Saturday, March 22, 2025
No menu items!
HomeNatureGluA2-containing AMPA receptors form a continuum of Ca2+-permeable channels

GluA2-containing AMPA receptors form a continuum of Ca2+-permeable channels

  • Hansen, K. B. et al. Structure, function, and pharmacology of glutamate receptor ion channels. Pharmacol. Rev. 73, 298–487 (2021).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Nicoll, R. A. A brief history of long-term potentiation. Neuron 93, 281–290 (2017).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Turrigiano, G. G. The self-tuning neuron: synaptic scaling of excitatory synapses. Cell 135, 422–435 (2008).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Salpietro, V. et al. AMPA receptor GluA2 subunit defects are a cause of neurodevelopmental disorders. Nat. Commun. 10, 3094 (2019).

    Article 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Martin, S. et al. De novo variants in GRIA4 lead to intellectual disability with or without seizures and gait abnormalities. Am. J. Hum. Genet. 101, 1013–1020 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Wu, Y. et al. Mutations in ionotropic AMPA receptor 3 alter channel properties and are associated with moderate cognitive impairment in humans. Proc. Natl Acad. Sci. USA 104, 18163–18168 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar
     

  • Peall, K. J., Owen, M. J. & Hall, J. Rare genetic brain disorders with overlapping neurological and psychiatric phenotypes. Nat. Rev. Neurol. 20, 7–21 (2024).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sommer, B., Kohler, M., Sprengel, R. & Seeburg, P. H. RNA editing in brain controls a determinant of ion flow in glutamate-gated channels. Cell 67, 11–19 (1991).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Burnashev, N., Monyer, H., Seeburg, P. H. & Sakmann, B. Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit. Neuron 8, 189–198 (1992).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Bowie, D. Polyamine-mediated channel block of ionotropic glutamate receptors and its regulation by auxiliary proteins. J. Biol. Chem. 293, 18789–18802 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Herring, B. E. & Nicoll, R. A. Long-term potentiation: from CaMKII to AMPA receptor trafficking. Annu. Rev. Physiol. 78, 351–365 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Turrigiano, G. G. The dialectic of Hebb and homeostasis. Philos. Trans. R. Soc. Lond. B Biol. Sci. 372, 20160258 (2017).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Bowie, D. Redefining the classification of AMPA-selective ionotropic glutamate receptors. J. Physiol. 590, 49–61 (2012).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Jonas, P. The time course of signaling at central glutamatergic synapses. News Physiol. Sci. 15, 83–89 (2000).

    CAS 
    PubMed 
    MATH 
    ADS 

    Google Scholar
     

  • Jonas, P., Racca, C., Sakmann, B., Seeburg, P. H. & Monyer, H. Differences in Ca2+ permeability of AMPA-type glutamate receptor channels in neocortical neurons caused by differential GluR-B subunit expression. Neuron 12, 1281–1289 (1994).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Geiger, J. R. et al. Relative abundance of subunit mRNAs determines gating and Ca2+ permeability of AMPA receptors in principal neurons and interneurons in rat CNS. Neuron 15, 193–204 (1995).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Mosbacher, J. et al. A molecular determinant for submillisecond desensitization in glutamate receptors. Science 266, 1059–1062 (1994).

    Article 
    CAS 
    PubMed 
    MATH 
    ADS 

    Google Scholar
     

  • Burnashev, N. et al. Calcium-permeable AMPA-kainate receptors in fusiform cerebellar glial cells. Science 256, 1566–1570 (1992).

    Article 
    CAS 
    PubMed 
    MATH 
    ADS 

    Google Scholar
     

  • Blaschke, M. et al. A single amino acid determines the subunit-specific spider toxin block of alpha-amino-3-hydroxy-5-methylisoxazole-4-propionate/kainate receptor channels. Proc. Natl Acad. Sci. USA 90, 6528–6532 (1993).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Herlitze, S. et al. Argiotoxin detects molecular differences in AMPA receptor channels. Neuron 10, 1131–1140 (1993).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Mahanty, N. K. & Sah, P. Calcium-permeable AMPA receptors mediate long-term potentiation in interneurons in the amygdala. Nature 394, 683–687 (1998).

