Regulation of AMPA receptor function by the human memory-associated gene KIBRA
Open accessAbstract
KIBRA has recently been identified as a gene associated with human memory performance. Despite the elucidation of the role of KIBRA in several diverse processes in nonneuronal cells, the molecular function of KIBRA in neurons is unknown. We found that KIBRA directly binds to the protein interacting with C-kinase 1 (PICK1) and forms a complex with α-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate receptors (AMPARs), the major excitatory neurotransmitter receptors in the brain. KIBRA knockdown accelerates the rate of AMPAR recycling following N-methyl-D-aspartate receptor-induced internalization. Genetic deletion of KIBRA in mice impairs both long-term depression and long-term potentiation at hippocampal Schaffer collateral-CA1 synapses. Moreover, KIBRA knockout mice have severe deficits in contextual fear learning and memory. These results indicate that KIBRA regulates higher brain function by regulating AMPAR trafficking and synaptic plasticity.
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Mice lacking PICK1, KIBRA or Grasp1 all show reductions in hippocampal LTP as well as defects in hippocampus-dependent learning and memory tasks.
“Mice lacking PICK1, KIBRA or Grasp1 all show reductions in hippocampal LTP as well as defects in hippocampus-dependent learning and memory tasks (Makuch et al., 2011, Volk et al., 2010, Chiu et al., 2017)”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Makuch et al., 2011
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Cites
AMPA Receptor Trafficking and Synaptic Plasticity
Malinow, R., & Malenka, R. C. (2002) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.25.112701.142758 · Cited by 2,588 · see citing works
Steinberg, J. P., Takamiya, K., Shen, Y., Xia, J., Rubio, M. E., Yu, S., Jin, W., Thomas, G. M., Linden, D. J., & Huganir, R. L. (2006) · Neuron · doi:10.1016/j.neuron.2006.02.025 · Cited by 288 · cited 14× · see citing works
“For LTD in the presence of AP5, AP5 was included throughout the experiment.”
BackgroundInfluentialSelf-citationGenetic background differences and nonassociative effects in mouse trace fear conditioning.
Smith, D. R., Gallagher, M., & Stanton, M. E. (2007) · Learning & Memory · doi:10.1101/lm.614807 · Cited by 47 · cited 1× · see citing works
“Intact hippocampal function is critical for eliciting both trace (freezing in response to tone presentation) and contextual (freezing in response to training context exposure) fear conditioning in response to this training protocol (McEchron et al., 1998; Smith et al., 2007).”
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Research works printed but not linked: 37
- Almeida OP Schwab SG Lautenschlager NT Morar B Greenop KR Flicker L Wildenauer D 2008 KIBRA genetic polymorphism influences episodic memory in later life, but does not increase the risk of mild cognitive impairment J Cell Mol Med 12 1672 1676 18194457 PMC3918083
- Ashby MC Ibaraki K Henley JM 2004 It's green outside: tracking cell surface proteins with pH-sensitive GFP Trends Neurosci 27 257 261 15111007
- Bates TC Price JF Harris SE Marioni RE Fowkes FG Stewart MC Murray GD Whalley LJ Starr JM Deary IJ 2009 Association of KIBRA and memory Neurosci Lett 19397951
- Baumgartner R Poernbacher I Buser N Hafen E Stocker H 2010 The WW domain protein Kibra acts upstream of Hippo in Drosophila Dev Cell 18 309 316 20159600
- Buther K Plaas C Barnekow A Kremerskothen J 2004 KIBRA is a novel substrate for protein kinase Czeta Biochem Biophys Res Commun 317 703 707 15081397
- Citri A Bhattacharyya S Ma C Morishita W Fang S Rizo J Malenka RC 2010 Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression J Neurosci 30 16437 16452 21147983 PMC3004477
- Clem RL Anggono V Huganir RL 2010 PICK1 regulates incorporation of calcium-permeable AMPA receptors during cortical synaptic strengthening J Neurosci 30 6360 6366 20445062 PMC2897179
