Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity

Seil Jang; Daeyoung Oh; Yeunkum Lee; Eric Hosy; Hyewon Shin; Christoph van Riesen; Daniel Whitcomb; Julia M Warburton; Jihoon Jo; Doyoun Kim; Sun Gyun Kim; Seung Min Um; Seok-Kyu Kwon; Myoung-Hwan Kim; Junyeop Daniel Roh; Jooyeon Woo; Heejung Jun; Dongmin Lee; Won Mah; Hyun Kim; Bong-Kiun Kaang; Kei Cho; Jeong-Seop Rhee; Daniel Choquet; Eunjoon Kim

doi:10.1038/nn.4176

Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity

Seil Jang, Daeyoung Oh, Yeunkum Lee, Eric Hosy, Hyewon Shin, Christoph van Riesen, Daniel Whitcomb, Julia M Warburton, Jihoon Jo, Doyoun Kim, Sun Gyun Kim, Seung Min Um, Seok-Kyu Kwon, Myoung-Hwan Kim, Junyeop Daniel Roh, Jooyeon Woo, Heejung Jun, Dongmin Lee, Won Mah, Hyun KimBong-Kiun Kaang, Kei Cho, Jeong-Seop Rhee, Daniel Choquet, Eunjoon Kim

Research output: Contribution to journal › Article (Academic Journal) › peer-review

46 Citations (Scopus)

Abstract

Synaptic adhesion molecules regulate synapse development and plasticity through mechanisms that include trans-synaptic adhesion and recruitment of diverse synaptic proteins. We found that the immunoglobulin superfamily member 11 (IgSF11), a homophilic adhesion molecule that preferentially expressed in the brain, is a dual-binding partner of the postsynaptic scaffolding protein PSD-95 and AMPA glutamate receptors (AMPARs). IgSF11 required PSD-95 binding for its excitatory synaptic localization. In addition, IgSF11 stabilized synaptic AMPARs, as determined by IgSF11 knockdown-induced suppression of AMPAR-mediated synaptic transmission and increased surface mobility of AMPARs, measured by high-throughput, single-molecule tracking. IgSF11 deletion in mice led to the suppression of AMPAR-mediated synaptic transmission in the dentate gyrus and long-term potentiation in the CA1 region of the hippocampus. IgSF11 did not regulate the functional characteristics of AMPARs, including desensitization, deactivation or recovery. These results suggest that IgSF11 regulates excitatory synaptic transmission and plasticity through its tripartite interactions with PSD-95 and AMPARs.

Original language	English
Pages (from-to)	84-93
Number of pages	10
Journal	Nature Neuroscience
Volume	19
Issue number	1
DOIs	https://doi.org/10.1038/nn.4176
Publication status	Published - 23 Nov 2015

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THE EFFECTS OF ACUTE STRESS ON GLUTAMATE RECEPTOR TRAFFICKING AND SYNAPTIC PLASTICITY IN THE HIPPOCAMPUS
Cho, K. (Principal Investigator)
4/01/12 → 4/01/15
Project: Research

Dr Daniel Whitcomb
- D.J.Whitcombbristol.acuk
- School of Physiology, Pharmacology & Neuroscience - Senior Lecturer in Translational Neuroscience
- Translational Neuroscience Research Group
Person: Academic , Member

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Jang, S., Oh, D., Lee, Y., Hosy, E., Shin, H., van Riesen, C., Whitcomb, D., Warburton, J. M., Jo, J., Kim, D., Kim, S. G., Um, S. M., Kwon, S.-K., Kim, M.-H., Roh, J. D., Woo, J., Jun, H., Lee, D., Mah, W., ... Kim, E. (2015). Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity. Nature Neuroscience, 19(1), 84-93. https://doi.org/10.1038/nn.4176

@article{f24912a96f134e4792ca8da7d291077d,

title = "Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity",

abstract = "Synaptic adhesion molecules regulate synapse development and plasticity through mechanisms that include trans-synaptic adhesion and recruitment of diverse synaptic proteins. We found that the immunoglobulin superfamily member 11 (IgSF11), a homophilic adhesion molecule that preferentially expressed in the brain, is a dual-binding partner of the postsynaptic scaffolding protein PSD-95 and AMPA glutamate receptors (AMPARs). IgSF11 required PSD-95 binding for its excitatory synaptic localization. In addition, IgSF11 stabilized synaptic AMPARs, as determined by IgSF11 knockdown-induced suppression of AMPAR-mediated synaptic transmission and increased surface mobility of AMPARs, measured by high-throughput, single-molecule tracking. IgSF11 deletion in mice led to the suppression of AMPAR-mediated synaptic transmission in the dentate gyrus and long-term potentiation in the CA1 region of the hippocampus. IgSF11 did not regulate the functional characteristics of AMPARs, including desensitization, deactivation or recovery. These results suggest that IgSF11 regulates excitatory synaptic transmission and plasticity through its tripartite interactions with PSD-95 and AMPARs.",

