Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells
In storing and transmitting epigenetic information, organisms must balance the need to maintain information about past conditions with the capacity to respond to information in their current and future environments. Some of this information is encoded by DNA methylation, which can be transmitted wit...
| Main Authors: | , , , , , , , , , , , , , |
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| Format: | Article |
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Public Library of Science
2017
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| Online Access: | https://eprints.nottingham.ac.uk/47167/ |
| _version_ | 1848797479907098624 |
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| author | Choi, Minseung Genereux, Diane P. Goodson, Jamie Al-Azzawi, Haneen Allain, Shannon Q. Simon, Noah Palasek, Stan Ware, Carol B. Cavanaugh, Chris Miller, Daniel G. Johnson, Winslow C. Sinclair, Kevin D. Stöger, Reinhard Laird, Charles D. |
| author_facet | Choi, Minseung Genereux, Diane P. Goodson, Jamie Al-Azzawi, Haneen Allain, Shannon Q. Simon, Noah Palasek, Stan Ware, Carol B. Cavanaugh, Chris Miller, Daniel G. Johnson, Winslow C. Sinclair, Kevin D. Stöger, Reinhard Laird, Charles D. |
| author_sort | Choi, Minseung |
| building | Nottingham Research Data Repository |
| collection | Online Access |
| description | In storing and transmitting epigenetic information, organisms must balance the need to maintain information about past conditions with the capacity to respond to information in their current and future environments. Some of this information is encoded by DNA methylation, which can be transmitted with variable fidelity from parent to daughter strand. High fidelity confers strong pattern matching between the strands of individual DNA molecules and thus pattern stability over rounds of DNA replication; lower fidelity confers reduced pattern matching, and thus greater flexibility. Here, we present a new conceptual framework, Ratio of Concordance Preference (RCP), that uses double-stranded methylation data to quantify the flexibility and stability of the system that gave rise to a given set of patterns. We find that differentiated mammalian cells operate with high DNA methylation stability, consistent with earlier reports. Stem cells in culture and in embryos, in contrast, operate with reduced, albeit significant, methylation stability. We conclude that preference for concordant DNA methylation is a consistent mode of information transfer, and thus provides epigenetic stability across cell divisions, even in stem cells and those undergoing developmental transitions. Broader application of our RCP framework will permit comparison of epigenetic-information systems across cells, developmental stages, and organisms whose methylation machineries differ substantially or are not yet well understood. |
| first_indexed | 2025-11-14T20:04:32Z |
| format | Article |
| id | nottingham-47167 |
| institution | University of Nottingham Malaysia Campus |
| institution_category | Local University |
| last_indexed | 2025-11-14T20:04:32Z |
| publishDate | 2017 |
| publisher | Public Library of Science |
| recordtype | eprints |
| repository_type | Digital Repository |
| spelling | nottingham-471672020-05-04T19:16:16Z https://eprints.nottingham.ac.uk/47167/ Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells Choi, Minseung Genereux, Diane P. Goodson, Jamie Al-Azzawi, Haneen Allain, Shannon Q. Simon, Noah Palasek, Stan Ware, Carol B. Cavanaugh, Chris Miller, Daniel G. Johnson, Winslow C. Sinclair, Kevin D. Stöger, Reinhard Laird, Charles D. In storing and transmitting epigenetic information, organisms must balance the need to maintain information about past conditions with the capacity to respond to information in their current and future environments. Some of this information is encoded by DNA methylation, which can be transmitted with variable fidelity from parent to daughter strand. High fidelity confers strong pattern matching between the strands of individual DNA molecules and thus pattern stability over rounds of DNA replication; lower fidelity confers reduced pattern matching, and thus greater flexibility. Here, we present a new conceptual framework, Ratio of Concordance Preference (RCP), that uses double-stranded methylation data to quantify the flexibility and stability of the system that gave rise to a given set of patterns. We find that differentiated mammalian cells operate with high DNA methylation stability, consistent with earlier reports. Stem cells in culture and in embryos, in contrast, operate with reduced, albeit significant, methylation stability. We conclude that preference for concordant DNA methylation is a consistent mode of information transfer, and thus provides epigenetic stability across cell divisions, even in stem cells and those undergoing developmental transitions. Broader application of our RCP framework will permit comparison of epigenetic-information systems across cells, developmental stages, and organisms whose methylation machineries differ substantially or are not yet well understood. Public Library of Science 2017-11-06 Article PeerReviewed Choi, Minseung, Genereux, Diane P., Goodson, Jamie, Al-Azzawi, Haneen, Allain, Shannon Q., Simon, Noah, Palasek, Stan, Ware, Carol B., Cavanaugh, Chris, Miller, Daniel G., Johnson, Winslow C., Sinclair, Kevin D., Stöger, Reinhard and Laird, Charles D. (2017) Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells. PLoS Genetics, 13 (11). e1007060/1-e1007060/23. ISSN 1553-7404 http://journals.plos.org/plosgenetics/article?id=10.1371/journal.pgen.1007060 doi:10.1371/journal.pgen.1007060 doi:10.1371/journal.pgen.1007060 |
| spellingShingle | Choi, Minseung Genereux, Diane P. Goodson, Jamie Al-Azzawi, Haneen Allain, Shannon Q. Simon, Noah Palasek, Stan Ware, Carol B. Cavanaugh, Chris Miller, Daniel G. Johnson, Winslow C. Sinclair, Kevin D. Stöger, Reinhard Laird, Charles D. Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title | Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title_full | Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title_fullStr | Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title_full_unstemmed | Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title_short | Epigenetic memory via concordant DNA methylation is inversely correlated to developmental potential of mammalian cells |
| title_sort | epigenetic memory via concordant dna methylation is inversely correlated to developmental potential of mammalian cells |
| url | https://eprints.nottingham.ac.uk/47167/ https://eprints.nottingham.ac.uk/47167/ https://eprints.nottingham.ac.uk/47167/ |