IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v13y2022i1d10.1038_s41467-022-35417-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-022-35417-9
    File Function: Abstract
    Download Restriction: no
    File URL: https://libkey.io/10.1038/s41467-022-35417-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    1. 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.
    2. 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.
    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.
    Full references (including those not matched with items on IDEAS)

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Yupu Wang & Ruiling Zhang & Sihao Huang & Parisa Tajalli Tehrani Valverde & Meike Lobb-Rabe & James Ashley & Lalanti Venkatasubramanian & Robert A. Carrillo, 2023. "Glial Draper signaling triggers cross-neuron plasticity in bystander neurons after neuronal cell death in Drosophila," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-022-35417-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.