Meta-analysis derived atopic dermatitis (MADAD) transcriptome defines a robust AD signature highlighting the involvement of atherosclerosis and lipid metabolism pathways

BMC Medical Genomics

Volumn 8, Issue 1, 2015, Pages

  Ewald, David A ^a,c,d   Malajian, Dana ^a,b,e   Krueger, James G ^a   Workman, Christopher T ^d   Wang, Tianjiao ^f   Tian, Suyan ^f   Litman, Thomas ^c   Guttman Yassky, Emma ^a,b   Suárez Fariñas, Mayte ^a,b  

^a ROCKEFELLER UNIVERSITY   (United States)

^b MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^c LEO PHARMA A S   (Denmark)

^d TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^e College of Physicians and Surg ^*  (United States)

^f JILIN UNIVERSITY   (China)

Author keywords

Atherosclerosis; Atopic dermatitis; Expression analysis; Meta analysis; Transcriptome

Indexed keywords

ACYL COENZYME A; ACYL COENZYME A DESATURASE 1; AQUAPORIN 5; CD1B ANTIGEN; CD48 ANTIGEN; CD6 ANTIGEN; COCHLIN; CXCL11 CHEMOKINE; CXCL2 CHEMOKINE; CYTOKERATIN 19; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; EOTAXIN 3; GELATINASE B; HEMATOPOIETIC CELL KINASE; INTERLEUKIN 12 RECEPTOR BETA1; INTERLEUKIN 13 RECEPTOR ALPHA2; INTERLEUKIN 23; INTERLEUKIN 37; MACROPHAGE DERIVED CHEMOKINE; MITOGEN ACTIVATED PROTEIN KINASE KINASE 1; MONOCYTE CHEMOTACTIC PROTEIN 2; MONOCYTE CHEMOTACTIC PROTEIN 4; PADGEM PROTEIN; PENTRAXIN 3; PURINERGIC P2Y1 RECEPTOR; RANTES; SECRETOGLOBIN; STROMELYSIN; UNINDEXED DRUG; ZINC FINGER PROTEIN;

ARTICLE; ATHEROSCLEROSIS; ATOPIC DERMATITIS; DISEASE SEVERITY; DOWN REGULATION; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE IDENTIFICATION; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; HUMAN; LYMPHOCYTE ACTIVATION; MICROARRAY ANALYSIS; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TH2 CELL; COMPLICATION; GENE REGULATORY NETWORK; GENETICS; IMMUNOLOGY; LIPID METABOLISM; META ANALYSIS; METABOLISM; PROCEDURES;

ATHEROSCLEROSIS; DERMATITIS, ATOPIC; GENE EXPRESSION PROFILING; GENE REGULATORY NETWORKS; HUMANS; LIPID METABOLISM; TH2 CELLS;

EID: 84944711493     PISSN: None     EISSN: 17558794     Source Type: Journal    
DOI: 10.1186/s12920-015-0133-x     Document Type: Article

References (123)

