The inactive X chromosome accumulates widespread epigenetic variability with age
Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to th...
Saved in:
| Published in | Clinical epigenetics Vol. 15; no. 1; pp. 1 - 12 |
|---|---|
| Main Authors | , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
BioMed Central Ltd
25.08.2023
BioMed Central BMC |
| Subjects | |
| Online Access | Get full text |
Cover
Loading…
| Abstract | Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women. Methods We analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age. Results In females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37). Conclusions Our results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. Keywords: DNA methylation, Aging, X chromosome, Women, Variance, Gene expression |
|---|---|
| AbstractList | Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women. We analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age. In females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37). Our results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. BackgroundLoss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women.MethodsWe analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age.ResultsIn females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37).ConclusionsOur results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women.BACKGROUNDLoss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women.We analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age.METHODSWe analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age.In females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37).RESULTSIn females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37).Our results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability.CONCLUSIONSOur results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. Abstract Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women. Methods We analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age. Results In females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37). Conclusions Our results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X chromosome in females through DNA methylation. Hence, age-related disruption of X-chromosome inactivation (XCI) may contribute to the aging process in women. Methods We analyzed 9,777 CpGs on the X chromosome in whole blood samples from 2343 females and 1688 males (Illumina 450k methylation array) and replicated findings in duplicate using one whole blood and one purified monocyte data set (in total, 991/924 females/males). We used double generalized linear models to detect age-related differentially methylated CpGs (aDMCs), whose mean methylation level differs with age, and age-related variably methylated CpGs (aVMCs), whose methylation level becomes more variable with age. Results In females, aDMCs were relatively uncommon (n = 33) and preferentially occurred in regions known to escape XCI. In contrast, many CpGs (n = 987) were found to display an increased variance with age (aVMCs). Of note, the replication rate of aVMCs was also high in purified monocytes (94%), indicating an independence of cell composition. aVMCs accumulated in CpG islands and regions subject to XCI suggesting that they stemmed from the inactive X. In males, carrying an active copy of the X chromosome only, aDMCs (n = 316) were primarily driven by cell composition, while aVMCs replicated well (95%) but were infrequent (n = 37). Conclusions Our results imply that age-related DNA methylation differences at the inactive X chromosome are dominated by the accumulation of variability. Keywords: DNA methylation, Aging, X chromosome, Women, Variance, Gene expression |
