Chromatin signature of embryonic pluripotency is established during genome activation
After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition. This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure...
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| Published in | Nature (London) Vol. 464; no. 7290; pp. 922 - 926 |
|---|---|
| Main Authors | , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
08.04.2010
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition. This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure that accompany pluripotency and genome activation, we mapped the genomic locations of histone H3 molecules bearing lysine trimethylation modifications before and after the maternal-zygotic transition in zebrafish. Histone H3 lysine 27 trimethylation (H3K27me3), which is repressive, and H3K4me3, which is activating, were not detected before the transition. After genome activation, more than 80% of genes were marked by H3K4me3, including many inactive developmental regulatory genes that were also marked by H3K27me3. Sequential chromatin immunoprecipitation demonstrated that the same promoter regions had both trimethylation marks. Such bivalent chromatin domains also exist in embryonic stem cells and are thought to poise genes for activation while keeping them repressed. Furthermore, we found many inactive genes that were uniquely marked by H3K4me3. Despite this activating modification, these monovalent genes were neither expressed nor stably bound by RNA polymerase II. Inspection of published data sets revealed similar monovalent domains in embryonic stem cells. Moreover, H3K4me3 marks could form in the absence of both sequence-specific transcriptional activators and stable association of RNA polymerase II, as indicated by the analysis of an inducible transgene. These results indicate that bivalent and monovalent domains might poise embryonic genes for activation and that the chromatin profile associated with pluripotency is established during the maternal-zygotic transition. |
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| AbstractList | After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition
1
,
2
,
3
. This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure that accompany pluripotency and genome activation, we mapped the genomic locations of histone H3 molecules bearing Lysine trimethylation modifications before and after the maternal-zygotic transition in zebrafish. Trimethylation of Lysine 27, which is repressive, and trimethylation of Lysine 4, which is activating, were not detected before the transition. After genome activation, more than 80% of genes were marked by Lysine 4 trimethylation, including many inactive developmental regulatory genes that were also marked by Lysine 27 trimethylation. Sequential chromatin immunoprecipitation demonstrated that the same promoter regions had both trimethylation marks. Such bivalent chromatin domains also exist in embryonic stem cells and are thought to poise genes for activation while keeping them repressed
4
,
5
,
6
,
7
,
8
. In addition, we found many inactive genes that were uniquely marked by Lysine 4 trimethylation. Despite this activating modification, these monovalent genes were neither expressed nor stably bound by RNA polymerase II. Inspection of published datasets revealed similar monovalent domains in embryonic stem cells. Moreover, Lysine 4 trimethylation marks could form in the absence of both sequence-specific transcriptional activators and stable association of RNA pol II, as indicated by the analysis of an inducible transgene. These results suggest that bivalent and monovalent domains might poise embryonic genes for activation and that the chromatin profile associated with pluripotency is established during the maternal-zygotic transition. After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition. This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure that accompany pluripotency and genome activation, we mapped the genomic locations of histone H3 molecules bearing lysine trimethylation modifications before and after the maternal-zygotic transition in zebrafish. Histone H3 lysine 27 trimethylation (H3K27me3), which is repressive, and H3K4me3, which is activating, were not detected before the transition. After genome activation, more than 80% of genes were marked by H3K4me3, including many inactive developmental regulatory genes that were also marked by H3K27me3. Sequential chromatin immunoprecipitation demonstrated that the same promoter regions had both trimethylation marks. Such bivalent chromatin domains also exist in embryonic stem cells and are thought to poise genes for activation while keeping them repressed. Furthermore, we found many inactive genes that were uniquely marked by H3K4me3. Despite this activating modification, these monovalent genes were neither expressed nor stably bound by RNA polymerase II. Inspection of published data sets revealed similar monovalent domains in embryonic stem cells. Moreover, H3K4me3 marks could form in the absence of both sequence-specific transcriptional activators and stable association of RNA polymerase II, as indicated by the analysis of an inducible transgene. These results indicate that bivalent and monovalent domains might poise embryonic genes for activation and that the