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ASH1L-MRG15 methyltransferase deposits H3K4me3 and FACT for damage verification in nucleotide excision repair

Author

Listed:
  • Corina Maritz

    (University of Zurich-Vetsuisse)

  • Reihaneh Khaleghi

    (University of Zurich-Vetsuisse)

  • Michelle N. Yancoskie

    (University of Zurich-Vetsuisse)

  • Sarah Diethelm

    (University of Zurich-Vetsuisse)

  • Sonja Brülisauer

    (University of Zurich-Vetsuisse)

  • Natalia Santos Ferreira

    (University of Zurich-Vetsuisse)

  • Yang Jiang

    (ETH Zurich)

  • Shana J. Sturla

    (ETH Zurich)

  • Hanspeter Naegeli

    (University of Zurich-Vetsuisse)

Abstract

To recognize DNA adducts, nucleotide excision repair (NER) deploys the XPC sensor, which detects damage-induced helical distortions, followed by engagement of TFIIH for lesion verification. Accessory players ensure that this factor handover takes place in chromatin where DNA is tightly wrapped around histones. Here, we describe how the histone methyltransferase ASH1L, once activated by MRG15, helps XPC and TFIIH to navigate through chromatin and induce global-genome NER hotspots. Upon UV irradiation, ASH1L adds H3K4me3 all over the genome (except in active gene promoters), thus priming chromatin for XPC relocations from native to damaged DNA. The ASH1L-MRG15 complex further recruits the histone chaperone FACT to DNA lesions. In the absence of ASH1L, MRG15 or FACT, XPC is misplaced and persists on damaged DNA without being able to deliver the lesions to TFIIH. We conclude that ASH1L-MRG15 makes damage verifiable by the NER machinery through the sequential deposition of H3K4me3 and FACT.

Suggested Citation

  • Corina Maritz & Reihaneh Khaleghi & Michelle N. Yancoskie & Sarah Diethelm & Sonja Brülisauer & Natalia Santos Ferreira & Yang Jiang & Shana J. Sturla & Hanspeter Naegeli, 2023. "ASH1L-MRG15 methyltransferase deposits H3K4me3 and FACT for damage verification in nucleotide excision repair," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39635-7
    DOI: 10.1038/s41467-023-39635-7
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    References listed on IDEAS

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    1. Marilyn G. Pray-Grant & Jeremy A. Daniel & David Schieltz & John R. Yates & Patrick A. Grant, 2005. "Chd1 chromodomain links histone H3 methylation with SAGA- and SLIK-dependent acetylation," Nature, Nature, vol. 433(7024), pages 434-438, January.
    2. Chang Huang & Fu Yang & Zhuqiang Zhang & Jing Zhang & Gaihong Cai & Lin Li & Yong Zheng & She Chen & Rongwen Xi & Bing Zhu, 2017. "Mrg15 stimulates Ash1 H3K36 methyltransferase activity and facilitates Ash1 Trithorax group protein function in Drosophila," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
    3. Jung-Hyun Min & Nikola P. Pavletich, 2007. "Recognition of DNA damage by the Rad4 nucleotide excision repair protein," Nature, Nature, vol. 449(7162), pages 570-575, October.
    4. Syota Matsumoto & Simone Cavadini & Richard D. Bunker & Ralph S. Grand & Alessandro Potenza & Julius Rabl & Junpei Yamamoto & Andreas D. Schenk & Dirk Schübeler & Shigenori Iwai & Kaoru Sugasawa & Hit, 2019. "DNA damage detection in nucleosomes involves DNA register shifting," Nature, Nature, vol. 571(7763), pages 79-84, July.
    5. Syota Matsumoto & Simone Cavadini & Richard D. Bunker & Ralph S. Grand & Alessandro Potenza & Julius Rabl & Junpei Yamamoto & Andreas D. Schenk & Dirk Schübeler & Shigenori Iwai & Kaoru Sugasawa & Hit, 2019. "Publisher Correction: DNA damage detection in nucleosomes involves DNA register shifting," Nature, Nature, vol. 571(7764), pages 6-6, July.
    6. John F. Flanagan & Li-Zhi Mi & Maksymilian Chruszcz & Marcin Cymborowski & Katrina L. Clines & Youngchang Kim & Wladek Minor & Fraydoon Rastinejad & Sepideh Khorasanizadeh, 2005. "Double chromodomains cooperate to recognize the methylated histone H3 tail," Nature, Nature, vol. 438(7071), pages 1181-1185, December.
    7. Trevor van Eeuwen & Yoonjung Shim & Hee Jong Kim & Tingting Zhao & Shrabani Basu & Benjamin A. Garcia & Craig D. Kaplan & Jung-Hyun Min & Kenji Murakami, 2021. "Cryo-EM structure of TFIIH/Rad4–Rad23–Rad33 in damaged DNA opening in nucleotide excision repair," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    8. Chiara Balbo Pogliano & Marco Gatti & Peter Rüthemann & Zuzana Garajovà & Lorenza Penengo & Hanspeter Naegeli, 2017. "ASH1L histone methyltransferase regulates the handoff between damage recognition factors in global-genome nucleotide excision repair," Nature Communications, Nature, vol. 8(1), pages 1-13, December.
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