| ArticleNumber | 135 |
| Audience | Academic |
| Author | Sinke, Lucy Daxinger, Lucia Slieker, Roderick C. van Zwet, Erik W. Heijmans, Bastiaan T. Liu, Yunfeng Jonkman, Thomas H. |
| Author_xml | – sequence: 1 givenname: Yunfeng surname: Liu fullname: Liu, Yunfeng – sequence: 2 givenname: Lucy surname: Sinke fullname: Sinke, Lucy – sequence: 3 givenname: Thomas H. surname: Jonkman fullname: Jonkman, Thomas H. – sequence: 4 givenname: Roderick C. surname: Slieker fullname: Slieker, Roderick C. – sequence: 5 givenname: Erik W. surname: van Zwet fullname: van Zwet, Erik W. – sequence: 6 givenname: Lucia surname: Daxinger fullname: Daxinger, Lucia – sequence: 7 givenname: Bastiaan T. surname: Heijmans fullname: Heijmans, Bastiaan T. |
| BookMark | eNp9Ustu1DAUjVARfdAfYBWJDZsUO37FK1RVPCpVgkWR2Fk3znXGoyQe7GTQ_D2eTiuYCmEvbF2fc-7D57w4mcKERfGGkitKG_k-UUZ5U5GaVYQKrqvdi-IsPzSVIg07-et-WlymtCZ5Ma01Ja-KU6ZkLRknZ8W3-xWWfgI7-y2WP0q7imEMKYxYgrXLuAwwYyp_-Q7TJiJ0JW58jxPO3pZbiB5aP_h5lxHzqoQeXxcvHQwJLx_Pi-L7p4_3N1-qu6-fb2-u7yorOJ2rjmkBTqKiWNdIHeGMgnAOCOec6Zpy3baysdJSy0FIWjPolFUKhVLOaXZR3B50uwBrs4l-hLgzAbx5CITYG4i5yAENF4JobC1XVnKCXUvQWa7BcU60gjZrfThobZZ2xM7iNEcYjkSPXya_Mn3YGkq4zIWLrPDuUSGGnwum2Yw-WRwGmDAsydSNUA1vCJMZ-vYZdB2WOOVZZZQUuXuq1R9UD7kDP7mQE9u9qLnOn1erpub7tFf_QOXd4ehtNozzOX5EaA4EG0NKEZ2xfobZh31ffsgNmb27zMFdJrvLPLjL7DK1fkZ9ms9_SL8BuYPSAw |
| CitedBy_id | crossref_primary_10_1111_eci_14215 crossref_primary_10_1016_j_fertnstert_2024_10_037 crossref_primary_10_3390_ijms25052648 crossref_primary_10_1007_s00412_024_00826_w crossref_primary_10_1186_s13072_024_00525_x crossref_primary_10_1126_sciadv_ads8169 crossref_primary_10_1007_s12975_024_01321_1 crossref_primary_10_1016_j_tig_2025_02_001 crossref_primary_10_1126_sciadv_adn6537 crossref_primary_10_1152_ajprenal_00140_2024 crossref_primary_10_1089_genbio_2024_29138_cbr crossref_primary_10_3390_epigenomes8040043 crossref_primary_10_3390_epigenomes7040029 |
| Cites_doi | 10.1038/s41401-020-00578-0 10.1093/hmg/ddu564 10.1186/s13072-021-00386-8 10.1186/gb-2013-14-11-r122 10.1093/bioinformatics/btn224 10.1186/s13059-020-02114-z 10.1101/gr.112680.110 10.1186/s13293-015-0053-7 10.1038/nature03479 10.1038/190372a0 10.1111/j.1365-2362.2010.02418.x 10.1038/ng.3721 10.1038/s41431-018-0291-3 10.1136/jnnp.2011.244939 10.1038/s41467-018-05714-3 10.1038/s41576-022-00477-6 10.1186/s13073-018-0585-7 10.1186/1756-8935-6-26 10.1111/j.2517-6161.1995.tb02031.x 10.1136/bmjopen-2014-006772 10.1038/s41467-022-33511-6 10.1093/bioinformatics/btu049 10.1186/s13073-019-0693-z 10.1016/j.gde.2016.12.002 10.1038/nrc1413 10.1089/omi.2011.0118 10.1038/sj.ejhg.5201508 10.1093/bioinformatics/btu566 10.1093/molbev/msv180 10.1038/13810 10.1016/j.cell.2022.11.001 10.1210/jc.2007-2771 10.1093/biostatistics/kxj037 10.1111/j.0006-341X.1999.00997.x 10.1038/ncomms6366 10.1186/s13059-016-1053-6 10.1073/pnas.1004594107 10.1186/s13073-020-00736-3 10.1371/journal.pone.0067378 10.1038/mp.2010.54 10.1186/s13072-021-00407-6 10.1038/nature24265 10.1159/000098184 10.1186/s13059-016-1131-9 10.1111/j.2517-6161.1989.tb01747.x 10.1007/s10654-013-9866-z 10.1038/ng.3737 10.1186/s13072-021-00404-9 10.1093/nar/gkv007 10.1375/136905202320906174 10.1093/bioinformatics/bty062 10.1186/bcr2191 10.1186/s13059-022-02787-8 |
