Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPAreceptors

Luchkina, N.V., Coleman, S.K., Huupponen, J., Cai, C., Kivisto, A., Taira, T., Keinanen, K. and Lauri, S.E. 2017. Molecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPAreceptors. Neuropharmacology. 112 (Part A), pp. 46-56. https://doi.org/10.1016/j.neuropharm.2016.04.049

TitleMolecular mechanisms controlling synaptic recruitment of GluA4 subunit-containing AMPAreceptors
TypeJournal article
AuthorsLuchkina, N.V., Coleman, S.K., Huupponen, J., Cai, C., Kivisto, A., Taira, T., Keinanen, K. and Lauri, S.E.
Abstract

Synaptic recruitment of AMPA receptors (AMPARs) represents a key postsynaptic mechanism driving functional development and maturation of glutamatergic synapses. At immature hippocampal synapses, PKA-driven synaptic insertion of GluA4 is the predominant mechanism for synaptic reinforcement. However, the physiological significance and molecular determinants of this developmentally restricted form of plasticity are not known. Here we show that PKA activation leads to insertion of GluA4 to synaptic sites with initially weak or silent AMPAR-mediated transmission. This effect depends on a novel mechanism involving the extreme C-terminal end of GluA4, which interacts with the membrane proximal region of the C-terminal domain to control GluA4 trafficking. In the absence of GluA4, strengthening of AMPAR-mediated transmission during postnatal development was significantly delayed. These data suggest that the GluA4-mediated activation of silent synapses is a critical mechanism facilitating the functional maturation of glutamatergic circuitry during the critical period of experience-dependent fine-tuning.

KeywordsAMPA –receptor, GluA4, silent synapse, development, synaptic targeting
JournalNeuropharmacology
Journal citation112 (Part A), pp. 46-56
ISSN0028-3908
Year2017
PublisherElsevier
Accepted author manuscript
Digital Object Identifier (DOI)https://doi.org/10.1016/j.neuropharm.2016.04.049
PubMed ID27157711
Publication dates
Published in printJan 2017
Published online05 May 2016
Published05 May 2016

Related outputs

New ways of working in School of Life Sciences
Smith, C.L. and Coleman, S.K. 2022. New ways of working in School of Life Sciences. University of Westminster Annual Learning and Teaching Symposium 2022. London 06 - 07 Sep 2022

Addressing the challenges of delivering a laboratory class when students are miles away
Smith, C.L. and Coleman, S.K. 2021. Addressing the challenges of delivering a laboratory class when students are miles away. Horizons in STEM Higher Education Conference Proceedings Making Connections, Innovating and Sharing Pedagogy. The Open University - Online 29 - 30 Jul 2021 Open University.

Adapting a large class practical skills examination during the Covid-19 pandemic
Smith, C.L. and Coleman, S.K. 2021. Adapting a large class practical skills examination during the Covid-19 pandemic. Evolving molecular bioscience education. Online 27 - 28 May 2021

Evaluating the benefits of virtual training for bioscience students
Coleman, S.K. and Smith, C.L. 2019. Evaluating the benefits of virtual training for bioscience students. Higher Education Pedagogies. 4 (1), pp. 287-299. https://doi.org/10.1080/23752696.2019.1599689

Employer and work-based student perceptions of virtual laboratory teaching and assessment resources
Smith, C.L., Coleman, S.K. and Ferrier, C. 2019. Employer and work-based student perceptions of virtual laboratory teaching and assessment resources. Work Based Learning e-Journal International. 8 (1), pp. 53-70.

Evaluating the benefits of virtual training for students
Coleman, S.K. and Smith, C.L. 2018. Evaluating the benefits of virtual training for students. Westminster Learning and Teaching Symposium. London, UK 26 Jun 2018

Employer and part-time student perceptions of virtual laboratory teaching and assessment resources
Smith, C.L., Ferrier, C. and Coleman, S.K. 2018. Employer and part-time student perceptions of virtual laboratory teaching and assessment resources. Creating Relevant Learning Experiences; employers ’ involvement with higher education. Leuven, Belgium 14 - 15 Jun 2018

Using virtual reality laboratories to improve engagement and understanding for wet laboratory practical sessions
Coleman, S.K., Smith, C.L. and Ferrier, C. 2018. Using virtual reality laboratories to improve engagement and understanding for wet laboratory practical sessions. Society for Experimental Biology: Masters of Biology. Florence, Italy 03 - 06 Jul 2018

Evaluating the benefits of virtual training for bioscience students
Smith, C.L. and Coleman, S.K. 2018. Evaluating the benefits of virtual training for bioscience students. Annual STEM Conference 2018 Creativity in Teaching, Learning and Student Engagement. Newcastle-upon-Tyne 31 Jan - 01 Feb 2018 Higher Education Academy.

