Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation

Mengjia Huang; Na Ryum Bin; Jayant Rai; Ke Ma; Chun Hin Chow; Sarah Eide; Hidekiyo Harada; Jianbing Xiao; Daorong Feng; Hong Shuo Sun; Zhong Ping Feng; Herbert Y. Gaisano; Jeffrey E. Pessin; Philippe P. Monnier; Kenichi Okamoto; Liang Zhang; Shuzo Sugita

doi:10.1016/j.isci.2023.106664

Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation

Mengjia Huang, Na Ryum Bin, Jayant Rai, Ke Ma, Chun Hin Chow, Sarah Eide, Hidekiyo Harada, Jianbing Xiao, Daorong Feng, Hong Shuo Sun, Zhong Ping Feng, Herbert Y. Gaisano, Jeffrey E. Pessin, Philippe P. Monnier, Kenichi Okamoto, Liang Zhang, Shuzo Sugita

Medicine

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Abstract

SNARE-mediated membrane fusion plays a crucial role in presynaptic vesicle exocytosis and also in postsynaptic receptor delivery. The latter is considered particularly important for synaptic plasticity and learning and memory, yet the identity of the key SNARE proteins remains elusive. Here, we investigate the role of neuronal synaptosomal-associated protein-23 (SNAP-23) by analyzing pyramidal-neuron specific SNAP-23 conditional knockout (cKO) mice. Electrophysiological analysis of SNAP-23 deficient neurons using acute hippocampal slices showed normal basal neurotransmission in CA3-CA1 synapses with unchanged AMPA and NMDA currents. Nevertheless, we found theta-burst stimulation-induced long-term potentiation (LTP) was vastly diminished in SNAP-23 cKO slices. Moreover, unlike syntaxin-4 cKO mice where both basal neurotransmission and LTP decrease manifested changes in a broad set of behavioral tasks, deficits of SNAP-23 cKO are more limited to spatial memory. Our data reveal that neuronal SNAP-23 is selectively crucial for synaptic plasticity and spatial memory without affecting basal glutamate receptor function.

Original language	English (US)
Article number	106664
Journal	iScience
Volume	26
Issue number	5
DOIs	https://doi.org/10.1016/j.isci.2023.106664
State	Published - May 19 2023

Keywords

Molecular biology
Molecular neuroscience
Neuroscience

ASJC Scopus subject areas

General

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10.1016/j.isci.2023.106664

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Huang, M., Bin, N. R., Rai, J., Ma, K., Chow, C. H., Eide, S., Harada, H., Xiao, J., Feng, D., Sun, H. S., Feng, Z. P., Gaisano, H. Y., Pessin, J. E., Monnier, P. P., Okamoto, K., Zhang, L., & Sugita, S. (2023). Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation. iScience, 26(5), Article 106664. https://doi.org/10.1016/j.isci.2023.106664

Huang, M, Bin, NR, Rai, J, Ma, K, Chow, CH, Eide, S, Harada, H, Xiao, J, Feng, D, Sun, HS, Feng, ZP, Gaisano, HY, Pessin, JE, Monnier, PP, Okamoto, K, Zhang, L & Sugita, S 2023, 'Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation', iScience, vol. 26, no. 5, 106664. https://doi.org/10.1016/j.isci.2023.106664

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title = "Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation",

abstract = "SNARE-mediated membrane fusion plays a crucial role in presynaptic vesicle exocytosis and also in postsynaptic receptor delivery. The latter is considered particularly important for synaptic plasticity and learning and memory, yet the identity of the key SNARE proteins remains elusive. Here, we investigate the role of neuronal synaptosomal-associated protein-23 (SNAP-23) by analyzing pyramidal-neuron specific SNAP-23 conditional knockout (cKO) mice. Electrophysiological analysis of SNAP-23 deficient neurons using acute hippocampal slices showed normal basal neurotransmission in CA3-CA1 synapses with unchanged AMPA and NMDA currents. Nevertheless, we found theta-burst stimulation-induced long-term potentiation (LTP) was vastly diminished in SNAP-23 cKO slices. Moreover, unlike syntaxin-4 cKO mice where both basal neurotransmission and LTP decrease manifested changes in a broad set of behavioral tasks, deficits of SNAP-23 cKO are more limited to spatial memory. Our data reveal that neuronal SNAP-23 is selectively crucial for synaptic plasticity and spatial memory without affecting basal glutamate receptor function.",

