Genome-Wide DNA Methylation and Transcription Analysis in Psoriatic Epidermis

References

• Griffiths CEM , ArmstrongAW , GudjonssonJE et al. Psoriasis. Lancet397(10281), 1301–1315 (2021).
   PubMed Web of Science ®Google Scholar
• Parisi R , IskandarIYK , KontopantelisE et al. National, regional, and worldwide epidemiology of psoriasis: systematic analysis and modelling study. BMJ369, m1590 (2020).
   PubMed Web of Science ®Google Scholar
• Fernández-Armenteros J , Gómez-ArbonésX , Buti-SolerMet al. Psoriasis, metabolic syndrome and cardiovascular risk factors. A population-based study. JEADV33(1), 128–135 (2019).
   Google Scholar
• Lee K . JAAD game changers: increased risk of diabetes mellitus in relation to the severity of psoriasis, concomitant medication, and comorbidity: a nationwide population-based cohort study. J. Am. Acad. Dermatol.S0190-9622(19), 33136–33136 (2019).
   Google Scholar
• Thomsen S , SkovL , DodgeRet al. Socioeconomic costs and health inequalities from psoriasis: a cohort study. Dermatology235(5), 372–379 (2019).
   PubMed Web of Science ®Google Scholar
• Fu Y , LeeCH , ChiCC. Association of psoriasis with inflammatory bowel disease: a systematic review and meta-analysis. JAMA Dermatol.154(12), 1417–1423 (2018).
   PubMed Web of Science ®Google Scholar
• Luo Y , QuK , KuaiLet al. Epigenetics in psoriasis: perspective of DNA methylation. MGG296(5), 1027–1040 (2021).
   Google Scholar
• Robertson KD . DNA methylation and human disease. Nat. Rev. Genet.6(8), 597–610 (2005).
   PubMed Web of Science ®Google Scholar
• Rosen ED , KaestnerKH , NatarajanRet al. Epigenetics and epigenomics: implications for diabetes and obesity. Diabetes67(10), 1923–1931 (2018).
   PubMed Web of Science ®Google Scholar
• Dopytalska K , CiechanowiczP , WiszniewskiK et al. The role of epigenetic factors in psoriasis. Int. J. Mol. Sci.22(17), 9294 (2021).
   PubMed Web of Science ®Google Scholar
• Doerfler W , TothM , KochanekSet al. Eukaryotic DNA methylation: facts and problems. FEBS Lett.268(2), 329–333 (1990).
   PubMed Web of Science ®Google Scholar
• Zhang P , SuY , ChenH et al. Abnormal DNA methylation in skin lesions and PBMCs of patients with psoriasis vulgaris. J. Dermatol. Sci.60(1), 40–42 (2010).
   PubMed Web of Science ®Google Scholar
• Roberson E , LiuY , RyanCet al. A subset of methylated CpG sites differentiate psoriatic from normal skin. J. Invest. Dermatol.132, 583–592 (2012).
   PubMed Web of Science ®Google Scholar
• Gu X , NylanderE , CoatesP et al. Correlation between reversal of DNA methylation and clinical symptoms in the psoriatic epidermis following narrow-band UVB phototherapy. J. Invest. Dermatol.135(8), 2077–2083 (2015).
   PubMed Web of Science ®Google Scholar
• Colombo I , SangiovanniE , MaggioRet al. HaCaT cells as a reliable in vitro differentiation model to dissect the inflammatory/repair response of human keratinocytes. Mediators Inflamm.2017, 7435621 (2017).
   PubMed Web of Science ®Google Scholar
• Quaresma JAS . Organization of the skin immune system and compartmentalized immune responses in infectious diseases. Clin. Microbiol. Rev.32(4), e00034–18 (2019).
   PubMed Web of Science ®Google Scholar
• Biernaskie J , ParisM , MorozovaOet al. SKPs derive from hair follicle precursors and exhibit properties of adult dermal stem cells. Cell Stem Cell5(6), 610–623 (2009).
   PubMed Web of Science ®Google Scholar
• Solé-Boldo L , RaddatzG , GutekunstJet al. Differentiation-related epigenomic changes define clinically distinct keratinocyte cancer subclasses. Mol. Syst. Biol.18(9), e11073 (2022).
