KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes

Research output: Contribution to journalJournal articlepeer-review

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KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes. / Sankar, Aditya; Lerdrup, Mads; Manaf, Adeel; Johansen, Jens Vilstrup; Gonzalez, Javier Martin; Borup, Rehannah; Blanshard, Robert; Klungland, Arne; Hansen, Klaus; Andersen, Claus Yding; Dahl, John Arne; Helin, Kristian; Hoffmann, Eva R.

In: Nature Cell Biology, Vol. 22, No. 4, 2020, p. 380-388.

Research output: Contribution to journalJournal articlepeer-review

Harvard

Sankar, A, Lerdrup, M, Manaf, A, Johansen, JV, Gonzalez, JM, Borup, R, Blanshard, R, Klungland, A, Hansen, K, Andersen, CY, Dahl, JA, Helin, K & Hoffmann, ER 2020, 'KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes', Nature Cell Biology, vol. 22, no. 4, pp. 380-388. https://doi.org/10.1038/s41556-020-0494-z

APA

Sankar, A., Lerdrup, M., Manaf, A., Johansen, J. V., Gonzalez, J. M., Borup, R., Blanshard, R., Klungland, A., Hansen, K., Andersen, C. Y., Dahl, J. A., Helin, K., & Hoffmann, E. R. (2020). KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes. Nature Cell Biology, 22(4), 380-388. https://doi.org/10.1038/s41556-020-0494-z

Vancouver

Sankar A, Lerdrup M, Manaf A, Johansen JV, Gonzalez JM, Borup R et al. KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes. Nature Cell Biology. 2020;22(4):380-388. https://doi.org/10.1038/s41556-020-0494-z

Author

Sankar, Aditya ; Lerdrup, Mads ; Manaf, Adeel ; Johansen, Jens Vilstrup ; Gonzalez, Javier Martin ; Borup, Rehannah ; Blanshard, Robert ; Klungland, Arne ; Hansen, Klaus ; Andersen, Claus Yding ; Dahl, John Arne ; Helin, Kristian ; Hoffmann, Eva R. / KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes. In: Nature Cell Biology. 2020 ; Vol. 22, No. 4. pp. 380-388.

Bibtex

@article{3f837c1144314574899b23ae0b5f19ac,
title = "KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes",
abstract = "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.",
author = "Aditya Sankar and Mads Lerdrup and Adeel Manaf and Johansen, {Jens Vilstrup} and Gonzalez, {Javier Martin} and Rehannah Borup and Robert Blanshard and Arne Klungland and Klaus Hansen and Andersen, {Claus Yding} and Dahl, {John Arne} and Kristian Helin and Hoffmann, {Eva R}",
year = "2020",
doi = "10.1038/s41556-020-0494-z",
language = "English",
volume = "22",
pages = "380--388",
journal = "Nature Cell Biology",
issn = "1465-7392",
publisher = "nature publishing group",
number = "4",

}

RIS

TY - JOUR

T1 - KDM4A regulates the maternal-to-zygotic transition by protecting broad H3K4me3 domains from H3K9me3 invasion in oocytes

AU - Sankar, Aditya

AU - Lerdrup, Mads

AU - Manaf, Adeel

AU - Johansen, Jens Vilstrup

AU - Gonzalez, Javier Martin

AU - Borup, Rehannah

AU - Blanshard, Robert

AU - Klungland, Arne

AU - Hansen, Klaus

AU - Andersen, Claus Yding

AU - Dahl, John Arne

AU - Helin, Kristian

AU - Hoffmann, Eva R

PY - 2020

Y1 - 2020

N2 - 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.

AB - 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.

U2 - 10.1038/s41556-020-0494-z

DO - 10.1038/s41556-020-0494-z

M3 - Journal article

C2 - 32231309

VL - 22

SP - 380

EP - 388

JO - Nature Cell Biology

JF - Nature Cell Biology

SN - 1465-7392

IS - 4

ER -

ID: 239212054