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author = "Mengjia Huang and Bin, {Na Ryum} and Jayant Rai and Ke Ma and Chow, {Chun Hin} and Sarah Eide and Hidekiyo Harada and Jianbing Xiao and Daorong Feng and Sun, {Hong Shuo} and Feng, {Zhong Ping} and Gaisano, {Herbert Y.} and Pessin, {Jeffrey E.} and Monnier, {Philippe P.} and Kenichi Okamoto and Liang Zhang and Shuzo Sugita",

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AU - Huang, Mengjia

AU - Bin, Na Ryum

AU - Rai, Jayant

AU - Ma, Ke

AU - Chow, Chun Hin

AU - Eide, Sarah

AU - Harada, Hidekiyo

AU - Xiao, Jianbing

AU - Feng, Daorong

AU - Sun, Hong Shuo

AU - Feng, Zhong Ping

AU - Gaisano, Herbert Y.

AU - Pessin, Jeffrey E.

AU - Monnier, Philippe P.

AU - Okamoto, Kenichi

AU - Zhang, Liang

AU - Sugita, Shuzo

PY - 2023/5/19

Y1 - 2023/5/19

N2 - SNARE-mediated membrane fusion plays a crucial role in presynaptic vesicle exocytosis and also in postsynaptic receptor delivery. The latter is considered particularly important for synaptic plasticity and learning and memory, yet the identity of the key SNARE proteins remains elusive. Here, we investigate the role of neuronal synaptosomal-associated protein-23 (SNAP-23) by analyzing pyramidal-neuron specific SNAP-23 conditional knockout (cKO) mice. Electrophysiological analysis of SNAP-23 deficient neurons using acute hippocampal slices showed normal basal neurotransmission in CA3-CA1 synapses with unchanged AMPA and NMDA currents. Nevertheless, we found theta-burst stimulation-induced long-term potentiation (LTP) was vastly diminished in SNAP-23 cKO slices. Moreover, unlike syntaxin-4 cKO mice where both basal neurotransmission and LTP decrease manifested changes in a broad set of behavioral tasks, deficits of SNAP-23 cKO are more limited to spatial memory. Our data reveal that neuronal SNAP-23 is selectively crucial for synaptic plasticity and spatial memory without affecting basal glutamate receptor function.

AB - SNARE-mediated membrane fusion plays a crucial role in presynaptic vesicle exocytosis and also in postsynaptic receptor delivery. The latter is considered particularly important for synaptic plasticity and learning and memory, yet the identity of the key SNARE proteins remains elusive. Here, we investigate the role of neuronal synaptosomal-associated protein-23 (SNAP-23) by analyzing pyramidal-neuron specific SNAP-23 conditional knockout (cKO) mice. Electrophysiological analysis of SNAP-23 deficient neurons using acute hippocampal slices showed normal basal neurotransmission in CA3-CA1 synapses with unchanged AMPA and NMDA currents. Nevertheless, we found theta-burst stimulation-induced long-term potentiation (LTP) was vastly diminished in SNAP-23 cKO slices. Moreover, unlike syntaxin-4 cKO mice where both basal neurotransmission and LTP decrease manifested changes in a broad set of behavioral tasks, deficits of SNAP-23 cKO are more limited to spatial memory. Our data reveal that neuronal SNAP-23 is selectively crucial for synaptic plasticity and spatial memory without affecting basal glutamate receptor function.

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Neuronal SNAP-23 is critical for synaptic plasticity and spatial memory independently of NMDA receptor regulation

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