| ContentType | Journal Article |
| Copyright | COPYRIGHT 2023 BioMed Central Ltd. 2023. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. 2023. BioMed Central Ltd., part of Springer Nature. BioMed Central Ltd., part of Springer Nature 2023 |
| Copyright_xml | – notice: COPYRIGHT 2023 BioMed Central Ltd. – notice: 2023. This work is licensed under http://creativecommons.org/licenses/by/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. – notice: 2023. BioMed Central Ltd., part of Springer Nature. – notice: BioMed Central Ltd., part of Springer Nature 2023 |
| CorporateAuthor | BIOS Consortium |
| CorporateAuthor_xml | – name: BIOS Consortium |
| DBID | AAYXX CITATION 3V. 7X7 7XB 88E 8FE 8FH 8FI 8FJ 8FK ABUWG AFKRA AZQEC BBNVY BENPR BHPHI CCPQU DWQXO FYUFA GHDGH GNUQQ HCIFZ K9. LK8 M0S M1P M7P PHGZM PHGZT PIMPY PJZUB PKEHL PPXIY PQEST PQGLB PQQKQ PQUKI 7X8 5PM DOA |
| DOI | 10.1186/s13148-023-01549-y |
| DatabaseName | CrossRef ProQuest Central (Corporate) ProQuest Health & Medical Collection ProQuest Central (purchase pre-March 2016) Medical Database (Alumni Edition) ProQuest SciTech Collection ProQuest Natural Science Collection Hospital Premium Collection Hospital Premium Collection (Alumni Edition) ProQuest Central (Alumni) (purchase pre-March 2016) ProQuest Central (Alumni) ProQuest Central UK/Ireland ProQuest Central Essentials Biological Science Collection ProQuest Central Natural Science Collection ProQuest One Community College ProQuest Central Korea Health Research Premium Collection Health Research Premium Collection (Alumni) ProQuest Central Student SciTech Premium Collection ProQuest Health & Medical Complete (Alumni) ProQuest Biological Science Collection Health & Medical Collection (Alumni Edition) Medical Database Biological Science Database ProQuest Central Premium ProQuest One Academic Publicly Available Content Database ProQuest Health & Medical Research Collection ProQuest One Academic Middle East (New) ProQuest One Health & Nursing ProQuest One Academic Eastern Edition (DO NOT USE) ProQuest One Applied & Life Sciences ProQuest One Academic ProQuest One Academic UKI Edition MEDLINE - Academic PubMed Central (Full Participant titles) DOAJ Directory of Open Access Journals |
| DatabaseTitle | CrossRef Publicly Available Content Database ProQuest Central Student ProQuest One Academic Middle East (New) ProQuest Central Essentials ProQuest Health & Medical Complete (Alumni) ProQuest Central (Alumni Edition) SciTech Premium Collection ProQuest One Community College ProQuest One Health & Nursing ProQuest Natural Science Collection ProQuest Central ProQuest One Applied & Life Sciences ProQuest Health & Medical Research Collection Health Research Premium Collection Health and Medicine Complete (Alumni Edition) Natural Science Collection ProQuest Central Korea Health & Medical Research Collection Biological Science Collection ProQuest Central (New) ProQuest Medical Library (Alumni) ProQuest Biological Science Collection ProQuest One Academic Eastern Edition ProQuest Hospital Collection Health Research Premium Collection (Alumni) Biological Science Database ProQuest SciTech Collection ProQuest Hospital Collection (Alumni) ProQuest Health & Medical Complete ProQuest Medical Library ProQuest One Academic UKI Edition ProQuest One Academic ProQuest One Academic (New) ProQuest Central (Alumni) MEDLINE - Academic |
