PMID- 37598461 OWN - NLM STAT- MEDLINE DCOM- 20230918 LR - 20240306 IS - 2352-3964 (Electronic) IS - 2352-3964 (Linking) VI - 95 DP - 2023 Sep TI - Epigenome-wide DNA methylation association study of circulating IgE levels identifies novel targets for asthma. PG - 104758 LID - S2352-3964(23)00323-7 [pii] LID - 10.1016/j.ebiom.2023.104758 [doi] LID - 104758 AB - BACKGROUND: Identifying novel epigenetic signatures associated with serum immunoglobulin E (IgE) may improve our understanding of molecular mechanisms underlying asthma and IgE-mediated diseases. METHODS: We performed an epigenome-wide association study using whole blood from Framingham Heart Study (FHS; n = 3,471, 46% females) participants and validated results using the Childhood Asthma Management Program (CAMP; n = 674, 39% females) and the Genetic Epidemiology of Asthma in Costa Rica Study (CRA; n = 787, 41% females). Using the closest gene to each IgE-associated CpG, we highlighted biologically plausible pathways underlying IgE regulation and analyzed the transcription patterns linked to IgE-associated CpGs (expression quantitative trait methylation loci; eQTMs). Using prior UK Biobank summary data from genome-wide association studies of asthma and allergy, we performed Mendelian randomization (MR) for causal inference testing using the IgE-associated CpGs from FHS with methylation quantitative trait loci (mQTLs) as instrumental variables. FINDINGS: We identified 490 statistically significant differentially methylated CpGs associated with IgE in FHS, of which 193 (39.3%) replicated in CAMP and CRA (FDR < 0.05). Gene ontology analysis revealed enrichment in pathways related to transcription factor binding, asthma, and other immunological processes. eQTM analysis identified 124 cis-eQTMs for 106 expressed genes (FDR < 0.05). MR in combination with drug-target analysis revealed CTSB and USP20 as putatively causal regulators of IgE levels (Bonferroni adjusted P < 7.94E-04) that can be explored as potential therapeutic targets. INTERPRETATION: By integrating eQTM and MR analyses in general and clinical asthma populations, our findings provide a deeper understanding of the multidimensional inter-relations of DNA methylation, gene expression, and IgE levels. FUNDING: US NIH/NHLBI grants: P01HL132825, K99HL159234. N01-HC-25195 and HHSN268201500001I. CI - Copyright (c) 2023 The Authors. Published by Elsevier B.V. All rights reserved. FAU - Recto, Kathryn AU - Recto K AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Kachroo, Priyadarshini AU - Kachroo P AD - Brigham and Women's Hospital, Channing Division of Network Medicine, Boston, MA 02115, USA. FAU - Huan, Tianxiao AU - Huan T AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Van Den Berg, David AU - Van Den Berg D AD - University of Southern California Methylation Characterization Center, University of Southern California, Los Angeles, CA 90033, USA. FAU - Lee, Gha Young AU - Lee GY AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Bui, Helena AU - Bui H AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Lee, Dong Heon AU - Lee DH AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Gereige, Jessica AU - Gereige J AD - Boston University School of Medicine, Pulmonary Center, Boston, MA 02118, USA. FAU - Yao, Chen AU - Yao C AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Hwang, Shih-Jen AU - Hwang SJ AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Joehanes, Roby AU - Joehanes R AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. FAU - Weiss, Scott T AU - Weiss ST AD - Brigham and Women's Hospital, Channing Division of Network Medicine, Boston, MA 02115, USA. CN - NHLBI Trans-Omics in Precision Medicine (TOPMed) Consortium FAU - O'Connor, George T AU - O'Connor GT AD - The Framingham Heart Study, Framingham, MA 01702, USA; Boston University School of Medicine, Pulmonary Center, Boston, MA 02118, USA. FAU - Levy, Daniel AU - Levy D AD - The Population Sciences Branch, National Heart, Lung, and Blood Institute, National Institutes of Health, Bethesda, MD 20892, USA; The Framingham Heart Study, Framingham, MA 01702, USA. Electronic address: levyd@nhlbi.nih.gov. FAU - DeMeo, Dawn L AU - DeMeo DL AD - Brigham and Women's Hospital, Channing Division of Network Medicine, Boston, MA 02115, USA. Electronic address: dawn.demeo@channing.harvard.edu. LA - eng GR - T32 HL007035/HL/NHLBI NIH HHS/United States GR - T32 GM007753/GM/NIGMS NIH HHS/United States GR - K08 HL141601/HL/NHLBI NIH HHS/United States GR - T32 GM144273/GM/NIGMS NIH HHS/United States GR - R01 HL167072/HL/NHLBI NIH HHS/United States PT - Journal Article DEP - 20230818 PL - Netherlands TA - EBioMedicine JT - EBioMedicine JID - 101647039 RN - 37341-29-0 (Immunoglobulin E) RN - 0 (USP20 protein, human) RN - EC 3.4.19.12 (Ubiquitin Thiolesterase) SB - IM MH - Female MH - Humans MH - Child MH - Male MH - *DNA Methylation MH - Epigenome MH - Genome-Wide Association Study MH - *Asthma/genetics MH - Immunoglobulin E MH - Ubiquitin Thiolesterase PMC - PMC10462855 OTO - NOTNLM OT - Asthma OT - DNA methylation OT - Drug targets OT - EWAS OT - IgE OT - Lung OT - Mendelian randomization OT - RNA-Sequencing OT - eQTM COIS- Declaration of interests DLD has received grants from Bayer and honoraria from Novartis. STW has received royalties from UpToDate and served on the Board of Histolix, a digital pathology company. Rest authors declared no conflicts of interest. 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Ruczinski I FIR - Runnels, Alexi IR - Runnels A FIR - Russell, Pamela IR - Russell P FIR - Ruuska, Sarah IR - Ruuska S FIR - Ryan, Kathleen IR - Ryan K FIR - Sabino, Ester Cerdeira IR - Sabino EC FIR - Saleheen, Danish IR - Saleheen D FIR - Salimi, Shabnam IR - Salimi S FIR - Salvi, Sejal IR - Salvi S FIR - Salzberg, Steven IR - Salzberg S FIR - Sandow, Kevin IR - Sandow K FIR - Sankaran, Vijay G IR - Sankaran VG FIR - Santibanez, Jireh IR - Santibanez J FIR - Schwander, Karen IR - Schwander K FIR - Schwartz, David IR - Schwartz D FIR - Sciurba, Frank IR - Sciurba F FIR - Seidman, Christine IR - Seidman C FIR - Seidman, Jonathan IR - Seidman J FIR - Series, Frederic IR - Series F FIR - Sheehan, Vivien IR - Sheehan V FIR - Sherman, Stephanie L IR - Sherman SL FIR - Shetty, Amol IR - Shetty A FIR - Shetty, Aniket IR - Shetty A FIR - Sheu, Wayne Hui-Heng IR - Sheu WH FIR - Shoemaker, M Benjamin