Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations

Manikkam, Mohan; Tracey, Rebecca; Guerrero-Bosagna, Carlos; Skinner, Michael K.

doi:10.1016/j.reprotox.2012.08.010

Cited by 188 publications

(156 citation statements)

References 60 publications

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“…There was no increase in ovarian disease in direct fetal exposed F1 or germline exposed F2 generation vinclozolin or DDT lineage rats compared to controls [30,31]. Therefore, as previously observed with most exposures, negligible ovarian disease is present following direct exposure [25,27–29], with the exception of BPA and phthalates [26]. This indicates that there was an epigenetic transgenerational increase in susceptibility to ovarian disease in rats ancestrally exposed to DDT or vinclozolin (Figure 1).…”

Section: Resultsmentioning

confidence: 71%

“…There was a significant increase in ovarian disease in transgenerational F3 generation DDT and vinclozolin lineage rats at one year of age compared to F3 generation controls (Figure 1). Previous studies have shown that transgenerational increases in ovarian disease were detected following exposures to plastic derived compounds bisphenol A (BPA) and phthalates (DBT & DEHP) [26], dioxin (TCCD) [25], pesticides permethrin and DEET [27], jet fuel hydrocarbons [28], and methoxychlor [29], with nearly 100% disease frequency. Therefore, the transgenerational inheritance of increased ovarian disease can occur after exposure to a variety of environmental toxicants.…”

Section: Resultsmentioning

confidence: 99%

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Environmental toxicant induced epigenetic transgenerational inheritance of ovarian pathology and granulosa cell epigenome and transcriptome alterations: ancestral origins of polycystic ovarian syndrome and primary ovarian insufficiency

et al. 2018

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Two of the most prevalent ovarian diseases affecting women’s fertility and health are Primary Ovarian Insufficiency (POI) and Polycystic Ovarian Syndrome (PCOS). Previous studies have shown that exposure to a number of environmental toxicants can promote the epigenetic transgenerational inheritance of ovarian disease. In the current study, transgenerational changes to the transcriptome and epigenome of ovarian granulosa cells are characterized in F3 generation rats after ancestral vinclozolin or DDT exposures. In purified granulosa cells from 20-day-old F3 generation females, 164 differentially methylated regions (DMRs) (P < 1 x 10−6) were found in the F3 generation vinclozolin lineage and 293 DMRs (P < 1 x 10−6) in the DDT lineage, compared to controls. Long noncoding RNAs (lncRNAs) and small noncoding RNAs (sncRNAs) were found to be differentially expressed in both the vinclozolin and DDT lineage granulosa cells. There were 492 sncRNAs (P < 1 x 10−4) in the vinclozolin lineage and 1,085 sncRNAs (P < 1 x 10−4) in the DDT lineage. There were 123 lncRNAs and 51 lncRNAs in the vinclozolin and DDT lineages, respectively (P < 1 x 10−4). Differentially expressed mRNAs were also found in the vinclozolin lineage (174 mRNAs at P < 1 x 10−4) and the DDT lineage (212 mRNAs at P < 1 x 10−4) granulosa cells. Comparisons with known ovarian disease associated genes were made. These transgenerational epigenetic changes appear to contribute to the dysregulation of the ovary and disease susceptibility that can occur in later life. Observations suggest that ancestral exposure to toxicants is a risk factor that must be considered in the molecular etiology of ovarian disease.

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Section: Resultsmentioning

confidence: 71%

Section: Resultsmentioning

confidence: 99%

Environmental toxicant induced epigenetic transgenerational inheritance of ovarian pathology and granulosa cell epigenome and transcriptome alterations: ancestral origins of polycystic ovarian syndrome and primary ovarian insufficiency

et al. 2018

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“…Recently, a series of studies have shown that exposing the gestating mammalian female F0 to environmental factors during embryonic gonadal sex determination causes changes in DNA methylation that are retained in adult F1–3 male progeny, which produce sperm with altered DNA methylation (8–12). The inherited changes were monitored in the third generation after treatment (13–15).…”

Section: Introductionmentioning

confidence: 99%

Exposure to the widely used herbicide atrazine results in deregulation of global tissue-specific RNA transcription in the third generation and is associated with a global decrease of histone trimethylation in mice

et al. 2016

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The epigenetic events imposed during germline reprogramming and affected by harmful exposure can be inherited and transferred to subsequent generations via gametes inheritance. In this study, we examine the transgenerational effects promoted by widely used herbicide atrazine (ATZ). We exposed pregnant outbred CD1 female mice and the male progeny was crossed for three generations with untreated females. We demonstrate here that exposure to ATZ affects meiosis, spermiogenesis and reduces the spermatozoa number in the third generation (F3) male mice. We suggest that changes in testis cell types originate from modified transcriptional network in undifferentiated spermatogonia. Importantly, exposure to ATZ dramatically increases the number of transcripts with novel transcription initiation sites, spliced variants and alternative polyadenylation sites. We found the global decrease in H3K4me3 occupancy in the third generation males. The regions with altered H3K4me3 occupancy in F3 ATZ-derived males correspond to altered H3K4me3 occupancy of F1 generation and 74% of changed peaks in F3 generation are associated with enhancers. The regions with altered H3K4me3 occupancy are enriched in SP family and WT1 transcription factor binding sites. Our data suggest that the embryonic exposure to ATZ affects the development and the changes induced by ATZ are transferred up to three generations.