   PubMed Web of Science ®Google Scholar
• Wang C , WuL , BulekKet al. The psoriasis-associated D10N variant of the adaptor Act1 with impaired regulation by the molecular chaperone hsp90. Nat. Immunol.14(1), 72–81 (2013).
   PubMed Web of Science ®Google Scholar
• Allakhverdi Z , ComeauMR , JessupHKet al. Thymic stromal lymphopoietin is released by human epithelial cells in response to microbes, trauma, or inflammation and potently activates mast cells. J. Exp. Med.204(2), 253–258 (2007).
   PubMed Web of Science ®Google Scholar
• Seifarth FG , LaxJE , HarveyJet al. Topical heat shock protein 70 prevents imiquimod-induced psoriasis-like inflammation in mice. Cell Stress Chaperones23(5), 1129–1135 (2018).
   PubMed Web of Science ®Google Scholar
• Lebwohl M . Psoriasis. Ann. Intern. Med.168(7), itc49–itc64 (2018).
   PubMed Web of Science ®Google Scholar
• Nickoloff BJ , NestleFO. Recent insights into the immunopathogenesis of psoriasis provide new therapeutic opportunities. J. Clin. Invest.113(12), 1664–1675 (2004).
   PubMed Web of Science ®Google Scholar
• Zhao W , LangfelderP , FullerT et al. Weighted gene coexpression network analysis: state of the art. J. Biopharm. Stat.20(2), 281–300 (2010).
   PubMed Web of Science ®Google Scholar
• Bolstad BM , IrizarryRA , AstrandM et al. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics19(2), 185–193 (2003).
   PubMed Web of Science ®Google Scholar
• Leek JT , JohnsonWE , ParkerHS et al. The sva package for removing batch effects and other unwanted variation in high-throughput experiments. Bioinformatics28(6), 882–883 (2012).
   PubMed Web of Science ®Google Scholar
• Ritchie ME , PhipsonB , WuDet al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res.43(7), e47 (2015).
   PubMed Web of Science ®Google Scholar
• Morris TJ , ButcherLM , FeberAet al. ChAMP: 450k Chip Analysis Methylation Pipeline. Bioinformatics30(3), 428–430 (2014).
   PubMed Web of Science ®Google Scholar
• Xu M , OuyangT , LvK et al. Integrated WGCNA and PPI network to screen hub genes signatures for infantile hemangioma. Front. Genet.11, 614195 (2020).
   PubMed Web of Science ®Google Scholar
• Langfelder P , HorvathS. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics9, 559 (2008).
   PubMed Web of Science ®Google Scholar
• Zhang B , HorvathS. A general framework for weighted gene co-expression network analysis. Stat. Appl. Genet. Mol. Biol.4, Article 17 (2005).
   Web of Science ®Google Scholar
• Goeman JJ . L1 penalized estimation in the Cox proportional hazards model. Biom. J.52(1), 70–84 (2010).
   PubMed Web of Science ®Google Scholar
• Tibshirani R . The LASSO method for variable selection in the Cox model. Stat. Med.16(4), 385–395 (1997).
   PubMed Web of Science ®Google Scholar
• Bindea G , MlecnikB , TosoliniMet al. Spatiotemporal dynamics of intratumoral immune cells reveal the immune landscape in human cancer. Immunity39(4), 782–795 (2013).
   PubMed Web of Science ®Google Scholar
• Hänzelmann S , CasteloR , GuinneyJ. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinformatics14, 7 (2013).
   PubMed Web of Science ®Google Scholar
• Guilloteau K , ParisI , PedrettiNet al. Skin inflammation induced by the synergistic action of IL-17A, IL-22, oncostatin M, IL-1{alpha}, and TNF-{alpha} recapitulates some features of psoriasis. J. Immunol.184(9), 5263–5270 (2010).
   PubMed Web of Science ®Google Scholar
• Teng X , HuZ , WeiXet al. IL-37 ameliorates the inflammatory process in psoriasis by suppressing proinflammatory cytokine production. J. Immunol.192(4), 1815–1823 (2014).
   PubMed Web of Science ®Google Scholar
• Mehta NN , AzfarRS , ShinDB et al. Patients with severe psoriasis are at increased risk of cardiovascular mortality: cohort study using the General Practice Research Database. Eur. Heart J.31(8), 1000–1006 (2010).