chromatin profile associated with pluripotency is established during the maternal-zygotic transition. After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition (1-3). This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure that accompany pluripotency and genome activation, we mapped the genomic locations of histone H3 molecules bearing lysine trimethylation modifications before and after the maternal-zygotic transition in zebrafish. Histone H3 lysine 27 trimethylation (H3K27me3), which is repressive, and H3K4me3, which is activating, were not detected before the transition. After genome activation, more than 80% of genes were marked by H3K4me3, including many inactive developmental regulatory genes that were also marked by H3K27me3. Sequential chromatin immunoprecipitation demonstrated that the same promoter regions had both trimethylation marks. Such bivalent chromatin domains also exist in embryonic stem cells and are thought to poise genes for activation while keeping them repressed (4-8). Furthermore, we found many inactive genes that were uniquely marked by H3K4me3. Despite this activating modification, these monovalent genes were neither expressed nor stably bound by RNA polymerase II. Inspection of published data sets revealed similar monovalent domains in embryonic stem cells. Moreover, H3K4me3 marks could form in the absence of both sequence-specific transcriptional activators and stable association of RNA polymerase II, as indicated by the analysis of an inducible transgene. These results indicate that bivalent and monovalent domains might poise embryonic genes for activation and that the chromatin profile associated with pluripotency is established during the maternal-zygotic transition. Chromatin signature of pluripotency To study the changes in chromatin structure that accompany zygotic genome activation and pluripotency during the maternal–zygotic transition (MZT), the genomic locations of histone H3 modifications and RNA polymerase II have been mapped during this transition in zebrafish embryos. H3 lysine 27 trimethylation and H3 lysine 4 trimethylation are only detected after MZT, and evidence is provided that the bivalent chromatin domains in cultured ES cells also exist in embryos. To study the changes in chromatin structure that accompany zygotic genome activation and pluripotency during the maternal–zygotic transition (MZT), the genomic locations of histone H3 modifications and RNA polymerase II have been mapped during this transition in zebrafish embryos. H3 lysine 27 trimethylation and H3 lysine 4 trimethylation are only detected after MZT; evidence is provided that the bivalent chromatin domains found in cultured embryonic stem cells also exist in embryos. After fertilization the embryonic genome is inactive until transcription is initiated during the maternal–zygotic transition 1 , 2 , 3 . This transition coincides with the formation of pluripotent cells, which in mammals can be used to generate embryonic stem cells. To study the changes in chromatin structure that accompany pluripotency and genome activation, we mapped the genomic locations of histone H3 molecules bearing lysine trimethylation modifications before and after the maternal–zygotic transition in zebrafish. Histone H3 lysine 27 trimethylation (H3K27me3), which is repressive, and H3K4me3, which is activating, were not detected before the transition. After genome activation, more than 80% of genes were marked by H3K4me3, including many inactive developmental regulatory genes that were also marked by H3K27me3. Sequential chromatin immunoprecipitation demonstrated that the same promoter regions had both trimethylation marks. Such bivalent chromatin domains also exist in embryonic stem cells and are thought to poise genes for activation while keeping them repressed 4 , 5 , 6 , 7 , 8 . Furthermore, we found many inactive genes that were uniquely marked by H3K4me3. Despite this activating modification, these monovalent genes were neither expressed nor stably bound by RNA polymerase II. Inspection of published data sets revealed similar monovalent domains in embryonic stem cells. Moreover, H3K4me3 marks could form in the absence of both sequence-specific transcriptional activators and stable association of RNA polymerase II, as indicated by the analysis of an inducible transgene. These results indicate that bivalent and monovalent domains might poise embryonic genes for activation and that the chromatin profile associated with pluripotency is established during the maternal–zygotic transition. To determine the genomic locations of RNA pol II, H3K36me3, H3K4me3 and H3K27me3 before and after the maternal-zygotic transition, we performed chromatin immunoprecipitation (ChIP) and identified co-precipitated DNA fragments by hybridization to custom-designed NimbleGen tiling microarrays12 covering ~31 megabases of the zebrafish genome (ChIP-chip). [...] we find that many genes are monovalently marked by H3K4me3 but inactive.This subset of genes has received little attention in ES cell studies, but our analysis of published data sets suggests that many non-expressed genes in ES cells also carry monovalent H3K4me3 marks. |
| Audience | Academic |
| Author | Woods, Ian G Liu, X. Shirley Imam, Farhad Schier, Alexander F Rinn, John Regev, Aviv Vastenhouw, Nadine L Zhang, Yong |