| DatabaseTitleList | Publicly Available Content Database MEDLINE - Academic |
| Database_xml | – sequence: 1 dbid: DOA name: DOAJ Directory of Open Access Journals url: https://www.doaj.org/ sourceTypes: Open Website – sequence: 2 dbid: BENPR name: ProQuest Central url: https://www.proquest.com/central sourceTypes: Aggregation Database |
| DeliveryMethod | fulltext_linktorsrc |
| Discipline | Zoology |
| EISSN | 1868-7083 1868-7075 |
| EndPage | 12 |
| ExternalDocumentID | oai_doaj_org_article_45509ebc47c640edb0efc49af44097ab PMC10464315 A762278245 10_1186_s13148_023_01549_y |
| GeographicLocations | Netherlands United States--US |
| GeographicLocations_xml | – name: Netherlands – name: United States--US |
| GrantInformation_xml | – fundername: ; grantid: 184.021.007 ,184.033.111 |
| GroupedDBID | --- 0R~ 2JY 4.4 53G 5C9 5VS 7X7 88E 8FE 8FH 8FI 8FJ AAFWJ AAJSJ AASML AAYXX ABDBF ABUWG ACGFS ACUHS ADBBV ADRAZ ADUKV AENEX AFKRA AFPKN AHBYD AHYZX ALIPV ALMA_UNASSIGNED_HOLDINGS AMKLP AOIJS BAPOH BAWUL BBNVY BCNDV BENPR BFQNJ BHPHI BMC BPHCQ BVXVI C6C CCPQU CITATION DIK EBLON EBS EN4 F5P FYUFA GROUPED_DOAJ GX1 HCIFZ HF~ HMCUK HYE HZ~ IAO IHR INH INR ITC KOV KQ8 LK8 M1P M48 M7P O9I OK1 PGMZT PHGZM PHGZT PIMPY PQQKQ PROAC PSQYO QOS R9I RBZ RNS ROL RPM RSV S27 SBL SOJ T13 U2A UKHRP WK8 PMFND 3V. 7XB 8FK AZQEC DWQXO GNUQQ K9. PJZUB PKEHL PPXIY PQEST PQGLB PQUKI 7X8 5PM PUEGO |
| ID | FETCH-LOGICAL-c541t-d395af6e71e22e1f0431a5ffa0444392149bb68c6c1c4a56123ad7c77e577ff93 |
| IEDL.DBID | M48 |
| ISSN | 1868-7083 1868-7075 |
| IngestDate | Wed Aug 27 01:17:26 EDT 2025 Thu Aug 21 18:36:17 EDT 2025 Fri Jul 11 11:32:27 EDT 2025 Fri Jul 25 11:52:50 EDT 2025 Tue Jun 17 21:47:17 EDT 2025 Tue Jun 10 21:19:42 EDT 2025 Tue Jul 01 04:01:58 EDT 2025 Thu Apr 24 22:53:34 EDT 2025 |
| IsDoiOpenAccess | true |
| IsOpenAccess | true |
| IsPeerReviewed | true |
| IsScholarly | true |
| Issue | 1 |
| Language | English |
| License | Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. |
| LinkModel | DirectLink |
| MergedId | FETCHMERGED-LOGICAL-c541t-d395af6e71e22e1f0431a5ffa0444392149bb68c6c1c4a56123ad7c77e577ff93 |
| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.1186/s13148-023-01549-y |
| PMID | 37626340 |
| PQID | 2865443197 |
| PQPubID | 2040146 |
| PageCount | 12 |
| ParticipantIDs | doaj_primary_oai_doaj_org_article_45509ebc47c640edb0efc49af44097ab pubmedcentral_primary_oai_pubmedcentral_nih_gov_10464315 proquest_miscellaneous_2857848036 proquest_journals_2865443197 gale_infotracmisc_A762278245 gale_infotracacademiconefile_A762278245 crossref_citationtrail_10_1186_s13148_023_01549_y crossref_primary_10_1186_s13148_023_01549_y |
| ProviderPackageCode | CITATION AAYXX |
| PublicationCentury | 2000 |
| PublicationDate | 2023-08-25 |
| PublicationDateYYYYMMDD | 2023-08-25 |
| PublicationDate_xml | – month: 08 year: 2023 text: 2023-08-25 day: 25 |
| PublicationDecade | 2020 |
| PublicationPlace | London |
| PublicationPlace_xml | – name: London |
| PublicationTitle | Clinical epigenetics |
| PublicationYear | 2023 |
| Publisher | BioMed Central Ltd BioMed Central BMC |
| Publisher_xml | – name: BioMed Central Ltd – name: BioMed Central – name: BMC |
