Hostname: page-component-848d4c4894-pftt2 Total loading time: 0 Render date: 2024-05-14T15:35:51.332Z Has data issue: false hasContentIssue false
  • English
  • Français

Adulthood asthma as a consequence of childhood adversity: a systematic review of epigenetically affected genes

Published online by Cambridge University Press:  08 March 2022

Yasemin Saygideger Open the ORCID record for Yasemin Saygideger [Opens in a new window] ,
Hakan Özkan ,
Oya Baydar  and
Ozge Yilmaz
Yasemin Saygideger*
Affiliation:
Department of Pulmonary, School of Medicine, Cukurova University, Adana, Turkey Department of Translational Medicine, Graduate School of Health Sciences, Cukurova University, Adana, Turkey
Hakan Özkan
Affiliation:
Department of Pediatrics, Division of Neonatal Intensive Care, Metro Hospital, Adana, Turkey
Oya Baydar
Affiliation:
Department of Pulmonary, School of Medicine, Cukurova University, Adana, Turkey
Ozge Yilmaz
Affiliation:
Department of Pediatric Allergy and Immunology, School of Medicine, Celal Bayar University, Manisa, Turkey
*
Address for correspondence: Yasemin Saygideger, Department of Pulmonary, School of Medicine, Cukurova University, Adana, Turkey. Email: ysaygideger@cu.edu.tr
Get access Rights & Permissions [Opens in a new window]

Abstract

There is an accumulating data that shows relation between childhood adversity and vulnerability to chronic diseases as well as epigenetic influences that in turn give rise to these diseases. Asthma is one of the chronic diseases that is influenced from genetic regulation of the inflammatory biomolecules and therefore the hypothesis in this research was childhood adversity might have caused epigenetic differentiation in the asthma-related genes in the population who had childhood trauma. To test this hypothesis, the literature was systematically reviewed to extract epigenetically modified gene data of the adults who had childhood adversity, and affected genes were further evaluated for their association with asthma. PRISMA guidelines were adopted and PubMed and Google Scholar were included in the searched databases, to evaluate epigenetic modifications in asthma-related genes of physically, emotionally or sexually abused children. After retrieving a total of 5245 articles, 36 of them were included in the study. Several genes and pathways that may contribute to pathogenesis of asthma development, increased inflammation, or response to asthma treatment were found epigenetically affected by childhood traumas. Childhood adversity, causing epigenetic changes in DNA, may lead to asthma development or influence the course of the disease and therefore should be taken into account for the prolonged health consequences.

Keywords

Asthmaepigeneticschild abusechildhood adversityasthma-related genesinflammation
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 13 , Issue 6 , December 2022 , pp. 674 - 682
Check for updates
Copyright
© The Author(s), 2022. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

Footnotes

Part of this work has been presented at Turkish Thoracic Society’s 22nd Annual Congress in April 2019.

