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Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain

Author

Listed:
  • Andrew J. Bannister

    (University of Cambridge)

  • Philip Zegerman

    (University of Cambridge)

  • Janet F. Partridge

    (MRC Human Genetics Unit, Western General Hospital)

  • Eric A. Miska

    (University of Cambridge)

  • Jean O. Thomas

    (University of Cambridge)

  • Robin C. Allshire

    (MRC Human Genetics Unit, Western General Hospital)

  • Tony Kouzarides

    (University of Cambridge)

Abstract

Heterochromatin protein 1 (HP1) is localized at heterochromatin sites where it mediates gene silencing1,2. The chromo domain of HP1 is necessary for both targeting and transcriptional repression3,4. In the fission yeast Schizosaccharomyces pombe, the correct localization of Swi6 (the HP1 equivalent) depends on Clr4, a homologue of the mammalian SUV39H1 histone methylase5,6. Both Clr4 and SUV39H1 methylate specifically lysine 9 of histone H3 (ref. 6). Here we show that HP1 can bind with high affinity to histone H3 methylated at lysine 9 but not at lysine 4. The chromo domain of HP1 is identified as its methyl-lysine-binding domain. A point mutation in the chromo domain, which destroys the gene silencing activity of HP1 in Drosophila3, abolishes methyl-lysine-binding activity. Genetic and biochemical analysis in S. pombe shows that the methylase activity of Clr4 is necessary for the correct localization of Swi6 at centromeric heterochromatin and for gene silencing. These results provide a stepwise model for the formation of a transcriptionally silent heterochromatin: SUV39H1 places a ‘methyl marker’ on histone H3, which is then recognized by HP1 through its chromo domain. This model may also explain the stable inheritance of the heterochromatic state.

Suggested Citation

  • Andrew J. Bannister & Philip Zegerman & Janet F. Partridge & Eric A. Miska & Jean O. Thomas & Robin C. Allshire & Tony Kouzarides, 2001. "Selective recognition of methylated lysine 9 on histone H3 by the HP1 chromo domain," Nature, Nature, vol. 410(6824), pages 120-124, March.
    • Handle: RePEc:nat:nature:v:410:y:2001:i:6824:d:10.1038_35065138
    DOI: 10.1038/35065138
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    Cited by:

    1. Naohiro Kuwayama & Tomoya Kujirai & Yusuke Kishi & Rina Hirano & Kenta Echigoya & Lingyan Fang & Sugiko Watanabe & Mitsuyoshi Nakao & Yutaka Suzuki & Kei-ichiro Ishiguro & Hitoshi Kurumizaka & Yukiko , 2023. "HMGA2 directly mediates chromatin condensation in association with neuronal fate regulation," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    2. Hyun-Soo Kim & Benjamin Roche & Sonali Bhattacharjee & Leila Todeschini & An-Yun Chang & Christopher Hammell & André Verdel & Robert A. Martienssen, 2024. "Clr4SUV39H1 ubiquitination and non-coding RNA mediate transcriptional silencing of heterochromatin via Swi6 phase separation," Nature Communications, Nature, vol. 15(1), pages 1-14, December.
    3. Zengyu Shao & Jiuwei Lu & Nelli Khudaverdyan & Jikui Song, 2024. "Multi-layered heterochromatin interaction as a switch for DIM2-mediated DNA methylation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Joke J F A van Vugt & Martijn de Jager & Magdalena Murawska & Alexander Brehm & John van Noort & Colin Logie, 2009. "Multiple Aspects of ATP-Dependent Nucleosome Translocation by RSC and Mi-2 Are Directed by the Underlying DNA Sequence," PLOS ONE, Public Library of Science, vol. 4(7), pages 1-14, July.
    5. Clara Lopes Novo & Emily V. Wong & Colin Hockings & Chetan Poudel & Eleanor Sheekey & Meike Wiese & Hanneke Okkenhaug & Simon J. Boulton & Srinjan Basu & Simon Walker & Gabriele S. Kaminski Schierle &, 2022. "Satellite repeat transcripts modulate heterochromatin condensates and safeguard chromosome stability in mouse embryonic stem cells," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    6. Amanda Ames & Melissa Seman & Ajay Larkin & Gulzhan Raiymbek & Ziyuan Chen & Alex Levashkevich & Bokyung Kim & Julie Suzanne Biteen & Kaushik Ragunathan, 2024. "Epigenetic memory is governed by an effector recruitment specificity toggle in Heterochromatin Protein 1," Nature Communications, Nature, vol. 15(1), pages 1-17, December.

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