DNMT3B PWWP mutations cause hypermethylation of heterochromatin

DNMT3B PWWP mutations cause hypermethylation of heterochromatin

The correct establishment of DNA methylation patterns is vital for mammalian development and is achieved by the de novo DNA methyltransferases DNMT3A and DNMT3B. DNMT3B localises to H3K36me3 at actively transcribing gene bodies via its PWWP domain. It also functions at heterochromatin through an unk...

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Published in:EMBO reports Vol. 25; no. 3; pp. 1130 - 1155
Main Authors: Taglini, Francesca, Kafetzopoulos, Ioannis, Rolls, Willow, Musialik, Kamila Irena, Lee, Heng Yang, Zhang, Yujie, Marenda, Mattia, Kerr, Lyndsay, Finan, Hannah, Rubio-Ramon, Cristina, Gautier, Philippe, Wapenaar, Hannah, Kumar, Dhananjay, Davidson-Smith, Hazel, Wills, Jimi, Murphy, Laura C, Wheeler, Ann, Wilson, Marcus D, Sproul, Duncan
Format: Journal Article
Language:English
Published: London Nature Publishing Group UK 12-03-2024
Subjects:
Biomedical and Life Sciences
EMBO09
Life Sciences
Epigenetics
DNA Methylation
Heterochromatin
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Abstract The correct establishment of DNA methylation patterns is vital for mammalian development and is achieved by the de novo DNA methyltransferases DNMT3A and DNMT3B. DNMT3B localises to H3K36me3 at actively transcribing gene bodies via its PWWP domain. It also functions at heterochromatin through an unknown recruitment mechanism. Here, we find that knockout of DNMT3B causes loss of methylation predominantly at H3K9me3-marked heterochromatin and that DNMT3B PWWP domain mutations or deletion result in striking increases of methylation in H3K9me3-marked heterochromatin. Removal of the N-terminal region of DNMT3B affects its ability to methylate H3K9me3-marked regions. This region of DNMT3B directly interacts with HP1α and facilitates the bridging of DNMT3B with H3K9me3-marked nucleosomes in vitro. Our results suggest that DNMT3B is recruited to H3K9me3-marked heterochromatin in a PWWP-independent manner that is facilitated by the protein’s N-terminal region through an interaction with a key heterochromatin protein. More generally, we suggest that DNMT3B plays a role in DNA methylation homeostasis at heterochromatin, a process which is disrupted in cancer, aging and Immunodeficiency, Centromeric Instability and Facial Anomalies (ICF) syndrome. Synopsis The DNA methyltransferase DNMT3B is recruited to gene bodies through its PWWP domain’s interaction with H3K36me3. This study shows DNMT3B PWWP mutations cause hypermethylation of H3K9me3-marked heterochromatin facilitated by DNMT3B’s N-terminal region. Removal of DNMT3B results in losses of DNA methylation from H3K9me3-methylated heterochromatin. Mutation or deletion of DNMT3B’s PWWP domain results in the hypermethylation of H3K9me3-marked heterochromatin. Recruitment of DNMT3B to H3K9me3 is facilitated by its N-terminal region, which interacts with HP1α. The DNA methyltransferase DNMT3B is recruited to gene bodies through its PWWP domain’s interaction with H3K36me3. This study shows DNMT3B PWWP mutations cause hypermethylation of H3K9me3-marked heterochromatin facilitated by DNMT3B’s N-terminal region.
AbstractList The correct establishment of DNA methylation patterns is vital for mammalian development and is achieved by the de novo DNA methyltransferases DNMT3A and DNMT3B. DNMT3B localises to H3K36me3 at actively transcribing gene bodies via its PWWP domain. It also functions at heterochromatin through an unknown recruitment mechanism. Here, we find that knockout of DNMT3B causes loss of methylation predominantly at H3K9me3-marked heterochromatin and that DNMT3B PWWP domain mutations or deletion result in striking increases of methylation in H3K9me3-marked heterochromatin. Removal of the N-terminal region of DNMT3B affects its ability to methylate H3K9me3-marked regions. This region of DNMT3B directly interacts with HP1α and facilitates the bridging of DNMT3B with H3K9me3-marked nucleosomes in vitro. Our results suggest that DNMT3B is recruited to H3K9me3-marked heterochromatin in a PWWP-independent manner that is facilitated by the protein's N-terminal region through an interaction with a key heterochromatin protein. More generally, we suggest that DNMT3B plays a role in DNA methylation homeostasis at heterochromatin, a process which is disrupted in cancer, aging and Immunodeficiency, Centromeric Instability and Facial Anomalies (ICF) syndrome.
The correct establishment of DNA methylation patterns is vital for mammalian development and is achieved by the de novo DNA methyltransferases DNMT3A and DNMT3B. DNMT3B localises to H3K36me3 at actively transcribing gene bodies via its PWWP domain. It also functions at heterochromatin through an unknown recruitment mechanism. Here, we find that knockout of DNMT3B causes loss of methylation predominantly at H3K9me3-marked heterochromatin and that DNMT3B PWWP domain mutations or deletion result in striking increases of methylation in H3K9me3-marked heterochromatin. Removal of the N-terminal region of DNMT3B affects its ability to methylate H3K9me3-marked regions. This region of DNMT3B directly interacts with HP1α and facilitates the bridging of DNMT3B with H3K9me3-marked nucleosomes in vitro. Our results suggest that DNMT3B is recruited to H3K9me3-marked heterochromatin in a PWWP-independent manner that is facilitated by