Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly
SUV39H is the major histone H3 lysine 9 (H3K9)-specific methyltransferase that targets pericentric regions and is crucial for assembling silent heterochromatin. SUV39H recognizes trimethylated H3K9 (H3K9me3) via its chromodomain (CD), and enriched H3K9me3 allows SUV39H to target specific chromosomal...
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2017-08-01
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| Series: | eLife |
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| Online Access: | https://elifesciences.org/articles/25317 |
| _version_ | 1811253217130971136 |
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| author | Atsuko Shirai Takayuki Kawaguchi Hideaki Shimojo Daisuke Muramatsu Mayumi Ishida-Yonetani Yoshifumi Nishimura Hiroshi Kimura Jun-ichi Nakayama Yoichi Shinkai |
| author_facet | Atsuko Shirai Takayuki Kawaguchi Hideaki Shimojo Daisuke Muramatsu Mayumi Ishida-Yonetani Yoshifumi Nishimura Hiroshi Kimura Jun-ichi Nakayama Yoichi Shinkai |
| author_sort | Atsuko Shirai |
| collection | DOAJ |
| description | SUV39H is the major histone H3 lysine 9 (H3K9)-specific methyltransferase that targets pericentric regions and is crucial for assembling silent heterochromatin. SUV39H recognizes trimethylated H3K9 (H3K9me3) via its chromodomain (CD), and enriched H3K9me3 allows SUV39H to target specific chromosomal regions. However, the detailed targeting mechanisms, especially for naïve chromatin without preexisting H3K9me3, are poorly understood. Here we show that Suv39h1’s CD (Suv39h1-CD) binds nucleic acids, and this binding is important for its function in heterochromatin assembly. Suv39h1-CD had higher binding affinity for RNA than DNA, and its ability to bind nucleic acids was independent of its H3K9me3 recognition. Suv39h1 bound major satellite RNAs in vivo, and knockdown of major satellite RNAs lowered Suv39h1 retention on pericentromere. Suv39h1 mutational studies indicated that both the nucleic acid–binding and H3K9me–binding activities of Suv39h1-CD were crucial for its pericentric heterochromatin assembly. These results suggest that chromatin-bound RNAs contribute to creating SUV39H’s target specificity. |
| first_indexed | 2024-04-12T16:46:36Z |
| format | Article |
| id | doaj.art-e66d8fc36bc849bc80e73bd16c0f8cdd |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:46:36Z |
| publishDate | 2017-08-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-e66d8fc36bc849bc80e73bd16c0f8cdd2022-12-22T03:24:33ZengeLife Sciences Publications LtdeLife2050-084X2017-08-01610.7554/eLife.25317Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assemblyAtsuko Shirai0https://orcid.org/0000-0003-1344-4746Takayuki Kawaguchi1Hideaki Shimojo2Daisuke Muramatsu3Mayumi Ishida-Yonetani4Yoshifumi Nishimura5Hiroshi Kimura6https://orcid.org/0000-0003-0854-083XJun-ichi Nakayama7https://orcid.org/0000-0002-5597-8239Yoichi Shinkai8https://orcid.org/0000-0002-6051-2484Cellular Memory Laboratory, RIKEN, Wako, JapanDivision of Chromatin Regulation, National Institute for Basic Biology, Okazaki, Japan; Graduate School of Natural Sciences, Nagoya City University, Nagoya, JapanGraduate School of Medical Life Science, Yokohama City University, Yokohama, JapanCellular Memory Laboratory, RIKEN, Wako, JapanLaboratory for Chromatin Dynamics, RIKEN Center for Developmental Biology, Kobe, JapanGraduate School of Medical Life Science, Yokohama City University, Yokohama, JapanCell Biology Unit, Institute of Innovative Research, Tokyo Institute of Technology, Yokohama, JapanDivision of Chromatin Regulation, National Institute for Basic Biology, Okazaki, Japan; Graduate School of Natural Sciences, Nagoya City University, Nagoya, JapanCellular Memory Laboratory, RIKEN, Wako, JapanSUV39H is the major histone H3 lysine 9 (H3K9)-specific methyltransferase that targets pericentric regions and is crucial for assembling silent heterochromatin. SUV39H recognizes trimethylated H3K9 (H3K9me3) via its chromodomain (CD), and enriched H3K9me3 allows SUV39H to target specific chromosomal regions. However, the detailed targeting mechanisms, especially for naïve chromatin without preexisting H3K9me3, are poorly understood. Here we show that Suv39h1’s CD (Suv39h1-CD) binds nucleic acids, and this binding is important for its function in heterochromatin assembly. Suv39h1-CD had higher binding affinity for RNA than DNA, and its ability to bind nucleic acids was independent of its H3K9me3 recognition. Suv39h1 bound major satellite RNAs in vivo, and knockdown of major satellite RNAs lowered Suv39h1 retention on pericentromere. Suv39h1 mutational studies indicated that both the nucleic acid–binding and H3K9me–binding activities of Suv39h1-CD were crucial for its pericentric heterochromatin assembly. These results suggest that chromatin-bound RNAs contribute to creating SUV39H’s target specificity.https://elifesciences.org/articles/25317Suv39h1chromodomainHP1pericentromereheterochromatinH3K9 methylation |
| spellingShingle | Atsuko Shirai Takayuki Kawaguchi Hideaki Shimojo Daisuke Muramatsu Mayumi Ishida-Yonetani Yoshifumi Nishimura Hiroshi Kimura Jun-ichi Nakayama Yoichi Shinkai Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly eLife Suv39h1 chromodomain HP1 pericentromere heterochromatin H3K9 methylation |
| title | Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly |
| title_full | Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly |
| title_fullStr | Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly |
| title_full_unstemmed | Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly |
| title_short | Impact of nucleic acid and methylated H3K9 binding activities of Suv39h1 on its heterochromatin assembly |
| title_sort | impact of nucleic acid and methylated h3k9 binding activities of suv39h1 on its heterochromatin assembly |
| topic | Suv39h1 chromodomain HP1 pericentromere heterochromatin H3K9 methylation |
| url | https://elifesciences.org/articles/25317 |
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