   PubMed Web of Science ®Google Scholar
• Qin W , WolfP , LiuNet al. DNA methylation requires a DNMT1 ubiquitin interacting motif (UIM) and histone ubiquitination. Cell Res.25(8), 911–929 (2015).
   PubMed Web of Science ®Google Scholar
• Schübeler D . Function and information content of DNA methylation. Nature517(7534), 321–326 (2015).
   PubMed Web of Science ®Google Scholar
• Yan W , HermanJG , GuoM. Epigenome-based personalized medicine in human cancer. Epigenomics8(1), 119–133 (2016).
   PubMed Web of Science ®Google Scholar
• Krainer J , WeinhäuselA , HanakKet al. EPIC-TABSAT: analysis tool for targeted bisulfite sequencing experiments and array-based methylation studies. Nucleic Acids Res.47(W1), W166–W170 (2019).
   PubMed Web of Science ®Google Scholar
• Zhang P , ZhaoM , LiangGet al. Whole-genome DNA methylation in skin lesions from patients with psoriasis vulgaris. J. Autoimmun.41, 17–24 (2013).
   PubMed Web of Science ®Google Scholar
• Mervis J , McGeeJ. DNA methylation and inflammatory skin diseases. Arch. Dermatol. Res.312(7), 461–466 (2020).
   PubMed Web of Science ®Google Scholar
• Deaton A , BirdA. CpG islands and the regulation of transcription. Genes Dev.25(10), 1010–1022 (2011).
   PubMed Web of Science ®Google Scholar
• Tang L , ChengY , ZhuCet al. Integrative methylome and transcriptome analysis to dissect key biological pathways for psoriasis in Chinese Han population. J. Dermatol. Sci.91(3), 285–291 (2018).
   PubMed Web of Science ®Google Scholar
• Chandra A , SenapatiS , RoyS et al. Epigenome-wide DNA methylation regulates cardinal pathological features of psoriasis. Clin. Epigenetics10(1), 108 (2018).
   PubMedGoogle Scholar
• Allum F , ShaoX , GuénardFet al. Characterization of functional methylomes by next-generation capture sequencing identifies novel disease-associated variants. Nat. Commun.6, 7211 (2015).
   PubMed Web of Science ®Google Scholar
• Rakyan VK , DownTA , BaldingDJ et al. Epigenome-wide association studies for common human diseases. Nat. Rev. Genet.12(8), 529–541 (2011).
   PubMed Web of Science ®Google Scholar
• Sapozhnikov DM , SzyfM. Unraveling the functional role of DNA demethylation at specific promoters by targeted steric blockage of DNA methyltransferase with CRISPR/dCas9. Nat. Commun.12(1), 5711 (2021).
   PubMed Web of Science ®Google Scholar
• Chen Y , ChenT , SuMet al. Whole genome DNA methylation analysis of obstructive sleep apnea: IL1R2, NPR2, AR, SP140 methylation and clinical phenotype. Sleep39(4), 743–755 (2016).
   PubMed Web of Science ®Google Scholar
• Fyhrquist N , MuirheadG , Prast-NielsenSet al. Microbe–host interplay in atopic dermatitis and psoriasis. Nat. Commun.10(1), 4703 (2019).
   PubMed Web of Science ®Google Scholar
• Tsoi LC , StuartPE , TianCet al. Large scale meta-analysis characterizes genetic architecture for common psoriasis associated variants. Nat. Commun.8, 15382 (2017).
   PubMed Web of Science ®Google Scholar
• Gudjonsson JE , ThorarinssonAM , SigurgeirssonB et al. Streptococcal throat infections and exacerbation of chronic plaque psoriasis: a prospective study. Br. J. Dermatol.149(3), 530–534 (2003).
   PubMed Web of Science ®Google Scholar
• Conrad C , DiDomizio J , MylonasAet al. TNF blockade induces a dysregulated type I interferon response without autoimmunity in paradoxical psoriasis. Nat. Commun.9(1), 25 (2018).
   PubMed Web of Science ®Google Scholar
• Wang X , ZhaoX , FengCet al. IL-36γ transforms the tumor microenvironment and promotes type 1 lymphocyte-mediated antitumor immune responses. Cancer Cell28(3), 296–306 (2015).