1. Boguniewicz M, Leung DYM. Atopic dermatitis: a disease of altered skin barrier and immune dysregulation. Immunol Rev. 2011;242(1):233-46.
2. Leung DYM. New insights into atopic dermatitis: role of skin barrier and immune dysregulation. Allergol Int. 2013;62(2):151-61.
3. Dhingra N, Suarez-Farinas M, Fuentes-Duculan J, Gittler JK, Shemer A, Raz A, et al. Attenuated neutrophil axis in atopic dermatitis compared to psoriasis reflects TH17 pathway differences between these diseases. J Allergy Clin Immunol. 2013;132(2):498-501.e3.
4. Malajian D, & Guttman-Yassky E. New pathogenic and therapeutic paradigms in atopic dermatitis. Cytokine. 2015;73(2):311-318.
5. N & Guttman-Yassky E. The translational revolution and use of biologics in patients with inflammatory skin diseases. Journal of Allergy and Clinical Immunology. 2015;135(2):324-336.
6. Olsson M, Broberg A, Jernås M, Carlsson L, Rudemo M, Suurküla M, et al. Increased expression of aquaporin 3 in atopic eczema. Allergy. 2006;61(9):1132-7.
7. Guttman-Yassky E, Suárez-Fariñas M, Chiricozzi A, Nograles KE, Shemer A, Fuentes-Duculan J, et al. Broad defects in epidermal cornification in atopic dermatitis identified through genomic analysis. J Allergy Clin Immunol. 2009;124(6):1235-1244.e58.
8. Elias PM, Hatano Y, Williams ML. Basis for the barrier abnormality in atopic dermatitis: Outside-inside-outside pathogenic mechanisms. J Allergy Clin Immunol. 2008;121(6):1337-43.
9. Gittler JK, Shemer A, Suárez-Fariñas M, Fuentes-Duculan J, Gulewicz KJ, Wang CQF, et al. Progressive activation of T(H)2/T(H)22 cytokines and selective epidermal proteins characterizes acute and chronic atopic dermatitis. J Allergy Clin Immunol. 2012;130(6):1344-54.
10. Beck L, Thaçi D, Hamilton JD, Graham NM, Bieber T, Rocklin R, et al. Dupilumab Treatment in Adults with Moderate-to-Severe Atopic Dermatitis. N Engl J Med. 2014;371(2):130-9.
11. Tintle S, Shemer A, Suárez-Fariñas M, Fujita H, Gilleaudeau P, Sullivan-Whalen M, et al. Reversal of atopic dermatitis with narrow-band UVB phototherapy and biomarkers for therapeutic response. J Allergy Clin Immunol. 2011;128(3):583-93.e1-4.
12. Khattri S, Shemer A, Rozenblit M, Dhingra N, Czarnowicki T, Finney R, & Guttman-Yassky E. Cyclosporine in patients with atopic dermatitis modulates activated inflammatory pathways and reverses epidermal pathology. Journal of Allergy and Clinical Immunology. 2014;133(6):1626-634.
13. Jensen JM, Pfeiffer S, Witt M, Bräutigam M, Neumann C, Weichenthal M, et al. Different effects of pimecrolimus and betamethasone on the skin barrier in patients with atopic dermatitis. J Allergy Clin Immunol. 2009;123:1124-33.
14. Plager A, Leontovich AA, Henke SA, Davis MDP, McEvoy MT, Sciallis GF, et al. Early cutaneous gene transcription changes in adult atopic dermatitis and potential clinical implications. Exp Dermatol. 2007;16(1):28-36.
15. Suárez-Fariñas M, Tintle SJ, Shemer A, Chiricozzi A, Nograles K, Cardinale I, et al. Nonlesional atopic dermatitis skin is characterized by broad terminal differentiation defects and variable immune abnormalities. J Allergy Clin Immunol. 2011;127(4):954-64.e1-4.
16. Zaba LC, Suárez-Fariñas M, Fuentes-Duculan J, Nograles KE, Guttman-Yassky E, Cardinale I, et al. Effective treatment of psoriasis with etanercept is linked to suppression of IL-17 signaling, not immediate response TNF genes. J Allergy Clin Immunol. 2009;124(5):1022-10.e1-395.
