An integrated epigenetic and transcriptomic analysis reveals distinct tissue-specific patterns of DNA methylation associated with atopic dermatitis

Journal of Investigative Dermatology

Volumn 134, Issue 7, 2014, Pages 1873-1883

  Rodríguez, Elke ^a   Baurecht, Hansjörg ^a,b   Wahn, Anna Franziska ^b   Kretschmer, Anja ^b,c   Hotze, Melanie ^a   Zeilinger, Sonja ^c   Klopp, Norman ^d   Illig, Thomas ^d   Schramm, Katharina ^c   Prokisch, Holger ^c   Kühnel, Brigitte ^c   Gieger, Christian ^c   Harder, Jürgen ^a   Cifuentes, Liliana ^b   Novak, Natalija ^e   Weidinger, Stephan ^a  

^a UNIVERSITY HOSPITAL SCHLESWIG HOLSTEIN   (Germany)

^b TECHNICAL UNIVERSITY OF MUNICH   (Germany)

^c INSTITUTE OF EPIDEMIOLOGY   (Germany)

^d HANNOVER MEDICAL SCHOOL   (Germany)

^e UNIVERSITY OF BONN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

DNA;

ADULT; ARTICLE; ATOPIC DERMATITIS; B LYMPHOCYTE; BLOOD ANALYSIS; CLINICAL ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; EPIDERMIS; EPIGENETICS; FEMALE; GENOME; HUMAN; INNATE IMMUNITY; MALE; PATTERN RECOGNITION; PRIORITY JOURNAL; RISK FACTOR; SKIN DEFECT; T LYMPHOCYTE; TRANSCRIPTOMICS;

ADULT; AGED; B-LYMPHOCYTES; CPG ISLANDS; DERMATITIS, ATOPIC; DNA METHYLATION; EPIDERMIS; EPIGENESIS, GENETIC; FEMALE; GENETIC COMPLEMENTATION TEST; HUMANS; IMMUNITY, INNATE; MALE; MIDDLE AGED; RNA, MESSENGER; T-LYMPHOCYTES; TRANSCRIPTOME; YOUNG ADULT;

EID: 84902543779     PISSN: 0022202X     EISSN: 15231747     Source Type: Journal    
DOI: 10.1038/jid.2014.87     Document Type: Article

References (54)