   PubMed Web of Science ®Google Scholar
• Dombrowski Y , PericM , KoglinSet al. Cytosolic DNA triggers inflammasome activation in keratinocytes in the psoriatic lesions. Sci. Transl. Med.3(82), 82ra38 (2011).
   PubMed Web of Science ®Google Scholar
• Guttman-Yassky E , NogralesKE , KruegerJG. Contrasting pathogenesis of atopic dermatitis and psoriasis – part I: clinical and pathologic concepts. J. Allergy Clin. Immunol.127(5), 1110–1118 (2011).
   PubMed Web of Science ®Google Scholar
• Weng Z , PatelAB , VasiadiM et al. Luteolin inhibits human keratinocyte activation and decreases NF-κB induction that is increased in psoriatic skin. PLoS One9(2), e90739 (2014).
   PubMed Web of Science ®Google Scholar
• Patel F , MarusinaA , DuongC et al. NKG2C, HLA-E and their association with psoriasis. Exp. Dermatol.22(12), 797–799 (2013).
   PubMed Web of Science ®Google Scholar
• Li G , DingH , YuXet al. Spermidine suppresses inflammatory DC function by activating the FOXO3 pathway and counteracts autoimmunity. iScience23(1), 100807 (2020).
   PubMed Web of Science ®Google Scholar
• Postat J , OlekhnovitchR , LemaîtreF et al. A metabolism-based quorum sensing mechanism contributes to termination of inflammatory responses. Immunity49(4), 654–665.e655 (2018).
   PubMed Web of Science ®Google Scholar
• Leonardi C , SeeK , GalloGet al. Psoriasis severity assessment combining physician and patient reported outcomes: the optimal psoriasis assessment tool. Dermatol. Ther. (Heidelb.)11(4), 1249–1263 (2021).
   PubMed Web of Science ®Google Scholar
• Ozdemir M , KiyiciA , BaleviA et al. Assessment of ischaemia-modified albumin level in patients with psoriasis. Clin. Exp. Dermatol.37(6), 610–614 (2012).
   PubMed Web of Science ®Google Scholar
• Cunden LS , GaillardA , NolanEM. Calcium ions tune the zinc-sequestering properties and antimicrobial activity of human S100A12. Chem. Sci.7(2), 1338–1348 (2016).
   PubMed Web of Science ®Google Scholar
• Wilsmann-Theis D , WagenpfeilJ , HolzingerDet al. Among the S100 proteins, S100A12 is the most significant marker for psoriasis disease activity. JEADV30(7), 1165–1170 (2016).
   Google Scholar
• Meijer B , GearryRB , DayAS. The role of S100A12 as a systemic marker of inflammation. Int. J. Inflam.2012, 907078 (2012).
   PubMedGoogle Scholar
• Perng Y , LenschowD. ISG15 in antiviral immunity and beyond. Nature reviews. Microbiology16(7), 423–439 (2018).
   Web of Science ®Google Scholar
• Dzimianski J , ScholteF , BergeronÉet al. ISG15: it’s complicated. J. Mol. Biol.431(21), 4203–4216 (2019).
   PubMed Web of Science ®Google Scholar
• Durfee LA , LyonN , SeoK et al. The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell38(5), 722–732 (2010).
   PubMed Web of Science ®Google Scholar
• Thery F , MartinaL , AsselmanCet al. Ring finger protein 213 assembles into a sensor for ISGylated proteins with antimicrobial activity. Nat. Commun.12(1), 5772 (2021).
   PubMed Web of Science ®Google Scholar
• Durfee L , LyonN , SeoK et al. The ISG15 conjugation system broadly targets newly synthesized proteins: implications for the antiviral function of ISG15. Mol. Cell38(5), 722–732 (2010).
   PubMed Web of Science ®Google Scholar
• Mitchell G , IsbergRR. Innate immunity to intracellular pathogens: balancing microbial elimination and inflammation. Cell Host Microbe22(2), 166–175 (2017).
   PubMed Web of Science ®Google Scholar
• Swaim C , ScottA , CanadeoL et al. Extracellular ISG15 signals cytokine secretion through the LFA-1 integrin receptor. Mol. Cell68(3), 581–590.e585 (2017).