References

Carraro, S, Scheltema, N, Bont, L, Baraldi, E. Early-life origins of chronic respiratory diseases: understanding and promoting healthy ageing. Eur Respir J. 2014; 44(6), 1682–1696. DOI 10.1183/09031936.00084114.CrossRefGoogle ScholarPubMed
Zhang, Y, Kutateladze, TG. Diet and the epigenome. Nat Commun. 2018; 9(1), 2376. DOI 10.1038/s41467-018-05778-1.Google ScholarPubMed
Shields, ME, Hovdestad, WE, Pelletier, C, Dykxhoorn, JL, O’Donnell, SC, Tonmyr, L. Childhood maltreatment as a risk factor for diabetes: findings from a population-based survey of Canadian adults. BMC Public Health. 2016; 16(1). DOI 10.1186/s12889-016-3491-1.Google ScholarPubMed
Bhan, N, Glymour, MM, Kawachi, I, Subramanian, SV. Childhood adversity and asthma prevalence: evidence from 10 US states (2009-2011. BMJ Open Respir Res. 2014; 1(1), e000016. DOI 10.1136/bmjresp-2013-000016.CrossRefGoogle ScholarPubMed
Ayaydin, H, Abali, O, Okumus Akdeniz, N, et al. Immune system changes after sexual abuse in adolescents. Pediatr Int. 2016; 58(2), 105–112. DOI 10.111/ped.12767.CrossRefGoogle ScholarPubMed
Remigio-Baker, RA, Hayes, DK, Reyes-Salvail, F. Adverse childhood events are related to the prevalence of asthma and chronic obstructive pulmonary disorder among adult women in Hawaii. Lung. 2015; 193(6), 885–891. DOI 10.1007/s00408-015-9777-8.Google Scholar
Clemens, V, Huber-Lang, M, Plener, PL, Brähler, E, Brown, RC, Fegert, JM. Association of child maltreatment subtypes and long-term physical health in a German representative sample. Eur J Psychotraumatol. 2018; 9(1), 1510278. DOI 10.1080/20008198.2018.1510278.CrossRefGoogle Scholar
Rosas-Salazar, C, Han, Y-Y, Brehm, JM, et al. Gun violence, African ancestry, and asthma. Chest. 2016; 149(6), 1436–1444. DOI 10.1016/j.chest.2016.02.639.CrossRefGoogle ScholarPubMed
Bonfim, CB, dos Santos, DN, Barreto, ML. The association of intrafamilial violence against children with symptoms of atopic and non-atopic asthma: a cross-sectional study in Salvador. Brazil Child Abuse Neglect. 2015; 50(2), 244–253. DOI 10.1016/j.chiabu.2015.05.021.CrossRefGoogle ScholarPubMed
Bellis, MA, Hughes, K, Leckenby, N, Hardcastle, KA, Perkins, C, Lowey, H. Measuring mortality and the burden of adult disease associated with adverse childhood experiences in England: a national survey. J Public Health. 2014; 37(3), 445–454. DOI 10.1093/pubmed/fdu065.CrossRefGoogle ScholarPubMed
Sinha, R. Chronic stress, drug use, and vulnerability to addiction. Ann NY Acad Sci. 2008; 1141(1), 105–130. DOI 10.1196/annals.1441.030.CrossRefGoogle ScholarPubMed
Yang, B-Z, Zhang, H, Ge, W, et al. Child abuse and epigenetic mechanisms of disease risk. Am J Prev Med. 2013; 44(2), 101–107. DOI 10.1016/j.amepre.2012.10.012.Google ScholarPubMed
Moher, D, Liberati, A, Tetzlaff, J, Altman, DG, PRISMA Group*. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med. 2009; 151(4), 264–269.CrossRefGoogle ScholarPubMed
Pomaznoy, M, Ha, B, Peters, B. GOnet: a tool for interactive gene ontology analysis. BMC Bioinform. 2018; 19(1), 470. DOI 10.1186/s12859-018-2533-3.CrossRefGoogle ScholarPubMed
Mehta, D, Klengel, T, Conneely, KN, et al. Childhood maltreatment is associated with distinct genomic and epigenetic profiles in posttraumatic stress disorder. Proc Natl Acad Sci USA. 2013; 110(20), 8302–8307. DOI 10.1073/pnas.1217750110.CrossRefGoogle ScholarPubMed
Provençal, N, Suderman, MJ, Caramaschi, D, et al. Differential DNA methylation regions in cytokine and transcription factor genomic loci associate with childhood physical aggression. PLoS ONE. 2013; 8(8), e71691. DOI 10.1371/journal.pone.0071691.CrossRefGoogle ScholarPubMed
Guillemin, C, Provençal, N, Suderman, M, et al. DNA methylation signature of childhood chronic physical aggression in T cells of both men and women. PLoS ONE. 2014; 9(1), e86822. DOI 10.1371/journal.pone.0086822.Google Scholar
