitemid 26038129)
49. Recht M, Borden EC, Knight E Jr (1991) A human 15-kDa IFN-induced protein induces the secretion of IFN-gamma. J Immunol 147: 2617-2623.
50. Owhashi M, Taoka Y, Ishii K, Nakazawa S, Uemura H, et al. (2003) Identification of a ubiquitin family protein as a novel neutrophil chemotactic factor. Biochem Biophys Res Commun 309: 533-539. (Pubitemid 37083284)
51. Terui T, Ozawa M, Tagami H (2000) Role of neutrophils in induction of acute inflammation in T-cell-mediated immune dermatosis, psoriasis: a neutrophil-associated inflammation-boosting loop. Exp Dermatol 9: 1-10. (Pubitemid 30093030)
52. Prens EP, Kant M, van Dijk G, van der Wel LI, Mourits S, et al. (2008) IFN-alpha enhances poly-IC responses in human keratinocytes by inducing expression of cytosolic innate RNA receptors: relevance for psoriasis. J Invest Dermatol 128: 932-938. (Pubitemid 351374290)
53. Kitamura H, Matsuzaki Y, Kimura K, Nakano H, Imaizumi T, et al. (2007) Cytokine modulation of retinoic acid-inducible gene-I (RIG-I) expression in human epidermal keratinocytes. J Dermatol Sci 45: 127-134. (Pubitemid 46108490)
54. Belgnaoui SM, Paz S, Hiscott J (2011) Orchestrating the interferon antiviral response through the mitochondrial antiviral signaling (MAVS) adapter. Curr Opin Immunol 23: 564-572.
55. Paz S, Sun Q, Nakhaei P, Romieu-Mourez R, Goubau D, et al.(2006) Induction of IRF-3 and IRF-7 phosphorylation following activation of the RIG-I pathway. Cell Mol Biol (Noisy-le-grand) 52: 17-28. (Pubitemid 43925157)
56. Liu F, Gu J (2011) Retinoic acid inducible gene-I, more than a virus sensor. Protein Cell 2: 351-357.
57. Zhang HX, Liu ZX, Sun YP, Zhu J, Lu SY, et al. (2013) Rig-I regulates NF-κB activity through binding to Nf-κb1 3′-UTR mRNA. Proc Natl Acad Sci U S A 110: 6459-6464.
58. Wang Y, Zhang HX, Sun YP, Liu ZX, Liu XS, et al. (2007) Rig-I-/- mice develop colitis associated with downregulation of G alpha i2. Cell Res 17: 858-868. (Pubitemid 47585114)
59. Tahara E Jr, Tahara H, Kanno M, Naka K, Takeda Y, et al. (2005) G1P3, an interferon inducible gene 6-16, is expressed in gastric cancers and inhibits mitochondrial-mediated apoptosis in gastric cancer cell line TMK-1 cell. Cancer Immunol Immunother 54: 729-740. (Pubitemid 40977141)
60. Cheriyath V, Kuhns MA, Jacobs BS, Evangelista P, Elson P, et al. (2012) G1P3, an interferon- and estrogen-induced survival protein contributes to hyperplasia, tamoxifen resistance and poor outcomes in breast cancer. Oncogene 31: 2222-2236.
61. Szegedi K, Sonkoly E, Nagy N, Németh IB, Bata-Csörgo Z, et al. (2010) The anti-apoptotic protein G1P3 is overexpressed in psoriasis and regulated by the non-coding RNA, PRINS. Exp Dermatol 19: 269-278.
62. Sahu SK, Gummadi SN, Manoj N, Aradhyam GK (2007) Phospholipid scramblases: an overview. Arch Biochem Biophys 462: 103-114. (Pubitemid 46755145)
63. Cui W, Li SY, Du JF, Zhu ZM, An P (2012) Silencing phospholipid scramblase 1 expression by RNA interference in colorectal cancer and metastatic liver cancer. Hepatobiliary Pancreat Dis Int 11: 393-400.
64. Kuo YB, Chan CC, Chang CA, Fan CW, Hung RP, et al. (2011) Identification of phospholipid scramblase 1 as a biomarker and determination of its prognostic value for colorectal cancer. Mol Med 17: 41-47.