17. Krueger JG, Fretzin S, Suárez-Fariñas M, Haslett PA, Phipps KM, Cameron GS, et al. IL-17A is essential for cell activation and inflammatory gene circuits in subjects with psoriasis. J Allergy Clin Immunol. 2012;130(1):1-18.
18. Hamilton JD, Suárez-Fariñas M, Dhingra N, Cardinale I, Li X, Kostic A, et al. Dupilumab improves the molecular signature in skin of patients with moderate-to-severe atopic dermatitis. J Allergy Clin Immunol. 2014;134(6):1293-300.
19. Jiang K, Frank MB, Chen Y, Osban J, Jarvis JN. Genomic characterization of remission in juvenile idiopathic arthritis. Arthritis Res Ther. 2013;15(4):R100.
20. Cahan P, Rovegno F, Mooney D, Newman JC, St Laurent G, McCaffrey TA. Meta-analysis of microarray results: challenges, opportunities, and recommendations for standardization. Gene. 2007;401(1-2):12-8.
21. Ramasamy A, Mondry A, Holmes CC, Altman DG. Key issues in conducting a meta-analysis of gene expression microarray datasets. PLoS Med. 2008;5(9):e184.
22. Zakharkin SO, Kim K, Mehta T, Chen L, Barnes S, Scheirer KE, et al. Sources of variation in Affymetrix microarray experiments. BMC Bioinformatics. 2005;6:214.
23. Suárez-Fariñas M, Noggle S, Heke M, Hemmati-Brivanlou A, Magnasco MO. Comparing independent microarray studies: the case of human embryonic stem cells. BMC Genomics. 2005;6:99.
24. Suárez-Fariñas M, Lowes MA, Zaba LC, Krueger JG. Evaluation of the psoriasis transcriptome across different studies by gene set enrichment analysis (GSEA). PLoS One. 2010;5(4):e10247.
25. Tian S, Krueger JG, Li K, Jabbari A, Brodmerkel C, Lowes MA, et al. Meta-analysis derived (MAD) transcriptome of psoriasis defines the 'core' pathogenesis of disease. PLoS One. 2012;7(9):e44274.
26. Chang L-C, Lin H-M, Sibille E, Tseng GC. Meta-analysis methods for combining multiple expression profiles: comparisons, statistical characterization and an application guideline. BMC Bioinformatics. 2013;14(vi):368.
27. Choi JK, Yu U, Kim S, Yoo OJ. Combining multiple microarray studies and modeling interstudy variation. Bioinformatics. 2003;19 Suppl 1:i84-90.
28. Tseng GC, Ghosh D, Feingold E. Comprehensive literature review and statistical considerations for microarray meta-analysis. Nucleic Acids Res. 2012;40(9):3785-99.
29. Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gøtzsche PC, Ioannidis JPA, et al. The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med. 2009;6(7):e1000100.
30. Team R, Core. "R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, 2012." (2014).
31. Gentleman RC, Carey VJ, Bates DM, Bolstad B, Dettling M, Dudoit S, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 2004;5(10):R80.
32. Wu Z, Irizarry RA, Gentleman R, Martinez-Murillo F, Spencer F. A Model-Based Background Adjustment for Oligonucleotide Expression Arrays. J Am Stat Assoc. 2004;99(468):909-17.
33. Johnson WE, Li C, Rabinovic A. Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics. 2007;8(1):118-27.
34. Leek JT, Johnson WE, Parker HS, Jaffe AE, Storey JD. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics. 2012;28(6):882-3.
35. Leek JT, Scharpf RB, Bravo HC, Simcha D, Langmead B, Johnson WE, et al. Tackling the widespread and critical impact of batch effects in highthroughput data. Nat Rev Genet. 2010;11:733-9.
