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

Sarah Perry, Yifu Han, Chengjie Qiu, Chun Chien, Pragya Goel, Samantha Nishimura, Manisha Sajnani, Andreas Schmid, Stephan J. Sigrist and Dion Dickman ()
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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
Stephan J. Sigrist: Freie Universität Berlin
Dion Dickman: University of Southern California

Nature Communications, 2022, vol. 13, issue 1, 1-16

Abstract: 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.

Date: 2022
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DOI: 10.1038/s41467-022-35417-9

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