S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors

Yunfei Huang; Heng Ye Man; Yoko Sekine-Aizawa; Yefei Han; Krishna Juluri; Hongbo Luo; Jaime Cheah; Charles Lowenstein; Richard L. Huganir; Solomon H. Snyder

doi:10.1016/j.neuron.2005.03.028

S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors

Yunfei Huang, Heng Ye Man, Yoko Sekine-Aizawa, Yefei Han, Krishna Juluri, Hongbo Luo, Jaime Cheah, Charles Lowenstein, Richard L. Huganir, Solomon H. Snyder

School of Medicine

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145 Scopus citations

Abstract

Postsynaptic AMPA receptor (AMPAR) trafficking mediates some forms of synaptic plasticity that are modulated by NMDA receptor (NMDAR) activation and N-ethylmaleimide sensitive factor (NSF). We report that NSF is physiologically S-nitrosylated by endogenous, neuronally derived nitric oxide (NO). S-nitrosylation of NSF augments its binding to the AMPAR GluR2 subunit. Surface insertion of GluR2 in response to activation of synaptic NMDARs requires endogenous NO, acting selectively upon the binding of NSF to GluR2. Thus, AMPAR recycling elicited by NMDA neurotransmission is mediated by a cascade involving NMDA activation of neuronal NO synthase to form NO, leading to S-nitrosylation of NSF which is thereby activated, enabling it to bind to GluR2 and promote the receptor's surface expression.

Original language	English (US)
Pages (from-to)	533-540
Number of pages	8
Journal	Neuron
Volume	46
Issue number	4
DOIs	https://doi.org/10.1016/j.neuron.2005.03.028
State	Published - May 19 2005

ASJC Scopus subject areas

Neuroscience(all)

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10.1016/j.neuron.2005.03.028

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title = "S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors",

abstract = "Postsynaptic AMPA receptor (AMPAR) trafficking mediates some forms of synaptic plasticity that are modulated by NMDA receptor (NMDAR) activation and N-ethylmaleimide sensitive factor (NSF). We report that NSF is physiologically S-nitrosylated by endogenous, neuronally derived nitric oxide (NO). S-nitrosylation of NSF augments its binding to the AMPAR GluR2 subunit. Surface insertion of GluR2 in response to activation of synaptic NMDARs requires endogenous NO, acting selectively upon the binding of NSF to GluR2. Thus, AMPAR recycling elicited by NMDA neurotransmission is mediated by a cascade involving NMDA activation of neuronal NO synthase to form NO, leading to S-nitrosylation of NSF which is thereby activated, enabling it to bind to GluR2 and promote the receptor's surface expression.",

author = "Yunfei Huang and Man, {Heng Ye} and Yoko Sekine-Aizawa and Yefei Han and Krishna Juluri and Hongbo Luo and Jaime Cheah and Charles Lowenstein and Huganir, {Richard L.} and Snyder, {Solomon H.}",

note = "Funding Information: The authors thank Dr. Morgan Sheng (MIT) for his generous gift of GFP-tagged GluR2 constructs, Anthony Lanahan for providing a rat brain cDNA library, Lynda Hester for assistance with primary cultures, Mahil Rao and Carley Benham for providing nNOS knockout mice, and Drs. Doug Murphy, Douglas Robinson, and Chris Janetopoulos for their assistance with TIRF microscopy. This work was funded by USPHS grant DA00266, Research Scientist Award DA-00074 (S.H.S.), and the Howard Hughes Medical Institute (R.L.H.). ",

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AU - Huang, Yunfei

AU - Man, Heng Ye

AU - Sekine-Aizawa, Yoko

AU - Han, Yefei

AU - Juluri, Krishna

AU - Luo, Hongbo

AU - Cheah, Jaime

AU - Lowenstein, Charles

AU - Huganir, Richard L.

AU - Snyder, Solomon H.

N1 - Funding Information: The authors thank Dr. Morgan Sheng (MIT) for his generous gift of GFP-tagged GluR2 constructs, Anthony Lanahan for providing a rat brain cDNA library, Lynda Hester for assistance with primary cultures, Mahil Rao and Carley Benham for providing nNOS knockout mice, and Drs. Doug Murphy, Douglas Robinson, and Chris Janetopoulos for their assistance with TIRF microscopy. This work was funded by USPHS grant DA00266, Research Scientist Award DA-00074 (S.H.S.), and the Howard Hughes Medical Institute (R.L.H.).

PY - 2005/5/19

Y1 - 2005/5/19

N2 - Postsynaptic AMPA receptor (AMPAR) trafficking mediates some forms of synaptic plasticity that are modulated by NMDA receptor (NMDAR) activation and N-ethylmaleimide sensitive factor (NSF). We report that NSF is physiologically S-nitrosylated by endogenous, neuronally derived nitric oxide (NO). S-nitrosylation of NSF augments its binding to the AMPAR GluR2 subunit. Surface insertion of GluR2 in response to activation of synaptic NMDARs requires endogenous NO, acting selectively upon the binding of NSF to GluR2. Thus, AMPAR recycling elicited by NMDA neurotransmission is mediated by a cascade involving NMDA activation of neuronal NO synthase to form NO, leading to S-nitrosylation of NSF which is thereby activated, enabling it to bind to GluR2 and promote the receptor's surface expression.

AB - Postsynaptic AMPA receptor (AMPAR) trafficking mediates some forms of synaptic plasticity that are modulated by NMDA receptor (NMDAR) activation and N-ethylmaleimide sensitive factor (NSF). We report that NSF is physiologically S-nitrosylated by endogenous, neuronally derived nitric oxide (NO). S-nitrosylation of NSF augments its binding to the AMPAR GluR2 subunit. Surface insertion of GluR2 in response to activation of synaptic NMDARs requires endogenous NO, acting selectively upon the binding of NSF to GluR2. Thus, AMPAR recycling elicited by NMDA neurotransmission is mediated by a cascade involving NMDA activation of neuronal NO synthase to form NO, leading to S-nitrosylation of NSF which is thereby activated, enabling it to bind to GluR2 and promote the receptor's surface expression.

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S-nitrosylation of N-ethylmaleimide sensitive factor mediates surface expression of AMPA receptors

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