36. Parmigiani G. A Cross-Study Comparison of Gene Expression Studies for the Molecular Classification of Lung Cancer. Clin Cancer Res. 2004;10(9):2922-7.
37. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc. 1995;57(1):289-300.
38. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4:44-57.
39. Suárez-Fariñas M, Arbeit R, Jiang W, Ortenzio FS, Sullivan T, Krueger JG. Suppression of molecular inflammatory pathways by Toll-like receptor 7, 8, and 9 antagonists in a model of IL-23-induced skin inflammation. PLoS One. 2013;8(12):e84634.
40. Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics. 2008;9:559.
41. Ma S, Huang J. Regularized gene selection in cancer microarray meta-analysis. BMC Bioinformatics. 2009;10:1.
42. Tian S, Suarez-Farinas M. Multi-TGDR: a regularization method for multi-class classification in microarray experiments. PLoS One. 2013;8(11):e78302.
43. Mitsui H, Suárez-Fariñas M, Belkin DA, Levenkova N, Fuentes-Duculan J, Coats I, et al. 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. 2012;132(6):1615-26.
44. Rappaport N, Nativ N, Stelzer G, Twik M, Guan-Golan Y, Stein TI, et al. MalaCards: an integrated compendium for diseases and their annotation. Database (Oxford). 2013;2013:bat018.
45. Appace. Solr. 2014.
46. Wittkowski KM, Song T. Nonparametric methods for molecular biology. Methods Mol Biol. 2010;620:105-53.
47. Irizarry RA, Warren D, Spencer F, Kim IF, Biswal S, Frank BC, et al. Multiplelaboratory comparison of microarray platforms. Nat Methods. 2005;2(5):345-50.
48. Lowes MA, Suárez-Fariñas M, Krueger JG. Immunology of psoriasis. Annu Rev Immunol. 2014;32:227-55.
49. Panzer R, Blobel C, Fölster-Holst R, Proksch E. TLR2 and TLR4 expression in atopic dermatitis, contact dermatitis and psoriasis. Exp Dermatol. 2014;23(5):364-6.
50. Kuo I-H, Carpenter-Mendini A, Yoshida T, McGirt LY, Ivanov AI, Barnes KC, et al. Activation of epidermal toll-like receptor 2 enhances tight junction function: implications for atopic dermatitis and skin barrier repair. J Invest Dermatol. 2013;133(4):988-98.
51. Hwang SJ, Ballantyne CM, Sharrett AR, Smith LC, Davis CE, Gotto AM, et al. Circulating adhesion molecules VCAM-1, ICAM-1, and E-selectin in carotid atherosclerosis and incident coronary heart disease cases: the Atherosclerosis Risk In Communities (ARIC) study. Circulation. 1997;96(12):4219-25.
52. Kiechl S, Paré G, Barbalic M, Qi L, Dupuis J, Dehghan A, et al. Association of variation at the ABO locus with circulating levels of soluble intercellular adhesion molecule-1, soluble P-selectin, and soluble E-selectin: a meta-analysis. Circ Cardiovasc Genet. 2011;4(6):681-6.
53. Mead JR, Ramji DP. The pivotal role of lipoprotein lipase in atherosclerosis. Cardiovasc Res. 2002;55(2):261-9.
54. Chen Q, Razzaghi H, Demirci FY, Kamboh MI. Functional significance of lipoprotein lipase Hind III polymorphism associated with the risk of coronary artery disease. Atherosclerosis. 2008;200(1):102-8.
55. Goldberg IJ. Lipoprotein lipase and lipolysis: central roles in lipoprotein metabolism and atherogenesis. J Lipid Res. 1996;37(4):693-707.
56. Xu X, Wang L, Xu C, Zhang P, Yong F, Liu H, et al. Variations in matrix metalloproteinase-1, -3, and -9 genes and the risk of acute coronary syndrome and coronary artery disease in the Chinese Han population. Coron Artery Dis. 2013;24(4):259-65.