    Article 
    CAS 
    PubMed 
    MATH 
    ADS 

    Google Scholar
     

  • Liu, S. Q. & Cull-Candy, S. G. Synaptic activity at calcium-permeable AMPA receptors induces a switch in receptor subtype. Nature 405, 454–458 (2000).

    Article 
    CAS 
    PubMed 
    ADS 

    Google Scholar
     

  • Plant, K. et al. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat. Neurosci. 9, 602–604 (2006).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Granzotto, A., Weiss, J. H. & Sensi, S. L. Editorial: excitotoxicity turns 50. The death that never dies. Front Neurosci 15, 831809 (2021).

    Article 
    PubMed 

    Google Scholar
     

  • Kwak, S. & Weiss, J. H. Calcium-permeable AMPA channels in neurodegenerative disease and ischemia. Curr. Opin. Neurobiol. 16, 281–287 (2006).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Weiss, J. H. & Sensi, S. L. Ca2+-Zn2+ permeable AMPA or kainate receptors: possible key factors in selective neurodegeneration. Trends Neurosci. 23, 365–371 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Cueva Vargas, J. L. et al. Soluble tumor necrosis factor alpha promotes retinal ganglion cell death in glaucoma via calcium-permeable AMPA receptor activation. J. Neurosci. 35, 12088–12102 (2015).

    Article 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Schwenk, J. et al. High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes. Neuron 74, 621–633 (2012).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Schwenk, J. et al. Functional proteomics identify cornichon proteins as auxiliary subunits of AMPA receptors. Science 323, 1313–1319 (2009).

    Article 
    CAS 
    PubMed 
    MATH 
    ADS 

    Google Scholar
     

  • Perozzo, A. M., Brown, P. & Bowie, D. Alternative splicing of the flip/flop cassette and TARP auxiliary subunits engage in a privileged relationship that fine-tunes AMPA receptor gating. J. Neurosci. 43, 2837–2849 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dawe, G. B. et al. Nanoscale mobility of the apo state and TARP stoichiometry dictate the gating behavior of alternatively spliced AMPA receptors. Neuron 102, 976–992 e975 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Zhao, Y., Chen, S., Swensen, A. C., Qian, W. J. & Gouaux, E. Architecture and subunit arrangement of native AMPA receptors elucidated by cryo-EM. Science 364, 355–362 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar
     

  • Twomey, E. C., Yelshanskaya, M. V., Grassucci, R. A., Frank, J. & Sobolevsky, A. I. Elucidation of AMPA receptor-stargazin complexes by cryo-electron microscopy. Science 353, 83–86 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar
     

  • Perozzo, A. M. et al. GSG1L-containing AMPA receptor complexes are defined by their spatiotemporal expression, native interactome and allosteric sites. Nat. Commun. 14, 6799 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Twomey, E. C., Yelshanskaya, M. V., Grassucci, R. A., Frank, J. & Sobolevsky, A. I. Structural bases of desensitization in AMPA receptor-auxiliary subunit complexes. Neuron 94, 569–580 e565 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Zhang, D., Watson, J. F., Matthews, P. M., Cais, O. & Greger, I. H. Gating and modulation of a hetero-octameric AMPA glutamate receptor. Nature 594, 454–458 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    ADS 

    Google Scholar
     

  • Nakagawa, T. Structures of the AMPA receptor in complex with its auxiliary subunit cornichon. Science 366, 1259–1263 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Matt, L. et al. SynDIG4/Prrt1 is required for excitatory synapse development and plasticity underlying cognitive function. Cell Rep. 22, 2246–2253 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Diaz, E. Beyond the AMPA receptor: diverse roles of SynDIG/PRRT brain-specific transmembrane proteins at excitatory synapses. Curr. Opin. Pharmacol. 58, 76–82 (2021).

    Article 
    MATH 

    Google Scholar
     

  • Yu, J. et al. Hippocampal AMPA receptor assemblies and mechanism of allosteric inhibition. Nature 594, 448–453 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Boudkkazi, S., Brechet, A., Schwenk, J. & Fakler, B. Cornichon2 dictates the time course of excitatory transmission at individual hippocampal synapses. Neuron 82, 848–858 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • von Engelhardt, J. et al. CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus. Science 327, 1518–1522 (2010).