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“…Shorter adult height, less schooling, reduced economic productivity, lower offspring birth weight, high glucose concentrations, high blood pressure, and harmful lipid profiles were more prevalent among those exposed to prenatal malnutrition. [57] This is a good example of how malnutrition without necessarily widespread famine as that of the Dutch (1944Dutch ( -1945, Chinese (1959Chinese ( -1961, or the Biafran (1967)(1968)(1969)(1970), could influence offsprings' adult Rat Maternal exposure to permethrin and DEET (pesticide and insect repellent mixture) during pregnancy [288] Increased pubertal abnormalities, testis disease, and ovarian disease (primordial follicle loss and polycystic ovarian disease) in F3 generation…”

Section: Hypomethylation Of the Pancreatic Il13ra2 Genementioning

confidence: 99%

“…[280][281][282][283][284] Other commonly available environmental and air pollutants including pesticides, agricultural chemicals, and others have also been shown to induce extensive epigenetic changes that are inherited transgenerationally with consequent increases in the risk of adult NCCDs. [285][286][287][288][289][290][291][292] From the beginning of the industrial revolution, humans have undoubtedly been exposed to a wide range of chemicals and environmental pollutants that could have programed the risk of many diseases in different communities. Moreover, at the beginning of the industrial revolution no legislations were available to control the industrial production of many pollutants or the use of chemicals to manufacture materials for domestic use as we have today.…”

Section: Smoking Alcohol Pollutants and Other Environmental Chemicalsmentioning

confidence: 99%

The Impact of Traditional Food and Lifestyle Behavior on Epigenetic Burden of Chronic Disease

Imam

Ismail

2017

Global Challenges

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There are already extensive reviews on the global burden of NCCDs in the public domain. [1][2][3][4][5][6] The consensus that can be surmised from the available data on NCCDs is that their overall prevalence appears to be rising globally and the projections indicate an upward trend. Epidemiological transition data suggests that the morbidity and mortality rate from these diseases is far more than that of communicable diseases in the developed world [7] and a similar trend is now occurring in the low to medium income countries (LMICs). [8] Among the NCCDs, cardiovascular diseases (CVDs) are the leading causes of morbidity and mortality, followed closely by metabolic diseases like Noncommunicable chronic diseases (NCCDs) are the leading causes of morbidity and mortality globally. The mismatch between present day diets and ancestral genome is suggested to contribute to the NCCDs burden, which is promoted by traditional risk factors like unhealthy diets, physical inactivity, alcohol and tobacco. However, epigenetic evidence now suggests that cumulatively inherited epigenetic modifications may have made humans more prone to the effects of present day lifestyle factors. Perinatal starvation was widespread in the 19th century. This together with more recent events like increasing consumption of western and low fiber diets, smoking, harmful use of alcohol, physical inactivity, and environmental pollutants may have programed the human epigenome for higher NCCDs risk. In this review, on the basis of available epigenetic data it is hypothesized that transgenerational effects of lifestyle factors may be contributing to the current global burden of NCCDs. Thus, there is a need to reconsider prevention strategies so that the subsequent generations will not have to pay for our sins and those of our ancestors. Cardiovascular DiseasesDr. M. U. Imam

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Pesticide and insect repellent mixture (permethrin and DEET) induces epigenetic transgenerational inheritance of disease and sperm epimutations

Cited by 188 publications

References 60 publications

Environmental toxicant induced epigenetic transgenerational inheritance of ovarian pathology and granulosa cell epigenome and transcriptome alterations: ancestral origins of polycystic ovarian syndrome and primary ovarian insufficiency

Environmental toxicant induced epigenetic transgenerational inheritance of ovarian pathology and granulosa cell epigenome and transcriptome alterations: ancestral origins of polycystic ovarian syndrome and primary ovarian insufficiency

Exposure to the widely used herbicide atrazine results in deregulation of global tissue-specific RNA transcription in the third generation and is associated with a global decrease of histone trimethylation in mice

The Impact of Traditional Food and Lifestyle Behavior on Epigenetic Burden of Chronic Disease

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