57. Abilleira S, Bevan S, Markus HS. The role of genetic variants of matrix metalloproteinases in coronary and carotid atherosclerosis. J Med Genet. 2006;43(12):897-901.
58. Averill MM, Kerkhoff C, Bornfeldt KE. S100A8 and S100A9 in cardiovascular biology and disease. Arterioscler Thromb Vasc Biol. 2012;32(2):223-9.
59. Jin S, Park CO, Shin JU, Noh JY, Lee YS, Lee NR, et al. DAMP molecules S100A9 and S100A8 activated by IL-17A and house-dust mites are increased in atopic dermatitis. Exp Dermatol. 2014;23(12):938-41.
60. Ji Q, Zeng Q, Huang Y, Shi Y, Lin Y, Lu Z, et al. Elevated plasma IL-37, IL-18, and IL-18BP concentrations in patients with acute coronary syndrome. Mediators Inflamm. 2014;2014:165742.
61. Inouye M, Ripatti S, Kettunen J, Lyytikäinen L-P, Oksala N, Laurila P-P, et al. Novel Loci for metabolic networks and multi-tissue expression studies reveal genes for atherosclerosis. PLoS Genet. 2012;8(8):e1002907.
62. Tregouet DA, Barbaux S, Poirier O, Blankenberg S, Bickel C, Escolano S, et al. SELPLG gene polymorphisms in relation to plasma SELPLG levels and coronary artery disease. Ann Hum Genet. 2003;67(Pt 6):504-11.
63. Esaki H, Ewald DA, Ungar B, Rozenblit M. Identification of novel immune and barrier genes in atopic dermatitis by means of laser capture microdissection. J Allergy Clin Immunol. 2015;135(1):153-63.
64. Choi UY, Kang JS, Hwang YS, Kim YJ. Oligoadenylate synthase-like (OASL) proteins: dual functions and associations with diseases. Experimental & molecular medicine. 2015;47(3):e144.
65. Wensink AC, Hack CE, Bovenschen N. Granzymes Regulate Proinflammatory Cytokine Responses. J Immunol. 2015;194(2):491-7.
66. Westerberg R, Mansson JE, Golozoubova V, Shabalina IG, Backlund EC, Tvrdik P, et al. ELOVL3 is an important component for early onset of lipid recruitment in brown adipose tissue. J Biol Chem. 2006;281(8):4958-68.
67. Turlo K, Leung CS, Seo JJ, Goulbourne CN, Adeyo O, Gin P, et al. Equivalent binding of wild-type lipoprotein lipase (LPL) and S447X-LPL to GPIHBP1, the endothelial cell LPL transporter. Biochim Biophys Acta. 2014;1841(7):963-9.
68. Goulbourne CN, Gin P, Tatar A, Nobumori C, Hoenger A, Jiang H, et al. The GPIHBP1-LPL complex is responsible for the margination of triglyceride-rich lipoproteins in capillaries. Cell Metab. 2014;19(5):849-60.
69. Pan Y-S, Lee Y-S, Lee Y-L, Lee W-C, Hsieh S-Y. Differentially profiling the low-expression transcriptomes of human hepatoma using a novel SSH/microarray approach. BMC Genomics. 2006;7:131.
70. Tortola L, Rosenwald E, Abel B, Blumberg H, Schäfer M, Coyle AJ, et al. Psoriasiform dermatitis is driven by IL-36-mediated DC-keratinocyte crosstalk. J Clin Invest. 2012;122(11):3965-76.
71. Nold MF, Nold-Petry CA, Zepp JA, Palmer BE, Bufler P, Dinarello CA. IL-37 is a fundamental inhibitor of innate immunity. Nat Immunol. 2010;11(11):1014-22.
72. da Rosa JC, Malajian D, Shemer A, Rozenblit M, Dhingra N, Czarnowicki T, et al. Patients with atopic dermatitis have attenuated and distinct contact hypersensitivity responses to common allergens in skin. Journal of Allergy and Clinical Immunology, 2015:135(3):712-20.
73. van Smeden J, Janssens M, Kaye ECJ, Caspers PJ, Lavrijsen AP, Vreeken RJ, et al. The importance of free fatty acid chain length for the skin barrier function in atopic eczema patients. Exp Dermatol. 2014;23:45-52.