    Article 
    MATH 
    ADS 

    Google Scholar
     

  • Nakagawa, T., Wang, X. T., Miguez-Cabello, F. J. & Bowie, D. The open gate of the AMPA receptor forms a Ca(2+) binding site critical in regulating ion transport. Nat. Struct. Mol. Biol. 31, 688–700 (2024).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Tempia, F. et al. Fractional calcium current through neuronal AMPA-receptor channels with a low calcium permeability. J. Neurosci. 16, 456–466 (1996).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Gangwar, S. P. et al. Modulation of GluA2-gamma5 synaptic complex desensitization, polyamine block and antiepileptic perampanel inhibition by auxiliary subunit cornichon-2. Nat. Struct. Mol. Biol. 30, 1481–1494 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Hawken, N. M., Zaika, E. I. & Nakagawa, T. Engineering defined membrane-embedded elements of AMPA receptor induces opposing gating modulation by cornichon 3 and stargazin. J. Physiol. 595, 6517–6539 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dingledine, R., Hume, R. I. & Heinemann, S. F. Structural determinants of barium permeation and rectification in non-NMDA glutamate receptor channels. J. Neurosci. 12, 4080–4087 (1992).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Brown, P., McGuire, H. & Bowie, D. Stargazin and cornichon-3 relieve polyamine block of AMPA receptors by enhancing blocker permeation. J. Gen. Physiol. 150, 67–82 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ohkura, M. et al. Genetically encoded green fluorescent Ca2+ indicators with improved detectability for neuronal Ca2+ signals. PLoS ONE 7, e51286 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 
    ADS 

    Google Scholar
     

  • Bowie, D., Lange, G. D. & Mayer, M. L. Activity-dependent modulation of glutamate receptors by polyamines. J. Neurosci. 18, 8175–8185 (1998).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Isaac, J. T., Ashby, M. C. & McBain, C. J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 54, 859–871 (2007).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Osswald, I. K., Galan, A. & Bowie, D. Light triggers expression of philanthotoxin-insensitive Ca2+-permeable AMPA receptors in the developing rat retina. J. Physiol. 582, 95–111 (2007).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Mattison, H. A. et al. Evidence of calcium-permeable AMPA receptors in dendritic spines of CA1 pyramidal neurons. J. Neurophysiol. 112, 263–275 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Schwenk, J. et al. Regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain. Neuron 84, 41–54 (2014).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • XiangWei, W. et al. Clinical and functional consequences of GRIA variants in patients with neurological diseases. Cell. Mol. Life Sci. 80, 345 (2023).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Brown, P. M., Aurousseau, M. R., Musgaard, M., Biggin, P. C. & Bowie, D. Kainate receptor pore-forming and auxiliary subunits regulate channel block by a novel mechanism. J. Physiol. 594, 1821–1840 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bowie, D., Garcia, E. P., Marshall, J., Traynelis, S. F. & Lange, G. D. Allosteric regulation and spatial distribution of kainate receptors bound to ancillary proteins. J. Physiol. 547, 373–385 (2003).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Alexander, R. P. D. & Bowie, D. Intrinsic plasticity of cerebellar stellate cells is mediated by NMDA receptor regulation of voltage-gated Na(+) channels. J. Physiol. 599, 647–665 (2021).

    Article 
    CAS 
    PubMed 
    MATH 

    Google Scholar
     

  • Wong, A. Y., Fay, A. M. & Bowie, D. External ions are coactivators of kainate receptors. J. Neurosci. 26, 5750–5755 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Woodhull, A. M. Ionic blockage of sodium channels in nerve. J. Gen. Physiol. 61, 687–708 (1973).

    Article 
    CAS 
    PubMed 
    PubMed Central 
    MATH 

    Google Scholar
     

  • Konishi, S. & Kitagawa, G. Information Criteria and Statistical Modeling (Springer, 2008).

  • Efron, B. & Tibshirani, R. An Introduction to the Bootstrap (Chapman and Hall, 1993).

  • RELATED ARTICLES

    Most Popular

    Recent Comments