Glutamate receptors regulate actin-based plasticity in dendritic spines
Abstract
Dendritic spines at excitatory synapses undergo rapid, actin-dependent shape changes which may contribute to plasticity in brain circuits. Here we show that actin dynamics in spines are potently inhibited by activation of either AMPA or NMDA subtype glutamate receptors. Activation of either receptor type inhibited actin-based protrusive activity from the spine head. This blockade of motility caused spines to round up so that spine morphology became both more stable and more regular. Inhibition of spine motility by AMPA receptors was dependent on postsynaptic membrane depolarization and influx of Ca 2+ through voltage-activated channels. In combination with previous studies, our results suggest a two-step process in which spines initially formed in response to NMDA receptor activation are subsequently stabilized by AMPA receptors.
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Spine motility was inhibited by application of AMPA-R agonists.
“and spine motility was inhibited by application of AMPA-R agonists (24).”
From AMPA receptor and GEF-H1/Lfc complex regulates dendritic spine development through RhoA signaling cascade (2009) · cites this paper as [24]
Cites
Rapid Actin-Based Plasticity in Dendritic Spines
Fischer, M., Kaech, S., Knutti, D., & Matus, A. (1998) · Neuron · doi:10.1016/s0896-6273(00)80467-5 · Cited by 905 · see citing works
Self-citationDevelopmental regulation of spine motility in the mammalian central nervous system
Dunaevsky, A., Tashiro, A., Majewska, A., Mason, C., & Yuste, R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.23.13438 · Cited by 412 · see citing works
Regulation of F-Actin Stability in Dendritic Spines by Glutamate Receptors and Calcineurin
Halpain, S., Hipolito, A., & Saffer, L. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09835.1998 · Cited by 408 · cited 1× · see citing works
“Spine motility is sensitive to AMPA receptor activation To eliminate NMDA receptor-induced excitotoxic effects that occur when hippocampal neurons are exposed to glutamat”
BackgroundChapter 6 Glutamate receptors and the induction of excitotoxic neuronal death
Choi, D. W. (1994) · Progress in Brain Research · doi:10.1016/s0079-6123(08)60767-0 · Cited by 385 · see citing works
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Cited by
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Distinct morphological stages of dentate granule neuron maturation in the adult mouse hippocampus
Zhao, C., Teng, E. M., Summers, R. G., Ming, G.-L., & Gage, F. H. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.3648-05.2006 · Cited by 1,257 · see citing works
Structure and function of dendritic spines
Nimchinsky, E. A., Sabatini, B. L., & Svoboda, K. (2002) · Annual Review of Physiology · doi:10.1146/annurev.physiol.64.081501.160008 · Cited by 1,208 · see citing works
Hoover, B. R., Reed, M. N., Su, J., Penrod, R. D., Kotilinek, L. A., Grant, M. K., Pitstick, R., Carlson, G. A., Lanier, L. M., Yuan, L.-L., et al. (2010) · Neuron · doi:10.1016/j.neuron.2010.11.030 · Cited by 1,118 · see citing works
Dentritic spines : structure, dynamics and regulation
Hering, H., & Sheng, M. (2001) · Nature Reviews Neuroscience · doi:10.1038/35104061 · Cited by 961 · see citing works
Stress duration modulates the spatiotemporal patterns of spine formation in the basolateral amygdala
Mitra, R., Jadhav, S., McEwen, B. S., Vyas, A., & Chattarji, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504011102 · Cited by 663 · 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
Dendritic spines and long-term plasticity
Segal, M. (2005) · Nature Reviews Neuroscience · doi:10.1038/nrn1649 · Cited by 489 · see citing works
Bonhoeffer, T., & Yuste, R. (2002) · Neuron · doi:10.1016/s0896-6273(02)00906-6 · Cited by 337 · see citing works
Raven, F., Van der Zee, E. A., Meerlo, P., & Havekes, R. (2018) · Sleep Medicine Reviews · doi:10.1016/j.smrv.2017.05.002 · Cited by 331 · see citing works
Restivo, L., Ferrari, F., Passino, E., Sgobio, C., Bock, J., Oostra, B. A., Bagni, C., & Ammassari-Teule, M. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504984102 · Cited by 299 · see citing works
Role of actin cytoskeleton in dendritic spine morphogenesis
Sekino, Y., Kojima, N., & Shirao, T. (2007) · Neurochemistry International · doi:10.1016/j.neuint.2007.04.029 · Cited by 294 · see citing works
Dendritic Spine Dynamics Are Regulated by Monocular Deprivation and Extracellular Matrix Degradation
Oray, S., Majewska, A., & Sur, M. (2004) · Neuron · doi:10.1016/j.neuron.2004.12.001 · Cited by 296 · see citing works
Activity-Dependent Redistribution and Essential Role of Cortactin in Dendritic Spine Morphogenesis
Hering, H., & Sheng, M. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-37-11759.2003 · Cited by 269 · see citing works
Lang, C., Barco, A., Zablow, L., Kandel, E. R., Siegelbaum, S. A., & Zakharenko, S. S. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0407581101 · Cited by 245 · see citing works
Pawlak, R., Rao, B. S. S., Melchor, J. P., Chattarji, S., McEwen, B., & Strickland, S. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0509232102 · Cited by 223 · see citing works
Shi, Y., & Ethell, I. M. (2006) · The Journal of Neuroscience · doi:10.1523/jneurosci.4091-05.2006 · Cited by 200 · see citing works
Protracted synaptogenesis after activity-dependent spinogenesis in hippocampal neurons
Nägerl, U. V., Köstinger, G., Anderson, J. C., Martin, K. A. C., & Bonhoeffer, T. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.0511-07.2007 · Cited by 178 · see citing works
Chen, N., & Napoli, J. L. (2008) · The FASEB Journal · doi:10.1096/fj.07-8739com · Cited by 166 · see citing works
Glutamate induces the rapid formation of spine head protrusions in hippocampal slice cultures
Richards, D. A., Mateos, J. M., Hugel, S., de Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0501881102 · Cited by 161 · see citing works
AMPA receptors as drug targets in neurological disease—advantages, caveats, and future outlook
Chang, P. K. ‐., Verbich, D., & McKinney, R. A. (2012) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2012.08165.x · Cited by 155 · see citing works
The ‘conscious pilot’ — dendritic synchrony moves through the brain to mediate consciousness.
