KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes
The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging 1 – 4 . Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change 5 , whereas histone H3 lysine 4 (H3K4...
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| Published in | Nature cell biology Vol. 22; no. 4; pp. 380 - 388 |
|---|---|
| Main Authors | , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
London
Nature Publishing Group UK
01.04.2020
Nature Publishing Group |
| Subjects | |
| Online Access | Get full text |
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| Abstract | The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging
1
–
4
. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change
5
, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters
6
. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3)
1
,
2
. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells
7
. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo.
Hoffmann and colleagues report that the mammalian maternal-to-zygotic transition requires KDM4A-mediated removal of H3K9me3 from the broad H3K4me3 domains in oocytes. |
|---|---|
| AbstractList | The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging
. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change
, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters
. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3)
. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells
. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo. The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging1-4. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change5, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters6. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3)1,2. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells7. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo.The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging1-4. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change5, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters6. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3)1,2. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells7. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo. The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging1–4. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change5, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters6. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3)1,2. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells7. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo.Hoffmann and colleagues report that the mammalian maternal-to-zygotic transition requires KDM4A-mediated removal of H3K9me3 from the broad H3K4me3 domains in oocytes. The importance of germline-inherited posttranslational histone modifications on priming early mammalian development is just emerging 1 – 4 . Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change 5 , while histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters 6 . Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3) 1 , 2 . It remains unknown as to which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells 7 . Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal preimplantation development and zygotic genome activation (ZGA) after fertilization. Loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and long terminal repeat initiated chimeric transcripts during ZGA. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and preimplantation development. Hence, KDM4A plays a crucial role in preserving maternal epigenome integrity required for proper ZGA and transfer of developmental control to the embryo. The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging.sup.1-4. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change.sup.5, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters.sup.6. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3).sup.1,2. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells.sup.7. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo. Hoffmann and colleagues report that the mammalian maternal-to-zygotic transition requires KDM4A-mediated removal of H3K9me3 from the broad H3K4me3 domains in oocytes. The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging.sup.1-4. Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change.sup.5, whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters.sup.6. Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3).sup.1,2. It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells.sup.7. Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo. The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging 1 – 4 . Histone H3 lysine 9 (H3K9) trimethylation is associated with heterochromatin and gene repression during cell-fate change 5 , whereas histone H3 lysine 4 (H3K4) trimethylation marks active gene promoters 6 . Mature oocytes are transcriptionally quiescent and possess remarkably broad domains of H3K4me3 (bdH3K4me3) 1 , 2 . It is unknown which factors contribute to the maintenance of the bdH3K4me3 landscape. Lysine-specific demethylase 4A (KDM4A) demethylates H3K9me3 at promoters marked by H3K4me3 in actively transcribing somatic cells 7 . Here, we report that KDM4A-mediated H3K9me3 demethylation at bdH3K4me3 in oocytes is crucial for normal pre-implantation development and zygotic genome activation after fertilization. The loss of KDM4A in oocytes causes aberrant H3K9me3 spreading over bdH3K4me3, resulting in insufficient transcriptional activation of genes, endogenous retroviral elements and chimeric transcripts initiated from long terminal repeats during zygotic genome activation. The catalytic activity of KDM4A is essential for normal epigenetic reprogramming and pre-implantation development. Hence, KDM4A plays a crucial role in preserving the maternal epigenome integrity required for proper zygotic genome activation and transfer of developmental control to the embryo. Hoffmann and colleagues report that the mammalian maternal-to-zygotic transition requires KDM4A-mediated removal of H3K9me3 from the broad H3K4me3 domains in oocytes. |
| Audience | Academic |
| Author | Lerdrup, Mads Johansen, Jens Vilstrup Blanshard, Robert Andersen, Claus Yding Dahl, John Arne Manaf, Adeel Hansen, Klaus Klungland, Arne Sankar, Aditya Helin, Kristian Hoffmann, Eva R. Gonzalez, Javier Martin Borup, Rehannah |