| References | P Du (1549_CR34) 2008; 24 JJ Peluso (1549_CR48) 2008; 93 ME Ritchie (1549_CR43) 2015; 43 MJ Aryee (1549_CR25) 2014; 30 B Devlin (1549_CR46) 1999; 55 L Carrel (1549_CR14) 2005; 434 LM Reynolds (1549_CR33) 2014; 5 L Kananen (1549_CR8) 2021; 14 RC Slieker (1549_CR10) 2016; 17 M Schoenmaker (1549_CR19) 2006; 14 A Hofman (1549_CR21) 2013; 28 E Shvetsova (1549_CR54) 2019; 27 DV Zhernakova (1549_CR31) 2017; 49 Y Benjamini (1549_CR37) 1995; 57 M van Iterson (1549_CR26) 2014; 30 PJ Hop (1549_CR30) 2020; 21 RE Amir (1549_CR4) 1999; 23 BP Balaton (1549_CR42) 2021; 14 WE Johnson (1549_CR28) 2007; 8 DL McCartney (1549_CR9) 2019; 12 W Zhou (1549_CR27) 2017; 45 RC Slieker (1549_CR38) 2013; 6 R Luijk (1549_CR29) 2018; 9 T Tukiainen (1549_CR16) 2017; 550 A Johansson (1549_CR32) 2013; 8 Q Zhang (1549_CR12) 2018; 10 YT Liu (1549_CR49) 2021; 42 C López-Otín (1549_CR1) 2023; 186 BP Balaton (1549_CR41) 2021; 14 MF Lyon (1549_CR2) 1961; 190 AM Cotton (1549_CR40) 2015; 24 M van Iterson (1549_CR23) 2018; 34 MJ Machiela (1549_CR53) 2017; 42 G Yu (1549_CR44) 2012; 16 GK Smyth (1549_CR35) 1989; 51 M van Iterson (1549_CR36) 2017; 18 MH Huisman (1549_CR22) 2011; 82 S Li (1549_CR7) 2020; 12 AJ Sharp (1549_CR6) 2011; 21 A Piton (1549_CR5) 2011; 16 EF Tigchelaar (1549_CR18) 2015; 5 LA Honigberg (1549_CR50) 2010; 107 J Bergstedt (1549_CR13) 2022; 13 LM Russell (1549_CR52) 2007; 116 Y Zhang (1549_CR51) 2016; 33 RJ Craven (1549_CR47) 2008; 10 A Spatz (1549_CR3) 2004; 4 MJ Bonder (1549_CR24) 2017; 49 MM van Greevenbroek (1549_CR17) 2011; 41 J Higham (1549_CR45) 2022; 23 DI Boomsma (1549_CR20) 2002; 5 BP Balaton (1549_CR39) 2015; 6 K Seale (1549_CR11) 2022; 23 AM Cotton (1549_CR15) 2013; 14 |
| References_xml | – volume: 42 start-page: 1653 year: 2021 ident: 1549_CR49 publication-title: Acta Pharmacol Sin doi: 10.1038/s41401-020-00578-0 – volume: 24 start-page: 1528 year: 2015 ident: 1549_CR40 publication-title: Hum Mol Genet doi: 10.1093/hmg/ddu564 – volume: 14 start-page: 12 year: 2021 ident: 1549_CR42 publication-title: Epigenetics Chromatin doi: 10.1186/s13072-021-00386-8 – volume: 14 start-page: R122 year: 2013 ident: 1549_CR15 publication-title: Genome Biol doi: 10.1186/gb-2013-14-11-r122 – volume: 24 start-page: 1547 year: 2008 ident: 1549_CR34 publication-title: Bioinformatics doi: 10.1093/bioinformatics/btn224 – volume: 21 start-page: 220 year: 2020 ident: 1549_CR30 publication-title: Genome Biol doi: 10.1186/s13059-020-02114-z – volume: 21 start-page: 1592 year: 2011 ident: 1549_CR6 publication-title: Genome Res doi: 10.1101/gr.112680.110 – volume: 6 start-page: 35 year: 2015 ident: 1549_CR39 publication-title: Biol Sex Differ doi: 10.1186/s13293-015-0053-7 – volume: 434 start-page: 400 year: 2005 ident: 1549_CR14 publication-title: Nature doi: 10.1038/nature03479 – volume: 190 start-page: 372 year: 1961 ident: 1549_CR2 publication-title: Nature doi: 10.1038/190372a0 – volume: 45 start-page: e22 year: 2017 ident: 1549_CR27 publication-title: Nucleic Acids Res – volume: 41 start-page: 372 year: 2011 ident: 1549_CR17 publication-title: Eur J Clin Invest doi: 10.1111/j.1365-2362.2010.02418.x – volume: 49 start-page: 131 year: 2017 ident: 1549_CR24 publication-title: Nat Genet doi: 10.1038/ng.3721 – volume: 27 start-page: 455 year: 2019 ident: 1549_CR54 publication-title: Eur J Hum Genet doi: 10.1038/s41431-018-0291-3 – volume: 82 start-page: 1165 year: 2011 ident: 1549_CR22 publication-title: J Neurol Neurosurg Psychiatry doi: 10.1136/jnnp.2011.244939 – volume: 9 start-page: 