| AuthorAffiliation | 5 Department of Pathology, Beth Israel Deaconess Medical Center, Boston, USA 7 Center for Brain Science, Harvard University, Cambridge, MA 02138, USA 3 School of Life Science and Technology, Tongji University, 1239 Siping Road, Shanghai, China 4 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA 1 Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA 2 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Harvard School of Public Health, Boston, USA 6 Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA |
| AuthorAffiliation_xml | – name: 7 Center for Brain Science, Harvard University, Cambridge, MA 02138, USA – name: 3 School of Life Science and Technology, Tongji University, 1239 Siping Road, Shanghai, China – name: 6 Harvard Stem Cell Institute, Harvard University, Cambridge, MA 02138, USA – name: 1 Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, Cambridge, MA 02138, USA – name: 2 Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Harvard School of Public Health, Boston, USA – name: 4 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – name: 5 Department of Pathology, Beth Israel Deaconess Medical Center, Boston, USA |
| Author_xml | – sequence: 1 givenname: X. Shirley surname: Liu fullname: Liu, X. Shirley organization: Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Harvard School of Public Health – sequence: 2 givenname: Alexander F surname: Schier fullname: Schier, Alexander F organization: Department of Molecular and Cellular Biology, Harvard University Broad Institute of MIT and Harvard – sequence: 3 givenname: Nadine L surname: Vastenhouw fullname: Vastenhouw, Nadine L organization: Department of Molecular and Cellular Biology, Harvard University – sequence: 4 givenname: Yong surname: Zhang fullname: Zhang, Yong organization: Department of Biostatistics and Computational Biology, Dana-Farber Cancer Institute, Harvard School of Public Health School of Life Science and Technology, Tongji University – sequence: 5 givenname: Ian G surname: Woods fullname: Woods, Ian G organization: Department of Molecular and Cellular Biology, Harvard University – sequence: 6 givenname: Farhad surname: Imam fullname: Imam, Farhad organization: Department of Molecular and Cellular Biology, Harvard University – sequence: 7 givenname: Aviv surname: Regev fullname: Regev, Aviv organization: Broad Institute of MIT and Harvard – sequence: 8 givenname: John surname: Rinn fullname: Rinn, John organization: Broad Institute of MIT and Harvard Department of Pathology, Beth Israel Deaconess Medical Center |
| BackLink | http://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=22565321$$DView record in Pascal Francis https://www.ncbi.nlm.nih.gov/pubmed/20336069$$D View this record in MEDLINE/PubMed |
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| CODEN | NATUAS |
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| Keywords | Chromatin Stem cell Chromosome Activation Deoxyribonucleoproteins Vertebrata Brachydanio rerio Regulation(control) Basic protein Pluripotent cell Pisces Genome Histone Methylation Nuclear protein |
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| Snippet | After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition. This transition coincides with... Chromatin signature of pluripotency To study the changes in chromatin structure that accompany zygotic genome activation and pluripotency during the... After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition (1-3). This transition coincides... To determine the genomic locations of RNA pol II, H3K36me3, H3K4me3 and H3K27me3 before and after the maternal-zygotic transition, we performed chromatin... After fertilization the embryonic genome is inactive until transcription is initiated during the maternal-zygotic transition 1 , 2 , 3 . This transition... |
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| SubjectTerms | 631/136/2444 631/136/532/2117 631/337/100/102 Analysis Animals Biological and medical sciences Chromatin Chromatin - genetics Chromatin - metabolism Chromatin Immunoprecipitation Chromatin. Chromosome Decision trees Embryonic development Embryonic stem cells Fundamental and applied biological sciences. Psychology Gene Expression Regulation, Developmental - genetics Gene Silencing Genetic aspects Genetics Genome - genetics Genomics Histones - chemistry Histones - metabolism Humanities and Social Sciences letter Lysine - metabolism Methods Methylation Molecular and cellular biology Molecular genetics multidisciplinary Oligonucleotide Array Sequence Analysis Physiological aspects Pluripotent Stem Cells - metabolism Promoter Regions, Genetic - genetics RNA polymerase RNA Polymerase II - metabolism Science Structure Studies Transcriptional Activation Transgenes Zebrafish Zebrafish - embryology Zebrafish - genetics Zebrafish - metabolism Zebrafish Proteins - genetics Zygote - cytology Zygote - metabolism |
| Title | Chromatin signature of embryonic pluripotency is established during genome activation |
| URI | http://dx.doi.org/10.1038/nature08866 https://link.springer.com/article/10.1038/nature08866 https://www.ncbi.nlm.nih.gov/pubmed/20336069 https://www.proquest.com/docview/204472484 https://search.proquest.com/docview/733525412 https://pubmed.ncbi.nlm.nih.gov/PMC2874748 |
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