Rainbow trout exposed to benzo[a]pyrene yields conserved microRNA binding sites in DNA methyltransferases across 500 million years of evolution

Kuc, Christopher; Richard, Daniel; Johnson, Samantha T.; Bragg, Leslie M.; Servos, Mark R.; Doxey, Andrew C.; Craig, Paul M.

doi:10.1038/s41598-017-17236-x

Cited by 20 publications

(10 citation statements)

References 61 publications

(61 reference statements)

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Evidence regarding the effect of PAH exposure on Casp8 methylation has not yet been retrieved. For global DNA methylation, the association between PAH exposure and decreased DNA methylation has been reported both in human and animal studies [19, 30, 31]. PAH metabolites in maternal urine are associated with decreased global methylation status in a Chinese cohort [32].…”

Section: Discussionmentioning

confidence: 99%

Casp8 hypomethylation and neural tube defects in association with polycyclic aromatic hydrocarbon exposure

et al. 2019

View full text Add to dashboard Cite

Background Epidemiological studies have found that prenatal exposure to polycyclic aromatic hydrocarbons (PAHs) is associated with increased risk for neural tube defects (NTDs). Aberrant DNA methylation, excessive apoptosis, and oxidative stress have been implied as the mechanism underlying the association between PAH exposure and NTDs, respectively. However, the role of DNA methylation aberration of apoptotic initiator CASP8 (caspase-8, apoptosis-related cysteine peptidase) in the formation of NTDs in association with PAH exposure is not known. By combining a case–control study and mouse model, we aimed to explore the full spectrum of the links from PAH exposure, oxidative stress, CASP8 methylation change, caspase-8 activation, apoptosis, to NTD formation. Results Hypomethylation of CASP8 promoter was noticed in the microarray profiled by Infinium HumanMethylation450 BeadChip using neural tissues from 10 terminated NTD fetuses and 8 terminated non-malformed fetuses (14 CpG sites, with β difference ranging between 8.8 and 26.3%), and was validated in a larger case–control sample performed with neural tissues from 80 NTD cases and 32 non-malformed fetuses, using the Sequenom MassARRAY system (7 CpG sites). Hypomethylation of CASP8 was a risk factor for NTDs (aOR = 1.11; 95% CI, 1.05–1.17) based on the logistic regression model. According to Pearson’s correlation, methylation levels of CASP8 were inversely correlated with PAH concentrations in maternal serum and with oxidative stress markers in fetal neural tissues ( p < 0.05). In the animal study, increased NTD rates (13.5% frequency), Casp8 hypomethylation, caspase-8 upregulation, increased caspase-8 cleavage, and excessive apoptosis were found in mouse embryos cultured with benz(a)pyrene (BaP) in vitro. Antioxidant N -acetyl-L-cysteine (NAC) and BaP co-treatment attenuated the changes found in BaP treatment group. Conclusions Hypomethylation of Casp8 promoter is associated with the formation of NTDs, and Casp8 hypomethylation may be induced by oxidative stress that resulted from exposure to PAHs. Electronic supplementary material The online version of this article (10.1186/s13148-019-0673-6) contains supplementary material, which is available to authorized users.

show abstract

Section: Discussionmentioning

confidence: 99%

Casp8 hypomethylation and neural tube defects in association with polycyclic aromatic hydrocarbon exposure

et al. 2019

View full text Add to dashboard Cite

show abstract

“…Evidence for crosstalk between DNA level epigenetic modifications and microRNAs remains correlational, as seen in studies using zebrafish and rainbow trout. For example, a strong occupancy of pri-miRNA promtors by H3K4me3 has been observed in zebrafish embryogenesis (Nepal, 2016), while in rainbow trout, a recent gene expression study coupled with in silico predictions suggested an evolutionary deeply conserved crosstalk between miRNA-29 and a dnmt1 paralogue (Kuc et al, 2017). Together, these studies ACCEPTED MANUSCRIPT…”

Section: A C C E P T E D Mmentioning

confidence: 91%

“…conducted in the zebrafish model, testifying to this emerging model's promise to further our understanding of the effects of contaminant exposure on mechanisms regulating DNA methylation dynamics (Kamstra et al, 2015a;Bouwmeester et al, 2016). As such, changes in zebrafish DNA methylation indices have been reported in response to a wide-range of aquatic contaminants, including metals (Gombeau et al, 2016, Zheng et al, 2017Sanchez et al, 2017;Carvan et al, 2017), industrial products (Laing et al, 2016;Santangeli et al, 2016;, pesticides (Wirbisky-Hershberger et al 2017, Qian et al 2017, persistent organic pollutants (POPs; Aluru et al 2014), and polycyclic aromatic hydrocarbons (PAHs;Gao et al 2017;Kuc et al, 2017). With regard to metals, adult zebrafish exposed to 20 g/L depleted uranium exhibited both sex-and tissue-specific changes in global DNA methylation between 7-24 days (Gombeau et al, 2016).…”

