Divalent ion permeability of AMPA receptor channels is dominated by the edited form of a single subunit
Abstract
Functionally diverse GluR channels of the AMPA subtype are generated by the assembly of GluR-A, -B, -C, and -D subunits into homo- and heteromeric channels. The GluR-B subunit is dominant in determining functional properties of heteromeric AMPA receptors. This subunit exists in developmentally distinct edited and unedited forms, GluR-B(R) and GluR-B(Q), which differ in a single amino acid in transmembrane segment TM2 (Q/R site). Homomeric GluR-B(R) channels expressed in 293 cells display a low divalent permeability, whereas homomeric GluR-B(Q) and GluR-D channels exhibit a high divalent permeability. Mutational analysis revealed that both the positive charge and the size of the amino acid side chain located at the Q/R site control the divalent permeability of homomeric channels. Coexpression of Q/R site arginine- and glutamine-containing subunits generates cells with varying divalent permeabilities depending on the amounts of expression vectors used for cell transfection. Intermediate divalent permeabilities were traced to the presence of both divalent permeant homomeric and impermeant heteromeric channels. It is suggested that the positive charge contributed by the arginine of the edited GluR-B(R) subunit determines low divalent permeability in heteromeric GluR channels and that changes in GluR-B(R) expression regulate the AMPA receptor-dependent divalent permeability of a cell.
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GluA2-containing receptors have a linear current-voltage relationship and are impermeable to Ca2+, while GluA2-lacking receptors show high conductance, rapid decay kinetics, inward-rectification due to voltage-dependent block by intracellular polyamines, and are permeable to Ca2+.
“The result of this modification is that GluA2 containing receptors have a linear current-voltage (I-V) relationship and are impermeable to Ca2+, while GluA2-lacking receptors show high conductance and rapid decay kinetics, inward-rectification due to voltage-dependent block by intracellular polyamines and are permeable to Ca2+, thus GluA2-lacking receptors are usually referred to as calcium-perme”
From The AMPA Receptor Code of Synaptic Plasticity (2018) · cites this paper as Burnashev et al., 1992
Cites
Two types of kainate response in cultured rat hippocampal neurons
Ozawa, S., Iino, M., & Tsuzuki, K. (1991) · Journal of Neurophysiology · doi:10.1152/jn.1991.66.1.2 · Cited by 115 · see citing works
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Glutamate Receptor Ion Channels: Structure, Regulation, and Function
Traynelis, S. F., Wollmuth, L. P., McBain, C. J., Menniti, F. S., Vance, K. M., Ogden, K. K., Hansen, K. B., Yuan, H., Myers, S. J., & Dingledine, R. (2010) · Pharmacological Reviews · doi:10.1124/pr.109.002451 · Cited by 3,568 · see citing works
Heteromeric NMDA receptors: molecular and functional distinction of subtypes
Monyer, H., Sprengel, R., Schoepfer, R., Herb, A., Higuchi, M., Lomeli, H., Burnashev, N., Sakmann, B., & Seeburg, P. H. (1992) · Science · doi:10.1126/science.256.5060.1217 · Cited by 2,541 · see citing works
Self-citationGeiger, J. R. P., Melcher, T., Koh, D.-S., Sakmann, B., Seeburg, P. H., Jonas, P., & Monyer, H. (1995) · Neuron · doi:10.1016/0896-6273(95)90076-4 · Cited by 1,260 · see citing works
Self-citationGlutamatergic synaptic input to glioma cells drives brain tumour progression
Venkataramani, V., Tanev, D. I., Strahle, C., Studier-Fischer, A., Fankhauser, L., Kessler, T., Körber, C., Kardorff, M., Ratliff, M., Xie, R., et al. (2019) · Nature · doi:10.1038/s41586-019-1564-x · Cited by 1,197 · see citing works
GABA and glutamate depolarize cortical progenitor cells and inhibit DNA synthesis
LoTurco, J. J., Owens, D. F., Heath, M. J. S., Davis, M. B. E., & Kriegstein, A. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90008-x · Cited by 1,064 · see citing works
The AMPA Receptor Code of Synaptic Plasticity
Diering, G. H., & Huganir, R. L. (2018) · Neuron · doi:10.1016/j.neuron.2018.10.018 · Cited by 844 · see citing works
Control of Kinetic Properties of AMPA Receptor Channels by Nuclear RNA Editing
Lomeli, H., Mosbacher, J., Melcher, T., Höger, T., Geiger, J. R. P., Kuner, T., Monyer, H., Higuchi, M., Bach, A., & Seeburg, P. H. (1994) · Science · doi:10.1126/science.7992055 · Cited by 746 · see citing works
Self-citationStructure, Function, and Pharmacology of Glutamate Receptor Ion Channels
Hansen, K. B., Wollmuth, L. P., Bowie, D., Furukawa, H., Menniti, F. S., Sobolevsky, A. I., Swanson, G. T., Swanger, S. A., Greger, I. H., Nakagawa, T., et al. (2021) · Pharmacological Reviews · doi:10.1124/pharmrev.120.000131 · Cited by 686 · see citing works
Regulatory mechanisms of AMPA receptors in synaptic plasticity
Derkach, V. A., Oh, M. C., Guire, E. S., & Soderling, T. R. (2007) · Nature Reviews Neuroscience · doi:10.1038/nrn2055 · Cited by 708 · see citing works