3738 year: 2018 ident: 1549_CR29 publication-title: Nat Commun doi: 10.1038/s41467-018-05714-3 – volume: 23 start-page: 585 year: 2022 ident: 1549_CR11 publication-title: Nat Rev Genet doi: 10.1038/s41576-022-00477-6 – volume: 10 start-page: 75 year: 2018 ident: 1549_CR12 publication-title: Genome Med doi: 10.1186/s13073-018-0585-7 – volume: 6 start-page: 26 year: 2013 ident: 1549_CR38 publication-title: Epigenet Chromatin doi: 10.1186/1756-8935-6-26 – volume: 57 start-page: 289 year: 1995 ident: 1549_CR37 publication-title: J R Stat Soc Ser B (Methodol) doi: 10.1111/j.2517-6161.1995.tb02031.x – volume: 5 start-page: e006772 year: 2015 ident: 1549_CR18 publication-title: BMJ Open doi: 10.1136/bmjopen-2014-006772 – volume: 13 start-page: 5895 year: 2022 ident: 1549_CR13 publication-title: Nat Commun doi: 10.1038/s41467-022-33511-6 – volume: 30 start-page: 1363 year: 2014 ident: 1549_CR25 publication-title: Bioinformatics doi: 10.1093/bioinformatics/btu049 – volume: 12 start-page: 1 year: 2019 ident: 1549_CR9 publication-title: Genome Med doi: 10.1186/s13073-019-0693-z – volume: 42 start-page: 8 year: 2017 ident: 1549_CR53 publication-title: Curr Opin Genet Dev doi: 10.1016/j.gde.2016.12.002 – volume: 4 start-page: 617 year: 2004 ident: 1549_CR3 publication-title: Nat Rev Cancer doi: 10.1038/nrc1413 – volume: 16 start-page: 284 year: 2012 ident: 1549_CR44 publication-title: OMICS doi: 10.1089/omi.2011.0118 – volume: 14 start-page: 79 year: 2006 ident: 1549_CR19 publication-title: Eur J Hum Genet doi: 10.1038/sj.ejhg.5201508 – volume: 30 start-page: 3435 year: 2014 ident: 1549_CR26 publication-title: Bioinformatics doi: 10.1093/bioinformatics/btu566 – volume: 33 start-page: 302 year: 2016 ident: 1549_CR51 publication-title: Mol Biol Evol doi: 10.1093/molbev/msv180 – volume: 23 start-page: 185 year: 1999 ident: 1549_CR4 publication-title: Nat Genet doi: 10.1038/13810 – volume: 186 start-page: 243 year: 2023 ident: 1549_CR1 publication-title: Cell doi: 10.1016/j.cell.2022.11.001 – volume: 93 start-page: 1592 year: 2008 ident: 1549_CR48 publication-title: J Clin Endocrinol Metab doi: 10.1210/jc.2007-2771 – volume: 8 start-page: 118 year: 2007 ident: 1549_CR28 publication-title: Biostatistics doi: 10.1093/biostatistics/kxj037 – volume: 55 start-page: 997 year: 1999 ident: 1549_CR46 publication-title: Biometrics doi: 10.1111/j.0006-341X.1999.00997.x – volume: 5 start-page: 5366 year: 2014 ident: 1549_CR33 publication-title: Nat Commun doi: 10.1038/ncomms6366 – volume: 17 start-page: 191 year: 2016 ident: 1549_CR10 publication-title: Genome Biol doi: 10.1186/s13059-016-1053-6 – volume: 107 start-page: 13075 year: 2010 ident: 1549_CR50 publication-title: Proc Natl Acad Sci USA doi: 10.1073/pnas.1004594107 – volume: 12 start-page: 39 year: 2020 ident: 1549_CR7 publication-title: Genome Med doi: 10.1186/s13073-020-00736-3 – volume: 8 start-page: e67378 year: 2013 ident: 1549_CR32 publication-title: PLoS ONE doi: 10.1371/journal.pone.0067378 – volume: 16 start-page: 867 year: 2011 ident: 1549_CR5 publication-title: Mol Psychiatry doi: 10.1038/mp.2010.54 – volume: 14 start-page: 33 year: 2021 ident: 1549_CR8 publication-title: Epigenetics Chromatin doi: 10.1186/s13072-021-00407-6 – volume: 550 start-page: 244 year: 2017 ident: 1549_CR16 publication-title: Nature doi: 10.1038/nature24265 – volume: 116 start-page: 181 year: 2007 ident: 1549_CR52 publication-title: Cytogenet