Section: Accepted Manuscriptmentioning

confidence: 99%

Epigenetics in teleost fish: From molecular mechanisms to physiological phenotypes

Best

Ikert

Kostyniuk

et al. 2018

Comparative Biochemistry and Physiology Part B: Biochemistry an

Self Cite

118

View full text Add to dashboard Cite

While the field of epigenetics is increasingly recognized to contribute to the emergence of phenotypes in mammalian research models across different developmental and generational timescales, the comparative biology of epigenetics in the large and physiologically diverse vertebrate infraclass of teleost fish remains comparatively understudied. The cypriniform zebrafish and the salmoniform rainbow trout and Atlantic salmon represent two especially important teleost orders, because they offer the unique possibility to comparatively investigate the role of epigenetic regulation in 3R and 4R duplicated genomes. In addition to their sequenced genomes, these teleost species are well-characterized model species for development and physiology, and therefore allow for an investigation of the role of epigenetic modifications in the emergence of physiological phenotypes during an organism's lifespan and in subsequent generations. This review aims firstly to describe the evolution of the repertoire of genes involved in key molecular epigenetic pathways including histone modifications, DNA methylation and microRNAs in zebrafish, rainbow trout, and Atlantic salmon, and secondly, to discuss recent advances in research highlighting a role for molecular epigenetics in shaping physiological phenotypes in these and other teleost models. Finally, by discussing themes and current limitations of the emerging field of teleost epigenetics from both theoretical and technical points of view, we will highlight future research needs and discuss how epigenetics will not only help address basic research questions in comparative teleost physiology, but also inform translational research including aquaculture, aquatic toxicology, and human disease.

show abstract

“…Methods were in alignment with previously published techniques by Kuc et al (2017). An alignment of the collagen transcript (type 1 alpha 1 in most species and type 1 alpha 3 in rainbow trout) was generated to understand the evolutionary conservation of miR-29b binding sites.…”

Section: Bioinformatics Analysismentioning

confidence: 99%

microRNA-29b knocks down collagen type I production in cultured rainbow trout (Oncorhynchus mykiss) cardiac fibroblasts

Johnston

Cadonic

Craig

et al. 2019

Journal of Experimental Biology

Self Cite

View full text Add to dashboard Cite

Warm acclimation of rainbow trout can cause a decrease in the collagen content of the heart. This ability to remove cardiac collagen is particularly interesting considering that collagen deposition in the mammalian heart, following an injury, is permanent. We hypothesized that collagen removal can be facilitated by microRNA-29b (miR-29b), a highly conserved, small, non-coding RNA, as a reduction in this microRNA has been reported during the development of fibrosis in the mammalian heart. We also used a bioinformatics approach to investigate the binding potential of miR-29b to the seed sequences of vertebrate collagen isoforms. Cultured trout cardiac fibroblasts were transfected with zebrafish mature miR-29b mimic for 7 days with re-transfection occurring after 3 days. Transfection induced a 17.8-fold increase in miR-29b transcript abundance (P<0.05) as well as a 54% decrease in the transcript levels of the col1a3 collagen isoform, compared with non-transfected controls (P<0.05). Western blotting demonstrated that the level of collagen type I protein was 85% lower in cells transfected with miR-29b than in control cells (P<0.05). Finally, bioinformatic analysis suggested that the predicted 3′-UTR of rainbow trout col1a3 has a comparatively higher binding affinity for miR-29b than the 3′-UTR of col1a1. Together, these results suggest that miR-29b is a highly conserved regulator of collagen type I protein in vertebrates and that this microRNA decreases collagen in the trout heart by targeting col1a3.

show abstract

Rainbow trout exposed to benzo[a]pyrene yields conserved microRNA binding sites in DNA methyltransferases across 500 million years of evolution

Cited by 20 publications

References 61 publications

Casp8 hypomethylation and neural tube defects in association with polycyclic aromatic hydrocarbon exposure

Casp8 hypomethylation and neural tube defects in association with polycyclic aromatic hydrocarbon exposure

Epigenetics in teleost fish: From molecular mechanisms to physiological phenotypes

microRNA-29b knocks down collagen type I production in cultured rainbow trout (Oncorhynchus mykiss) cardiac fibroblasts

Contact Info

Product

Resources

About