Atrazine induced transgenerational reproductive effects in medaka (Oryzias latipes)

Cleary, Jacob; Tillitt, Donald E.; Saal, Frederick S. vom; Nicks, Diane; Claunch, Rachel A.; Bhandari, Ramji Kumar

doi:10.1016/j.envpol.2019.05.013

Cited by 72 publications

(21 citation statements)

References 79 publications

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“…the effect must be observed in the first generation where the germ line was not developmentally exposed [136,137], which would be the F2 generation in fish. However, previous research has shown that atrazine (at 25 mg/kg BW/day and 100 mg/kg/ day) can induce transgenerational effects of disease in mice [138,139] and produce transgenerational reproductive defects (at 5ppb and 50ppb) in medaka [140]. Additionally, it appears that disease phenotypes can be exacerbated with each generation [139], suggesting that transgenerational effects on behavior are likely.…”

Section: Possible Mechanisms Underlying Effects Of Atrazine On F1 Promentioning

confidence: 99%

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring

2020

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Increasingly, studies are revealing that endocrine disrupting chemicals (EDCs) can alter animal behavior. Early life exposure to EDCs may permanently alter phenotypes through to adulthood. In addition, the effects of EDCs may not be isolated to a single generation − offspring may indirectly be impacted, via non-genetic processes. Here, we analyzed the effects of paternal atrazine exposure on behavioral traits (distance moved, exploration, bottomdwelling time, latency to enter the top zone, and interaction with a mirror) and whole-brain mRNA of genes involved in the serotonergic system regulation (slc6a4a, slc6a4b, htr1Aa, htr1B, htr2B) of zebrafish (Danio rerio). F0 male zebraFIsh were exposed to atrazine at 0.3, 3 or 30 part per billion (ppb) during early juvenile development, the behavior of F1 progeny was tested at adulthood, and the effect of 0.3 ppb atrazine treatment on mRNA transcription was quantified. Paternal exposure to atrazine significantly reduced interactions with a mirror (a proxy for aggression) and altered the latency to enter the top zone of a tank in unexposed F1 offspring. Bottom-dwelling time (a proxy for anxiety) also appeared to be somewhat affected, and activity (distance moved) was reduced in the context of aggression. slc6a4a and htr1Aa mRNA transcript levels were found to correlate positively with anxiety levels in controls, but we found that this relationship was disrupted in the 0.3 ppb atrazine treatment group. Overall, paternal atrazine exposure resulted in alterations across a variety of behavioral traits and showed signs of serotonergic system dysregulation, demonstrating intergenerational effects. Further research is needed to explore transgenerational effects on behavior and possible mechanisms underpinning behavioral effects. OPEN ACCESSCitation: Lamb SD, Chia JHZ, Johnson SL (2020) Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring. PLoS ONE 15(4): e0228357. https://doi.

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Section: Possible Mechanisms Underlying Effects Of Atrazine On F1 Promentioning

confidence: 99%

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring

2020

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“…The pesticide and endocrine disruptor DDT (dichloro-diphenyl-trichloroethane) has also been shown to induce alterations in DNA methylation which are transmitted across multiple generations [31,32]. Atrazine has been further shown to suppress genes associated with DNA methylation ultimately resulting in hypomethylation in an F0 generation of medaka (Oryzias latipes) [33]. In this same study, abnormal sperm counts and abnormal sperm motility were observed in the F2 generation representing a transgenerational effect of atrazine exposure.…”

Section: Plos Onementioning

confidence: 56%

Epigenome-wide association study for atrazine induced transgenerational DNA methylation and histone retention sperm epigenetic biomarkers for disease