| AuthorAffiliation | 1 DNRF Centre for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark 8 Cell Biology Program and Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, USA 4 Department of Microbiology, Oslo University Hospital, Rikshospitalet, Norway 7 Laboratory of Reproductive Biology, Section 5712, University Hospital of Copenhagen, Denmark 6 Transgenic Core Facility, Department of Experimental Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark 5 Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo, NO-0317, Oslo, Norway 2 Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Denmark 3 The Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen, Denmark |
| AuthorAffiliation_xml | – name: 6 Transgenic Core Facility, Department of Experimental Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark – name: 1 DNRF Centre for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Denmark – name: 8 Cell Biology Program and Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center, New York, USA – name: 4 Department of Microbiology, Oslo University Hospital, Rikshospitalet, Norway – name: 7 Laboratory of Reproductive Biology, Section 5712, University Hospital of Copenhagen, Denmark – name: 3 The Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen, Denmark – name: 2 Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, Denmark – name: 5 Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo, NO-0317, Oslo, Norway |
| Author_xml | – sequence: 1 givenname: Aditya orcidid: 0000-0002-1840-3356 surname: Sankar fullname: Sankar, Aditya email: cnj376@ku.dk organization: DNRF Center for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, The Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen – sequence: 2 givenname: Mads orcidid: 0000-0002-7730-8973 surname: Lerdrup fullname: Lerdrup, Mads organization: DNRF Center for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen, Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 3 givenname: Adeel orcidid: 0000-0002-9958-8654 surname: Manaf fullname: Manaf, Adeel organization: Department of Microbiology, Oslo University Hospital – sequence: 4 givenname: Jens Vilstrup surname: Johansen fullname: Johansen, Jens Vilstrup organization: Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 5 givenname: Javier Martin surname: Gonzalez fullname: Gonzalez, Javier Martin organization: Transgenic Core Facility, Department of Experimental Medicine, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 6 givenname: Rehannah surname: Borup fullname: Borup, Rehannah organization: DNRF Center for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 7 givenname: Robert surname: Blanshard fullname: Blanshard, Robert organization: DNRF Center for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 8 givenname: Arne orcidid: 0000-0001-7274-3661 surname: Klungland fullname: Klungland, Arne organization: Department of Microbiology, Oslo University Hospital, Department of Molecular Medicine, Institute of Basic Medical Sciences, University of Oslo – sequence: 9 givenname: Klaus surname: Hansen fullname: Hansen, Klaus organization: Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen – sequence: 10 givenname: Claus Yding surname: Andersen fullname: Andersen, Claus Yding organization: Laboratory of Reproductive Biology, Section 5712, University Hospital of Copenhagen – sequence: 11 givenname: John Arne orcidid: 0000-0002-4375-2697 surname: Dahl fullname: Dahl, John Arne email: j.a.dahl@medisin.uio.no organization: Department of Microbiology, Oslo University Hospital – sequence: 12 givenname: Kristian orcidid: 0000-0003-1975-6097 surname: Helin fullname: Helin, Kristian email: kristian.helin@bric.ku.dk organization: Biotech Research Innovation Centre (BRIC), Faculty of Health and Medical Sciences, University of Copenhagen, The Novo Nordisk Foundation Center for Stem Cell Biology (DanStem), University of Copenhagen, Cell Biology Program and Center for Epigenetics Research, Memorial Sloan Kettering Cancer Center – sequence: 13 givenname: Eva R. orcidid: 0000-0002-2588-0652 surname: Hoffmann fullname: Hoffmann, Eva R. email: eva@sund.ku.dk organization: DNRF Center for Chromosome Stability (CCS), Department of Cellular and Molecular Medicine, Faculty of Health and Medical Sciences, University of Copenhagen |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32231309$$D View this record in MEDLINE/PubMed |
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| Snippet | The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging
1
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. Histone H3 lysine... The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging . Histone H3 lysine 9... The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging.sup.1-4. Histone H3... The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging1–4. Histone H3 lysine 9... The importance of germline-inherited post-translational histone modifications on priming early mammalian development is just emerging1-4. Histone H3 lysine 9... The importance of germline-inherited posttranslational histone modifications on priming early mammalian development is just emerging 1 – 4 . Histone H3 lysine... |
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| SubjectTerms | 14/1 14/19 14/34 38/1 38/91 45/15 45/91 631/136/2086 631/337/176 64/110 Animals Biomedical and Life Sciences Cancer Research Catalytic activity Cell Biology Demethylation Developmental Biology Domains Embryo Implantation Embryo, Mammalian Embryonic development Embryos Enzymes Epigenetic inheritance Epigenetics Female Fertilization Fertilization - genetics Gametocytes Genetic aspects Genetic research Genomes Heterochromatin Heterochromatin - chemistry Heterochromatin - metabolism Histone Demethylases - genetics Histone Demethylases - metabolism Histone H3 Histones Histones - genetics Histones - metabolism Hydrolases Implantation Letter Life Sciences Lysine Male Mammals Metaphase Methylation Mice Mice, Knockout Oocytes Oocytes - cytology Oocytes - growth & development Oocytes - metabolism Post-translation Post-translational modification Priming Promoter Regions, Genetic Protein Processing, Post-Translational Stem Cells Transcription activation Transcription, Genetic Zygote - cytology Zygote - growth & development Zygote - metabolism Zygotes |
| Title | KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes |
| URI | https://link.springer.com/article/10.1038/s41556-020-0494-z https://www.ncbi.nlm.nih.gov/pubmed/32231309 https://www.proquest.com/docview/2386859795 https://www.proquest.com/docview/2385268955 https://pubmed.ncbi.nlm.nih.gov/PMC7212036 |
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