Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos
Full-term development has now been achieved in several mammalian species by transfer of somatic nuclei into enucleated oocytes [1, 2]. Although a high proportion of such reconstructed embryos can evolve until the blastocyst stage, only a few percent develop into live offspring, which often exhibit d...
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creator | Bourc'his, D Le Bourhis, D Patin, D Niveleau, A Comizzoli, P Renard, J.-P Viegas-Péquignot, E |
description | Full-term development has now been achieved in several mammalian species by transfer of somatic nuclei into enucleated oocytes [1, 2]. Although a high proportion of such reconstructed embryos can evolve until the blastocyst stage, only a few percent develop into live offspring, which often exhibit developmental abnormalities [3, 4]. Regulatory epigenetic markers such as DNA methylation are imposed on embryonic cells as normal development proceeds, creating differentiated cell states. Cloned embryos require the erasure of their somatic epigenetic markers so as to regain a totipotent state [5]. Here we report on differences in the dynamics of chromosome methylation between cloned and normal bovine embryos before implantation. We show that cloned embryos fail to reproduce distinguishable parental-chromosome methylation patterns after fusion and maintain their somatic pattern during subsequent stages, mainly by a highly reduced efficiency of the passive demethylation process. Surprisingly, chromosomes appear constantly undermethylated on euchromatin in morulae and blastocysts, while centromeric heterochromatin remains more methylated than that of normal embryos. We propose that the abnormal time-dependent methylation events spanning the preimplantation development of clones may significantly interfere with the epigenetic reprogramming, contributing to the high incidence of physiological anomalies occurring later during pregnancy or after clone birth. |
doi_str_mv | 10.1016/S0960-9822(01)00480-8 |
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Although a high proportion of such reconstructed embryos can evolve until the blastocyst stage, only a few percent develop into live offspring, which often exhibit developmental abnormalities [3, 4]. Regulatory epigenetic markers such as DNA methylation are imposed on embryonic cells as normal development proceeds, creating differentiated cell states. Cloned embryos require the erasure of their somatic epigenetic markers so as to regain a totipotent state [5]. Here we report on differences in the dynamics of chromosome methylation between cloned and normal bovine embryos before implantation. We show that cloned embryos fail to reproduce distinguishable parental-chromosome methylation patterns after fusion and maintain their somatic pattern during subsequent stages, mainly by a highly reduced efficiency of the passive demethylation process. Surprisingly, chromosomes appear constantly undermethylated on euchromatin in morulae and blastocysts, while centromeric heterochromatin remains more methylated than that of normal embryos. We propose that the abnormal time-dependent methylation events spanning the preimplantation development of clones may significantly interfere with the epigenetic reprogramming, contributing to the high incidence of physiological anomalies occurring later during pregnancy or after clone birth.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/S0960-9822(01)00480-8</identifier><identifier>PMID: 11591324</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Animals ; Bos ; Cattle ; Centromere ; Chromosomes ; Cloning, Organism ; DNA Methylation ; Embryonic and Fetal Development ; Euchromatin ; Heterochromatin ; Life Sciences</subject><ispartof>Current biology, 2001-10, Vol.11 (19), p.1542-1546</ispartof><rights>2001 Elsevier Science Ltd</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c591t-f9f206b81d848fd9f0d6b2ff60f16f6067e37aa851da8cca51654ee310ff84753</citedby><cites>FETCH-LOGICAL-c591t-f9f206b81d848fd9f0d6b2ff60f16f6067e37aa851da8cca51654ee310ff84753</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982201004808$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65534</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11591324$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.inrae.fr/hal-02671049$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Bourc'his, D</creatorcontrib><creatorcontrib>Le Bourhis, D</creatorcontrib><creatorcontrib>Patin, D</creatorcontrib><creatorcontrib>Niveleau, A</creatorcontrib><creatorcontrib>Comizzoli, P</creatorcontrib><creatorcontrib>Renard, J.-P</creatorcontrib><creatorcontrib>Viegas-Péquignot, E</creatorcontrib><title>Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Full-term development has now been achieved in several mammalian species by transfer of somatic nuclei into enucleated oocytes [1, 2]. Although a high proportion of such reconstructed embryos can evolve until the blastocyst stage, only a few percent develop into live offspring, which often exhibit developmental abnormalities [3, 4]. Regulatory epigenetic markers such as DNA methylation are imposed on embryonic cells as normal development proceeds, creating differentiated cell states. Cloned embryos require the erasure of their somatic epigenetic markers so as to regain a totipotent state [5]. Here we report on differences in the dynamics of chromosome methylation between cloned and normal bovine embryos before implantation. We show that cloned embryos fail to reproduce distinguishable parental-chromosome methylation patterns after fusion and maintain their somatic pattern during subsequent stages, mainly by a highly reduced efficiency of the passive demethylation process. Surprisingly, chromosomes appear constantly undermethylated on euchromatin in morulae and blastocysts, while centromeric heterochromatin remains more methylated than that of normal embryos. We propose that the abnormal time-dependent methylation events spanning the preimplantation development of clones may significantly interfere with the epigenetic reprogramming, contributing to the high incidence of physiological anomalies occurring later during pregnancy or after clone birth.