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Research Article

The hMeDIP-Seq Identified INPP4A as a Novel Biomarker for Eosinophilic Chronic Rhinosinusitis with Nasal Polyps

ORCID Icon, , , , , , & ORCID Icon show all
Pages 757-775 | Received 13 Feb 2022, Accepted 08 Jun 2022, Published online: 29 Jun 2022

References

  • Fokkens WJ , LundVJ , HopkinsCet al. European Position Paper on Rhinosinusitis and Nasal Polyps 2020. Rhinology58(Suppl. S29), 1–464 (2020).
  • Wang X , ZhangN , BoMet al. Diversity of TH cytokine profiles in patients with chronic rhinosinusitis: a multicenter study in Europe, Asia, and Oceania. J. Allergy Clin. Immunol.138(5), 1344–1353 (2016).
  • Fujieda S , ImotoY , KatoYet al. Eosinophilic chronic rhinosinusitis. Allergol. Int.68(4), 403–412 (2019).
  • Grgić MV , ĆupićH , KalogjeraL , BaudoinT. Surgical treatment for nasal polyposis: predictors of outcome. Eur. Arch. Otorhinolaryngol.272(12), 3735–3743 (2015).
  • Lou H , MengY , PiaoY , WangC , ZhangL , BachertC. Predictive significance of tissue eosinophilia for nasal polyp recurrence in the Chinese population. Am. J. Rhinol. Allergy29(5), 350–356 (2015).
  • Kim SJ , LeeKH , KimSW , ChoJS , ParkYK , ShinSY. Changes in histological features of nasal polyps in a Korean population over a 17-year period. Otolaryngol. Head Neck Surg.149(3), 431–437 (2013).
  • Wang W , GaoY , ZhuZet al. Changes in the clinical and histological characteristics of Chinese chronic rhinosinusitis with nasal polyps over 11 years. Int. Forum Allergy Rhinol.9(2), 149–157 (2019).
  • Johansson L , AkerlundA , HolmbergK , MelénI , BendeM. Prevalence of nasal polyps in adults: the Skövde population-based study. Ann. Otol. Rhinol. Laryngol.112(7), 625–629 (2003).
  • Maher B . Personal genomes: the case of the missing heritability. Nature456(7218), 18–21 (2008).
  • Vercelli D . Genetics, epigenetics, and the environment: switching, buffering, releasing. J. Allergy Clin. Immunol.113(3), 381–386 (2004).
  • Li J , JiaoJ , WangMet al. Hypomethylation of the IL8 promoter in nasal epithelial cells of patients with chronic rhinosinusitis with nasal polyps. J. Allergy Clin. Immunol.144(4), 993–1003.e1012 (2019).
  • Li J , JiaoJ , GaoY , ZhangY , ZhangL. Association between methylation in nasal epithelial TSLP gene and chronic rhinosinusitis with nasal polyps. Allergy Asthma Clin. Immunol.15, 71 (2019).
  • Pérez-Novo CA , ZhangY , DenilSet al. Staphylococcal enterotoxin B influences the DNA methylation pattern in nasal polyp tissue: a preliminary study. Allergy Asthma Clin. Immunol.9(1), 48 (2013).
  • Kidoguchi M , NoguchiE , NakamuraTet al. DNA methylation of proximal PLAT promoter in chronic rhinosinusitis with nasal polyps. Am. J. Rhinol. Allergy32(5), 374–379 (2018).
  • Haimerl P , BernhardtU , SchindelaSet al. Inflammatory macrophage memory in nonsteroidal anti-inflammatory drug-exacerbated respiratory disease. J. Allergy Clin. Immunol.147(2), 587–599 (2021).
  • Cheong HS , ParkSM , KimMOet al. Genome-wide methylation profile of nasal polyps: relation to aspirin hypersensitivity in asthmatics. Allergy66(5), 637–644 (2011).
  • Ito S , D’alessioAC , TaranovaOV , HongK , SowersLC , ZhangY. Role of TET proteins in 5mC to 5hmC conversion, ES-cell self-renewal and inner cell mass specification. Nature466(7310), 1129–1133 (2010).
