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Opposing LSD1 complexes function in developmental gene activation and repression programmes

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  • Jianxun Wang

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA
    Molecular Pathology Graduate Program,)

  • Kathleen Scully

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Xiaoyan Zhu

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Ling Cai

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA
    Department of Biology Graduate Program,)

  • Jie Zhang

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Gratien G. Prefontaine

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Anna Krones

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Kenneth A. Ohgi

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Ping Zhu

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Ivan Garcia-Bassets

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Forrest Liu

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Havilah Taylor

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

  • Jean Lozach

    (University of California, San Diego, La Jolla, California 92093, USA)

  • Friederike L. Jayes

    (National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, USA)

  • Kenneth S. Korach

    (National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, USA)

  • Christopher K. Glass

    (University of California, San Diego, La Jolla, California 92093, USA)

  • Xiang-Dong Fu

    (University of California, San Diego, La Jolla, California 92093, USA)

  • Michael G. Rosenfeld

    (Howard Hughes Medical Institute, University of California, San Diego, 9500 Gilman Drive, Room 345, La Jolla, California 92093-0648, USA)

Abstract

Precise control of transcriptional programmes underlying metazoan development is modulated by enzymatically active co-regulatory complexes, coupled with epigenetic strategies. One thing that remains unclear is how specific members of histone modification enzyme families, such as histone methyltransferases and demethylases, are used in vivo to simultaneously orchestrate distinct developmental gene activation and repression programmes. Here, we report that the histone lysine demethylase, LSD1—a component of the CoREST-CtBP co-repressor complex—is required for late cell-lineage determination and differentiation during pituitary organogenesis. LSD1 seems to act primarily on target gene activation programmes, as well as in gene repression programmes, on the basis of recruitment of distinct LSD1-containing co-activator or co-repressor complexes. LSD1-dependent gene repression programmes can be extended late in development with the induced expression of ZEB1, a Krüppel-like repressor that can act as a molecular beacon for recruitment of the LSD1-containing CoREST-CtBP co-repressor complex, causing repression of an additional cohort of genes, such as Gh, which previously required LSD1 for activation. These findings suggest that temporal patterns of expression of specific components of LSD1 complexes modulate gene regulatory programmes in many mammalian organs.

Suggested Citation

  • Jianxun Wang & Kathleen Scully & Xiaoyan Zhu & Ling Cai & Jie Zhang & Gratien G. Prefontaine & Anna Krones & Kenneth A. Ohgi & Ping Zhu & Ivan Garcia-Bassets & Forrest Liu & Havilah Taylor & Jean Loza, 2007. "Opposing LSD1 complexes function in developmental gene activation and repression programmes," Nature, Nature, vol. 446(7138), pages 882-887, April.
  • Handle: RePEc:nat:nature:v:446:y:2007:i:7138:d:10.1038_nature05671
    DOI: 10.1038/nature05671
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    Cited by:

    1. Cheng Zeng & Jiwei Chen & Emmalee W. Cooke & Arijita Subuddhi & Eliana T. Roodman & Fei Xavier Chen & Kaixiang Cao, 2023. "Demethylase-independent roles of LSD1 in regulating enhancers and cell fate transition," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Beatriz del Blanco & Sergio Niñerola & Ana M. Martín-González & Juan Paraíso-Luna & Minji Kim & Rafael Muñoz-Viana & Carina Racovac & Jose V. Sanchez-Mut & Yijun Ruan & Ángel Barco, 2024. "Kdm1a safeguards the topological boundaries of PRC2-repressed genes and prevents aging-related euchromatinization in neurons," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    3. Pengfei Guo & Nam Hoang & Joseph Sanchez & Elaine H. Zhang & Keshari Rajawasam & Kristiana Trinidad & Hong Sun & Hui Zhang, 2022. "The assembly of mammalian SWI/SNF chromatin remodeling complexes is regulated by lysine-methylation dependent proteolysis," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    4. Sandhya Malla & Kanchan Kumari & Carlos A. García-Prieto & Jonatan Caroli & Anna Nordin & Trinh T. T. Phan & Devi Prasad Bhattarai & Carlos Martinez-Gamero & Eshagh Dorafshan & Stephanie Stransky & Da, 2024. "The scaffolding function of LSD1 controls DNA methylation in mouse ESCs," Nature Communications, Nature, vol. 15(1), pages 1-24, December.
    5. Tiantian Jing & Dianhui Wei & Xiaoli Xu & Chengsi Wu & Lili Yuan & Yiwen Huang & Yizhen Liu & Yanyi Jiang & Boshi Wang, 2024. "Transposable elements-mediated recruitment of KDM1A epigenetically silences HNF4A expression to promote hepatocellular carcinoma," Nature Communications, Nature, vol. 15(1), pages 1-21, December.

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