   PubMed Web of Science ®Google Scholar
• Bogunovic D , Boisson-DupuisS , CasanovaJ. ISG15: leading a double life as a secreted molecule. Exp. Mol. Med.45, e18 (2013).
   PubMed Web of Science ®Google Scholar
• Wang X , YuY , HuangYet al. Identification of potential diagnostic gene biomarkers in patients with osteoarthritis. Sci. Rep.10(1), 13591 (2020).
   PubMed Web of Science ®Google Scholar
• Hao J , SerohijosAW , NewtonGet al. Identification and rational redesign of peptide ligands to CRIP1, a novel biomarker for cancers. PLoS Comput. Biol.4(8), e1000138 (2008).
   PubMed Web of Science ®Google Scholar
• Chen C , TanL , ZhuWet al. Targeting myeloid-derived suppressor cells is a novel strategy for anti-psoriasis therapy. Mediators Inflamm.2020, 8567320 (2020).
   PubMed Web of Science ®Google Scholar
• Ilkovitch D , FerrisLK. Myeloid-derived suppressor cells are elevated in patients with psoriasis and produce various molecules. Mol. Med. Rep.14(4), 3935–3940 (2016).
   PubMed Web of Science ®Google Scholar
• Soler D , YoungA , FiessingerLet al. Increased, but functionally impaired, CD14(+) HLA-DR(-/low) myeloid-derived suppressor cells in psoriasis: a mechanism of dysregulated T cells. J. Invest. Dermatol.136(4), 798–808 (2016).
   PubMed Web of Science ®Google Scholar
• Gabrilovich DI , NagarajS. Myeloid-derived suppressor cells as regulators of the immune system. Nat. Rev. Immunol.9(3), 162–174 (2009).
   PubMed Web of Science ®Google Scholar
• Auffray C , SiewekeMH , GeissmannF. Blood monocytes: development, heterogeneity, and relationship with dendritic cells. Annu. Rev. Immunol.27, 669–692 (2009).
   PubMed Web of Science ®Google Scholar
• Cao L , ChungJ , TeshimaTet al. Myeloid-derived suppressor cells in psoriasis are an expanded population exhibiting diverse T-cell-suppressor mechanisms. J. Invest. Dermatol.136(9), 1801–1810 (2016).
   PubMed Web of Science ®Google Scholar
• Wang Y , YinK , TianJet al. Granulocytic myeloid-derived suppressor cells promote the stemness of colorectal cancer cells through exosomal S100A9. Adv. Sci. (Weinh.)6(18), 1901278 (2019).
   PubMedGoogle Scholar
• Soler D , SugiyamaH , YoungA et al. Psoriasis patients exhibit impairment of the high potency CCR5(+) T regulatory cell subset. Clin. Immunol.149(1), 111–118 (2013).
   PubMed Web of Science ®Google Scholar
• Oka T , SugayaM , TakahashiNet al. CXCL17 attenuates imiquimod-induced psoriasis-like skin inflammation by recruiting myeloid-derived suppressor cells and regulatory T cells. J. Immunol.198(10), 3897–3908 (2017).
   PubMed Web of Science ®Google Scholar
• Mellor L , Gago-LopezN , BakiriLet al. Keratinocyte-derived S100A9 modulates neutrophil infiltration and affects psoriasis-like skin and joint disease. Ann. Rheum. Dis.81(10), 1400–1408 (2022).
   PubMed Web of Science ®Google Scholar
• Müller A , DickmannsA , ReschCet al. The CDK4/6-EZH2 pathway is a potential therapeutic target for psoriasis. J. Clin. Invest.130(11), 5765–5781 (2020).
   PubMed Web of Science ®Google Scholar
• Zimmermann M , KoreckA , MeyerNet al. TNF-like weak inducer of apoptosis (TWEAK) and TNF-α cooperate in the induction of keratinocyte apoptosis. J. Allergy Clin. Immunol.127(1), 200–207; 207.e201-210 (2011).
   PubMed Web of Science ®Google Scholar
• Andres-Ejarque R , AleH , GrysKet al. Enhanced NF-κB signaling in type-2 dendritic cells at baseline predicts non-response to adalimumab in psoriasis. Nat. Commun.12(1), 4741 (2021).
   PubMed Web of Science ®Google Scholar