Provençal, N, Suderman, MJ, Guillemin, C, et al. Association of childhood chronic physical aggression with a DNA methylation signature in adult human T cells. PLoS ONE. 2014; 9(4), e89839. DOI 10.1371/journal.pone.0089839.CrossRefGoogle ScholarPubMed
Suderman, M, Borghol, N, Pappas, JJ, et al. Childhood abuse is associated with methylation of multiple loci in adult DNA. BMC Med Genom. 2014; 7(1), 68. DOI 10.1186/1755-8794-7-13.CrossRefGoogle ScholarPubMed
Labonté, B, Turecki, G. Epigenetic effects of childhood adversity in the brain and suicide risk (Chapter 13). In The Neurobiological Basis of Suicide (ed. Dwivedi Y), 2012, CRC Press/Taylor & Francis, Boca Raton, FL.Google ScholarPubMed
Schwaiger, M, Grinberg, M, Moser, D, et al. Altered stress-induced regulation of genes in monocytes in adults with a history of childhood adversity. Neuropsychopharmacol. 2016; 41(10), 2530–2540. DOI 10.1038/npp.2016.57.CrossRefGoogle ScholarPubMed
Cicchetti, D, Hetzel, S, Rogosch, FA, Handley, ED, Toth, SL. An investigation of child maltreatment and epigenetic mechanisms of mental and physical health risk. Dev Psychopathol. 2016; 28(4pt2), 1305–1317. DOI 10.1017/s0954579416000869.Google ScholarPubMed
Cecil, CAM, Smith, RG, Walton, E, Mill, J, McCrory, EJ, Viding, E. Epigenetic signatures of childhood abuse and neglect: implications for psychiatric vulnerability. J Psychiatr Res. 2016; 83(7), 184–194. DOI 10.1016/j.jpsychires.2016.09.010.CrossRefGoogle ScholarPubMed
Kaufman, J, Montalvo-Ortiz, JL, Holbrook, H, et al. Adverse childhood experiences, epigenetic measures, and obesity in youth. J Pediatr. 2018; 202, 150–156.e3. DOI 10.1016/j.jpeds.2018.06.051.CrossRefGoogle ScholarPubMed
Marzi, SJ, Sugden, K, Arseneault, L, et al. Analysis of DNA methylation in young people: limited evidence for an association between victimization stress and epigenetic variation in blood. Am J Psychiatry. 2018; 175(6), 517–529. DOI 10.1176/appi.ajp.2017.17060693.CrossRefGoogle ScholarPubMed
Houtepen, LC, Hardy, R, Maddock, J, et al. Childhood adversity and DNA methylation in two population-based cohorts. Transl Psychiatry. 2018; 8(1), 378. DOI 10.1038/s41398-018-0307-3.Google ScholarPubMed
Marinova, Z, Maercker, A, Küffer, A, et al. DNA methylation profiles of elderly individuals subjected to indentured childhood labor and trauma. BMC Med Genet. 2017; 18(1), 608. DOI 10.1186/s12881-017-0370-2.CrossRefGoogle ScholarPubMed
Khulan, B, Manning, JR, Dunbar, DR, et al. Epigenomic profiling of men exposed to early-life stress reveals DNA methylation differences in association with current mental state. Transl Psychiatry. 2014; 4(9), e448. DOI 10.1038/tp.2014.94.CrossRefGoogle ScholarPubMed
Panek, M, Jonakowski, M, ZioŁo, J, et al. A novel approach to understanding the role of polymorphic forms of the NR3C1 and TGF-β1 genes in the modulation of the expression of IL-5 and IL-15 mRNA in asthmatic inflammation. Mol Med Rep. 2016; 13(6), 4879–4887. DOI 10.3892/mmr.2016.5104.CrossRefGoogle ScholarPubMed
Riba, M, Garcia Manteiga, JM, Bošnjak, B, et al. Revealing the acute asthma ignorome: characterization and validation of uninvestigated gene networks. Sci Rep. 2016; 6(1), 2055. DOI 10.1038/srep24647.CrossRefGoogle ScholarPubMed
Panek, M, Pietras, T, Fabijan, A, et al. The NR3C1 glucocorticoid receptor gene polymorphisms may modulate the TGF-beta mRNA expression in asthma patients. Inflammation. 2015; 38(4), 1479–1492. DOI 10.1007/s10753-015-0123-3.Google ScholarPubMed
Al‐Hussainy, A, Mohammed, R. Consequences of maternal psychological stress during pregnancy for the risk of asthma in the offspring. Scand J Immunol. 2021; 93(1), e12919.CrossRefGoogle ScholarPubMed