1. Barrera V, Peinado MA (2012) Evaluation of single CpG sites as proxies of CpG island methylation states at the genome scale. Nucleic Acids Res 40: 11490-8
2. Bell JT, Pai AA, Pickrell JK et al. (2011) DNA methylation patterns associate with genetic and gene expression variation in HapMap cell lines. Genome Biol 12:R10
3. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate - a practical and powerful approach to multiple testing. J Roy Stat Soc B Met 57: 289-300
4. Bieber T (2008) Atopic dermatitis. N Engl J Med 358: 1483-94
5. Bin L, Howell MD, Kim BE et al. (2011) Specificity protein 1 is pivotal in the skin's antiviral response. J Allergy Clin Immunol 127(2): 430-8
6. Christensen BC, Houseman EA, Marsit CJ et al. (2009) Aging and environmental exposures alter tissue-specific DNA methylation dependent upon CpG island context. PLoS Genet 5:e1000602
7. Du P, Kibbe WA, Lin SM (2008) lumi: a pipeline for processing Illumina microarray. Bioinformatics 24: 1547-8
8. Ehrich M, Nelson MR, Stanssens P et al. (2005) Quantitative high-throughput analysis of DNA methylation patterns by base-specific cleavage and mass spectrometry. Proc Natl Acad Sci USA 102: 15785-90
9. Ellinghaus D, Baurecht H, Esparza-Gordillo J et al. (2013) High-density genotyping study identifies four new susceptibility loci for atopic dermatitis. Nat Genet 45: 808-12
10. Fujimoto E, Kobayashi T, Fujimoto N et al. (2010) AGE-modified collagens I and III induce keratinocyte terminal differentiation through AGE receptor CD36: epidermal-dermal interaction in acquired perforating dermatosis. J Invest Dermatol 130: 405-14
11. Gibbs JR, van der Brug MP, Hernandez DG et al. (2010) Abundant quantitative trait loci exist for DNA methylation and gene expression in human brain. PLoS Genet 6:e1000952
12. Gläser R, Meyer-Hoffert U, Harder J et al. (2009) The antimicrobial protein psoriasin (S100A7) is upregulated in atopic dermatitis and after experimental skin barrier disruption. J Invest Dermatol 129: 641-9
13. Gronniger E, Weber B, Heil O et al. (2010) Aging and chronic sun exposure cause distinct epigenetic changes in human skin. PLoS Genet 6:e1000971
14. Halawi A, Abbas O, Mahalingam M (2013) S100 proteins and the skin: a review. J Eur Acad Dermatol Venereol 28: 405-14
15. Harder J, Dressel S, Wittersheim M et al. (2010) Enhanced expression and secretion of antimicrobial peptides in atopic dermatitis and after superficial skin injury. J Invest Dermatol 130: 1355-64
16. Hegyi Z, Zwicker S, Bureik D et al. (2012) Vitamin D analog calcipotriol suppresses the Th17 cytokine-induced proinflammatory S100 "alarmins" psoriasin (S100A7) and koebnerisin (S100A15) in psoriasis. J Invest Dermatol 132: 1416-24
17. Huang da W, Sherman BT, Lempicki RA (2009a) Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 37: 1-13
18. Huang da W, Sherman BT, Lempicki RA (2009b) Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 4: 44-57
19. Illingworth R, Kerr A, Desousa D et al. (2008) A novel CpG island set identifies tissue-specific methylation at developmental gene loci. PLoS Biol 6:e22
20. Jarzab J, Filipowska B, Zebracka J et al. (2010) Locus 1q21 Gene expression changes in atopic dermatitis skin lesions: deregulation of small prolinerich region 1A. Int Arch Allergy Immunol 151: 28-37
21. Johannes F, Porcher E, Teixeira FK et al. (2009) Assessing the impact of transgenerational epigenetic variation on complex traits. PLoS Genet 5:e1000530
22. Jones PA (1999) The DNA methylation paradox. Trends in Genetics 15: 34-7
23. Jones PA (2012) Functions of DNA methylation: islands, start sites, gene bodies and beyond. Nat Rev Genet 13: 484-92
24. Kerkhoff C, Voss A, Scholzen TE et al. (2012) Novel insights into the role of S100A8/A9 in skin biology. Exp Dermatol 21: 822-6
25. Koenker R (2012) Package ''quantreg'' http://cran.r-project.org/web/ packages/ quantreg/quantreg.pdf, accessed on 21 April 2013
26. Langevin SM, Houseman EA, Christensen BC et al. (2011) The influence of aging, environmental exposures and local sequence features on the variation of DNA methylation in blood. Epigenetics 6: 908-19
27. Liang Y,Wang P, Zhao M et al. (2012) Demethylation of the FCER1G promoter leads to FcepsilonRI overexpression on monocytes of patients with atopic dermatitis. Allergy 67: 424-30
28. Martino DJ, Prescott SL (2010) Silent mysteries: epigenetic paradigms could hold the key to conquering the epidemic of allergy and immune disease. Allergy 65: 7-15
29. McLean WH, Hansen CD, Eliason MJ et al. (2011) The phenotypic and molecular genetic features of pachyonychia congenita. J Invest Dermatol 131: 1015-7