IR - Shoemaker MB FIR - Silver, Brian IR - Silver B FIR - Silverman, Edwin IR - Silverman E FIR - Skomro, Robert IR - Skomro R FIR - Smith, Albert Vernon IR - Smith AV FIR - Smith, Jennifer IR - Smith J FIR - Smith, Josh IR - Smith J FIR - Smith, Nicholas IR - Smith N FIR - Smith, Tanja IR - Smith T FIR - Smoller, Sylvia IR - Smoller S FIR - Snively, Beverly IR - Snively B FIR - Snyder, Michael IR - Snyder M FIR - Sofer, Tamar IR - Sofer T FIR - Sotoodehnia, Nona IR - Sotoodehnia N FIR - Stilp, Adrienne M IR - Stilp AM FIR - Storm, Garrett IR - Storm G FIR - Streeten, Elizabeth IR - Streeten E FIR - Su, Jessica Lasky IR - Su JL FIR - Sung, Yun Ju IR - Sung YJ FIR - Sylvia, Jody IR - Sylvia J FIR - Szpiro, Adam IR - Szpiro A FIR - Taliun, Daniel IR - Taliun D FIR - Tang, Hua IR - Tang H FIR - Taub, Margaret IR - Taub M FIR - Taylor, Kent IR - Taylor K FIR - Taylor, Matthew IR - Taylor M FIR - Taylor, Simeon IR - Taylor S FIR - Telen, Marilyn IR - Telen M FIR - Thornton, Timothy A IR - Thornton TA FIR - Threlkeld, Machiko IR - Threlkeld M FIR - Tinker, Lesley IR - Tinker L FIR - Tirschwell, David IR - Tirschwell D FIR - Tishkoff, Sarah IR - Tishkoff S FIR - Tiwari, Hemant IR - Tiwari H FIR - Tong, Catherine IR - Tong C FIR - Tracy, Russell IR - Tracy R FIR - Tsai, Michael IR - Tsai M FIR - Vaidya, Dhananjay IR - Vaidya D FIR - Van Den Berg, David IR - Van Den Berg D FIR - VandeHaar, Peter IR - VandeHaar P FIR - Vrieze, Scott IR - Vrieze S FIR - Walker, Tarik IR - Walker T FIR - Wallace, Robert IR - Wallace R FIR - Walts, Avram IR - Walts A FIR - Wang, Fei Fei IR - Wang FF FIR - Wang, Heming IR - Wang H FIR - Wang, Jiongming IR - Wang J FIR - Watson, Karol IR - Watson K FIR - Watt, Jennifer IR - Watt J FIR - Weeks, Daniel E IR - Weeks DE FIR - Weinstock, Joshua IR - Weinstock J FIR - Weir, Bruce IR - Weir B FIR - Weiss, Scott T IR - Weiss ST FIR - Weng, Lu-Chen IR - Weng LC FIR - Wessel, Jennifer IR - Wessel J FIR - Willer, Cristen IR - Willer C FIR - Williams, Kayleen IR - Williams K FIR - Williams, L Keoki IR - Williams LK FIR - Williams, Scott IR - Williams S FIR - Wilson, Carla IR - Wilson C FIR - Wilson, James IR - Wilson J FIR - Winterkorn, Lara IR - Winterkorn L FIR - Wong, Quenna IR - Wong Q FIR - Wu, Baojun IR - Wu B FIR - Wu, Joseph IR - Wu J FIR - Xu, Huichun IR - Xu H FIR - Yanek, Lisa IR - Yanek L FIR - Yang, Ivana IR - Yang I FIR - Yu, Ketian IR - Yu K FIR - Zekavat, Seyedeh Maryam IR - Zekavat SM FIR - Zhang, Yingze IR - Zhang Y FIR - Zhao, Snow Xueyan IR - Zhao SX FIR - Zhao, Wei IR - Zhao W FIR - Zhu, Xiaofeng IR - Zhu X FIR - Ziv, Elad IR - Ziv E FIR - Zody, Michael IR - Zody M FIR - Zoellner, Sebastian IR - Zoellner S EDAT- 2023/08/21 00:41 MHDA- 2023/09/18 12:42 PMCR- 2023/08/18 CRDT- 2023/08/20 18:02 PHST- 2023/03/14 00:00 [received] PHST- 2023/08/01 00:00 [revised] PHST- 2023/08/02 00:00 [accepted] PHST- 2023/09/18 12:42 [medline] PHST- 2023/08/21 00:41 [pubmed] PHST- 2023/08/20 18:02 [entrez] PHST- 2023/08/18 00:00 [pmc-release] AID - S2352-3964(23)00323-7 [pii] AID - 104758 [pii] AID - 10.1016/j.ebiom.2023.104758 [doi] PST - ppublish SO - EBioMedicine. 2023 Sep;95:104758. doi: 10.1016/j.ebiom.2023.104758. Epub 2023 Aug 18.