the protein’s N-terminal region through an interaction with a key heterochromatin protein. More generally, we suggest that DNMT3B plays a role in DNA methylation homeostasis at heterochromatin, a process which is disrupted in cancer, aging and Immunodeficiency, Centromeric Instability and Facial Anomalies (ICF) syndrome. Synopsis The DNA methyltransferase DNMT3B is recruited to gene bodies through its PWWP domain’s interaction with H3K36me3. This study shows DNMT3B PWWP mutations cause hypermethylation of H3K9me3-marked heterochromatin facilitated by DNMT3B’s N-terminal region. Removal of DNMT3B results in losses of DNA methylation from H3K9me3-methylated heterochromatin. Mutation or deletion of DNMT3B’s PWWP domain results in the hypermethylation of H3K9me3-marked heterochromatin. Recruitment of DNMT3B to H3K9me3 is facilitated by its N-terminal region, which interacts with HP1α. The DNA methyltransferase DNMT3B is recruited to gene bodies through its PWWP domain’s interaction with H3K36me3. This study shows DNMT3B PWWP mutations cause hypermethylation of H3K9me3-marked heterochromatin facilitated by DNMT3B’s N-terminal region.
Author Sproul, Duncan
Lee, Heng Yang
Kerr, Lyndsay
Kumar, Dhananjay
Wapenaar, Hannah
Marenda, Mattia
Wills, Jimi
Kafetzopoulos, Ioannis
Zhang, Yujie
Davidson-Smith, Hazel
Wilson, Marcus D
Rolls, Willow
Rubio-Ramon, Cristina
Taglini, Francesca
Wheeler, Ann
Murphy, Laura C
Musialik, Kamila Irena
Finan, Hannah
Gautier, Philippe
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  surname: Kafetzopoulos
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, CRUK Edinburgh Centre, Institute of Genetics and Cancer, University of Edinburgh, Altos Labs, Cambridge Institute
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  givenname: Willow
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, Wellcome Centre for Cell Biology, University of Edinburgh
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  givenname: Kamila Irena
  orcidid: 0000-0003-2543-5011
  surname: Musialik
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, CRUK Edinburgh Centre, Institute of Genetics and Cancer, University of Edinburgh, MRC London Institute of Medical Sciences and Institute of Clinical Sciences, Imperial College London
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  givenname: Heng Yang
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  surname: Lee
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, CRUK Edinburgh Centre, Institute of Genetics and Cancer, University of Edinburgh, Endocrine Oncology Research Group, Department of Surgery, The Royal College of Surgeons RCSI, University of Medicine and Health Sciences
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  surname: Zhang
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  organization: Wellcome Centre for Cell Biology, University of Edinburgh
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  organization: IEO, European Institute of Oncology IRCCS, Department of Experimental Oncology
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  surname: Rubio-Ramon
  fullname: Rubio-Ramon, Cristina
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  surname: Wapenaar
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  organization: Wellcome Centre for Cell Biology, University of Edinburgh
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  surname: Wills
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  organization: MRC Human Genetics Unit, Institute of Genetics and Cancer, University of Edinburgh, CRUK Edinburgh Centre, Institute of Genetics and Cancer, University of Edinburgh
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Issue 3
Keywords Epigenetics
DNA Methylation
Heterochromatin
Language English
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Present address: Université Paris Cité, CNRS, Institut Jacques Monod, Paris, France.
Present address: Endocrine Oncology Research Group, Department of Surgery, The Royal College of Surgeons RCSI, University of Medicine and Health Sciences, Dublin, Ireland.
Present address: MRC London Institute of Medical Sciences and Institute of Clinical Sciences, Imperial College London, London, UK.
Present address: Altos Labs, Cambridge Institute, Cambridge, UK.
Present address: Department of Mathematics and Statistics, University of Strathclyde, Glasgow, UK.
Present address: Swiss Federal Institute of Technology, ETH Zürich, Institute of Molecular Health Sciences, Zürich, Switzerland.
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  ident: 61_CR84
  publication-title: Cell
  doi: 10.1016/j.cell.2017.04.022
  contributor:
    fullname: B van Steensel
SSID ssj0005978
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Snippet The correct establishment of DNA methylation patterns is vital for mammalian development and is achieved by the de novo DNA methyltransferases DNMT3A and...
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pubmed
springer
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SubjectTerms Biomedical and Life Sciences
EMBO09
Life Sciences
Title DNMT3B PWWP mutations cause hypermethylation of heterochromatin
URI https://link.springer.com/article/10.1038/s44319-024-00061-5
https://www.ncbi.nlm.nih.gov/pubmed/38291337
https://search.proquest.com/docview/2920572009
https://pubmed.ncbi.nlm.nih.gov/PMC7615734
Volume 25
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