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Articles, Cellular/Molecular

ANKS1B Gene Product AIDA-1 Controls Hippocampal Synaptic Transmission by Regulating GluN2B Subunit Localization

Jaafar O. Tindi, Andrés E. Chávez, Svetlana Cvejic, Erika Calvo-Ochoa, Pablo E. Castillo and Bryen A. Jordan
Journal of Neuroscience 17 June 2015, 35 (24) 8986-8996; DOI: https://doi.org/10.1523/JNEUROSCI.4029-14.2015
Jaafar O. Tindi
1Dominick P. Purpura Department of Neuroscience,
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Andrés E. Chávez
1Dominick P. Purpura Department of Neuroscience,
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Svetlana Cvejic
1Dominick P. Purpura Department of Neuroscience,
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Erika Calvo-Ochoa
1Dominick P. Purpura Department of Neuroscience,
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Pablo E. Castillo
1Dominick P. Purpura Department of Neuroscience,
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Bryen A. Jordan
1Dominick P. Purpura Department of Neuroscience,
2Department of Psychiatry and Behavioral Sciences, Albert Einstein College of Medicine, Bronx, New York 10461
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Abstract

NMDA receptors (NMDARs) are key mediators of glutamatergic transmission and synaptic plasticity, and their dysregulation has been linked to diverse neuropsychiatric and neurodegenerative disorders. While normal NMDAR function requires regulated expression and trafficking of its different subunits, the molecular mechanisms underlying these processes are not fully understood. Here we report that the amyloid precursor protein intracellular domain associated-1 protein (AIDA-1), which associates with NMDARs and is encoded by ANKS1B, a gene recently linked to schizophrenia, regulates synaptic NMDAR subunit composition. Forebrain-specific AIDA-1 conditional knock-out (cKO) mice exhibit reduced GluN2B-mediated and increased GluN2A-mediated synaptic transmission, and biochemical analyses show AIDA-1 cKO mice have low GluN2B and high GluN2A protein levels at isolated hippocampal synaptic junctions compared with controls. These results are corroborated by immunocytochemical and electrophysiological analyses in primary neuronal cultures following acute lentiviral shRNA-mediated knockdown of AIDA-1. Moreover, hippocampal NMDAR-dependent but not metabotropic glutamate receptor-dependent plasticity is impaired in AIDA-1 cKO mice, further supporting a role for AIDA-1 in synaptic NMDAR function. We also demonstrate that AIDA-1 preferentially associates with GluN2B and with the adaptor protein Ca2+/calmodulin-dependent serine protein kinase and kinesin KIF17, which regulate the transport of GluN2B-containing NMDARs from the endoplasmic reticulum (ER) to synapses. Consistent with this function, GluN2B accumulates in ER-enriched fractions in AIDA-1 cKO mice. These findings suggest that AIDA-1 regulates NMDAR subunit composition at synapses by facilitating transport of GluN2B from the ER to synapses, which is critical for NMDAR plasticity. Our work provides an explanation for how AIDA-1 dysfunction might contribute to neuropsychiatric conditions, such as schizophrenia.

  • CASK
  • endoplasmic reticulum
  • KIF17
  • NMDAR
  • plasticity
  • trafficking
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The Journal of Neuroscience: 35 (24)
Journal of Neuroscience
Vol. 35, Issue 24
17 Jun 2015
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ANKS1B Gene Product AIDA-1 Controls Hippocampal Synaptic Transmission by Regulating GluN2B Subunit Localization
Jaafar O. Tindi, Andrés E. Chávez, Svetlana Cvejic, Erika Calvo-Ochoa, Pablo E. Castillo, Bryen A. Jordan
Journal of Neuroscience 17 June 2015, 35 (24) 8986-8996; DOI: 10.1523/JNEUROSCI.4029-14.2015

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ANKS1B Gene Product AIDA-1 Controls Hippocampal Synaptic Transmission by Regulating GluN2B Subunit Localization
Jaafar O. Tindi, Andrés E. Chávez, Svetlana Cvejic, Erika Calvo-Ochoa, Pablo E. Castillo, Bryen A. Jordan
Journal of Neuroscience 17 June 2015, 35 (24) 8986-8996; DOI: 10.1523/JNEUROSCI.4029-14.2015
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Keywords

  • CASK
  • endoplasmic reticulum
  • KIF17
  • NMDAR
  • plasticity
  • trafficking

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