author = "Seil Jang and Daeyoung Oh and Yeunkum Lee and Eric Hosy and Hyewon Shin and \{van Riesen\}, Christoph and Daniel Whitcomb and Warburton, \{Julia M\} and Jihoon Jo and Doyoun Kim and Kim, \{Sun Gyun\} and Um, \{Seung Min\} and Seok-Kyu Kwon and Myoung-Hwan Kim and Roh, \{Junyeop Daniel\} and Jooyeon Woo and Heejung Jun and Dongmin Lee and Won Mah and Hyun Kim and Bong-Kiun Kaang and Kei Cho and Jeong-Seop Rhee and Daniel Choquet and Eunjoon Kim",

year = "2015",

month = nov,

day = "23",

doi = "10.1038/nn.4176",

language = "English",

volume = "19",

pages = "84--93",

journal = "Nature Neuroscience",

issn = "1097-6256",

publisher = "Nature Research",

number = "1",

}

Jang, S, Oh, D, Lee, Y, Hosy, E, Shin, H, van Riesen, C, Whitcomb, D, Warburton, JM, Jo, J, Kim, D, Kim, SG, Um, SM, Kwon, S-K, Kim, M-H, Roh, JD, Woo, J, Jun, H, Lee, D, Mah, W, Kim, H, Kaang, B-K, Cho, K, Rhee, J-S, Choquet, D & Kim, E 2015, 'Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity', Nature Neuroscience, vol. 19, no. 1, pp. 84-93. https://doi.org/10.1038/nn.4176

TY - JOUR

T1 - Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity

AU - Jang, Seil

AU - Oh, Daeyoung

AU - Lee, Yeunkum

AU - Hosy, Eric

AU - Shin, Hyewon

AU - van Riesen, Christoph

AU - Whitcomb, Daniel

AU - Warburton, Julia M

AU - Jo, Jihoon

AU - Kim, Doyoun

AU - Kim, Sun Gyun

AU - Um, Seung Min

AU - Kwon, Seok-Kyu

AU - Kim, Myoung-Hwan

AU - Roh, Junyeop Daniel

AU - Woo, Jooyeon

AU - Jun, Heejung

AU - Lee, Dongmin

AU - Mah, Won

AU - Kim, Hyun

AU - Kaang, Bong-Kiun

AU - Cho, Kei

AU - Rhee, Jeong-Seop

AU - Choquet, Daniel

AU - Kim, Eunjoon

PY - 2015/11/23

Y1 - 2015/11/23

N2 - Synaptic adhesion molecules regulate synapse development and plasticity through mechanisms that include trans-synaptic adhesion and recruitment of diverse synaptic proteins. We found that the immunoglobulin superfamily member 11 (IgSF11), a homophilic adhesion molecule that preferentially expressed in the brain, is a dual-binding partner of the postsynaptic scaffolding protein PSD-95 and AMPA glutamate receptors (AMPARs). IgSF11 required PSD-95 binding for its excitatory synaptic localization. In addition, IgSF11 stabilized synaptic AMPARs, as determined by IgSF11 knockdown-induced suppression of AMPAR-mediated synaptic transmission and increased surface mobility of AMPARs, measured by high-throughput, single-molecule tracking. IgSF11 deletion in mice led to the suppression of AMPAR-mediated synaptic transmission in the dentate gyrus and long-term potentiation in the CA1 region of the hippocampus. IgSF11 did not regulate the functional characteristics of AMPARs, including desensitization, deactivation or recovery. These results suggest that IgSF11 regulates excitatory synaptic transmission and plasticity through its tripartite interactions with PSD-95 and AMPARs.

AB - Synaptic adhesion molecules regulate synapse development and plasticity through mechanisms that include trans-synaptic adhesion and recruitment of diverse synaptic proteins. We found that the immunoglobulin superfamily member 11 (IgSF11), a homophilic adhesion molecule that preferentially expressed in the brain, is a dual-binding partner of the postsynaptic scaffolding protein PSD-95 and AMPA glutamate receptors (AMPARs). IgSF11 required PSD-95 binding for its excitatory synaptic localization. In addition, IgSF11 stabilized synaptic AMPARs, as determined by IgSF11 knockdown-induced suppression of AMPAR-mediated synaptic transmission and increased surface mobility of AMPARs, measured by high-throughput, single-molecule tracking. IgSF11 deletion in mice led to the suppression of AMPAR-mediated synaptic transmission in the dentate gyrus and long-term potentiation in the CA1 region of the hippocampus. IgSF11 did not regulate the functional characteristics of AMPARs, including desensitization, deactivation or recovery. These results suggest that IgSF11 regulates excitatory synaptic transmission and plasticity through its tripartite interactions with PSD-95 and AMPARs.

U2 - 10.1038/nn.4176

DO - 10.1038/nn.4176

M3 - Article (Academic Journal)

C2 - 26595655

SN - 1097-6256

VL - 19

SP - 84

EP - 93

JO - Nature Neuroscience

JF - Nature Neuroscience

IS - 1

ER -

Synaptic adhesion molecule IgSF11 regulates synaptic transmission and plasticity

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THE EFFECTS OF ACUTE STRESS ON GLUTAMATE RECEPTOR TRAFFICKING AND SYNAPTIC PLASTICITY IN THE HIPPOCAMPUS

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