Maternal atopy and offspring epigenome-wide methylation signature

Danielewicz, Hanna; Gurgul, Artur; Dębińska, Anna; Myszczyszyn, Grzegorz; Szmatoła, Tomasz; Myszkal, Anna; Jasielczuk, Igor; Drabik-Chamerska, Anna; Hirnle, Lidia; Boznański, Andrzej

doi:10.1080/15592294.2020.1814504

Cited by 13 publications

(12 citation statements)

References 71 publications

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“…Murine studies have shown that epigenetically modified dendritic cells transmit the allergic risk from mothers to offspring [ 70 ]. Another study demonstrated that maternal and paternal allergy were important risk factors for AR in offspring [ 71 , 72 ]. Consistent with the findings of this study, the current study also found that a history of allergies was intensely relevant to the development of AR.…”

Section: Discussionmentioning

confidence: 99%

Prevalence and Risk Factors for Allergic Rhinitis in China: A Systematic Review and Meta-Analysis

Pang

et al. 2022

Evidence-Based Complementary and Alternative Medicine

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The prevalence of allergic rhinitis (AR) has increased tremendously in the recent year in China. Evidence-based medicine to objectively evaluate the prevalence and risk factors for AR in China is urgently required. Toward this, we systematically searched four English and four Chinese databases to identify the literature on the same, from the year of website establishment until November 2021. A total of 51 studies were evaluated, and data were obtained through Stata 16 analysis. Overall pooled risk factors for adult AR were smoking (odds ratio [OR] = 1.89, 95% confidence interval [CI]: 1.25, 2.87), asthma (OR = 3.30, 95% CI: 1.48, 7.39), a family history of AR (OR = 3.17, 95% CI: 2.31, 4.34), a family history of asthma (OR = 3.99, 95% CI: 2.58, 6.16), drug allergy (OR = 1.62, 95% CI: 1.38, 1.89), food allergy (OR = 2.29, 95% CI: 1.39, 3.78), pollen allergy history (OR = 2.41, 95% CI: 1.67, 3.46), antibiotic use (OR = 2.08, 95% CI: 1.28, 3.36), occupational dust exposure (OR = 2.05, 95% CI: 1.70, 2.47), home renovation (OR = 1.73, 95% CI: 0.99, 3.02), and middle school education (OR = 1.99, 95% CI: 1.29, 3.06). Overall pooled risk factors for AR in children were passive smoking (OR = 1.70, 95% CI: 1.02, 2.82), asthma (OR = 3.26, 95% CI: 2.42, 4.39), a family history of AR (OR = 2.59, 95% CI: 2.07, 3.24), a family history of allergy (OR = 4.84, 95% CI: 3.22, 7.26), a history of allergic diseases (OR = 2.11, 95% CI: 1.52, 2.94), eczema(OR = 2.29, 95% CI: 1.36, 3.85), owning pets (OR = 1.56, 95% CI: 1.37, 1.77), eating seafood (OR = 1.30, 95% CI: 1.10, 1.55), boys (OR = 1.58, 95% CI: 1.43, 1.74), and breastfeeding (OR = 0.82, 95% CI: 0.55, 1.22). The results of our meta-analysis showed that the prevalence of allergy rhinitis was 19% (95% CI 14–25) among adults and 22% (95% CI 17–27) among children, with boys showing a higher prevalence than girls. The development of AR in China is associated with several factors, including allergic diseases (eczema, asthma, pollen allergy, and food allergy), a family history of allergy (AR, asthma, and other allergies), and dwelling and working environment (smoking or passive smoking, occupational dust exposure, and owning pets); conversely, breastfeeding can reduce the risk.

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Section: Discussionmentioning

confidence: 99%

Prevalence and Risk Factors for Allergic Rhinitis in China: A Systematic Review and Meta-Analysis

Pang

et al. 2022

Evidence-Based Complementary and Alternative Medicine

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“…Previous studies report that maternal asthma is a greater risk factor than paternal asthma for the inheritance of the disease (5- fold greater) ( 9 ) and a lack of maternal asthma control during pregnancy imparts a greater risk of asthma/recurrent wheeze in the offspring when compared to a controlled maternal asthma status throughout pregnancy ( 9 ). During in utero development, the fetus is constantly exposed to an environment in which it is surrounded by the maternal metabolic and immune milieu ( 99 ). A growing number of studies indicate that the in utero environment of asthmatic mothers is distinct from that of non-asthmatic mothers, where the presence of those cytokines associated with asthma may cause developmental alterations ( 100 ), with reports indicating that both asthma and atopy have their origins during in utero development ( 93 , 100 ).…”

Section: Asthma and The Transfer Of Maternal Immune Factorsmentioning

confidence: 99%

“…A growing number of studies indicate that the in utero environment of asthmatic mothers is distinct from that of non-asthmatic mothers, where the presence of those cytokines associated with asthma may cause developmental alterations ( 100 ), with reports indicating that both asthma and atopy have their origins during in utero development ( 93 , 100 ). Maternal atopy has been found to be associated with differential methylation patterns in the cord blood of neonates ( 99 ). A study of 36 patients enrolled in the Infant Immune Study looking for DNA methylation signatures predictive of childhood asthma identified that cord blood mononuclear cells (CBMCs) harbored 589 differentially methylated regions (DMRs) associated with childhood asthma; further analysis of which showed a significant enrichment of DMRs in genes controlled by immunoregulatory TGF-β1 and pro-inflammatory IL-1β ( 101 ).…”