74. Lee Y, Je Y-J, Lee S-S, Li ZJ, Choi D-K, Kwon Y-B, et al. Changes in transepidermal water loss and skin hydration according to expression of aquaporin-3 in psoriasis. Ann Dermatol. 2012;24(2):168-74.
75. Stachowitz S, Alessandrini F, Abeck D, Ring J, Behrendt H. Permeability barrier disruption increases the level of serine palmitoyltransferase in human epidermis. J Invest Dermatol. 2002;119(5):1048-52.
76. Sawada E, Yoshida N, Sugiura A, Imokawa G. Th1 cytokines accentuate but Th2 cytokines attenuate ceramide production in the stratum corneum of human epidermal equivalents: an implication for the disrupted barrier mechanism in atopic dermatitis. J Dermatol Sci. 2012;68(1):25-35.
77. Tanno O, Ota Y, Kitamura N, Katsube T, Inoue S. Nicotinamide increases biosynthesis of ceramides as well as other stratum corneum lipids to improve the epidermal permeability barrier. Br J Dermatol. 2000;143(3):524-31.
78. Danso MO, van Drongelen V, Mulder A, van Esch J, Scott H, van Smeden J, et al. TNF-α and Th2 Cytokines Induce Atopic Dermatitis-Like Features on Epidermal Differentiation Proteins and Stratum Corneum Lipids in Human Skin Equivalents. J Invest Dermatol. 2014;134(7):1941-50.
79. Hirota T, Saeki H, Tomita K, Tanaka S, Ebe K, Sakashita M, et al. Variants of C-C motif chemokine 22 (CCL22) are associated with susceptibility to atopic dermatitis: case-control studies. PLoS One. 2011;6(11):e26987.
80. Hussein YM, Shalaby SM, Nassar A, Alzahrani SS, Alharbi AS, Nouh M. Association between genes encoding components of the IL-4/IL-4 receptor pathway and dermatitis in children. Gene. 2014;545(2):276-81.
81. Gao P-S, Rafaels NM, Mu D, Hand T, Murray T, Boguniewicz M, et al. Genetic variants in thymic stromal lymphopoietin are associated with atopic dermatitis and eczema herpeticum. J Allergy Clin Immunol. 2010;125(6):1403-1407.e4.
82. Langfelder P, Horvath S. WGCNA package FAQ. 2014 [Online]. Available: http://labs.genetics.ucla.edu/horvath/CoexpressionNetwork/Rpackages/WGCNA/faq.html. [Accessed: 03-Mar-2015].
83. Hon KL, Ching GK, Ng PC, Leung TF. Exploring CCL18, eczema severity and atopy. Pediatr Allergy Immunol. 2011;22(7):704-7.
84. Niebuhr M, Mamerow D, Heratizadeh A, Satzger I, Werfel T. Staphylococcal alpha-toxin induces a higher T cell proliferation and interleukin-31 in atopic dermatitis. Int Arch Allergy Immunol. 2011;156(4):412-5.
85. Guttman-Yassky E, Dhingra N, Leung DYM. New era of biologic therapeutics in atopic dermatitis. Expert Opin Biol Ther. 2013;13(4):549-61.
86. Rozenblit M, Suarez-Farinas M, Shemer A, Khattri S, Gilleaudeau P, Sullivan-Whalen M, et al. Residual genomic profile after cyclosporine treatment may offer insights into atopic dermatitis reoccurrence. J Allergy Clin Immunol. 2014;134(4):955-7.
87. Brandt C, Pavlovic V, Radbruch A, Worm M, Baumgrass R. Low-dose cyclosporine A therapy increases the regulatory T cell population in patients with atopic dermatitis. Allergy. 2009;64(11):1588-96.
88. Marinović Kulišić S, Lipozenčić J, Gregorović G, Gregurek G, Lacković G, Jurić-Lekić G. Expression of e-selectin in the skin of patients with atopic dermatitis: morphometric study. Acta Dermatovenerol Croat. 2010;18(3):141-5.
89. Tsao C-H, Shiau M-Y, Chuang P-H, Chang Y-H, Hwang J. Interleukin-4 regulates lipid metabolism by inhibiting adipogenesis and promoting lipolysis. J Lipid Res. 2014;55(3):385-97.
