Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline

Potabattula, Ramya; Zacchini, Federica; Ptak, Grazyna; Dittrich, Marcus; Müller, Tobias; Hajj, Nady El; Hahn, Thomas von; Drummer, Charis; Behr, Rüdiger; Lucas‐Hahn, Andrea; Niemann, Heiner; Schorsch, Martin; Haaf, Thomas

doi:10.1111/acel.13181

Cited by 32 publications

(37 citation statements)

References 46 publications

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“…The observation is consistent with numerous studies that put into context aberrant sperm quality parameters and changes in mCpG levels in aged and/or infertile males [ 17 , 49 , 50 ]. Surprisingly, the majority of these studies, which also include other vertebrate species, observed an increase [ 51 , 52 , 53 , 54 , 55 ] rather than a decrease [ 23 ] in global DNA methylation. The DNA methylation change after 24 HPS can be explained in relation to the environmental changes that have occurred by the spermatozoa.…”

Section: Discussionmentioning

confidence: 99%

Changes in Phenotypes and DNA Methylation of In Vitro Aging Sperm in Common Carp Cyprinus carpio

Cheng

Vechtova

Füssy

et al. 2021

IJMS

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The purpose of the current study was to analyze phenotypic and functional characteristics of common carp (Cyprinus carpio) spermatozoa during in vitro aging and to investigate whether global DNA methylation is affected by sperm aging. Milt was collected from five individual males, stored in vitro on ice in a refrigerator for up to 96 h post stripping (HPS) and used to fertilize eggs with intervals of 1, 24 and 96 h. Computer-assisted sperm analysis and a S3e Cell Sorter was employed to determine the spermatozoa phenotypic characteristics (motility, velocity, concentration and viability). In addition, pH and osmolality of the seminal fluid and the capacity of the spermatozoa to fertilize, hatching rate and health of the resulting embryos were examined at different aging times. Whole-genome bisulfite sequencing was used to compare the global and gene-specific DNA methylation in fresh and aged spermatozoa. The results demonstrated that spermatozoa aging in common carp significantly affects their performance and thus the success of artificial fertilization. The methylation level at the cytosine-phosphate-guanine (CpG) sites increased significantly with 24 HPS spermatozoa compared to the fresh group at 1 HPS and then decreased significantly at 96 HPS. A more detailed investigation of gene specific differences in the DNA methylation was hindered by incomplete annotation of the C. carpio genome in the public databases.

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Section: Discussionmentioning

confidence: 99%

Changes in Phenotypes and DNA Methylation of In Vitro Aging Sperm in Common Carp Cyprinus carpio

Cheng

Vechtova

Füssy

et al. 2021

IJMS

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“…Notwithstanding, we did not observed changes in DNA fragmentation, our data showed that aging was associated with increased chromatin condensation over time in mouse sperm. One of the mechanisms behind the observed high condensation may be the increasing methylation in aging sperm, recently described by us and others [15, 19]. The occurrence of epigenome changes in aging sperm is of great concern.…”

Section: Discussionmentioning

confidence: 95%

The age and mouse sperm quality – a flow cytometry investigation

Zacchini

Bochenek²,

Bisogno³

et al. 2021

Preprint

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Postponement of fatherhood is growing worldwide due to socio-economic factors. The choice to conceive the first child above the age of 35 years is often associated with reduced fertility and poor pregnancy outcome. As widely known, several factors (e.g., lifestyle, environment, health problems) can affect spermatogenesis leading to poor reproductive outcome. Currently, the debate on the influence of aging on male gametes and safety/risk of conception at advanced age is still ongoing. Controversial results have been published so far on the changes in semen features of aging men and other mammalian species (mainly rodents). In this study, we aimed to assess how aging affects sperm quality in an inbreed mouse model, without underlying infertility, using a flow cytometry approach. Our data showed that aging is associated with increased sperm chromatin condensation, but not changes in the DNA integrity, metabolic activity or viability. These data suggest a mild effect of aging on sperm quality in a mouse model without underlying infertility.

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“…Stable DNA methylation changes in sperm ribosomal DNA were also shown to occur in response to a protein restricted diet during intrauterine development 42 . Recently, we have shown a hypermethylation of the rDNA locus in aging germ cells across several mammalian species 43 . Therefore, epigenetic modifications of www.nature.com/scientificreports/ germ cells might be a possible mechanism via which a paternal high fat diet might influence the regulation of Gata6 and Samd4b, in embryos.…”

Section: Discussionmentioning

confidence: 98%

A genome-wide transcriptomic analysis of embryos fathered by obese males in a murine model of diet-induced obesity

Bernhardt¹,

Dittrich

El‐Merahbi

et al. 2021

Sci Rep

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Paternal obesity is known to have a negative impact on the male’s reproductive health as well as the health of his offspring. Although epigenetic mechanisms have been implicated in the non-genetic transmission of acquired traits, the effect of paternal obesity on gene expression in the preimplantation embryo has not been fully studied. To this end, we investigated whether paternal obesity is associated with gene expression changes in eight-cell stage embryos fathered by males on a high-fat diet. We used single embryo RNA-seq to compare the gene expression profile of embryos generated by males on a high fat (HFD) versus control (CD) diet. This analysis revealed significant upregulation of the Samd4b and Gata6 gene in embryos in response to a paternal HFD. Furthermore, we could show a significant increase in expression of both Gata6 and Samd4b during differentiation of stromal vascular cells into mature adipocytes. These findings suggest that paternal obesity may induce changes in the male germ cells which are associated with the gene expression changes in the resulting preimplantation embryos.

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Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 32 publications

References 46 publications

Changes in Phenotypes and DNA Methylation of In Vitro Aging Sperm in Common Carp Cyprinus carpio

Changes in Phenotypes and DNA Methylation of In Vitro Aging Sperm in Common Carp Cyprinus carpio

The age and mouse sperm quality – a flow cytometry investigation

A genome-wide transcriptomic analysis of embryos fathered by obese males in a murine model of diet-induced obesity

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