Section: Asthma and The Transfer Of Maternal Immune Factorsmentioning

confidence: 99%

“…showed that higher methylation of GATA3 CpGs-2211/-2209 at birth was associated with a reduced risk of asthma at 3 years of age ( 103 ). A very recent EWAS of cord-blood samples in a cohort of 96 mother-child pairs, recruited as part of the ongoing ELMA- Epigenetic Hallmark of Maternal Atopy and Diet study, indicated that maternal atopy was associated with specific epigenetic signatures in the offspring, identifying 83 CpG islands mapping to 50 genes associated with maternal atopy ( 99 ). The genes C20orf166, STAC, SYT8, KCNJ15, SCD, LINCOO669, PLEKHA2, ITM2C, NT5C3A and NPEPL1 had the most significant differentially methylated sites of which SCD, ITM2C, NT5C3A and NPEPL1 genes are known to impact the immune system, allergy, and asthma; thereby suggesting that maternal atopy constitutes a unique intrauterine environment which is associated with the induction of distinct methylation patterns associated with the inheritance of a pro-atopic state ( 99 ).…”

Section: Asthma and The Transfer Of Maternal Immune Factorsmentioning

confidence: 99%

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Asthma and the Missing Heritability Problem: Necessity for Multiomics Approaches in Determining Accurate Risk Profiles

et al. 2022

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Asthma is ranked among the most common chronic conditions and has become a significant public health issue due to the recent and rapid increase in its prevalence. Investigations into the underlying genetic factors predict a heritable component for its incidence, estimated between 35% and 90% of causation. Despite the application of large-scale genome-wide association studies (GWAS) and admixture mapping approaches, the proportion of variants identified accounts for less than 15% of the observed heritability of the disease. The discrepancy between the predicted heritable component of disease and the proportion of heritability mapped to the currently identified susceptibility loci has been termed the ‘missing heritability problem.’ Here, we examine recent studies involving both the analysis of genetically encoded features that contribute to asthma and also the role of non-encoded heritable characteristics, including epigenetic, environmental, and developmental aspects of disease. The importance of vertical maternal microbiome transfer and the influence of maternal immune factors on fetal conditioning in the inheritance of disease are also discussed. In order to highlight the broad array of biological inputs that contribute to the sum of heritable risk factors associated with allergic disease incidence that, together, contribute to the induction of a pro-atopic state. Currently, there is a need to develop in-depth models of asthma risk factors to overcome the limitations encountered in the interpretation of GWAS results in isolation, which have resulted in the missing heritability problem. Hence, multiomics analyses need to be established considering genetic, epigenetic, and functional data to create a true systems biology-based approach for analyzing the regulatory pathways that underlie the inheritance of asthma and to develop accurate risk profiles for disease.

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“…As recent studies have emphasized the importance of maternal effects on chromatin structure and the interrelationship between the genome, epigenome, and environment [ 35 , 36 ], our aim was to investigate whether RST elicited molecular epigenetic events such as histone methylation in the brains of the newborn rats whose mothers had been treated chronically with the drug.…”

Section: Introductionmentioning

confidence: 99%

Epigenetic Consequences of in Utero Exposure to Rosuvastatin: Alteration of Histone Methylation Patterns in Newborn Rat Brains

Dulka

Szabó

Lajkó

et al. 2021

IJMS

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Rosuvastatin (RST) is primarily used to treat high cholesterol levels. As it has potentially harmful but not well-documented effects on embryos, RST is contraindicated during pregnancy. To demonstrate whether RST could induce molecular epigenetic events in the brains of newborn rats, pregnant mothers were treated daily with oral RST from the 11th day of pregnancy for 10 days (or until delivery). On postnatal day 1, the brains of the control and RST-treated rats were removed for Western blot or immunohistochemical analyses. Several antibodies that recognize different methylation sites for H2A, H2B, H3, and H4 histones were quantified. Analyses of cell-type-specific markers in the newborn brains demonstrated that prenatal RST administration did not affect the composition and cell type ratios as compared to the controls. Prenatal RST administration did, however, induce a general, nonsignificant increase in H2AK118me1, H2BK5me1, H3, H3K9me3, H3K27me3, H3K36me2, H4, H4K20me2, and H4K20me3 levels, compared to the controls. Moreover, significant changes were detected in the number of H3K4me1 and H3K4me3 sites (134.3% ± 19.2% and 127.8% ± 8.5% of the controls, respectively), which are generally recognized as transcriptional activators. Fluorescent/confocal immunohistochemistry for cell-type-specific markers and histone methylation marks on tissue sections indicated that most of the increase at these sites belonged to neuronal cell nuclei. Thus, prenatal RST treatment induces epigenetic changes that could affect neuronal differentiation and development.

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Maternal atopy and offspring epigenome-wide methylation signature

Cited by 13 publications

References 71 publications

Prevalence and Risk Factors for Allergic Rhinitis in China: A Systematic Review and Meta-Analysis

Prevalence and Risk Factors for Allergic Rhinitis in China: A Systematic Review and Meta-Analysis

Asthma and the Missing Heritability Problem: Necessity for Multiomics Approaches in Determining Accurate Risk Profiles

Epigenetic Consequences of in Utero Exposure to Rosuvastatin: Alteration of Histone Methylation Patterns in Newborn Rat Brains

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