  • He YF , LiBZ , LiZet al. TET-mediated formation of 5-carboxylcytosine and its excision by TDG in mammalian DNA. Science333(6047), 1303–1307 (2011).
  • Hahn MA , SzabóPE , PfeiferGP. 5-Hydroxymethylcytosine: a stable or transient DNA modification?Genomics104(5), 314–323 (2014).
  • Zhou T , XiongJ , WangMet al. Structural basis for hydroxymethylcytosine recognition by the SRA domain of UHRF2. Mol. Cell54(5), 879–886 (2014).
  • Hashimoto H , LiuY , UpadhyayAKet al. Recognition and potential mechanisms for replication and erasure of cytosine hydroxymethylation. Nucleic Acids Res.40(11), 4841–4849 (2012).
  • Yao C , XuY. The expression and significance of TET gene and 5hmC in chronic rhinosinusitis. Lin Chuang Er Bi Yan Hou Tou Jing Wai Ke Za Zhi35(1), 52–56 (2021).
  • Lund VJ , KennedyDW. Staging for rhinosinusitis. Otolaryngol. Head Neck Surg.117(3 Pt 2), S35–S40 (1997).
  • Bhattacharyya N . Test–retest reliability of computed tomography in the assessment of chronic rhinosinusitis. Laryngoscope109(7 Pt 1), 1055–1058 (1999).
  • Meng Y , LouH , WangC , ZhangL. Predictive significance of computed tomography in eosinophilic chronic rhinosinusitis with nasal polyps. Int. Forum Allergy Rhinol.6(8), 812–819 (2016).
  • Chen J , WuS , WenSet al. The mechanism of environmental endocrine disruptors (DEHP) induces epigenetic transgenerational inheritance of cryptorchidism. PLoS ONE10(6), e0126403 (2015).
  • Weng YI , HuangTH , YanPS. Methylated DNA immunoprecipitation and microarray-based analysis: detection of DNA methylation in breast cancer cell lines. Methods Mol. Biol.590, 165–176 (2009).
  • Langmead B , SalzbergSL. Fast gapped-read alignment with Bowtie 2. Nature Methods9(4), 357–9 (2012 Mar 4). doi:10.1038/nmeth.1923
  • Zhang Y , LiuT , MeyerCAet al. Model-based analysis of ChIP-Seq (MACS). Genome biology9(9), R137 (2008).
  • Ho J , HamizanAW , AlvaradoR , RimmerJ , SewellWA , HarveyRJ. Systemic predictors of eosinophilic chronic rhinosinusitis. Am. J. Rhinol. Allergy32(4), 252–257 (2018).
  • Kim JY , ChaMJ , ParkYSet al. Upregulation of FZD5 in eosinophilic chronic rhinosinusitis with nasal polyps by epigenetic modification. Mol. Cells42(4), 345–355 (2019).
  • Zhang XH , ZhangYN , LiHBet al. Overexpression of miR-125b, a novel regulator of innate immunity, in eosinophilic chronic rhinosinusitis with nasal polyps. Am. J. Respir. Crit. Care Med.185(2), 140–151 (2012).
  • Tsagaratou A , ÄijöT , LioCWet al. Dissecting the dynamic changes of 5-hydroxymethylcytosine in T-cell development and differentiation. Proc. Natl Acad. Sci. USA111(32), E3306–3315 (2014).
  • Dutta A , VenkataganeshH , LovePE. New insights into epigenetic regulation of T cell differentiation. Cells10(12), 3459 (2021).
  • Gao X , SongY , WuJet al. Iron-dependent epigenetic modulation promotes pathogenic T cell differentiation in lupus. J. Clin. Invest.132(9), e152345 (2022).
  • Peng V , XingX , BandoJKet al. Whole-genome profiling of DNA methylation and hydroxymethylation identifies distinct regulatory programs among innate lymphocytes. Nat. Immunol.23(4), 619–631 (2022).
  • Li Y , WangW , YingS , LanF , ZhangL. A potential role of group 2 innate lymphoid cells in eosinophilic chronic rhinosinusitis with nasal polyps. Allergy Asthma Immunol. Res.13(3), 363–374 (2021).