Genome Res doi: 10.1159/000098184 – volume: 18 start-page: 19 year: 2017 ident: 1549_CR36 publication-title: Genome Biol doi: 10.1186/s13059-016-1131-9 – volume: 51 start-page: 47 year: 1989 ident: 1549_CR35 publication-title: J R Stat Soc Ser B (Methodol) doi: 10.1111/j.2517-6161.1989.tb01747.x – volume: 28 start-page: 889 year: 2013 ident: 1549_CR21 publication-title: Eur J Epidemiol doi: 10.1007/s10654-013-9866-z – volume: 49 start-page: 139 year: 2017 ident: 1549_CR31 publication-title: Nat Genet doi: 10.1038/ng.3737 – volume: 14 start-page: 30 year: 2021 ident: 1549_CR41 publication-title: Epigenetics Chromatin doi: 10.1186/s13072-021-00404-9 – volume: 43 start-page: e47 year: 2015 ident: 1549_CR43 publication-title: Nucleic Acids Res doi: 10.1093/nar/gkv007 – volume: 5 start-page: 401 year: 2002 ident: 1549_CR20 publication-title: Twin Res doi: 10.1375/136905202320906174 – volume: 34 start-page: 2142 year: 2018 ident: 1549_CR23 publication-title: Bioinformatics doi: 10.1093/bioinformatics/bty062 – volume: 10 start-page: 113 year: 2008 ident: 1549_CR47 publication-title: Breast Cancer Res doi: 10.1186/bcr2191 – volume: 23 start-page: 216 year: 2022 ident: 1549_CR45 publication-title: Genome Biol doi: 10.1186/s13059-022-02787-8 |
| SSID | ssj0000399910 |
| Score | 2.375427 |
| Snippet | Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies... Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies of the X... BackgroundLoss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of two copies... Abstract Background Loss of epigenetic control is a hallmark of aging. Among the most prominent roles of epigenetic mechanisms is the inactivation of one of... |
| SourceID | doaj pubmedcentral proquest gale crossref |
| SourceType | Open Website Open Access Repository Aggregation Database Enrichment Source Index Database |
| StartPage | 1 |
| SubjectTerms | Age Aging Analysis Atherosclerosis Biobanks Blood CpG islands Datasets DNA methylation Epigenetic inheritance Epigenetics Females Gene expression Generalized linear models Genes Genomes Granulocytes Males Methylation Monocytes Quality control Variance Women X chromosome X chromosomes X-chromosome inactivation |
| SummonAdditionalLinks | – databaseName: DOAJ Directory of Open Access Journals dbid: DOA link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV1La9wwEBYhUMil9EndpkWFQg_BZG297GNaEkKhJYcEllyELI3IQuNd6t2E_fedkb3LOoHm0puxRkYajeYha75h7AtauEI7CLkRBgMU34S8ErrOtcFn0cSoE8TGz1_6_Er-mKrpTqkvuhPWwwP3jDumrNsaGi-N13ICoZlA9LJ2URJSk2tI-6LN2wmmkg4W5PhMNlkylT7uCkFnZ2ii8gRLlq9HligB9j9Wyw-vSu7YnrMX7PngNPKTfrAv2R60r9iz63k6En_NLnCt-ax1SXXxKfc3dMeum98Cd96vbqlCF3T8fhagW6CTGDgsCIST8hf5HQbLPVb3mtOhLEcF84ZdnZ1efj_Ph0oJuVeyWOZB1MpFDaaAsoQiEmKOUzE6QoNDDwjDoKbRlde-8NJRQUzhgvHGgDImxlq8ZfvtvIV3jAMI8KWOzrggMXysRFDo03oJDmLpJhkrNlyzfoARp2oWv20KJypte05b5LRNnLbrjB1t-yx6EI1_Un-jxdhSEgB2eoFiYQexsE-JRca-0lJa2qY4PO-GbAOcJAFe2RM0AiV6R1Jl7HBEidvLj5s3wmCH7d1ZSudFxha1ydjnbTP1pCtrLcxXRIPKUFboIWSsGgnRaGbjlnZ2kyC-6c87fl-9_x-8-MAOyiT3qBPVIdtf_lnBR3Slls2ntGv-ArIFHOo priority: 102 providerName: Directory of Open Access Journals – databaseName: ProQuest Health & Medical Collection dbid: 7X7 link: http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwfV3fi9QwEA56Ivgi_sTqKREEHyTctkmT9ElO8TgExQcPFl9Cmky8hbt2ve4q-987k-2uVuHelk262yaZmW-mM98w9gotXKk9RGGkQQcltFFYqRuhDX6WbUo6U2x8-qxPz9THeT0fA27DmFa504lZUcc-UIz8iCooFVq7xrxd_hDUNYrero4tNG6yW0RdRildZm72MZaZJPiTayKttsIg3NjVzVh9NJSSomlotEQmKhObiW3KFP7_K-p_kyf_skYn99jdEUby4-2-32c3oHvAbn_rc5D8IfuCu88Xnc_KjM95OKesu6G_BO5DWF9Szy4Y-K9FhGGJsDFyWBItJ1U08p_oPm_ZuzecwrQcVc4jdnby4ev7UzH2ThChVuVKRNnUPmkwJVQVlIk4dHydkid-OMRE6Bi1rbZBhzIoTy0ypY8mGAO1MSk18jE76PoOnjAOICFUOnnjo0KH0spYI8oNCjykys8KVu5WzYWRWJz6W1y47GBY7bYr7XClXV5ptynYm_01yy2txrWz39Fm7GcSJXb-or_67kYJc1Se3UAblAlazSC2M0hBNT4povTybcFe01Y6Ely8veDH-gN8SKLAcsdoFirES6ou2OFkJgpcmA7vDoMbBX5wf45nwV7uh-lKSmLroF_THFSPyiJmKJidHKLJk01HusV5Jv2md_H4-_XT6__9GbtT5RON-q8-ZAerqzU8R9i0al9k2fgNBtwVig priority: 102 providerName: ProQuest |
| Title | The inactive X chromosome accumulates widespread epigenetic variability with age |
| URI | https://www.proquest.com/docview/2865443197 https://www.proquest.com/docview/2857848036 https://pubmed.ncbi.nlm.nih.gov/PMC10464315 https://doaj.org/article/45509ebc47c640edb0efc49af44097ab |
| Volume | 15 |
| hasFullText | 1 |
| inHoldings | 1 |
| isFullTextHit | |
| isPrint | |
| link | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV3da9RAEB_6gdIX8ROj9VhB8EGil-xmN3kQaaW1CC1FPDh8WTab3fagTc77UO-_d2YvORotPvgSQnY3JJP5zs5vAF6hhUukcVWsuMIAxZZVnHNZxFLhOS-9lwFi4_RMnozE53E23oKu3VFLwPmtoR31kxrNrt7--r76gAL_Pgh8Lt_NE05pMbQ-cUAci1fbsIuWSZGgnrbuftDMnNyhUCOZyzxWaC67Oppbb7MHd1H-UskpNXLDbAV0_791-J_7Km8YquP7cK_1MNnBmiUewJarH8Kdb03Inz-Cc2QMNqlN0HNszOwlbcibN9eOGWuX19TOy83Zz0nl5lP0KCvmpoTYScWO7AdG1mtg7xWjDC5DbfQYRsdHXz-exG1bhdhmIlnEFS8y46VTiUtTl3iC1zGZ94ag49BdwpipLGVupU2sMNQ9k5tKWaVcppT3BX8CO3VTu6fAnOPOptIbZSqBsWbOqwwdYCuccT41wwiSjmratpjj1PriSofYI5d6TXSNRNeB6HoVwZvNmukaceOfsw_pY2xmElp2uNDMLnQrfJoqtwtXWqGsFENXlUPnrSiMF4T2ZcoIXtOn1MRl-HjWtKUJ-JKEjqUPkAlSdKVEFsF-bybKou0Pd8ygO1bWVPuLhE0KFcHLzTCtpP1ttWuWNAc1p8jRnYgg7zFR7836I_XkMuCB0296vH_27P-XPoe9NDA-qs1sH3YWs6V7gd7WohzAthqrAeweHp2dfxmEnAUeP42TQRCu3zzZKso |
| linkProvider | Scholars Portal |
| linkToHtml | http://utb.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwtV3db9MwELemTghe0PgSgQFGAvGAojWJY6cPCG2wqWNbNaFNqngxjnPeKrGkW1qm_lP8jdy5SSEg7W1vUex8ne87vt8x9gYtXCQNFKFKFAYoNi_CLJGDUCo8TnLnpIfYOBrJ4an4Mk7Ha-xXWwtD2ypbnegVdVFZypFvUQWlQGs3UB-nlyF1jaK_q20LjSVbHMDiGkO2-sP-Z1zft3G8t3vyaRg2XQVCm4poFhbJIDVOgoogjiFyhC5jUucMIaeht4AhQ57LzEobWWGoeWRiCmWVglQp5wh8CVX-ukgwlOmx9Z3d0fHXVVann5DD5aswM5mFCh2ctlInk1t1lFD-Ds1k6KHRwkXHGvqmAf-bhn-3a_5l__Y22P3GceXbS057wNagfMjufKt8Wv4RO0Z-45PSePXJx9ye0z6_uroAbqydX1CXMKj59aSAeoqOasFhSkCgVEPJf2LAvsQLX3BKDHNUco_Z6a3Q9QnrlVUJTxkHSMDG0hllCoEhbJYUKfrVVoABF5t-wKKWato2UObUUeOH9iFNJvWS0hoprT2l9SJg71fXTJdAHjfO3qHFWM0kEG5_oro6041MayoIH0BuhbJS9KHI--CsGBgnCETM5AF7R0upSVXg61nTVDzgRxLolt5GQxSjhybSgG12ZqKI2-5wywy6UTG1_iMQAXu9GqYradtcCdWc5qBCFhl6KQHLOkzU-bLuSDk59zDj9Pcf758-u_npr9jd4cnRoT7cHx08Z_diz92ofdNN1ptdzeEFOm2z_GUjKZx9v23h_A07gFMz |
| openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=The+inactive+X+chromosome+accumulates+widespread+epigenetic+variability+with+age&rft.jtitle=Clinical+epigenetics&rft.au=Liu%2C+Yunfeng&rft.au=Sinke%2C+Lucy&rft.au=Jonkman%2C+Thomas+H.&rft.au=Slieker%2C+Roderick+C.&rft.date=2023-08-25&rft.pub=BioMed+Central&rft.issn=1868-7075&rft.eissn=1868-7083&rft.volume=15&rft_id=info:doi/10.1186%2Fs13148-023-01549-y&rft_id=info%3Apmid%2F37626340&rft.externalDocID=PMC10464315 |
| thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1868-7083&client=summon |
| thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1868-7083&client=summon |
| thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1868-7083&client=summon |