30. Miller RL, Ho SM (2008) Environmental epigenetics and asthma: current concepts and call for studies. Am J Respir Crit Care Med 177: 567-73
31. Miller SA, Dykes DD, Polesky HF (1988) A simple salting out procedure for extracting DNA from human nucleated cells. Nucleic Acids Res 16:1215
32. Moll R, Divo M, Langbein L (2008) The human keratins: biology and pathology. Histochem Cell Biol 129: 705-33
33. Nakamura T, Sekigawa I, Ogasawara H et al. (2006) Expression of DNMT-1 in patients with atopic dermatitis. Arch Dermatol Res 298: 253-6
34. Petersen AK, Zeilinger S, Kastenmuller G et al. (2013) Epigenetics meets metabolomics: an epigenome-wide association study with blood serum metabolic traits. Hum Mol Genet 23: 534-45
35. Roberson ED, Liu Y, Ryan C et al. (2011) A subset of methylated CpG sites differentiate psoriatic from normal skin. J Invest Dermatol 132: 583-92
36. Roth SA, Simanski M, Rademacher F et al. (2013) The pattern recognition receptor NOD2 mediates Staphylococcus aureus-induced IL-17C expression in keratinocytes. J Invest Dermatol 134: 374-80
37. Schmuth M, Ortegon AM, Mao-Qiang M et al. (2005) Differential expression of fatty acid transport proteins in epidermis and skin appendages. J Invest Dermatol 125: 1174-81
38. Schoggins JW, Rice CM (2011) Interferon-stimulated genes and their antiviral effector functions. Curr Opin Virol 1: 519-25
39. Suarez-Farinas M, Dhingra N, Gittler J et al. (2013) Intrinsic atopic dermatitis shows similar TH2 and higher TH17 immune activation compared with extrinsic atopic dermatitis. J Allergy Clin Immunol 132: 361-70
40. Sugiura H, Ebise H, Tazawa T et al. (2005) Large-scale DNA microarray analysis of atopic skin lesions shows overexpression of an epidermal differentiation gene cluster in the alternative pathway and lack of protective gene expression in the cornified envelope. Br J Dermatol 152: 146-9
41. Suomela S, Cao L, Bowcock A et al. (2004) Interferon alpha-inducible protein 27 (IFI27) is upregulated in psoriatic skin and certain epithelial cancers. J Invest Dermatol 122: 717-21
42. Takahashi K, Paladini RD, Coulombe PA (1995) Cloning and characterization of multiple human genes and cDNAs encoding highly related type II keratin 6 isoforms. J Biol Chem 270: 18581-92
43. Thompson RF, Suzuki M, Lau KW et al. (2009) A pipeline for the quantitative analysis of CG dinucleotide methylation using mass spectrometry. Bioinformatics 25: 2164-70
44. Touleimat N, Tost J (2012) Complete pipeline for Infinium((R)) Human Methylation 450K BeadChip data processing using subset quantile normalization for accurate DNA methylation estimation. Epigenomics 4: 325-41
45. van Eijk KR, de Jong S, Boks MP et al. (2012) Genetic analysis of DNA methylation and gene expression levels in whole blood of healthy human subjects. BMC Genomics 13:636
46. Varley KE, Gertz J, Bowling KM et al. (2013) Dynamic DNA methylation across diverse human cell lines and tissues. Genome Res 23: 555-67
47. Weidinger S, Willis-Owen SA, Kamatani Y et al. (2013) A genome-wide association study of atopic dermatitis identifies loci with overlapping effects on asthma and psoriasis. Hum Mol Genet 22: 4841-56
48. Westergaard M, Henningsen J, Johansen C et al. (2003) Expression and localization of peroxisome proliferator-activated receptors and nuclear factor kappaB in normal and lesional psoriatic skin. J Invest Dermatol 121: 1104-17
49. Westergaard M, Henningsen J, Svendsen ML et al. (2001) Modulation of keratinocyte gene expression and differentiation by PPAR-selective ligands and tetradecylthioacetic acid. J Invest Dermatol 116: 702-12
50. Wolf R, Lewerenz V, Buchau AS et al. (2007) Human S100A15 splice variants are differentially expressed in inflammatory skin diseases and regulated through Th1 cytokines and calcium. Exp Dermatol 16: 685-91
51. Wolf R, Ruzicka T, Yuspa SH (2011) Novel S100A7 (psoriasin)/S100A15 (koebnerisin) subfamily: highly homologous but distinct in regulation and function. Amino Acids 41: 789-96
52. Zhang B, Zhou Y, Lin N et al. (2013) Functional DNA methylation differences between tissues, cell types, and across individuals discovered using the M&M algorithm. Genome Res 23: 1522-40
53. Ziller MJ, Gu H, Muller F et al. (2013) Charting a dynamic DNA methylation landscape of the human genome. Nature 500: 477-81
54. Ziyab AH, Karmaus W, Holloway JW et al. (2012) DNA methylation of the filaggrin gene adds to the risk of eczema associated with loss-of-function variants. J Eur Acad Dermatol Venereol 27:e420-3