  • Walford HH , LundSJ , BaumREet al. Increased ILC2s in the eosinophilic nasal polyp endotype are associated with corticosteroid responsiveness. Clin. Immunol.155(1), 126–135 (2014).
  • Efimova OA , KoltsovaAS , KrapivinMI , TikhonovAV , PendinaAA. Environmental epigenetics and genome flexibility: focus on 5-hydroxymethylcytosine. Int. J. Mol. Sci.21(9), 3223 (2020).
  • Avram GE , MarcuA , MoatarAet al. Changes in global DNA methylation and hydroxymethylation in oral mucosa according to tobacco smoke exposure. J. Int. Med. Res.48(9), 300060520954677 (2020).
  • Delatte B , JeschkeJ , DefranceMet al. Genome-wide hydroxymethylcytosine pattern changes in response to oxidative stress. Sci. Rep.5, 12714 (2015).
  • Guo J , XiangQ , XinY , HuangY , ZouG , LiuT. miR-544 promotes maturity and antioxidation of stem cell-derived endothelial like cells by regulating the YY1/TET2 signalling axis. Cell Commun. Signal.18(1), 35 (2020).
  • Stefan-Lifshitz M , KarakoseE , CuiLet al. Epigenetic modulation of β cells by interferon-α via PNPT1/mir-26a/TET2 triggers autoimmune diabetes. JCI Insight4(5), e126663 (2019).
  • Gao X , SongY , DuPet al. Administration of a microRNA-21 inhibitor improves the lupus-like phenotype in MRL/lpr mice by repressing Tfh cell-mediated autoimmune responses. Int. Immunopharmacol.106, 108578 (2022).
  • Jones DT , ReedRR. Golf: an olfactory neuron specific-G protein involved in odorant signal transduction. Science244(4906), 790–795 (1989).
  • Kerr DS , Von DanneckerLE , DavalosM , MichaloskiJS , MalnicB. Ric-8B interacts with G alpha olf and G gamma 13 and co-localizes with G alpha olf, G beta 1 and G gamma 13 in the cilia of olfactory sensory neurons. Mol. Cell. Neurosci.38(3), 341–348 (2008).
  • Fuchs T , Saunders-PullmanR , MasuhoIet al. Mutations in GNAL cause primary torsion dystonia. Nat. Genet.45(1), 88–92 (2013).
  • Bakalyar HA , ReedRR. Identification of a specialized adenylyl cyclase that may mediate odorant detection. Science250(4986), 1403–1406 (1990).
  • Munger SD , LaneAP , ZhongHet al. Central role of the CNGA4 channel subunit in Ca2+-calmodulin-dependent odor adaptation. Science294(5549), 2172–2175 (2001).
  • Li F , Ponissery-SaiduS , YeeKKet al. Heterotrimeric G protein subunit Gγ13 is critical to olfaction. J. Neurosci.33(18), 7975–7984 (2013).
  • Bhutta MF , Al-ShaikhS , LatifM , LeeR , UraibyJ. Nasal polyps do not contain olfactory structures. Rhinology49(2), 185–189 (2011).
  • Wettschureck N , OffermannsS. Mammalian G proteins and their cell type specific functions. Physiol. Rev.85(4), 1159–1204 (2005).
  • Zhang HG , ChengYQ , LiuYet al. Gαq-protein carboxyl terminus imitation polypeptide GCIP-27 attenuates proliferation of vascular smooth muscle cells and vascular remodeling in spontaneously hypertensive rats. Biol. Pharm. Bull.34(10), 1527–1532 (2011).
  • Zou QY , ZhaoYJ , ZhouCet al. G Protein α subunit 14 mediates fibroblast growth factor 2-induced cellular responses in human endothelial cells. J. Cell. Physiol.234(7), 10184–10195 (2019).
  • Lachmann P , HickmannL , SteglichAet al. Interference with Gsα-coupled receptor signaling in renin-producing cells leads to renal endothelial damage. J. Am. Soc. Nephrol.28(12), 3479–3489 (2017).
  • Gosepath J , BriegerJ , LehrHA , MannWJ. Expression, localization, and significance of vascular permeability/vascular endothelial growth factor in nasal polyps. Am. J. Rhinol.19(1), 7–13 (2005).
