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Phosphorylation of Gephyrin in Zebrafish Mauthner Cells Governs Research Articles: Behavioral/Cognitive Phosphorylation of gephyrin in zebrafish Mauthner cells governs glycine receptor clustering and behavioral desensitization to sound https://doi.org/10.1523/JNEUROSCI.1315-19.2019 Cite as: J. Neurosci 2019; 10.1523/JNEUROSCI.1315-19.2019 Received: 7 June 2019 Revised: 16 September 2019 Accepted: 20 September 2019 This Early Release article has been peer-reviewed and accepted, but has not been through the composition and copyediting processes. The final version may differ slightly in style or formatting and will contain links to any extended data. Alerts: Sign up at www.jneurosci.org/alerts to receive customized email alerts when the fully formatted version of this article is published. Copyright © 2019 the authors 㻌 㻝㻌 Title: Phosphorylation of gephyrin in zebrafish Mauthner cells governs glycine receptor clustering 㻞㻌 and behavioral desensitization to sound (16/50 words) 㻟㻌 㻠㻌 Abbreviated title: GlyR clustering governs behavioral desensitization (46/50 characters) 㻡㻌 㻢㻌 Authors: Kazutoyo Ogino1, Kenta Yamada2, Tomoki Nishioka3, Yoichi Oda4, Kozo Kaibuchi3 and 㻣㻌 Hiromi Hirata1,* 㻤㻌 1Department of Chemistry and Biological Science, College of Science and Engineering, Aoyama 㻥㻌 Gakuin University, Sagamihara, Kanagawa, 252-5258, Japan; 2Center for Frontier Research, 㻝㻜㻌 National Institute of Genetics, Mishima, Shizuoka, 411-8540, Japan; 3Department of Cell 㻝㻝㻌 Pharmacology, Graduate School of Medicine, Nagoya University, Nagoya, Aichi, 466-8650, Japan; 㻝㻞㻌 4Division of Biological Science, Graduate School of Science, Nagoya University, Nagoya, Aichi, 㻝㻟㻌 464-8602, Japan. 㻝㻠㻌 *Corresponding author: [email protected] 㻝㻡㻌 㻝㻢㻌 Number of pages: 31 㻝㻣㻌 Number of figures and tables: 7 and 1, respectively. 㻝㻤㻌 Number of words for abstract, introduction and discussion: 218, 583, 1500 respectively. 㻝㻥㻌 Number of words for significance statement: 118. 㻞㻜㻌 㻞㻝㻌 Conflict of interest 㻞㻞㻌 The authors declare no competing interests. 㻞㻟㻌 㻞㻠㻌 Acknowledgements 㻝㻌 㻌 GlyR clustering governs behavioral desensitization 㻞㻡㻌 We thank Drs. Sean E. Low and Koichi Kawakami for technical support of electrophysiology and 㻞㻢㻌 distribution of the transgenic line Tg(hspGFFDMA130A)㻌through the National BioResource Project, 㻞㻣㻌 Japan, respectively. We also thank Hirata Lab members for fish care. This work was supported by a 㻞㻤㻌 Grant-in-Aid for Scientific Research C (18K06489), Scientific Research B (16H04657, 19H03329) 㻞㻥㻌 and Scientific Research on Innovative Areas (17H05578) from the MEXT, Japan, the Takeda 㻟㻜㻌 Science Foundation, the Naito Foundation, the Japan Epilepsy Research Foundation, a 㻟㻝㻌 Collaborative Research Grant from the National Institute of Genetics. The authors declare no 㻟㻞㻌 competing financial interests. 㻟㻟㻌 2 㻌 GlyR clustering governs behavioral desensitization 㻟㻠㻌 Abstract 㻟㻡㻌 The process by which future behavioral responses are shaped by past experiences is one of the 㻟㻢㻌 central questions in neuroscience. To gain insight into this process at the molecular and cellular 㻟㻣㻌 levels, we have applied zebrafish larvae to explore behavioral desensitization to sound. A sudden 㻟㻤㻌 loud noise often evokes a defensive response known as the acoustic startle response (ASR), which 㻟㻥㻌 is triggered by firing Mauthner cells in teleosts and amphibians. The probability of evoking ASR by 㻠㻜㻌 suprathreshold sound is reduced after exposure to repetitive auditory stimuli insufficient in 㻠㻝㻌 amplitude to evoke the ASR (subthreshold). Although it has been suggested that the potentiation of 㻠㻞㻌 inhibitory glycinergic inputs into Mauthner cell is involved in this desensitization of the ASR, the 㻠㻟㻌 molecular basis for the potentiation of glycinergic transmission has been unclear. Through the in 㻠㻠㻌 vivo monitoring of fluorescently-tagged glycine receptors (GlyRs), we here showed that behavioral 㻠㻡㻌 desensitization to sound in zebrafish is governed by GlyR clustering in Mauthner cells. We further 㻠㻢㻌 revealed that CaMKII-dependent phosphorylation of the scaffolding protein gephyrin at serine 325 㻠㻣㻌 promoted the synaptic accumulation of GlyR on Mauthner neurons through the enhancement of the 㻠㻤㻌 gephyrin-GlyR binding, which was indispensable for and could induce desensitization of the ASR. 㻠㻥㻌 Our study demonstrates an essential molecular and cellular basis of sound-induced receptor 㻡㻜㻌 dynamics and thus of behavioral desensitization to sound. 