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A glutamate receptor C-tail recruits CaMKII to suppress retrograde homeostatic signaling

Author

Listed:
  • Sarah Perry

    (University of Southern California)

  • Yifu Han

    (University of Southern California)

  • Chengjie Qiu

    (University of Southern California)

  • Chun Chien

    (University of Southern California)

  • Pragya Goel

    (University of Southern California)

  • Samantha Nishimura

    (University of Southern California)

  • Manisha Sajnani

    (University of Southern California)

  • Andreas Schmid

    (Freie Universität Berlin
    Albstadt-Sigmaringen University)

  • Stephan J. Sigrist

    (Freie Universität Berlin
    NeuroCure Cluster of Excellence, Charité Universitätsmedizin)

  • Dion Dickman

    (University of Southern California)

Abstract

Presynaptic homeostatic plasticity (PHP) adaptively enhances neurotransmitter release following diminished postsynaptic glutamate receptor (GluR) functionality to maintain synaptic strength. While much is known about PHP expression mechanisms, postsynaptic induction remains enigmatic. For over 20 years, diminished postsynaptic Ca2+ influx was hypothesized to reduce CaMKII activity and enable retrograde PHP signaling at the Drosophila neuromuscular junction. Here, we have interrogated inductive signaling and find that active CaMKII colocalizes with and requires the GluRIIA receptor subunit. Next, we generated Ca2+-impermeable GluRs to reveal that both CaMKII activity and PHP induction are Ca2+-insensitive. Rather, a GluRIIA C-tail domain is necessary and sufficient to recruit active CaMKII. Finally, chimeric receptors demonstrate that the GluRIIA tail constitutively occludes retrograde homeostatic signaling by stabilizing active CaMKII. Thus, the physical loss of the GluRIIA tail is sensed, rather than reduced Ca2+, to enable retrograde PHP signaling, highlighting a unique, Ca2+-independent control mechanism for CaMKII in gating homeostatic plasticity.

Suggested Citation

  • Sarah Perry & Yifu Han & Chengjie Qiu & Chun Chien & Pragya Goel & Samantha Nishimura & Manisha Sajnani & Andreas Schmid & Stephan J. Sigrist & Dion Dickman, 2022. "A glutamate receptor C-tail recruits CaMKII to suppress retrograde homeostatic signaling," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35417-9
    DOI: 10.1038/s41467-022-35417-9
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    References listed on IDEAS

    as
    1. Koto Kikuma & Xiling Li & Sarah Perry & Qiuling Li & Pragya Goel & Catherine Chen & Daniel Kim & Nicholas Stavropoulos & Dion Dickman, 2019. "Cul3 and insomniac are required for rapid ubiquitination of postsynaptic targets and retrograde homeostatic signaling," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    2. Brian O. Orr & Richard D. Fetter & Graeme W. Davis, 2017. "Retrograde semaphorin–plexin signalling drives homeostatic synaptic plasticity," Nature, Nature, vol. 550(7674), pages 109-113, October.
    3. Jay Penney & Kazuya Tsurudome & Edward H. Liao & Grant Kauwe & Lindsay Gray & Akiko Yanagiya & Mario R. Calderon & Nahum Sonenberg & A. Pejmun Haghighi, 2016. "LRRK2 regulates retrograde synaptic compensation at the Drosophila neuromuscular junction," Nature Communications, Nature, vol. 7(1), pages 1-14, November.
    4. Melissa B. Ramocki & Huda Y. Zoghbi, 2008. "Failure of neuronal homeostasis results in common neuropsychiatric phenotypes," Nature, Nature, vol. 455(7215), pages 912-918, October.
    5. Pragya Goel & Dion Dickman, 2018. "Distinct homeostatic modulations stabilize reduced postsynaptic receptivity in response to presynaptic DLK signaling," Nature Communications, Nature, vol. 9(1), pages 1-14, December.
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