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Systematic characterization of chromodomain proteins reveals an H3K9me1/2 reader regulating aging in C. elegans

Author

Listed:
  • Xinhao Hou

    (University of Science and Technology of China)

  • Mingjing Xu

    (University of Science and Technology of China)

  • Chengming Zhu

    (University of Science and Technology of China)

  • Jianing Gao

    (University of Science and Technology of China)

  • Meili Li

    (University of Science and Technology of China)

  • Xiangyang Chen

    (University of Science and Technology of China)

  • Cheng Sun

    (University of Science and Technology of China)

  • Björn Nashan

    (University of Science and Technology of China)

  • Jianye Zang

    (University of Science and Technology of China)

  • Ying Zhou

    (University of Science and Technology of China)

  • Shouhong Guang

    (University of Science and Technology of China
    Chinese Academy of Sciences)

  • Xuezhu Feng

    (University of Science and Technology of China)

Abstract

The chromatin organization modifier domain (chromodomain) is an evolutionally conserved motif across eukaryotic species. The chromodomain mainly functions as a histone methyl-lysine reader to modulate gene expression, chromatin spatial conformation and genome stability. Mutations or aberrant expression of chromodomain proteins can result in cancer and other human diseases. Here, we systematically tag chromodomain proteins with green fluorescent protein (GFP) using CRISPR/Cas9 technology in C. elegans. By combining ChIP-seq analysis and imaging, we delineate a comprehensive expression and functional map of chromodomain proteins. We then conduct a candidate-based RNAi screening and identify factors that regulate the expression and subcellular localization of the chromodomain proteins. Specifically, we reveal an H3K9me1/2 reader, CEC-5, both by in vitro biochemistry and in vivo ChIP assays. MET-2, an H3K9me1/2 writer, is required for CEC-5 association with heterochromatin. Both MET-2 and CEC-5 are required for the normal lifespan of C. elegans. Furthermore, a forward genetic screening identifies a conserved Arginine124 of CEC-5’s chromodomain, which is essential for CEC-5’s association with chromatin and life span regulation. Thus, our work will serve as a reference to explore chromodomain functions and regulation in C. elegans and allow potential applications in aging-related human diseases.

Suggested Citation

  • Xinhao Hou & Mingjing Xu & Chengming Zhu & Jianing Gao & Meili Li & Xiangyang Chen & Cheng Sun & Björn Nashan & Jianye Zang & Ying Zhou & Shouhong Guang & Xuezhu Feng, 2023. "Systematic characterization of chromodomain proteins reveals an H3K9me1/2 reader regulating aging in C. elegans," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-36898-y
    DOI: 10.1038/s41467-023-36898-y
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    References listed on IDEAS

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    1. Daphne S. Cabianca & Celia Muñoz-Jiménez & Véronique Kalck & Dimos Gaidatzis & Jan Padeken & Andrew Seeber & Peter Askjaer & Susan M. Gasser, 2019. "Active chromatin marks drive spatial sequestration of heterochromatin in C. elegans nuclei," Nature, Nature, vol. 569(7758), pages 734-739, May.
    2. Eric L. Greer & Travis J. Maures & Anna G. Hauswirth & Erin M. Green & Dena S. Leeman & Géraldine S. Maro & Shuo Han & Max R. Banko & Or Gozani & Anne Brunet, 2010. "Members of the H3K4 trimethylation complex regulate lifespan in a germline-dependent manner in C. elegans," Nature, Nature, vol. 466(7304), pages 383-387, July.
    3. Eric L. Greer & Travis J. Maures & Duygu Ucar & Anna G. Hauswirth & Elena Mancini & Jana P. Lim & Bérénice A. Benayoun & Yang Shi & Anne Brunet, 2011. "Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans," Nature, Nature, vol. 479(7373), pages 365-371, November.
    4. 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.
    5. Susan E. Celniker & Laura A. L. Dillon & Mark B. Gerstein & Kristin C. Gunsalus & Steven Henikoff & Gary H. Karpen & Manolis Kellis & Eric C. Lai & Jason D. Lieb & David M. MacAlpine & Gos Micklem & F, 2009. "Unlocking the secrets of the genome," Nature, Nature, vol. 459(7249), pages 927-930, June.
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