90. Morgan SA, McCabe EL, Gathercole LL, Hassan-Smith ZK, Larner DP, Bujalska IJ, et al. 11β-HSD1 is the major regulator of the tissue-specific effects of circulating glucocorticoid excess. Proc Natl Acad Sci U S A. 2014;111(24):E2482-91.
91. Pérez-Montarelo D, Hudson NJ, Fernández AI, Ramayo-Caldas Y, Dalrymple BP, Reverter A. Porcine tissue-specific regulatory networks derived from meta-analysis of the transcriptome. PLoS One. 2012;7(9):e46159.
92. Voiculescu VM, Lupu M, Papagheorghe L, Giurcaneanu C, Micu E. Psoriasis and Metabolic Syndrome-scientific evidence and therapeutic implications. Journal of medicine and life. 2014;7(4):468.
93. Oliveira Mde F, Rocha Bde O, Duarte GV. Psoriasis: classical and emerging comorbidities. An Bras Dermatol. 2015;90(1):9-20.
94. Czarnowicki T, Gonzalez J, Shemer A, Malajian D, Xu H, Zheng X, et al. Severe atopic dermatitis is characterized by selective expansion of circulating TH2/TC2 and TH22/TC22, but not TH17/TC17, cells within the skin-homing T-cell population. J Allergy Clin Immunol. 2015.
95. Niwa Y, Sumi H, Akamatsu H. An association between ulcerative colitis and atopic dermatitis, diseases of impaired superficial barriers. J Invest Dermatol. 2004;123(5):999-1000.
96. Myrelid P, Dufmats M, Lilja I, Grinn C, Lannerstad O, Sjödahl R. Atopic manifestations are more common in patients with Crohn disease than in the general population. Scand J Gastroenterol. 2004;39(8):731-6.
97. Cardwell CR, Shields MD, Carson DJ, Patterson CC. A meta-analysis of the association between childhood type 1 diabetes and atopic disease. Diabetes Care. 2003;26(9):2568-74.
98. Schmitt J, Buske-Kirschbaum A, Roessner V. Is atopic disease a risk factor for attention-deficit/hyperactivity disorder? A systematic review. Allergy. 2010;65(12):1506-24.
99. 7 th International Congress of Psoriasis: from Gene to Clinic The Queen Elizabeth II Conference Centre, London, U.K. 11th-13th December 2014. Br. J. Dermatol. 2014;171:6, e105-e173.
100. Dave J, Ahlman MA, Lockshin BN, Bluemke DA, Mehta NN. Vascular inflammation in psoriasis localizes to the arterial wall using a novel imaging technique. J Am Acad Dermatol. 2014;70(6):1137-8.
101. Rose S, Sheth NH, Baker JF, Ogdie A, Raper A, Saboury B, et al. A comparison of vascular inflammation in psoriasis, rheumatoid arthritis, and healthy subjects by FDG-PET/CT: a pilot study. Am J Cardiovasc Dis. 2013;3(4):273-8.
102. Jiang XC, Paultre F, Pearson TA, Reed RG, Francis CK, Lin M, et al. Plasma sphingomyelin level as a risk factor for coronary artery disease. Arterioscler Thromb Vasc Biol. 2000;20(12):2614-8.
103. Nelson JC, Jiang X-C, Tabas I, Tall A, Shea S. Plasma sphingomyelin and subclinical atherosclerosis: findings from the multi-ethnic study of atherosclerosis. Am J Epidemiol. 2006;163(10):903-12.
104. Park T-S, Panek RL, Mueller SB, Hanselman JC, Rosebury WS, Robertson AW, et al. Inhibition of sphingomyelin synthesis reduces atherogenesis in apolipoprotein E-knockout mice. Circulation. 2004;110(22):3465-71.
105. Tabas I. Sphingolipids and atherosclerosis: a mechanistic connection? A therapeutic opportunity? Circulation. 2004;110(22):3400-1.
106. van Smeden J, Janssens M, Gooris GS, Bouwstra JA. The important role of stratum corneum lipids for the cutaneous barrier function. Biochim Biophys Acta. 2014;1841(3):295-313.
