Prenatal exposure to tobacco smoke sex dependently influences methylation and mRNA levels of the <i>Igf</i> axis in lungs of mouse offspring

Meyer, Karolin F; Krauss‐Etschmann, Susanne; Kooistra, Wierd; Reinders-Luinge, Marjan; Timens, Wim; Kobzik, Lester; Plösch, Torsten; Hylkema, Machteld N.

doi:10.1152/ajplung.00271.2016

Cited by 30 publications

(32 citation statements)

References 36 publications

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“…32 Another study also demonstrated sex-differences, as decreased body weight was observed in female but not male murine offspring after in utero smoke exposure. 33 These studies confirm that the influence of cigarette smoke on fetal growth observed in humans is largely reproducible in mice.…”

Section: Intrauterine Growth Restrictionsupporting

confidence: 70%

“…Smoking either only during the pre‐implantation period, or throughout the entire pregnancy decreased fetal weight significantly, while fetal length was decreased only by exposure in early pregnancy . Another study also demonstrated sex‐differences, as decreased body weight was observed in female but not male murine offspring after in utero smoke exposure . These studies confirm that the influence of cigarette smoke on fetal growth observed in humans is largely reproducible in mice.…”

Section: Models Of Active Cigarette Smoking During Pregnancymentioning

confidence: 62%

“…Further, epigenetic modifications were suggested by DNA methylation of the IGF‐1R promoter region. Meyer et al concluded that the changes in IGF‐1 and IGF‐1R expression, growth restriction and alterations in DNA methylation can lead to higher asthma susceptibility later in life due to the involvement of the IGF axis in lung development. This is of interest as epidemiology studies show that alterations in DNA methylation are associated with increased asthma risk later in life .…”

Section: Models Of Active Cigarette Smoking During Pregnancymentioning

confidence: 99%

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In utero exposure to cigarette smoke and effects across generations: A conference of animals on asthma

Hammer

Wagner

Rankov

et al. 2018

Clin Experimental Allergy

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Summary Background The prevalence of asthma and chronic obstructive pulmonary disease (COPD) has risen markedly over the last decades and is reaching epidemic proportions. However, underlying molecular mechanisms are not fully understood, hampering the urgently needed development of approaches to prevent these diseases. It is well established from epidemiological studies that prenatal exposure to cigarette smoke is one of the main risk factors for aberrant lung function development or reduced fetal growth, but also for the development of asthma and possibly COPD later in life. Of note, recent evidence suggests that the disease risk can be transferred across generations, that is, from grandparents to their grandchildren. While initial studies in mouse models on in utero smoke exposure have provided important mechanistic insights, there are still knowledge gaps that need to be filled. Objective Thus, in this review, we summarize current knowledge on this topic derived from mouse models, while also introducing two other relevant animal models: the fruit fly Drosophila melanogaster and the zebrafish Danio rerio. Methods This review is based on an intensive review of PubMed‐listed transgenerational animal studies from 1902 to 2018 and focuses in detail on selected literature due to space limitations. Results This review gives a comprehensive overview of mechanistic insights obtained in studies with the three species, while highlighting the remaining knowledge gaps. We will further discuss potential (dis)advantages of all three animal models. Conclusion/Clinical Relevance Many studies have already addressed transgenerational inheritance of disease risk in mouse, zebrafish or fly models. We here propose a novel strategy for how these three model organisms can be synergistically combined to achieve a more detailed understanding of in utero cigarette smoke‐induced transgenerational inheritance of disease risk.

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Section: Intrauterine Growth Restrictionsupporting

confidence: 70%

Section: Models Of Active Cigarette Smoking During Pregnancymentioning

confidence: 62%

Section: Models Of Active Cigarette Smoking During Pregnancymentioning

confidence: 99%

See 1 more Smart Citation

In utero exposure to cigarette smoke and effects across generations: A conference of animals on asthma