Singhania, A, Rupani, H, Jayasekera, N, et al. Altered epithelial gene expression in peripheral airways of severe asthma. PLOS ONE. 2017; 12(1), e0168680. DOI 10.1371/journal.pone.0168680.Google ScholarPubMed
Zannas, AS, Wiechmann, T, Gassen, NC, Binder, EB. Gene-stress–epigenetic regulation of FKBP5: clinical and translational implications. Neuropsychopharmacolo. 2015; 41(1), 261–274. DOI 10.1038/npp.2015.235.CrossRefGoogle ScholarPubMed
Zannas, AS, Jia, M, Hafner, K, et al. Epigenetic upregulation of FKBP5 by aging and stress contributes to NF-κB-driven inflammation and cardiovascular risk. Proc Natl Acad Sci USA. 2019; 116(23), 11370–11379. DOI 10.1073/pnas.1816847116.CrossRefGoogle ScholarPubMed
Wu, C, Orozco, C, Boyer, J, et al. BioGPS: an extensible and customizable portal for querying and organizing gene annotation resources 2021, http://biogps.org/#goto=genereport&id=92565.Google Scholar
Tremblay, K, Lemire, M, Potvin, C, et al. Genes to diseases (G2D) computational method to identify asthma candidate genes. PLoS ONE. 2008; 3(8), e2907. DOI 10.1371/journal.pone.0002907.CrossRefGoogle ScholarPubMed
Wilk, JB, Shrine, NRG, Loehr, LR, et al. Genome-wide association studies identify chrna5/3andHTR4 in the development of airflow obstruction. Am J Respir Crit Care Med. 2012; 186(7), 622–632. DOI 10.1164/rccm.201202-0366oc.CrossRefGoogle ScholarPubMed
Krais, AM, Hautefeuille, AH, Cros, M-P, et al. CHRNA5 as negative regulator of nicotine signaling in normal and cancer bronchial cells: effects on motility, migration and p63 expression. Carcinogenesis. 2011; 32(9), 1388–1395. DOI 10.1093/carcin/bgr090.CrossRefGoogle ScholarPubMed
Xie, P, Kranzler, HR, Zhang, H, et al. Childhood adversity increases risk for nicotine dependence and interacts with α5 nicotinic acetylcholine receptor genotype specifically in males. Neuropsychopharmacol. 2011; 37(3), 669–676. DOI 10.1038/npp.2011.240.Google ScholarPubMed
Zhang, N-Z, Chen, X-J, Mu, Y-H, Wang, H. Identification of differentially expressed genes in childhood asthma. Medicine. 2018; 97(21), e10861. DOI 10.1097/md.0000000000010861.Google ScholarPubMed
Dreymueller, D, Uhlig, S, Ludwig, A. ADAM-family metalloproteinases in lung inflammation: potential therapeutic targets. Am J Physiol Lung Cell Mol Physiol. 2015; 308(4), L325–L343. DOI 10.1152/ajplung.00294.2014.CrossRefGoogle ScholarPubMed
Kang, BN, Ha, SG, Bahaie, NS, et al. Regulation of serotonin-induced trafficking and migration of Eosinophils. PLoS ONE. 2013; 8(1), e54840. DOI 10.1371/journal.pone.0054840.CrossRefGoogle ScholarPubMed
Flanagan, TW, Sebastian, MN, Battaglia, DM, Foster, TP, Cormier, SA, Nichols, CD. 5-HT2 receptor activation alleviates airway inflammation and structural remodeling in a chronic mouse asthma model. Life Sci. 2019; 236(Suppl 2), 116790. DOI 10.1016/j.lfs.2019.116790.CrossRefGoogle Scholar
Farjadian, S, Moghtaderi, M, Fakhraei, B, Nasiri, M, Farjam, M. Association between serotonin transporter gene polymorphisms and childhood asthma. J Asthma. 2013; 50(10), 1031–1035. DOI 10.3109/02770903.2013.834503.CrossRefGoogle ScholarPubMed
Amrani, Y, Syed, F, Huang, C, et al. Expression and activation of the oxytocin receptor in airway smooth muscle cells: regulation by TNFα and IL-13. Respir Res. 2010; 11(1), 629. DOI 10.1186/1465-9921-11-104.CrossRefGoogle ScholarPubMed
Yick, CY, Zwinderman, AH, Kunst, PW, et al. Gene expression profiling of laser microdissected airway smooth muscle tissue in asthma and atopy. Allergy. 2014; 69(9), 1233–1240. DOI 10.1111/all.12452.Google ScholarPubMed
Zhang, Y, Jing, Y, Qiao, J, et al. Activation of the mTOR signaling pathway is required for asthma onset. Sci Rep. 2017; 7(1), 143. DOI 10.1038/s41598-017-04826-y.Google ScholarPubMed
Williams, JW, Yau, D, Sethakorn, N, et al. RGS3 controls T lymphocyte migration in a model of Th2-mediated airway inflammation. Am J Physiol Lung Cell Mol Physiol. 2013; 305(10), L693–L701. DOI 10.1152/ajplung.00214.2013.CrossRefGoogle Scholar