107. Janssens M, van Smeden J, Gooris GS, Bras W, Portale G, Caspers PJ, et al. Increase in short-chain ceramides correlates with an altered lipid organization and decreased barrier function in atopic eczema patients. J Lipid Res. 2012;53(12):2755-66.
108. Fujita H, Shemer A, Suárez-Fariñas M, Johnson-Huang LM, Tintle S, Cardinale I, et al. Lesional dendritic cells in patients with chronic atopic dermatitis and psoriasis exhibit parallel ability to activate T-cell subsets. J Allergy Clin Immunol. 2011;128(3):574-82.e1-12.
109. Sääf AM, Tengvall-Linder M, Chang HY, Adler AS, Wahlgren C-FF, Scheynius A, et al. Global expression profiling in atopic eczema reveals reciprocal expression of inflammatory and lipid genes. PLoS One. 2008;3(12):e4017.
110. Hatano Y, Terashi H, Arakawa S, Katagiri K. Interleukin-4 suppresses the enhancement of ceramide synthesis and cutaneous permeability barrier functions induced by tumor necrosis factor-alpha and interferon-gamma in human epidermis. J Invest Dermatol. 2005;124(4):786-92.
111. Hama H. Fatty acid 2-Hydroxylation in mammalian sphingolipid biology. Biochim Biophys Acta. 2010;1801(4):405-14.
112. Pappas A. Epidermal surface lipids. Dermatoendocrinol. 2009;1(2):72-6.
113. Westerberg R, Tvrdik P, Unden AB, Mansson JE, Norlen L, Jakobsson A, et al. Role for ELOVL3 and fatty acid chain length in development of hair and skin function. J Biol Chem. 2004;279(7):5621-9.
114. Fehrenschild D, Galli U, Breiden B, Bloch W, Schettina P, Brodesser S, et al. TCF/Lef1-mediated control of lipid metabolism regulates skin barrier function. J Invest Dermatol. 2012;132(2):337-45.
115. Blaydon DC, Lind LK, Plagnol V, Linton KJ, Smith FJ, Wilson NJ, et al. Mutations in AQP5, encoding a water-channel protein, cause autosomaldominant diffuse nonepidermolytic palmoplantar keratoderma. Am J Hum Genet. 2013;93(2):330-5.
116. Boury-Jamot M, Daraspe J, Bonte F, Perrier E, Schnebert S, Dumas M, et al. Skin aquaporins: function in hydration, wound healing, and skin epidermis homeostasis. Handb Exp Pharmacol. 2009;190:205-17.
117. Nejsum LN, Kwon TH, Jensen UB, Fumagalli O, Frokiaer J, Krane CM, et al. Functional requirement of aquaporin-5 in plasma membranes of sweat glands. Proc Natl Acad Sci U S A. 2002;99(1):511-6.
118. Breuer K, Haussler S, Kapp A, Werfel T. Staphylococcus aureus: colonizing features and influence of an antibacterial treatment in adults with atopic dermatitis. Br J Dermatol. 2002;147(1):55-61.
119. Higaki S, Morohashi M, Yamagishi T, Hasegawa Y. Comparative study of staphylococci from the skin of atopic dermatitis patients and from healthy subjects. Int J Dermatol. 1999;38(4):265-9.
120. Park H-Y, Kim C-R, Huh I-S, Jung M-Y, Seo E-Y, Park J-H, et al. Staphylococcus aureus Colonization in Acute and Chronic Skin Lesions of Patients with Atopic Dermatitis. Ann Dermatol. 2013;25(4):410-6.
121. Matsui K, Nishikawa A. Peptidoglycan from Staphylococcus aureus induces T(H)2 immune response in mice. J Investig Allergol Clin Immunol. 2012;22(2):80-6.
122. Warner JA, McGirt LY, Beck LA. Biomarkers of Th2 polarity are predictive of staphylococcal colonization in subjects with atopic dermatitis. Br J Dermatol. 2009;160(1):183-5.
123. Niebuhr M, Scharonow H, Gathmann M, Mamerow D, Werfel T. Staphylococcal exotoxins are strong inducers of IL-22: A potential role in atopic dermatitis. J Allergy Clin Immunol. 2010;126(6):1176-83.e4.