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Epigenetic regulation of the circadian gene Per1 contributes to age-related changes in hippocampal memory

Author

Listed:
  • Janine L. Kwapis

    (University of California
    Center for the Neurobiology of Learning and Memory
    University of California)

  • Yasaman Alaghband

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Enikö A. Kramár

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Alberto J. López

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Annie Vogel Ciernia

    (University of California)

  • André O. White

    (Mount Holyoke College)

  • Guanhua Shu

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Diane Rhee

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Christina M. Michael

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Emilie Montellier

    (University of California)

  • Yu Liu

    (University of California
    University of California)

  • Christophe N. Magnan

    (University of California
    University of California)

  • Siwei Chen

    (University of California
    University of California)

  • Paolo Sassone-Corsi

    (University of California)

  • Pierre Baldi

    (University of California
    University of California)

  • Dina P. Matheos

    (University of California
    Center for the Neurobiology of Learning and Memory)

  • Marcelo A. Wood

    (University of California
    Center for the Neurobiology of Learning and Memory
    University of California)

Abstract

Aging is accompanied by impairments in both circadian rhythmicity and long-term memory. Although it is clear that memory performance is affected by circadian cycling, it is unknown whether age-related disruption of the circadian clock causes impaired hippocampal memory. Here, we show that the repressive histone deacetylase HDAC3 restricts long-term memory, synaptic plasticity, and experience-induced expression of the circadian gene Per1 in the aging hippocampus without affecting rhythmic circadian activity patterns. We also demonstrate that hippocampal Per1 is critical for long-term memory formation. Together, our data challenge the traditional idea that alterations in the core circadian clock drive circadian-related changes in memory formation and instead argue for a more autonomous role for circadian clock gene function in hippocampal cells to gate the likelihood of long-term memory formation.

Suggested Citation

  • Janine L. Kwapis & Yasaman Alaghband & Enikö A. Kramár & Alberto J. López & Annie Vogel Ciernia & André O. White & Guanhua Shu & Diane Rhee & Christina M. Michael & Emilie Montellier & Yu Liu & Christ, 2018. "Epigenetic regulation of the circadian gene Per1 contributes to age-related changes in hippocampal memory," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
    • Handle: RePEc:nat:natcom:v:9:y:2018:i:1:d:10.1038_s41467-018-05868-0
    DOI: 10.1038/s41467-018-05868-0
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    Cited by:

    1. Yann Vanrobaeys & Utsav Mukherjee & Lucy Langmack & Stacy E. Beyer & Ethan Bahl & Li-Chun Lin & Jacob J. Michaelson & Ted Abel & Snehajyoti Chatterjee, 2023. "Mapping the spatial transcriptomic signature of the hippocampus during memory consolidation," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    2. Pengfei Lv & Xingzhuo Yang & Juan Du, 2024. "LKRSDH-dependent histone modifications of insulin-like peptide sites contribute to age-related circadian rhythm changes," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    3. Dominik Saul & Robyn Laura Kosinsky & Elizabeth J. Atkinson & Madison L. Doolittle & Xu Zhang & Nathan K. LeBrasseur & Robert J. Pignolo & Paul D. Robbins & Laura J. Niedernhofer & Yuji Ikeno & Diana , 2022. "A new gene set identifies senescent cells and predicts senescence-associated pathways across tissues," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Ashley A. Keiser & Tri N. Dong & Enikö A. Kramár & Christopher W. Butler & Siwei Chen & Dina P. Matheos & Jacob S. Rounds & Alyssa Rodriguez & Joy H. Beardwood & Agatha S. Augustynski & Ameer Al-Shamm, 2024. "Specific exercise patterns generate an epigenetic molecular memory window that drives long-term memory formation and identifies ACVR1C as a bidirectional regulator of memory in mice," Nature Communications, Nature, vol. 15(1), pages 1-16, December.

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