Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline
<p dir="ltr">In somatic cells/tissues, methylation of ribosomal DNA (rDNA) increases with age and age‐related pathologies, which has a direct impact on the regulation of nucleolar activity and cellular metabolism. Here, we used bisulfite pyrosequencing and show that methylation of th...
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2020
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| _version_ | 1864513512328396800 |
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| author | Ramya Potabattula (4401160) |
| author2 | Federica Zacchini (289957) Grazyna Ewa Ptak (18877204) Marcus Dittrich (167737) Tobias Müller (163591) Nady El Hajj (686554) Thomas Hahn (146530) Charis Drummer (18710925) Rüdiger Behr (705041) Andrea Lucas‐Hahn (18877207) Heiner Niemann (196135) Martin Schorsch (686559) Thomas Haaf (342924) |
| author2_role | author author author author author author author author author author author author |
| author_facet | Ramya Potabattula (4401160) Federica Zacchini (289957) Grazyna Ewa Ptak (18877204) Marcus Dittrich (167737) Tobias Müller (163591) Nady El Hajj (686554) Thomas Hahn (146530) Charis Drummer (18710925) Rüdiger Behr (705041) Andrea Lucas‐Hahn (18877207) Heiner Niemann (196135) Martin Schorsch (686559) Thomas Haaf (342924) |
| author_role | author |
| dc.creator.none.fl_str_mv | Ramya Potabattula (4401160) Federica Zacchini (289957) Grazyna Ewa Ptak (18877204) Marcus Dittrich (167737) Tobias Müller (163591) Nady El Hajj (686554) Thomas Hahn (146530) Charis Drummer (18710925) Rüdiger Behr (705041) Andrea Lucas‐Hahn (18877207) Heiner Niemann (196135) Martin Schorsch (686559) Thomas Haaf (342924) |
| dc.date.none.fl_str_mv | 2020-07-01T00:00:00Z |
| dc.identifier.none.fl_str_mv | 10.1111/acel.13181 |
| dc.relation.none.fl_str_mv | https://figshare.com/articles/journal_contribution/Increasing_methylation_of_sperm_rDNA_and_other_repetitive_elements_in_the_aging_male_mammalian_germline/26095081 |
| dc.rights.none.fl_str_mv | CC BY 4.0 info:eu-repo/semantics/openAccess |
| dc.subject.none.fl_str_mv | Biological sciences Genetics Biomedical and clinical sciences Reproductive medicine embryo developmental potential epigenetic clock germline aging repetitive DNA elements ribosomal DNA sperm DNA methylation |
| dc.title.none.fl_str_mv | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| dc.type.none.fl_str_mv | Text Journal contribution info:eu-repo/semantics/publishedVersion text contribution to journal |
| description | <p dir="ltr">In somatic cells/tissues, methylation of ribosomal DNA (rDNA) increases with age and age‐related pathologies, which has a direct impact on the regulation of nucleolar activity and cellular metabolism. Here, we used bisulfite pyrosequencing and show that methylation of the rDNA transcription unit including upstream control element (UCE), core promoter, 18S rDNA, and 28S rDNA in human sperm also significantly increases with donor's age. This positive correlation between sperm rDNA methylation and biological age is evolutionarily conserved among mammals with widely different life spans such as humans, marmoset, bovine, and mouse. Similar to the tandemly repeated rDNA, methylation of human α‐satellite and interspersed LINE1 repeats, marmoset α‐satellite, bovine alpha‐ and testis satellite I, mouse minor and major satellite, and LINE1‐T repeats increases in the aging male germline, probably related to their sperm histone packaging. Deep bisulfite sequencing of single rDNA molecules in human sperm revealed that methylation does not only depend on donor's age, but also depend on the region and sequence context (A vs. G alleles). Both average rDNA methylation of all analyzed DNA molecules and the number of fully (>50%) methylated alleles, which are thought to be epigenetically silenced, increase with donor's age. All analyzed CpGs in the sperm rDNA transcription unit show comparable age‐related methylation changes. Unlike other epigenetic aging markers, the rDNA clock appears to operate in similar ways in germline and soma in different mammalian species. We propose that sperm rDNA methylation, directly or indirectly, influences nucleolar formation and developmental potential in the early embryo.</p><h2>Other Information</h2><p dir="ltr">Published in: Aging Cell<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1111/acel.13181" target="_blank">https://dx.doi.org/10.1111/acel.13181</a></p> |