Hameroff, S. (2010) · Journal of Biological Physics · doi:10.1007/s10867-009-9148-x · Cited by 107 · see citing works
Scaffolding proteins at the postsynaptic density: shank as the architectural framework
Kreienkamp, H. J. (2008) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-72843-6_15 · Cited by 105 · see citing works
Chen, Y.-K., & Hsueh, Y.-P. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.4405-11.2012 · Cited by 90 · see citing works
Tropea, D., Majewska, A. K., Garcia, R., & Sur, M. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1661-10.2010 · Cited by 92 · see citing works
Kang, M.-G., Guo, Y., & Huganir, R. L. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812861106 · Cited by 82 · see citing works
Dendritic spine actin cytoskeleton in autism spectrum disorder
Joensuu, M., Lanoue, V., & Hotulainen, P. (2018) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2017.08.023 · Cited by 65 · see citing works
Neurotransmitters and the Development of Neuronal Circuits
Ruediger, T., & Bolz, J. (2007) · Advances in Experimental Medicine and Biology · doi:10.1007/978-0-387-76715-4_8 · Cited by 62 · see citing works
Spolidoro, M., Putignano, E., Munafò, C., Maffei, L., & Pizzorusso, T. (2012) · Cerebral Cortex · doi:10.1093/cercor/bhr158 · Cited by 58 · see citing works
Principal cell activity induces spine relocation of adult-born interneurons in the olfactory bulb
Breton-Provencher, V., Bakhshetyan, K., Hardy, D., Bammann, R. R., Cavarretta, F., Snapyan, M., Côté, D., Migliore, M., & Saghatelyan, A. (2016) · Nature Communications · doi:10.1038/ncomms12659 · Cited by 60 · see citing works
Richards, D. A., De Paola, V., Caroni, P., Gähwiler, B. H., & McKinney, R. A. (2004) · The Journal of Physiology · doi:10.1113/jphysiol.2004.062091 · Cited by 49 · see citing works
Zago, W. M., Massey, K. A., & Berg, D. K. (2006) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2005.11.009 · Cited by 24 · see citing works
Waller, J. A., Chen, F., & Sánchez, C. (2016) · Neuropharmacology · doi:10.1016/j.neuropharm.2015.12.012 · Cited by 25 · see citing works
Schätzle, P., Ster, J., Verbich, D., McKinney, R. A., Gerber, U., Sonderegger, P., & María Mateos, J. (2011) · The Journal of Physiology · doi:10.1113/jphysiol.2010.204446 · Cited by 20 · see citing works
Time-lapse imaging of dendritic spines in vitro
Verkuyl, J. M., & Matus, A. (2006) · Nature Protocols · doi:10.1038/nprot.2006.357 · Cited by 13 · see citing works
Self-citation
- Authors
- Fischer, M., Kaech, S., Wagner, U., Brinkhaus, H., & Matus, A.
- Affiliations
- Friedrich Miescher Institute (CH)
- Corresponding author
- Matus, Andrew
- ORCID
- Kaech, Stefanie
- Venue
- Nature Neuroscience
- Published
- 2000-09
- Volume
- 3
- Issue
- 9
- Pages
- 887-894
- ISSN
- 1097-6256 (ISSN-L)
- 1546-1726
- OpenAlex
- W1479736082
- Cited by
- 446
- References
- 4
- Citations by year
- 2026: 6 · 2025: 1 · 2024: 7 · 2023: 1 · 2022: 5 · 2021: 8 · 2020: 7 · 2019: 13 · 2018: 8 · 2017: 13 · 2016: 10 · 2015: 12 · 2014: 19 · 2013: 14 · 2012: 27
- FWCI
- 11.08
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Nature Neuroscience (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Health Sciences › Medicine › Pharmacology › Treatment of Major Depression
- Keywords
- dendritic spines, glutamate receptors, AMPA receptors, NMDA receptor, actin dynamics, spine motility, synaptic plasticity, dendritic spine morphology, postsynaptic depolarization, calcium influx, spinal stabilization
- MeSH terms
- Actins, Animals, Calcium, Cell Movement, Cells, Cultured, Dendrites, Hippocampus, Luminescent Proteins, Membrane Potentials, Mice, Transgenic, Neuronal Plasticity, Organ Culture Techniques, Synapses, Receptors, N-Methyl-D-Aspartate, Receptors, Glutamate, Receptors, AMPA, Cell Size, Green Fluorescent Proteins, Mice
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