IDEAS home Printed from https://ideas.repec.org/a/gam/jijerp/v16y2019i4p600-d207116.html
   My bibliography  Save this article

DNA Methylation in Inflammatory Pathways Modifies the Association between BMI and Adult-Onset Non-Atopic Asthma

Author

Listed:
  • Ayoung Jeong

    (Swiss Tropical and Public Health Institute, 4051 Basel, Switzerland
    Department of Public Health, University of Basel, 4001 Basel, Switzerland)

  • Medea Imboden

    (Swiss Tropical and Public Health Institute, 4051 Basel, Switzerland
    Department of Public Health, University of Basel, 4001 Basel, Switzerland)

  • Akram Ghantous

    (International Agency for Research on Cancer, 69372 Lyon, France)

  • Alexei Novoloaca

    (International Agency for Research on Cancer, 69372 Lyon, France)

  • Anne-Elie Carsin

    (ISGlobal, Barcelona Institute for Global Health, 08003 Barcelona, Spain
    Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain
    CIBER Epidemiología y Salud Pública (CIBERESP), 08005 Barcelona, Spain)

  • Manolis Kogevinas

    (ISGlobal, Barcelona Institute for Global Health, 08003 Barcelona, Spain
    Universitat Pompeu Fabra (UPF), 08002 Barcelona, Spain
    CIBER Epidemiología y Salud Pública (CIBERESP), 08005 Barcelona, Spain)

  • Christian Schindler

    (Swiss Tropical and Public Health Institute, 4051 Basel, Switzerland
    Department of Public Health, University of Basel, 4001 Basel, Switzerland)

  • Gianfranco Lovison

    (Department of Economics, Business and Statistics, University of Palermo, 90128 Palermo, Italy)

  • Zdenko Herceg

    (International Agency for Research on Cancer, 69372 Lyon, France)

  • Cyrille Cuenin

    (International Agency for Research on Cancer, 69372 Lyon, France)

  • Roel Vermeulen

    (Environmental Epidemiology Division, Utrecht University, Institute for Risk Assessment Sciences, 3584CM Utrecht, The Netherlands)

  • Deborah Jarvis

    (Population Health and Occupational Disease, National Heart and Lung Institute, Imperial College, London SW3 6LR, UK)

  • André F. S. Amaral

    (Population Health and Occupational Disease, National Heart and Lung Institute, Imperial College, London SW3 6LR, UK)

  • Florian Kronenberg

    (Division of Genetic Epidemiology, Medical University of Innsbruck, 6020 Innsbruck, Austria)

  • Paolo Vineis

    (MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London, London W2 1PG, UK
    Italian Institute for Genomic Medicine (IIGM), 10126 Turin, Italy)

  • Nicole Probst-Hensch

    (Swiss Tropical and Public Health Institute, 4051 Basel, Switzerland
    Department of Public Health, University of Basel, 4001 Basel, Switzerland)

Abstract

A high body mass (BMI) index has repeatedly been associated with non-atopic asthma, but the biological mechanism linking obesity to asthma is still poorly understood. We aimed to test the hypothesis that inflammation and/or innate immunity plays a role in the obesity-asthma link. DNA methylome was measured in blood samples of 61 non-atopic participants with asthma and 146 non-atopic participants without asthma (non-smokers for at least 10 years) taking part in the Swiss Cohort Study on Air Pollution and Lung and Heart Diseases in Adults (SAPALDIA) study. Modification by DNA methylation of the association of BMI or BMI change over 10 years with adult-onset asthma was examined at each CpG site and differentially methylated region. Pathway enrichment tests were conducted for genes in a priori curated inflammatory pathways and the NLRP3-IL1B-IL17 axis. The latter was chosen on the basis of previous work in mice. Inflammatory pathways including glucocorticoid/PPAR signaling ( p = 0.0023), MAPK signaling ( p = 0.013), NF-κB signaling ( p = 0.031), and PI3K/AKT signaling ( p = 0.031) were enriched for the effect modification of BMI, while NLRP3-IL1B-IL17 axis was enriched for the effect modification of BMI change over 10 years ( p = 0.046). DNA methylation measured in peripheral blood is consistent with inflammation as a link between BMI and adult-onset asthma and with the NLRP3-IL1B-IL17 axis as a link between BMI change over 10 years and adult-onset asthma in non-atopic participants.