| eu_rights_str_mv | openAccess |
| id | Manara2_99fc8a1d324536ca1de0c101698ca787 |
| identifier_str_mv | 10.1111/acel.13181 |
| network_acronym_str | Manara2 |
| network_name_str | Manara2 |
| oai_identifier_str | oai:figshare.com:article/26095081 |
| publishDate | 2020 |
| repository.mail.fl_str_mv | |
| repository.name.fl_str_mv | |
| repository_id_str | |
| rights_invalid_str_mv | CC BY 4.0 |
| spelling | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germlineRamya Potabattula (4401160)Federica Zacchini (289957)Grazyna Ewa Ptak (18877204)Marcus Dittrich (167737)Tobias Müller (163591)Nady El Hajj (686554)Thomas Hahn (146530)Charis Drummer (18710925)Rüdiger Behr (705041)Andrea Lucas‐Hahn (18877207)Heiner Niemann (196135)Martin Schorsch (686559)Thomas Haaf (342924)Biological sciencesGeneticsBiomedical and clinical sciencesReproductive medicineembryo developmental potentialepigenetic clockgermline agingrepetitive DNA elementsribosomal DNAsperm DNA methylation<p dir="ltr">In somatic cells/tissues, methylation of ribosomal DNA (rDNA) increases with age and age‐related pathologies, which has a direct impact on the regulation of nucleolar activity and cellular metabolism. Here, we used bisulfite pyrosequencing and show that methylation of the rDNA transcription unit including upstream control element (UCE), core promoter, 18S rDNA, and 28S rDNA in human sperm also significantly increases with donor's age. This positive correlation between sperm rDNA methylation and biological age is evolutionarily conserved among mammals with widely different life spans such as humans, marmoset, bovine, and mouse. Similar to the tandemly repeated rDNA, methylation of human α‐satellite and interspersed LINE1 repeats, marmoset α‐satellite, bovine alpha‐ and testis satellite I, mouse minor and major satellite, and LINE1‐T repeats increases in the aging male germline, probably related to their sperm histone packaging. Deep bisulfite sequencing of single rDNA molecules in human sperm revealed that methylation does not only depend on donor's age, but also depend on the region and sequence context (A vs. G alleles). Both average rDNA methylation of all analyzed DNA molecules and the number of fully (>50%) methylated alleles, which are thought to be epigenetically silenced, increase with donor's age. All analyzed CpGs in the sperm rDNA transcription unit show comparable age‐related methylation changes. Unlike other epigenetic aging markers, the rDNA clock appears to operate in similar ways in germline and soma in different mammalian species. We propose that sperm rDNA methylation, directly or indirectly, influences nucleolar formation and developmental potential in the early embryo.</p><h2>Other Information</h2><p dir="ltr">Published in: Aging Cell<br>License: <a href="http://creativecommons.org/licenses/by/4.0/" target="_blank">http://creativecommons.org/licenses/by/4.0/</a><br>See article on publisher's website: <a href="https://dx.doi.org/10.1111/acel.13181" target="_blank">https://dx.doi.org/10.1111/acel.13181</a></p>2020-07-01T00:00:00ZTextJournal contributioninfo:eu-repo/semantics/publishedVersiontextcontribution to journal10.1111/acel.13181https://figshare.com/articles/journal_contribution/Increasing_methylation_of_sperm_rDNA_and_other_repetitive_elements_in_the_aging_male_mammalian_germline/26095081CC BY 4.0info:eu-repo/semantics/openAccessoai:figshare.com:article/260950812020-07-01T00:00:00Z |
| spellingShingle | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline Ramya Potabattula (4401160) Biological sciences Genetics Biomedical and clinical sciences Reproductive medicine embryo developmental potential epigenetic clock germline aging repetitive DNA elements ribosomal DNA sperm DNA methylation |
| status_str | publishedVersion |
| title | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| title_full | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| title_fullStr | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| title_full_unstemmed | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| title_short | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| title_sort | Increasing methylation of sperm rDNA and other repetitive elements in the aging male mammalian germline |
| topic | Biological sciences Genetics Biomedical and clinical sciences Reproductive medicine embryo developmental potential epigenetic clock germline aging repetitive DNA elements ribosomal DNA sperm DNA methylation |