65. Sun J, Nanjundan M, Pike LJ, Wiedmer T, Sims PJ (2002) Plasma membrane phospholipid scramblase 1 is enriched in lipid rafts and interacts with the epidermal growth factor receptor. Biochemistry 41: 6338-6345. (Pubitemid 34525998)
66. Nanjundan M, Sun J, Zhao J, Zhou Q, Sims PJ, et al. (2003) Plasma membrane phospholipid scramblase 1 promotes EGF-dependent activation of c-Src through the epidermal growth factor receptor. J Biol Chem 278: 37413-37418. (Pubitemid 37175261)
67. Kanno Y, Levi BZ, Tamura T, Ozato K (2005) Immune cell-specific amplification of interferon signaling by the IRF-4/8-PU.1 complex. J Interferon Cytokine Res 25: 770-779. (Pubitemid 43068488)
68. Decker T, Kovarik P, Meinke A (1997) GAS elements: a few nucleotides with a major impact on cytokine-induced gene expression. J Interferon Cytokine Res 17: 121-134. (Pubitemid 27148701)
69. Levy DE, Kessler DS, Pine R, Reich N, Darnell JE Jr (1988) Interferon-induced nuclear factors that bind a shared promoter element correlate with positive and negative transcriptional control. Genes Dev 2: 383-393.
70. Hald A, Andrés RM, Salskov-Iversen ML, Kjellerup RB, Iversen L, et al. (2013) STAT1 expression and activation is increased in lesional psoriatic skin. Br J Dermatol 168: 302-310.
71. van der Fits L, van der Wel LI, Laman JD, Prens EP, Verschuren MC (2004) In psoriasis lesional skin the type I interferon signaling pathway is activated, whereas interferon-alpha sensitivity is unaltered. J Invest Dermatol 122: 51-60. (Pubitemid 38114638)
72. Wang X, Dalkic E, Wu M, Chan C (2008) Gene module level analysis: identification to networks and dynamics. Curr Opin Biotechnol 19: 482-491.
73. Dong J, Horvath S (2007) Understanding network concepts in modules. BMC Syst Biol 1: 24.
74. Swindell WR (2009) Genes and gene expression modules associated with caloric restriction and aging in the laboratory mouse. BMC Genomics 10: 585.
75. Zaba LC, Suárez-Fariñas M, Fuentes-Duculan J, Nograles KE, Guttman-Yassky E, et al. (2009) Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J Allergy Clin Immunol 124: 1022-1030.
76. Bolstad BM, Collin F, Brettschneider J, Simpson K, Cope L, et al. (2005) Quality assessment of Affymetrix GeneChip Data. In: Gentleman R, Carey V, Huber W, Irizarry R, Dudoit S, editors. Bioinformatics and Computational Biology Solutions Using R and Bioconductor. New York: Springer. 33-47.
77. Popova T, Mennerich D, Weith A, Quast K (2008) Effect of RNA quality on transcript intensity levels in microarray analysis of human post-mortem brain tissues. BMC Genomics 9: 91.
78. Irizarry RA, Bolstad BM, Collin F, Cope LM, Hobbs B, et al. (2003) Summaries of Affymetrix GeneChip probe level data. Nucleic Acids Res 31: e15.
79. Stalteri MA, Harrison AP (2007) Interpretation of multiple probe sets mapping to the same gene in Affymetrix GeneChips. BMC Bioinformatics 8: 13.
80. Smyth GK (2004) Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 3: 3.
81. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a powerful and practical approach to multiple testing. J Roy Stat Soc B 57: 289-300.
82. Hindorff LA, Sethupathy P, Junkins HA, Ramos EM, Mehta JP, et al. (2009) Potential etiologic and functional implications of genome-wide association loci for human diseases and traits. Proc Natl Acad Sci U S A 106: 9362-9367.