Suggested Citation

  • Ayoung Jeong & Medea Imboden & Akram Ghantous & Alexei Novoloaca & Anne-Elie Carsin & Manolis Kogevinas & Christian Schindler & Gianfranco Lovison & Zdenko Herceg & Cyrille Cuenin & Roel Vermeulen & D, 2019. "DNA Methylation in Inflammatory Pathways Modifies the Association between BMI and Adult-Onset Non-Atopic Asthma," IJERPH, MDPI, vol. 16(4), pages 1-15, February.
    • Handle: RePEc:gam:jijerp:v:16:y:2019:i:4:p:600-:d:207116
    as

    Download full text from publisher

    File URL: https://www.mdpi.com/1660-4601/16/4/600/pdf
    Download Restriction: no
    File URL: https://www.mdpi.com/1660-4601/16/4/600/
    Download Restriction: no
    ---><---

    References listed on IDEAS

    as
    1. van der Laan Mark J. & Birkner Merrill D. & Hubbard Alan E., 2005. "Empirical Bayes and Resampling Based Multiple Testing Procedure Controlling Tail Probability of the Proportion of False Positives," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 4(1), pages 1-32, October.
    2. Simone Wahl & Alexander Drong & Benjamin Lehne & Marie Loh & William R. Scott & Sonja Kunze & Pei-Chien Tsai & Janina S. Ried & Weihua Zhang & Youwen Yang & Sili Tan & Giovanni Fiorito & Lude Franke &, 2017. "Epigenome-wide association study of body mass index, and the adverse outcomes of adiposity," Nature, Nature, vol. 541(7635), pages 81-86, January.
    3. Ursula Ackermann-Liebrich & Birgit Kuna-Dibbert & Nicole Probst-Hensch & Christian Schindler & Denise Dietrich & Elisabeth Stutz & Lucy Bayer-Oglesby & Felix Baum & Otto Brändli & Martin Brutsche & Sa, 2005. "Follow-up of the Swiss Cohort Study on Air Pollution and Lung Diseases in Adults (SAPALDIA 2) 1991–2003: methods and characterization of participants," International Journal of Public Health, Springer;Swiss School of Public Health (SSPH+), vol. 50(4), pages 245-263, August.
    4. Brian Martin & Ursula Ackermann-Liebrich & Philippe Leuenberger & Nino Künzli & Elisabeth Stutz & Roland Keller & Jean-Pierrre Zellweger & Brunello Wüthrich & Christian Monn & Kurt Blaser & Gianfranco, 1997. "SAPALDIA: Methods and participation in the cross-sectional part of the Swiss Study on Air Pollution and Lung Diseases in Adults," International Journal of Public Health, Springer;Swiss School of Public Health (SSPH+), vol. 42(2), pages 67-84, March.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Ikenna C. Eze & Medea Imboden & Maria Foraster & Emmanuel Schaffner & Ashish Kumar & Danielle Vienneau & Harris Héritier & Franziska Rudzik & Laurie Thiesse & Reto Pieren & Arnold Von Eckardstein & Ch, 2017. "Exposure to Night-Time Traffic Noise, Melatonin-Regulating Gene Variants and Change in Glycemia in Adults," IJERPH, MDPI, vol. 14(12), pages 1-18, December.
    2. Matthias Wielscher & Pooja R. Mandaviya & Brigitte Kuehnel & Roby Joehanes & Rima Mustafa & Oliver Robinson & Yan Zhang & Barbara Bodinier & Esther Walton & Pashupati P. Mishra & Pascal Schlosser & Ro, 2022. "DNA methylation signature of chronic low-grade inflammation and its role in cardio-respiratory diseases," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    3. Nyangoma Stephen O. & Collins Stuart I. & Altman Douglas G. & Johnson Philip & Billingham Lucinda J., 2012. "Sample Size Calculations for Designing Clinical Proteomic Profiling Studies Using Mass Spectrometry," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 11(3), pages 1-42, February.
    4. Adrienne Tin & Pascal Schlosser & Pamela R. Matias-Garcia & Chris H. L. Thio & Roby Joehanes & Hongbo Liu & Zhi Yu & Antoine Weihs & Anselm Hoppmann & Franziska Grundner-Culemann & Josine L. Min & Vic, 2021. "Epigenome-wide association study of serum urate reveals insights into urate co-regulation and the SLC2A9 locus," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    5. Wang, Li & Xu, Xingzhong, 2012. "Step-up procedure controlling generalized family-wise error rate," Statistics & Probability Letters, Elsevier, vol. 82(4), pages 775-782.
    6. Wei Zhao & Farah Ammous & Scott Ratliff & Jiaxuan Liu & Miao Yu & Thomas H. Mosley & Sharon L. R. Kardia & Jennifer A. Smith, 2019. "Education and Lifestyle Factors Are Associated with DNA Methylation Clocks in Older African Americans," IJERPH, MDPI, vol. 16(17), pages 1-18, August.