et al. 2020

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Atrazine is a common agricultural herbicide previously shown to promote epigenetic transgenerational inheritance of disease to subsequent generations. The current study was designed as an epigenome-wide association study (EWAS) to identify transgenerational sperm disease associated differential DNA methylation regions (DMRs) and differential histone retention regions (DHRs). Gestating female F0 generation rats were transiently exposed to atrazine during the period of embryonic gonadal sex determination, and then subsequent F1, F2, and F3 generations obtained in the absence of any continued exposure. The transgenerational F3 generation males were assessed for disease and sperm collected for epigenetic analysis. Pathology was observed in pubertal onset and for testis disease, prostate disease, kidney disease, lean pathology, and multiple disease. For these pathologies, sufficient numbers of individual males with only a single specific disease were identified. The sperm DNA and chromatin were isolated from adult one-year animals with the specific diseases and analyzed for DMRs with methylated DNA immunoprecipitation (MeDIP) sequencing and DHRs with histone chromatin immunoprecipitation (ChIP) sequencing. Transgenerational F3 generation males with or without disease were compared to identify the disease specific epimutation biomarkers. All pathologies were found to have disease specific DMRs and DHRs which were found to predominantly be distinct for each disease. No common DMRs or DHRs were found among all the pathologies. Epimutation gene associations were identified and found to correlate to previously known disease linked genes. This is one of the first observations of potential sperm disease biomarkers for histone retention sites. Although further studies with expanded animal numbers are required, the current study provides evidence the EWAS analysis is effective for the identification of potential pathology epimutation biomarkers for disease susceptibility.

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“…Exposure of rat to 25 mg/kg BW/day ATZ was shown to promote epigenetic transgenerational inheritance, expressed by sperm differential DNA methylation regions over three generations (McBirney et al, 2017). Significant transgenerational differences in expression of genes involved in DNA methylation were reported in Medaka fish exposed to 5 or 50 μg/L ATZ (Cleary et al, 2019). Zebrafish larvae exposure to 3 ppb ATZ through embryogenesis lead to decreased expression of DNA methyltransferase and decreased DNA methylation levels (Wirbisky-Hershberger et al, 2017).…”

Section: Effect Of Atz On the Spermatozoamentioning

confidence: 99%

Effect of environmental contamination on female and male gametes – A lesson from bovines

2020

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Endocrine-disrupting compounds (EDCs) and foodborne contaminants are environmental pollutants that are considered reproductive toxicants due to their deleterious effects on female and male gametes. Among the EDCs, the phthalate plasticizers are of growing concern. In-vivo and in-vitro models indicate that the oocyte is highly sensitive to phthalates. This review summarizes the effects of di(2-ethylhexyl) phthalate and its major metabolite mono(2-ethyhexyl) phthalate (MEHP) on the oocyte. MEHP reduces the proportion of oocytes that fertilize, cleave and develop to the blastocyst stage. This is associated with negative effects on meiotic progression, and disruption of cortical granules, endoplasmic reticulum and mitochondrial reorganization. MEHP alters mitochondrial membrane polarity, increases reactive oxygen species levels and induces alterations in genes associated with oxidative phosphorylation. A carryover effect from the oocyte to the blastocyst is manifested by alterations in the transcriptomic profile of blastocysts developed from MEHP-treated oocytes. Among foodborne contaminants, the pesticide atrazine (ATZ) and the mycotoxin aflatoxin B1 (AFB1) are of high concern. The potential hazards associated with exposure of spermatozoa to these contaminants and their carryover effect to the blastocyst are described. AFB1 and ATZ reduce spermatozoa's viability, as reflected by a high proportion of cells with damaged plasma membrane; induce acrosome reaction, expressed as damage to the acrosomal membrane; and interfere with mitochondrial function, characterized by hyperpolarization of the membrane. ATZ and AFB1-treated spermatozoa show a high proportion of cells with fragmented DNA. Exposure of spermatozoa to AFB1 and ATZ reduces fertilization and cleavage rates, but not that of blastocyst formation. However, fertilization with AFB1-or ATZ-treated spermatozoa impairs transcript expression in the formed blastocysts, implying a carryover effect. Taken together, the review indicates the risk of exposing farm animals to environmental contaminants, and their deleterious effects on female and male gametes and the developing embryo.

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Atrazine induced transgenerational reproductive effects in medaka (Oryzias latipes)

Cited by 72 publications

References 79 publications

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring

Paternal exposure to a common herbicide alters the behavior and serotonergic system of zebrafish offspring

Epigenome-wide association study for atrazine induced transgenerational DNA methylation and histone retention sperm epigenetic biomarkers for disease

Effect of environmental contamination on female and male gametes – A lesson from bovines

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