83. Langfelder P, Zhang B, Horvath S (2008) Defining clusters from a hierarchical cluster tree: the Dynamic Tree Cut package for R. Bioinformatics 24: 719-720. (Pubitemid 351321220)
84. Philippakis AA, Busser BW, Gisselbrecht SS, He FS, Estrada B, et al. (2006) Expression-guided in silico evaluation of candidate cis regulatory codes for Drosophila muscle founder cells. PLoS Comput Biol 2: e53.
85. Gene Ontology Consortium (2013) Gene Ontology annotations and resources. Nucleic Acids Res 41: D530-D535.
86. Kanehisa M, Goto S, Kawashima S, Okuno Y, Hattori M (2004) The KEGG resource for deciphering the genome. Nucleic Acids Res 32: D277-D280. (Pubitemid 38081656)
87. Croft D, O'Kelly G, Wu G, Haw R, Gillespie M, et al. (2011) Reactome: a database of reactions, pathways and biological processes. Nucleic Acids Res 39: D691-D697.
88. Hewett M, Oliver DE, Rubin DL, Easton KL, Stuart JM, et al. (2002) PharmGKB: the Pharmacogenetics Knowledge Base. Nucleic Acids Res 30: 163-165. (Pubitemid 34679530)
89. Falcon S, Gentleman R (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23: 257-258. (Pubitemid 46189622)
90. Krueger JG, Fretzin S, Suárez-Fariñas M, Haslett PA, Phipps KM, et al. (2012) IL-17A is essential for cell activation and inflammatory gene circuits in subjects with psoriasis. J Allergy Clin Immunol 130: 145-154.
91. Johnson-Huang LM, Pensabene CA, Shah KR, Pierson KC, Kikuchi T, et al. (2012) Post-therapeutic relapse of psoriasis after CD11a blockade is associated with T cells and inflammatory myeloid DCs. PLoS ONE 7: e30308.
92. Greco JA 3rd, Pollins AC, Boone BE, Levy SE, Nanney LB (2010) A microarray analysis of temporal gene expression profiles in thermally injured human skin. Burns 36: 192-204.
93. Padilla RS, Sebastian S, Jiang Z, Nindl I, Larson R (2010) Gene expression patterns of normal human skin, actinic keratosis, and squamous cell carcinoma: a spectrum of disease progression. Arch Dermatol 146: 288-293.
94. Riker AI, Enkemann SA, Fodstad O, Liu S, Ren S, et al. (2008) The gene expression profiles of primary and metastatic melanoma yields a transition point of tumor progression and metastasis. BMC Med Genomics 1: 13.
95. Stojadinovic O, Lee B, Vouthounis C, Vukelic S, Pastar I, et al. (2007) Novel genomic effects of glucocorticoids in epidermal keratinocytes: inhibition of apoptosis, interferon-gamma pathway, and wound healing along with promotion of terminal differentiation. J Biol Chem 282: 4021-4034. (Pubitemid 47084434)
96. Portales-Casamar E, Thongjuea S, Kwon AT, Arenillas D, Zhao X, et al. (2010) JASPAR 2010: the greatly expanded open-access database of transcription factor binding profiles. Nucleic Acids Res 38: D105-D110.
97. Robasky K, Bulyk ML (2011) UniPROBE, update 2011: expanded content and search tools in the online database of protein-binding microarray data on protein-DNA interactions. Nucleic Acids Res 39: D124-D128.
98. Xie Z, Hu S, Blackshaw S, Zhu H, Qian J (2010) hPDI: a database of experimental human protein-DNA interactions. Bioinformatics 26: 287-289.
99. Matys V, Kel-Margoulis OV, Fricke E, Liebich I, Land S, et al. (2006) TRANSFAC and its module TRANSCompel: transcriptional gene regulation in eukaryotes. Nucleic Acids Res 34: D108-D110.
100. Swindell WR, Johnston A, Xing X, Little A, Robichaud P, et al. (2013) Robust shifts in S100a9 expression with aging: a novel mechanism for chronic inflammation. Sci Rep 3: 1215.
101. Siepel A, Bejerano G, Pedersen JS, Hinrichs AS, Hou M, et al. (2005) Evolutionarily conserved elements in vertebrate, insect, worm, and yeast genomes. Genome Res 15: 1034-1050. (Pubitemid 41126859)