    7. Qin Zeng & Jianfeng Song & Xiaoxiao Sun & Dandan Wang & Xiyan Liao & Yujin Ding & Wanyu Hu & Yayi Jiao & Wuqian Mai & Wufuer Aini & Fanqi Wang & Hui Zhou & Limin Xie & Ying Mei & Yuan Tang & Zhiguo Xi, 2024. "A negative feedback loop between TET2 and leptin in adipocyte regulates body weight," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    8. Christina C. Bartenschlager & Michael Krapp, 2015. "Theorie und Methoden multipler statistischer Vergleiche," AStA Wirtschafts- und Sozialstatistisches Archiv, Springer;Deutsche Statistische Gesellschaft - German Statistical Society, vol. 9(2), pages 107-129, November.
    9. Joseph P. Romano & Azeem M. Shaikh & Michael Wolf, 2010. "Hypothesis Testing in Econometrics," Annual Review of Economics, Annual Reviews, vol. 2(1), pages 75-104, September.
    10. Hannah Lui Park, 2020. "Epigenetic Biomarkers for Environmental Exposures and Personalized Breast Cancer Prevention," IJERPH, MDPI, vol. 17(4), pages 1-18, February.
    11. Mathur, Maya B & VanderWeele, Tyler, 2018. "Statistical methods for evidence synthesis," Thesis Commons kd6ja, Center for Open Science.
    12. Park, DoHwan & Park, Junyong & Zhong, Xiaosong & Sadelain, Michel, 2011. "Estimation of empirical null using a mixture of normals and its use in local false discovery rate," Computational Statistics & Data Analysis, Elsevier, vol. 55(7), pages 2421-2432, July.
    13. Thomas Battram & Tom R. Gaunt & Caroline L. Relton & Nicholas J. Timpson & Gibran Hemani, 2022. "A comparison of the genes and genesets identified by GWAS and EWAS of fifteen complex traits," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    14. Schumi Jennifer & DiRienzo A. Gregory & DeGruttola Victor, 2008. "Testing for Associations with Missing High-Dimensional Categorical Covariates," The International Journal of Biostatistics, De Gruyter, vol. 4(1), pages 1-17, September.
    15. Alessio Farcomeni, 2009. "Generalized Augmentation to Control the False Discovery Exceedance in Multiple Testing," Scandinavian Journal of Statistics, Danish Society for Theoretical Statistics;Finnish Statistical Society;Norwegian Statistical Association;Swedish Statistical Association, vol. 36(3), pages 501-517, September.
    16. Anna Ulrich & Yukyee Wu & Harmen Draisma & John Wharton & Emilia M. Swietlik & Inês Cebola & Eleni Vasilaki & Zhanna Balkhiyarova & Marjo-Riitta Jarvelin & Juha Auvinen & Karl-Heinz Herzig & J. Gerry , 2024. "Blood DNA methylation profiling identifies cathepsin Z dysregulation in pulmonary arterial hypertension," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    17. Pallavi Basu & Luella Fu & Alessio Saretto & Wenguang Sun, 2021. "Empirical Bayes Control of the False Discovery Exceedance," Working Papers 2115, Federal Reserve Bank of Dallas.
    18. Paola Monti & Simona Iodice & Letizia Tarantini & Francesca Sacchi & Luca Ferrari & Massimiliano Ruscica & Massimiliano Buoli & Luisella Vigna & Angela Cecilia Pesatori & Valentina Bollati, 2021. "Effects of PM Exposure on the Methylation of Clock Genes in A Population of Subjects with Overweight or Obesity," IJERPH, MDPI, vol. 18(3), pages 1-14, January.
    19. Liam McAllan & Damir Baranasic & Sergio Villicaña & Scarlett Brown & Weihua Zhang & Benjamin Lehne & Marco Adamo & Andrew Jenkinson & Mohamed Elkalaawy & Borzoueh Mohammadi & Majid Hashemi & Nadia Fer, 2023. "Integrative genomic analyses in adipocytes implicate DNA methylation in human obesity and diabetes," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    20. Joseph P. Romano & Michael Wolf, 2008. "Balanced Control of Generalized Error Rates," IEW - Working Papers 379, Institute for Empirical Research in Economics - University of Zurich.

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:gam:jijerp:v:16:y:2019:i:4:p:600-:d:207116. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: MDPI Indexing Manager (email available below). General contact details of provider: https://www.mdpi.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.