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Parental copper stress induces offspring developmental defects by altering DNA methylation in zebrafish [WGBS]

ABSTRACT: Here, we describe environmental Cu2+ in promoting zebrafish (Danio rerio) developmental abnormalities in subsequent generation. This study for the first time demonstrated that: 1. Cu2+ induced alterations in sperm methylome could be passed down to offspring and cause developmental defects in the nervous and digestive system, even the Cu2+ concentration is at 10 μg/L, the National Quality Standards of fishery water (GB11607-89); 2. DNA methylomes of F0 sperms and F1 offspring were altered in a loci-specific manner and were correlated with transcriptional expression of genes which function importantly in the development of CNS, retina, and digestive system development during F1 embryogenesis; 3. Loci-specific hypoDMRs in the pmpcb promoter and loci-specific hyperDMRs in the crebl2 and tab2 promoters might show adaptive and harmful responses to Cu2+ stresses in next generational inheritance, respectively. Those data revealed that Cu2+ induced alterations in sperm methylome may be passed down to offspring and cause the embryonic developmental defects and the resulted inferior seeding, suggesting that environmental Cu2+ might pose a dramatic and long-lasting threat to the sustainability of fish population and even to humans with imbalanced copper homeostasis.

ORGANISM(S): Danio rerio

PROVIDER: GSE182944 | GEO | 2022/08/27

REPOSITORIES: GEO

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Project description:Purpose: Paternal life experiences impact offspring health via germline, and epigenetic inheritance provides a potential mechanism. However, global reprogramming during offspring embryogenesis and gametogenesis represents the largest hurdle to conceptualize it. Yet, detailed characterization of how sperm epigenetic alterations carrying “environmental memory” can evade offspring embryonic reprogramming remains elusive. Methods: we profiled the sperm DNA methylation patterns of three consecutive generations (F0, F1 and F2) in both control and stress groups by using whole-genome bisulfite sequencing (WGBS). A total of 18 sperm samples were analyzed, including three biological replicates for each generation under each treatment. In addition, small RNA sequencing was carried out on paternal sperm samples to investigate whether long-term psychological stress affected the enrichment of certain sncRNAs and to identify whether they participated in mediating the occurrence and paternal inheritance of the stress-induced DMRs Rsults: Using an optimized data analysis workflow, we obtained approximately 800 million clean reads per sample (build mm10) with strand-specific coverage ~21×, and the data covered ~96.00% of the total 21,867,837 reference CpG dinucleotides. A total of 24,427, 7,975, and 5,173 differentially methylated regions (DMRs) between control and stress groups were found in the F0, F1, and F2 generations, respectively. Inter- and transgenerational inheritance of paternal DMRs were at frequencies approximately 11.36% and 0.48%, respectively. These DMRs related to genes with functional implications for psychological stress response, and tissue inheritance of these DMRs passed paternal disorders epigenetically to offspring. More importantly, these DMRs evaded offspring embryonic reprogramming through erasure and subsequent reestablishment, but not via un-erasure way. Nonetheless, their reestablishment proportions in the primitive streak (E7.5) stage were altered. Furthermore, sncRNA-seq revealed that stress-induced tsRNA, miRNA and rsRNA dysregulation in paternal sperm might play important roles in DMRs occurrence and paternal inheritance.

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Parental copper stress induces offspring developmental defects by altering DNA methylation in zebrafish [WGBS]

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