  • Khurana N , PulsipherA , JedrzkiewiczJet al. Inflammation-driven vascular dysregulation in chronic rhinosinusitis. Int. Forum Allergy Rhinol.11(6), 976–983 (2021).
  • Abbas EE , LiC , XieAet al. Distinct clinical pathology and microbiota in chronic rhinosinusitis with nasal polyps endotypes. Laryngoscope131(1), E34–e44 (2021).
  • Shimizu S , TojimaI , NakamuraK , AraiH , KouzakiH , ShimizuT. Nasal polyp fibroblasts (NPFs)-derived exosomes are important for the release of vascular endothelial growth factor from cocultured eosinophils and NPFs. Auris Nasus Larynx49(3), 407–414 (2021).
  • Li X , MurrayF , KoideNet al. Divergent requirement for Gαs and cAMP in the differentiation and inflammatory profile of distinct mouse Th subsets. J. Clin. Invest.122(3), 963–973 (2012).
  • Norris FA , MajerusPW. Hydrolysis of phosphatidylinositol 3,4-bisphosphate by inositol polyphosphate 4-phosphatase isolated by affinity elution chromatography. J. Biol. Chem.269(12), 8716–8720 (1994).
  • Ivetac I , GurungR , HakimSet al. Regulation of PI(3)K/Akt signalling and cellular transformation by inositol polyphosphate 4-phosphatase-1. EMBO Rep.10(5), 487–493 (2009).
  • Shin HW , HayashiM , ChristoforidisSet al. An enzymatic cascade of Rab5 effectors regulates phosphoinositide turnover in the endocytic pathway. J. Cell Biol.170(4), 607–618 (2005).
  • Khanna K , ChaudhuriR , AichJet al. Secretory inositol polyphosphate 4-phosphatase protects against airway inflammation and remodeling. Am. J. Respir. Cell Mol. Biol.60(4), 399–412 (2019).
  • Sharma M , BatraJ , MabalirajanUet al. A genetic variation in inositol polyphosphate 4 phosphatase a enhances susceptibility to asthma. Am. J. Respir. Crit. Care Med.177(7), 712–719 (2008).
  • Aich J , MabalirajanU , AhmadT , AgrawalA , GhoshB. Loss-of-function of inositol polyphosphate-4-phosphatase reversibly increases the severity of allergic airway inflammation. Nat. Commun.3, 877 (2012).
  • Aich J , MabalirajanU , AhmadTet al. Resveratrol attenuates experimental allergic asthma in mice by restoring inositol polyphosphate 4 phosphatase (INPP4A). Int. Immunopharmacol.14(4), 438–443 (2012).
  • Remesh SG , SantoshV , EscalanteCR. Structural studies of IRF4 reveal a flexible autoinhibitory region and a compact linker domain. J. Biol. Chem.290(46), 27779–27790 (2015).
  • Agnarelli A , ChevassutT , ManciniEJ. IRF4 in multiple myeloma – biology, disease and therapeutic target. Leuk. Res.72, 52–58 (2018).
  • Brass AL , ZhuAQ , SinghH. Assembly requirements of PU.1-Pip (IRF-4) activator complexes: inhibiting function in vivo using fused dimers. EMBO J.18(4), 977–991 (1999).
  • Tussiwand R , LeeWL , MurphyTLet al. Compensatory dendritic cell development mediated by BATF–IRF interactions. Nature490(7421), 502–507 (2012).
  • Ochiai K , Maienschein-ClineM , SimonettiGet al. Transcriptional regulation of germinal center B and plasma cell fates by dynamical control of IRF4. Immunity38(5), 918–929 (2013).
  • Van Der Ploeg EK , GolebskiK , Van NimwegenMet al. Steroid-resistant human inflammatory ILC2s are marked by CD45RO and elevated in type 2 respiratory diseases. Sci. Immunol.6(55), eabd3489 (2021).
  • Monteiro M , Agua-DoceA , AlmeidaCF , Fonseca-PereiraD , Veiga-FernandesH , GracaL. IL-9 Expression by invariant NKT cells is not imprinted during thymic development. J. Immunol.195(7), 3463–3471 (2015).