- Corneveaux JJ Liang WS Reiman EM Webster JA Myers AJ Zismann VL Joshipura KD Pearson JV Hu-Lince D Craig DW 2008 Evidence for an association between KIBRA and late-onset Alzheimer's disease Neurobiol Aging PMC2913703 18789830
- Dong H O'Brien RJ Fung ET Lanahan AA Worley PF Huganir RL 1997 GRIP: a synaptic PDZ domain-containing protein that interacts with AMPA receptors Nature 386 279 284 9069286
- Drier EA Tello MK Cowan M Wu P Blace N Sacktor TC Yin JC 2002 Memory enhancement and formation by atypical PKM activity in Drosophila melanogaster Nat Neurosci 5 316 324 11914720
- Duning K Schurek EM Schluter M Bayer M Reinhardt HC Schwab A Schaefer L Benzing T Schermer B Saleem MA 2008 KIBRA modulates directional migration of podocytes J Am Soc Nephrol 19 1891 1903 18596123 PMC2551571
- Esclassan F Coutureau E Di Scala G Marchand AR 2009 A cholinergic-dependent role for the entorhinal cortex in trace fear conditioning J Neurosci 29 8087 8093 19553448 PMC6666060
- Gardner SM Takamiya K Xia J Suh JG Johnson R Yu S Huganir RL 2005 Calcium-permeable AMPA receptor plasticity is mediated by subunit-specific interactions with PICK1 and NSF Neuron 45 903 915 15797551
- Genevet A Wehr MC Brain R Thompson BJ Tapon N 2010 Kibra is a regulator of the Salvador/Warts/Hippo signaling network Dev Cell 18 300 308 20159599 PMC2845807
- Hsieh H Boehm J Sato C Iwatsubo T Tomita T Sisodia S Malinow R 2006 AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss Neuron 52 831 843 17145504 PMC1850952
- Jo J Heon S Kim MJ Son GH Park Y Henley JM Weiss JL Sheng M Collingridge GL Cho K 2008 Metabotropic glutamate receptor-mediated LTD involves two interacting Ca(2+) sensors, NCS-1 and PICK1 Neuron 60 1095 1111 19109914 PMC3310905
- Johannsen S Duning K Pavenstadt H Kremerskothen J Boeckers TM 2008 Temporal-spatial expression and novel biochemical properties of the memory-related protein KIBRA Neuroscience 155 1165 1173 18672031
- Kremerskothen J Plaas C Buther K Finger I Veltel S Matanis T Liedtke T Barnekow A 2003 Characterization of KIBRA, a novel WW domain-containing protein Biochem Biophys Res Commun 300 862 867 12559952
- Lin DT Huganir RL 2007 PICK1 and phosphorylation of the glutamate receptor 2 (GluR2) AMPA receptor subunit regulates GluR2 recycling after NMDA receptor-induced internalization J Neurosci 27 13903 13908 18077702 PMC6673624
- Liu SJ Cull-Candy SG 2005 Subunit interaction with PICK and GRIP controls Ca2+ permeability of AMPARs at cerebellar synapses Nat Neurosci 8 768 775 15895086
- Mao L Takamiya K Thomas G Lin DT Huganir RL 2010 GRIP1 and 2 regulate activity-dependent AMPA receptor recycling via exocyst complex interactions Proc Natl Acad Sci U S A 107 19038 19043 20956289 PMC2973854
- McEchron MD Bouwmeester H Tseng W Weiss C Disterhoft JF 1998 Hippocampectomy disrupts auditory trace fear conditioning and contextual fear conditioning in the rat Hippocampus 8 638 646 9882021
- Papassotiropoulos A Stephan DA Huentelman MJ Hoerndli FJ Craig DW Pearson JV Huynh KD Brunner F Corneveaux J Osborne D 2006 Common Kibra alleles are associated with human memory performance Science 314 475 478 17053149
- Rayala SK den Hollander P Manavathi B Talukder AH Song C Peng S Barnekow A Kremerskothen J Kumar R 2006 Essential role of KIBRA in co-activator function of dynein light chain 1 in mammalian cells J Biol Chem 281 19092 19099 16684779
- Rizo J Sudhof TC 1998 C2-domains, structure and function of a universal Ca2+-binding domain J Biol Chem 273 15879 15882 9632630
- Rosse C Formstecher E Boeckeler K Zhao Y Kremerskothen J White MD Camonis JH Parker PJ 2009 An aPKC-exocyst complex controls paxillin phosphorylation and migration through localised JNK1 activation PLoS Biol 7 e1000235 19885391 PMC2762617
- Sacktor TC Osten P Valsamis H Jiang X Naik MU Sublette E 1993 Persistent activation of the zeta isoform of protein kinase C in the maintenance of long-term potentiation Proc Natl Acad Sci USA 90 8342 8346 8378304 PMC47352