</description><subject>Animals</subject><subject>Bos</subject><subject>Cattle</subject><subject>Centromere</subject><subject>Chromosomes</subject><subject>Cloning, Organism</subject><subject>DNA Methylation</subject><subject>Embryonic and Fetal Development</subject><subject>Euchromatin</subject><subject>Heterochromatin</subject><subject>Life Sciences</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2001</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkUtvEzEURi0EoqHwE0BeIboYuHceHnuFqvIoUiQWwNp4PNeN0Xgc7Emk_HucJirLbmzJOt99-DD2GuE9AooPP0AJqJSs63eAVwCthEo-YSuUvaqgbbunbPWAXLAXOf8BwFoq8ZxdIHYKm7pdsd-faDIHGrmZR-5nG8N2ooV4om2Kd8mE4Oc7Hh23mxRDzDEQD7RsDpNZfJz51iwLpTmXLB_i3s_E7RTnUpDCkA4xv2TPnJkyvTrfl-zXl88_b26r9fev326u15UtoyyVU64GMUgcZSvdqByMYqidE-BQlFP01PTGyA5HI601HYquJWoQnJNt3zWX7OpUd2MmvU0-mHTQ0Xh9e73WxzeoRY_Qqj0W9u2JLTv-3VFedPDZ0jSZmeIu675G2RT4URBljY3qVQG7E2hTzDmRexgBQR996Xtf-ihDA-p7X1qW3Jtzg90QaPyfOgsqwMcTQOXv9p6SztbTbGn0ieyix-gfafEPvr6lnQ</recordid><startdate>20011002</startdate><enddate>20011002</enddate><creator>Bourc'his, D</creator><creator>Le Bourhis, D</creator><creator>Patin, D</creator><creator>Niveleau, A</creator><creator>Comizzoli, P</creator><creator>Renard, J.-P</creator><creator>Viegas-Péquignot, E</creator><general>Elsevier Inc</general><general>Elsevier</general><scope>6I.</scope><scope>AAFTH</scope><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QO</scope><scope>8FD</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>1XC</scope></search><sort><creationdate>20011002</creationdate><title>Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos</title><author>Bourc'his, D ; Le Bourhis, D ; Patin, D ; Niveleau, A ; Comizzoli, P ; Renard, J.-P ; Viegas-Péquignot, E</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c591t-f9f206b81d848fd9f0d6b2ff60f16f6067e37aa851da8cca51654ee310ff84753</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2001</creationdate><topic>Animals</topic><topic>Bos</topic><topic>Cattle</topic><topic>Centromere</topic><topic>Chromosomes</topic><topic>Cloning, Organism</topic><topic>DNA Methylation</topic><topic>Embryonic and Fetal Development</topic><topic>Euchromatin</topic><topic>Heterochromatin</topic><topic>Life Sciences</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bourc'his, D</creatorcontrib><creatorcontrib>Le Bourhis, D</creatorcontrib><creatorcontrib>Patin, D</creatorcontrib><creatorcontrib>Niveleau, A</creatorcontrib><creatorcontrib>Comizzoli, P</creatorcontrib><creatorcontrib>Renard, J.-P</creatorcontrib><creatorcontrib>Viegas-Péquignot, E</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bourc'his, D</au><au>Le Bourhis, D</au><au>Patin, D</au><au>Niveleau, A</au><au>Comizzoli, P</au><au>Renard, J.-P</au><au>Viegas-Péquignot, E</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2001-10-02</date><risdate>2001</risdate><volume>11</volume><issue>19</issue><spage>1542</spage><epage>1546</epage><pages>1542-1546</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Full-term development has now been achieved in several mammalian species by transfer of somatic nuclei into enucleated oocytes [1, 2]. Although a high proportion of such reconstructed embryos can evolve until the blastocyst stage, only a few percent develop into live offspring, which often exhibit developmental abnormalities [3, 4]. Regulatory epigenetic markers such as DNA methylation are imposed on embryonic cells as normal development proceeds, creating differentiated cell states. Cloned embryos require the erasure of their somatic epigenetic markers so as to regain a totipotent state [5]. Here we report on differences in the dynamics of chromosome methylation between cloned and normal bovine embryos before implantation. We show that cloned embryos fail to reproduce distinguishable parental-chromosome methylation patterns after fusion and maintain their somatic pattern during subsequent stages, mainly by a highly reduced efficiency of the passive demethylation process. Surprisingly, chromosomes appear constantly undermethylated on euchromatin in morulae and blastocysts, while centromeric heterochromatin remains more methylated than that of normal embryos. We propose that the abnormal time-dependent methylation events spanning the preimplantation development of clones may significantly interfere with the epigenetic reprogramming, contributing to the high incidence of physiological anomalies occurring later during pregnancy or after clone birth.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>11591324</pmid><doi>10.1016/S0960-9822(01)00480-8</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Animals Bos Cattle Centromere Chromosomes Cloning, Organism DNA Methylation Embryonic and Fetal Development Euchromatin Heterochromatin Life Sciences |
title | Delayed and incomplete reprogramming of chromosome methylation patterns in bovine cloned embryos |
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