Hammer

Wagner

Rankov

et al. 2018

Clin Experimental Allergy

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“…DNA methylation appears to be dispensable in undifferentiated cells, whereas it is absolutely required in differentiated cells, as genetic deletion of DNA methyltransferase results in embryonic or post-partum lethality [40]. Moreover, DNA methylation plays a pivotal role in regulating gene expression in response to external stimuli, as in the expression of metabolic or developmental genes in the offspring of pregnant mice exposed to different insults [2,41]. Further studies have delineated the biological impact of DNA methylation in cancer by silencing DNA methyltransferases, or by treating cells with DNA demethylating agents [40].…”

Section: Introductionmentioning

confidence: 99%

Coordinated Actions of MicroRNAs with other Epigenetic Factors Regulate Skeletal Muscle Development and Adaptation

Bianchi

Renzini

Adamo

et al. 2017

IJMS

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Epigenetics plays a pivotal role in regulating gene expression in development, in response to cellular stress or in disease states, in virtually all cell types. MicroRNAs (miRNAs) are short, non-coding RNA molecules that mediate RNA silencing and regulate gene expression. miRNAs were discovered in 1993 and have been extensively studied ever since. They can be expressed in a tissue-specific manner and play a crucial role in tissue development and many biological processes. miRNAs are responsible for changes in the cell epigenome because of their ability to modulate gene expression post-transcriptionally. Recently, numerous studies have shown that miRNAs and other epigenetic factors can regulate each other or cooperate in regulating several biological processes. On the one hand, the expression of some miRNAs is silenced by DNA methylation, and histone modifications have been demonstrated to modulate miRNA expression in many cell types or disease states. On the other hand, miRNAs can directly target epigenetic factors, such as DNA methyltransferases or histone deacetylases, thus regulating chromatin structure. Moreover, several studies have reported coordinated actions between miRNAs and other epigenetic mechanisms to reinforce the regulation of gene expression. This paper reviews multiple interactions between miRNAs and epigenetic factors in skeletal muscle development and in response to stimuli or disease.

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“…Epigenetic mechanisms, which can be heritable and sensitive to exogenous influence, are independent of the consequences of changes in DNA sequence for regulating gene expression (Feil and Fraga, 2011). Epidemiological and experimental studies have reported an association between prenatal smoke exposure and altered epigenetic methylation patterns in both elementary school-aged children and 30 days post-birth mice (Breton et al, 2009; Meyer et al, 2017). DNA methylation alteration is the process of adding or removing methyl groups to DNA, particularly within gene promoter regions, which can then influence gene regulation, without altering the genetic sequence (Smith and Meissner, 2013).…”

Section: Introductionmentioning

confidence: 99%

Perinatal exposure to environmental tobacco smoke is associated with changes in DNA methylation that precede the adult onset of lung disease in a mouse model

Cole

Brown

Pinkerton

et al. 2017

Inhalation Toxicology

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Prenatal and early-life environmental tobacco smoke (ETS) exposure can induce epigenetic alterations associated with inflammation and respiratory disease. The objective of this study was to address the long-term epigenetic consequences of perinatal ETS exposure on latent respiratory disease risk, which are still largely unknown. C57BL/6 mice were exposed to prenatal and early-life ETS; offspring lung pathology, global DNA, and gene-specific methylation were measured at two adult ages. Significant alterations in global DNA methylation and promoter methylation of IFN-γ and Thy-1 were found in ETS-exposed offspring at 10–12 and 20 weeks of age. These sustained epigenetic alterations preceded the onset of significant pulmonary pathologies observed at 20 weeks of age. This study suggests that perinatal ETS exposure induces persistent epigenetic alterations in global DNA, as well as IFN-γ and Thy-1 promoter methylation that precede the adult onset of fibrotic lung pathology. These epigenetic findings could represent potential biomarkers of latent respiratory disease risk.

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Prenatal exposure to tobacco smoke sex dependently influences methylation and mRNA levels of the Igf axis in lungs of mouse offspring

Cited by 30 publications

References 36 publications

In utero exposure to cigarette smoke and effects across generations: A conference of animals on asthma

In utero exposure to cigarette smoke and effects across generations: A conference of animals on asthma

Coordinated Actions of MicroRNAs with other Epigenetic Factors Regulate Skeletal Muscle Development and Adaptation

Perinatal exposure to environmental tobacco smoke is associated with changes in DNA methylation that precede the adult onset of lung disease in a mouse model

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