- Schaper K Kolsch H Popp J Wagner M Jessen F 2008 KIBRA gene variants are associated with episodic memory in healthy elderly Neurobiol Aging 29 1123 1125 17353070
- Schneider A Huentelman MJ Kremerskothen J Duning K Spoelgen R Nikolich K 2010 KIBRA: A New Gateway to Learning and Memory? Front Aging Neurosci 2 4 20552044 PMC2874402
- Shepherd JD Huganir RL 2007 The Cell Biology of Synaptic Plasticity: AMPA Receptor Trafficking Annu Rev Cell Dev Biol 23 613 643 17506699
- Song I Kamboj S Xia J Dong H Liao D Huganir RL 1998 Interaction of the N-ethylmaleimide-sensitive factor with AMPA receptors Neuron 21 393 400 9728920
- Takamiya K Mao L Huganir RL Linden DJ 2008 The glutamate receptor-interacting protein family of GluR2-binding proteins is required for long-term synaptic depression expression in cerebellar Purkinje cells J Neurosci 28 5752 5755 18509036 PMC2587083
- Terashima A Pelkey KA Rah JC Suh YH Roche KW Collingridge GL McBain CJ Isaac JT 2008 An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity Neuron 57 872 882 18367088 PMC2336895
- Traer CJ Rutherford AC Palmer KJ Wassmer T Oakley J Attar N Carlton JG Kremerskothen J Stephens DJ Cullen PJ 2007 SNX4 coordinates endosomal sorting of TfnR with dynein-mediated transport into the endocytic recycling compartment Nat Cell Biol 9 1370 1380 17994011
- Volk L Kim CH Takamiya K Yu Y Huganir RL 2010 Developmental regulation of protein interacting with C kinase 1 (PICK1) function in hippocampal synaptic plasticity and learning Proc Natl Acad Sci U S A PMC3003028 21106762
- Xia J Zhang X Staudinger J Huganir RL 1999 Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1 Neuron 22 179 187 10027300
- Yu J Zheng Y Dong J Klusza S Deng WM Pan D 2010 Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded Dev Cell 18 288 299 20159598 PMC2858562
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Self-citation
- Authors
- Makuch, L., Volk, L., Anggono, V., Johnson, R. C., Yu, Y., Duning, K., Kremerskothen, J., Xia, J., Takamiya, K., & Huganir, R. L.
- Affiliations
- Howard Hughes Medical Institute (US)
- University of Münster (DE)
- Hong Kong University of Science and Technology (HK)
- University of Miyazaki (JP)
- Corresponding author
- Huganir, Richard L.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2011-09
- Volume
- 71
- Issue
- 6
- Pages
- 1022-1029
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC3200575
- OpenAlex
- W2085596648
- Cited by
- 143
- References
- 3
- Citations by year
- 2026: 6 · 2025: 6 · 2024: 12 · 2023: 8 · 2022: 6 · 2021: 12 · 2020: 5 · 2019: 9 · 2018: 9 · 2017: 10 · 2016: 9 · 2015: 11 · 2014: 15 · 2013: 16 · 2012: 8
- FWCI
- 5.30
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Rare & Special e-Zone (The Hong Kong University of Science and Technology) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Japan Society for the Promotion of Science (22300122)
- National Institute of Mental Health (T32MH15330, MH64856, T32MH015330, R01MH064856)
- National Eye Institute (T32EY017203)
- National Institute of Neurological Disorders and Stroke (NS36715, R01NS036715, R37NS036715)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Neuroscience › Cognitive Neuroscience › Memory and Neural Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- KIBRA, AMPA receptors, PICK1, receptor trafficking, synaptic plasticity, long-term depression, long-term potentiation, hippocampus, contextual fear memory, NMDA receptor
- MeSH terms
- Animals, Behavior, Animal, Carrier Proteins, Cells, Cultured, Conditioning, Classical, Electrophysiology, Fear, Humans, Learning, Male, Memory, Mice, Inbred C57BL, Neuronal Plasticity, Neurons, Nuclear Proteins, Phosphoproteins, Receptors, AMPA, Mice, Knockout, Intracellular Signaling Peptides and Proteins, Mice
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