Sakai, H, Nishimura, A, Watanabe, Y, et al. Involvement of Src family kinase activation in angiotensin II-induced hyperresponsiveness of rat bronchial smooth muscle. Peptides. 2010; 31(12), 2216–2221. DOI 10.1016/j.peptides.2010.09.012.CrossRefGoogle ScholarPubMed
Gauthier, M, Chakraborty, K, Oriss, TB, et al. Severe asthma in humans and mouse model suggests a CXCL10 signature underlies corticosteroid resistant Th1 bias. JCI Insight. 2017; 2(13), e94580. DOI 10.1172/jci.insight.94580.Google ScholarPubMed
Qian, X, Gao, Y, Ye, X, Lu, M. Association of STAT6 variants with asthma risk: a systematic review and meta-analysis. Hum Immunol. 2014; 75(8), 847–853. DOI 10.1016/j.humimm.2014.06.007.CrossRefGoogle ScholarPubMed
Kim, D, Cho, S, Woo, JA, Liggett, SB. A CREB-mediated increase in miRNA let-7f during prolonged β-agonist exposure: a novel mechanism of β2-adrenergic receptor down-regulation in airway smooth muscle. The FASEB J. 2018; 32(7), 3680–3688. DOI 10.1096/fj.201701278r.Google ScholarPubMed
Jeong, A, Imboden, M, Ghantous, A, et al. DNA methylation in inflammatory pathways modifies the association between BMI and adult-onset non-atopic asthma. Int J Environ Res Public Health. 2019; 16(4), 600. DOI 10.3390/ijerph16040600.Google ScholarPubMed
Kuroda, A, Hegab, AE, Jingtao, G, et al. Effects of the common polymorphism in the human aldehyde dehydrogenase 2 (ALDH2) gene on the lung. Respir Res. 2017; 18(1), 583. DOI 10.1186/s12931-017-0554-5.CrossRefGoogle ScholarPubMed
Shimoda, T, Obase, Y, Matsuse, H, Asai, S, Iwanaga, T. The pathogenesis of alcohol-induced airflow limitation in acetaldehyde dehydrogenase 2-deficient mice. Intl Arch Allergy Immunol. 2016; 171(3-4), 276–284. DOI 10.1159/000452709.Google ScholarPubMed
Chung, KF. p38 mitogen-activated protein kinase pathways in asthma and COPD. Chest. 2011; 139(6), 1470–1479. DOI 10.1378/chest.10-1914.CrossRefGoogle ScholarPubMed
Makinde, TO, Steininger, R, Agrawal, DK. NPY and NPY receptors in airway structural and inflammatory cells in allergic asthma. Exp Mol Pathol. 2013; 94(1), 45–50. DOI 10.1016/j.yexmp.2012.05.009.Google ScholarPubMed
Li, S, Koziol-White, C, Jude, J, et al. Epithelium-generated neuropeptide Y induces smooth muscle contraction to promote airway hyperresponsiveness. J Clin Invest. 2016; 126(5), 1978–1982. DOI 10.1172/JCI81389.CrossRefGoogle ScholarPubMed
Boeck, A, Landgraf-Rauf, K, Vogelsang, V, et al. Ca2+ and innate immune pathways are activated and differentially expressed in childhood asthma phenotypes. Pediatr Allergy Immunol. 2018; 29(8), 823–833. DOI 10.1111/pai.12971.CrossRefGoogle ScholarPubMed
Fabregat, A, Sidiropoulos, K, Viteri, G, et al. Reactome pathway analysis: a high-performance in-memory approach. BMC Bioinform. 2017; 18(1), 383. DOI 10.1186/s12859-017-1559-2.Google ScholarPubMed
DeVries, A, Vercelli, D. Epigenetic mechanisms in asthma. Ann Am Thorac Soc. 2016; 13(Suppl 1), S48–S50. DOI 10.1513/AnnalsATS.201507-420MG.CrossRefGoogle ScholarPubMed
Chogtu, B, Bhattacharjee, D, Magazine, R. Epigenetics: the new frontier in the landscape of asthma. Scientifica. 2016; 2016(2), 4638949. DOI 10.1155/2016/4638949.Google ScholarPubMed
Supplementary material: PDF

Saygideger et al. supplementary material

Saygideger et al. supplementary material 1

Download Saygideger et al. supplementary material(PDF)
PDF 425.4 KB
Supplementary material: File

Saygideger et al. supplementary material

Saygideger et al. supplementary material 2

Download Saygideger et al. supplementary material(File)
File 25.2 KB
Supplementary material: File

Saygideger et al. supplementary material

Saygideger et al. supplementary material 3

Download Saygideger et al. supplementary material(File)
File 15.1 KB