  • Moon HG , KimSJ , JeongJJet al. Airway epithelial cell-derived colony stimulating factor-1 promotes allergen sensitization. Immunity49(2), 275–287.e275 (2018).
  • Williams JW , TjotaMY , ClayBSet al. Transcription factor IRF4 drives dendritic cells to promote Th2 differentiation. Nat. Commun.4, 2990 (2013).
  • Liu Y , GaoX , MiaoYet al. NLRP3 regulates macrophage M2 polarization through up-regulation of IL-4 in asthma. Biochem. J.475(12), 1995–2008 (2018).
  • Xia L , WangX , LiuLet al. lnc-BAZ2B promotes M2 macrophage activation and inflammation in children with asthma through stabilizing BAZ2B pre-mRNA. J. Allergy Clin. Immunol.147(3), 921–932.e929 (2021).
  • Chung S , KimJY , SongMAet al. FoxO1 is a critical regulator of M2-like macrophage activation in allergic asthma. Allergy74(3), 535–548 (2019).
  • Brüstle A , HeinkS , HuberMet al. The development of inflammatory T(H)-17 cells requires interferon-regulatory factor 4. Nat. Immunol.8(9), 958–966 (2007).
  • Staudt V , BothurE , KleinMet al. Interferon-regulatory factor 4 is essential for the developmental program of T helper 9 cells. Immunity33(2), 192–202 (2010).
  • Tousa S , SemitekolouM , MorianosIet al. Activin-A co-opts IRF4 and AhR signaling to induce human regulatory T cells that restrain asthmatic responses. Proc. Natl Acad. Sci. USA114(14), E2891–e2900 (2017).
  • Lu Y , KaredH , TanSWet al. Dynamics of helper CD4 T cells during acute and stable allergic asthma. Mucosal Immunol.11(6), 1640–1652 (2018).
  • Jia A , WangY , SunWet al. MBD2 Regulates Th17 cell differentiation and experimental severe asthma by affecting IRF4 expression. Mediators Inflamm.2017, 6249685 (2017).
  • Koch S , MoussetS , GraserAet al. IL-6 activated integrated BATF/IRF4 functions in lymphocytes are T-bet-independent and reversed by subcutaneous immunotherapy. Sci. Rep.3, 1754 (2013).
  • Wang Y , WangY , MaY , PuX. The role of Th9, Th17 and Treg cells on pathogenesis of nasal polyps. Lin Chuang Er Bi Yan Hou Tou Jing Wai Ke Za Zhi30(4), 277–281 (2016).
  • Wu D , LiL , ZhangM , WangJ , WeiY. Two inflammatory phenotypes of nasal polyps and comorbid asthma. Ann. Allergy Asthma Immunol.118(3), 318–325 (2017).
  • Sakuma Y , IshitoyaJ , KomatsuMet al. New clinical diagnostic criteria for eosinophilic chronic rhinosinusitis. Auris Nasus Larynx38(5), 583–588 (2011).
  • Liu C , YanB , QiS , ZhangY , ZhangL , WangC. Predictive significance of Charcot–Leyden crystals for eosinophilic chronic rhinosinusitis with nasal polyps. Am. J. Rhinol. Allergy33(6), 671–680 (2019).
  • Liang Z , YanB , LiuC , TanR , WangC , ZhangL. Predictive significance of arachidonate 15-lipoxygenase for eosinophilic chronic rhinosinusitis with nasal polyps. Allergy Asthma Clin. Immunol.16, 82 (2020).
  • Lv H , LiuPQ , XiangRet al. Predictive and diagnostic value of nasal nitric oxide in eosinophilic chronic rhinosinusitis with nasal polyps. Int. Arch. Allergy Immunol.181(11), 853–861 (2020).
  • Guler GD , NingY , KuCJet al. Detection of early stage pancreatic cancer using 5-hydroxymethylcytosine signatures in circulating cell free DNA. Nat. Commun.11(1), 5270 (2020).
  • Xu X , TanX , TampeBet al. High-fidelity CRISPR/Cas9- based gene-specific hydroxymethylation rescues gene expression and attenuates renal fibrosis. Nat. Commun.9(1), 3509 (2018).

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