Scofield, M. D., Heinsbroek, J. A., Gipson, C. D., Kupchik, Y. M., Spencer, S., Smith, A. C. W., Roberts-Wolfe, D., & Kalivas, P. W. (2016) · Pharmacological Reviews · doi:10.1124/pr.116.012484 · Cited by 598 · see citing works
Fuchs, E. C., Zivkovic, A. R., Cunningham, M. O., Middleton, S., LeBeau, F. E. N., Bannerman, D. M., Rozov, A., Whittington, M. A., Traub, R. D., Rawlins, J. N. P., et al. (2007) · Neuron · doi:10.1016/j.neuron.2007.01.031 · Cited by 532 · see citing works
Self-citationDeep molecular diversity of mammalian synapses: why it matters and how to measure it
O'Rourke, N. A., Weiler, N. C., Micheva, K. D., & Smith, S. J. (2012) · Nature Reviews Neuroscience · doi:10.1038/nrn3170 · Cited by 210 · see citing works
McBain, C. J., & Dingledine, R. (1993) · The Journal of Physiology · doi:10.1113/jphysiol.1993.sp019560 · Cited by 221 · see citing works
The lateral habenula in addiction and depression: an anatomical, synaptic and behavioral overview
Lecca, S., Meye, F. J., & Mameli, M. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12480 · Cited by 196 · see citing works
Muir, J. L., Page, K. J., Sirinathsinghji, D. J. S., Robbins, T. W., & Everitt, B. J. (1993) · Behavioural Brain Research · doi:10.1016/0166-4328(93)90128-d · Cited by 199 · see citing works
Akbarian, S., Smith, M. A., & Jones, E. G. (1995) · Brain Research · doi:10.1016/0006-8993(95)00922-d · Cited by 183 · see citing works
Lambolez, B., Ropert, N., Perrais, D., Rossier, J., & Hestrin, S. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.5.1797 · Cited by 147 · see citing works
Cueva Vargas, J. L., Osswald, I. K., Unsain, N., Aurousseau, M. R., Barker, P. A., Bowie, D., & Di Polo, A. (2015) · The Journal of Neuroscience · doi:10.1523/jneurosci.1273-15.2015 · Cited by 132 · see citing works
Immature Dentate Gyrus: An Endophenotype of Neuropsychiatric Disorders
Hagihara, H., Takao, K., Walton, N. M., Matsumoto, M., & Miyakawa, T. (2013) · Neural Plasticity · doi:10.1155/2013/318596 · Cited by 123 · see citing works
Jia, Y., Jeng, J., Sensi, S. L., & Weiss, J. H. (2002) · The Journal of Physiology · doi:10.1113/jphysiol.2002.020172 · Cited by 118 · see citing works
Rozov, A., Zilberter, Y., Wollmuth, L. P., & Burnashev, N. (1998) · The Journal of Physiology · doi:10.1111/j.1469-7793.1998.361bh.x · Cited by 114 · see citing works
Self-citationApproaches and Limitations in the Investigation of Synaptic Transmission and Plasticity
Glasgow, S. D., McPhedrain, R., Madranges, J. F., Kennedy, T. E., & Ruthazer, E. S. (2019) · Frontiers in Synaptic Neuroscience · doi:10.3389/fnsyn.2019.00020 · Cited by 100 · see citing works
Ho, M. T.-W., Pelkey, K. A., Topolnik, L., Petralia, R. S., Takamiya, K., Xia, J., Huganir, R. L., Lacaille, J.-C., & McBain, C. J. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2671-07.2007 · Cited by 98 · see citing works
Vulnerability of mesostriatal dopaminergic neurons in Parkinson’s disease
González-Hernández, T. (2010) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2010.00140 · Cited by 65 · see citing works
Memory, plasticity and sleep - A role for calcium permeable AMPA receptors?
Shepherd, J. D. (2012) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2012.00049 · Cited by 49 · see citing works
audinat, E., Lambolez, B., & Rossier, J. (1996) · Neurochemistry International · doi:10.1016/0197-0186(95)00075-5 · Cited by 41 · see citing works
Coombs, I. D., Ziobro, J., Krotov, V., Surtees, T., Cull‐Candy, S. G., & Farrant, M. (2022) · Epilepsia · doi:10.1111/epi.17419 · Cited by 32 · see citing works
Turcu, A. L., Companys-Alemany, J., Phillips, M. B., Patel, D. S., Griñán-Ferré, C., Loza, M. I., Brea, J. M., Pérez, B., Soto, D., Sureda, F. X., et al. (2022) · European Journal of Medicinal Chemistry · doi:10.1016/j.ejmech.2022.114354 · Cited by 27 · see citing works
- Authors
- Burnashev, N., Monyer, H., Seeburg, P. H., & Sakmann, B.
- Affiliations
- Max Planck Institute for Medical Research (DE)
- Max Planck Society (DE)
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1992-01
- Volume
- 8
- Issue
- 1
- Pages
- 189-198
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2051084778
- Cited by
- 1,087
- References
- 1
- Citations by year
- 2026: 9 · 2025: 17 · 2024: 19 · 2023: 20 · 2022: 13 · 2021: 19 · 2020: 24 · 2019: 19 · 2018: 17 · 2017: 24 · 2016: 16 · 2015: 20 · 2014: 29 · 2013: 25 · 2012: 35
- FWCI
- 28.94
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Max Planck Institute for Plasma Physics (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Keywords
- AMPA receptors, RNA editing, heteromeric channels, homomeric channels, ion channel permeation
- MeSH terms
- Base Sequence, Calcium, Cations, Divalent, Cell Line, Electrophysiology, Glutamates, Humans, Ion Channels, Magnesium, Membrane Potentials, Molecular Sequence Data, Permeability, Recombinant Proteins, RNA, Messenger, Sodium, Transfection, Gene Expression, Receptors, Neurotransmitter, Receptors, AMPA, Glutamic Acid, Macromolecular Substances
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