㻡㻝㻌 3 㻌 GlyR clustering governs behavioral desensitization 㻡㻞㻌 Significance statement 㻡㻟㻌 Behavioral desensitization in the acoustic startle response of fish is known to involve the 㻡㻠㻌 potentiation of inhibitory glycinergic input to the Mauthner cell which is a command neuron for the 㻡㻡㻌 acoustic startle response. However, the molecular and cellular basis for this potentiation has been 㻡㻢㻌 unknown. Here we show that an increase in glycine receptor (GlyR) clustering at synaptic sites on 㻡㻣㻌 zebrafish Mauthner cells is indispensable for and could induce desensitization. Furthermore, we 㻡㻤㻌 demonstrate that CaMKII-mediated phosphorylation of the scaffolding protein gephyrin promotes 㻡㻥㻌 GlyR clustering by increasing the binding between the ß-loop of GlyRs and gephyrin. Thus, the 㻢㻜㻌 phosphorylation of gephyrin is a key event which accounts for the potentiation of inhibitory 㻢㻝㻌 glycinergic inputs observed during sound-evoked behavioral desensitization. 㻢㻞㻌 㻢㻟㻌 Introduction 㻢㻠㻌 Animals must continually integrate information from their environment in order to modify 㻢㻡㻌 behavioral responses to both threatening and non-threating stimuli. For instance, a sudden loud 㻢㻢㻌 noise often evokes a largely unconscious defensive response known as the acoustic startle response 㻢㻣㻌 (ASR). However, if animals are repeatedly exposed to the same noise (conditioned), and experience 㻢㻤㻌 no adverse effects, they will often habituate to the sound and fail to show an ASR. As habituation 㻢㻥㻌 represents a simple form of learning and memory, it has been extensively studied in animals ranging 㻣㻜㻌 from jellyfish to humans (Thompson and Spencer, 1966; Kandel, 2001; Takahashi et al., 2008; 㻣㻝㻌 Williams et al., 2013; Ramaswami, 2014; Wolman et al., 2015). A comparatively less characterized 㻣㻞㻌 form of learning and memory that also decreases the probability of ASRs is behavioral 㻣㻟㻌 desensitization, which differs from habituation in that the conditioning stimulus consists of 㻣㻠㻌 repetitive auditory stimuli at levels insufficient to evoke an ASR (Oda et al., 1998). To gain insight 㻣㻡㻌 into the molecular and cellular basis of sound-evoked behavioral desensitization, we and others 4 㻌 GlyR clustering governs behavioral desensitization 㻣㻢㻌 have used fish, such as goldfish and zebrafish, because the neural circuity mediating the ASR is 㻣㻣㻌 both simple and experimentally amenable. 㻣㻤㻌 In fish, fast ASRs are triggered by the initiation of a single action potential within 㻣㻥㻌 Mauthner cells, a pair of large reticulospinal neurons located in rhombomere 4 of the hindbrain 㻤㻜㻌 (Fig. 1A) (Korn and Faber, 2005). Mauthner cells receive electrical and glutamatergic inputs from 㻤㻝㻌 ipsilateral hair cells via the auditory nerve, and in turn make excitatory monosynaptic contacts with 㻤㻞㻌 contralateral spinal motor neurons (Fig. 1B). In addition to connecting hair cells with Mauthner 㻤㻟㻌 cells, the auditory nerve also activates glycinergic interneurons that provide bilateral feedforward 㻤㻠㻌 inhibition to Mauthner cells to suppress their activation in response to subthreshold stimuli, as well 㻤㻡㻌 as concurrent activation of ipsilateral Mauthner cell in response to suprathreshold stimuli. The 㻤㻢㻌 simplicity of the ASR circuit has fostered its use for investigations into how neural circuits are 㻤㻣㻌 modified by experience. For instance, while searching for evidence of long-term potentiation (LTP) 㻤㻤㻌 at inhibitory synapses in adult goldfish, Korn and his colleagues discovered that repetitive electrical 㻤㻥㻌 stimulation of the VIII nerve, at amplitudes insufficient to activate ipsilateral Mauthner cells, 㻥㻜㻌 nonetheless potentiated glycinergic transmission between feedforward inhibitory neurons and 㻥㻝㻌 Mauthner cells (Korn et al., 1992). Subsequent efforts revealed that a more behaviorally relevant 㻥㻞㻌 conditioning paradigm composed of repetitive audible tones, likewise insufficient in amplitude to 㻥㻟㻌 activate Mauthner cells, also potentiated glycinergic transmission between feedforward inhibitory 㻥㻠㻌 neurons and Mauthner cells (Oda et al., 1998). As potentiation of glycinergic transmission between 㻥㻡㻌 these two neurons was found to coincide with a reduction in the ability to evoke an ASR in 㻥㻢㻌 free-swimming goldfish, it represented one of the earliest demonstrations that inhibitory LTP at the 㻥㻣㻌 cellular level could affect outcomes at the behavioral level. 㻥㻤㻌 In an attempt to better connect changes at the cellular level with changes at the behavioral 㻥㻥㻌 level, we explored molecular mechanisms that might account for behavioral desensitization. To this 㻝㻜㻜㻌 end, we generated transgenic zebrafish whose Mauthner cells expressed fluorescently-tagged 5 㻌 GlyR clustering governs behavioral desensitization 㻝㻜㻝㻌 glycine receptors (GlyRs). Employing these fish, we demonstrate that an increase in GlyR 㻝㻜㻞㻌 clustering in Mauthner cells is indispensable for and could induce sound-evoked behavioral 㻝㻜㻟㻌 desensitization. Furthermore, we show that GlyR clustering requires CaMKII-dependent 㻝㻜㻠㻌 phosphorylation of the postsynaptic scaffolding protein gephyrin at serine 325, an event which acts 㻝㻜㻡㻌 as a molecular switch for increased binding
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