Using virtual reality to prepare Bioscience students for practical classes
Coleman, S.K., Volpi, E. and Smith, C.L. 2017. Using virtual reality to prepare Bioscience students for practical classes. 16th Westminster Symposium Innovate!. University of Westminster, London 22 - 22 Jun 2017

Increasing accessibility of students to laboratory classes through the use of Virtual laboratory simulations
Smith, C.L. and Coleman, S.K. 2017. Increasing accessibility of students to laboratory classes through the use of Virtual laboratory simulations . UALL Work and Learning Network Annual Conference 2017 - Leading the Way: Shaping Practice in the Workplace and the Academy.. Middlesex University 23 - 23 Jun 2017

Using Labster to improve Bioscience student learning and engagement in practical classes
Smith, C.L. and Coleman, S.K. 2017. Using Labster to improve Bioscience student learning and engagement in practical classes. Heads of Biological Sciences, Royal Society of Biology. Spring 2017 meeting.. University of Leicester 10 - 11 May 2017

Cysteine 893 is a target of regulatory thiol modifications of GluA1 AMPA receptors
von Ossowski, L., Li, L-L., Moykkynen, T., Coleman, S.K., Courtney, M.J. and Keinänen, K. 2017. Cysteine 893 is a target of regulatory thiol modifications of GluA1 AMPA receptors. PLoS ONE. 12 (2) e0171489. https://doi.org/10.1371/journal.pone.0171489

Art Science Collaboration: Life in a New Light
Smith, R.A.J., Coleman, S.K. and Ramashye, P. 2016. Art Science Collaboration: Life in a New Light. Creativity in Science Teaching, Society of Experimental Biology. Charles Darwin House, London, UK 12 - 14 Dec 2016

Aggregation Limits Surface Expression of Homomeric GluA3 Receptors
Coleman, S.K., Hou, Y., Willibald, M., Semenov, A., Moykkynen, T. and Keinänen, K. 2016. Aggregation Limits Surface Expression of Homomeric GluA3 Receptors. Journal of Biological Chemistry. 291, pp. 8784-8794 jbc.M115.689125. . https://doi.org/10.1074/jbc.M115.689125

The N-terminal domain modulates α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor desensitization
Moykkynen, T., Coleman, S.K., Semenov, A. and Keinänen, K. 2014. The N-terminal domain modulates α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor desensitization. Journal of Biological Chemistry. 289 (19), pp. 13197-13205. https://doi.org/10.1074/jbc.M113.526301

Developmental switch in the kinase dependency of long-term potentiation depends on expression of GluA4 subunit-containing AMPA receptors.
Luchkina, N.V., Huupponen, J., Clarke, V.R., Coleman, S.K., Keinänen, K., Taira, T. and Lauri SE 2014. Developmental switch in the kinase dependency of long-term potentiation depends on expression of GluA4 subunit-containing AMPA receptors. Proceedings of the National Academy of Sciences of the United States of America. 111 (11), p. 4321–4326. https://doi.org/10.1073/pnas.1315769111

Post-Synapse Model Cell for Synaptic Glutamate Receptor (GluR)-Based Biosensing: Strategy and Engineering to Maximize Ligand-Gated Ion-Flux Achieving High Signal-to-Noise Ratio
Akito Tateishi, Sarah K. Coleman, Satoshi Migita, Kari Keinänen and Tetsuya Haruyama 2012. Post-Synapse Model Cell for Synaptic Glutamate Receptor (GluR)-Based Biosensing: Strategy and Engineering to Maximize Ligand-Gated Ion-Flux Achieving High Signal-to-Noise Ratio. Sensors. 12 (1), pp. 1035-1041. https://doi.org/10.3390/s120101035

Autoinactivation of the stargazin-AMPA receptor complex: subunit-dependency and independence from physical dissociation.
Semenov, A., Möykkynen, T., Coleman, S.K., Korpi, E.R. and Keinänen, K. 2012. Autoinactivation of the stargazin-AMPA receptor complex: subunit-dependency and independence from physical dissociation. PLoS ONE. 7 (11) e49282. https://doi.org/10.1371/journal.pone.0049282

Cold-adapted protease enables quantitation of surface proteins in the absence of membrane trafficking.
Ahmad, F., Coleman, S.K., Kaila, K. and Blaesse, P. 2011. Cold-adapted protease enables quantitation of surface proteins in the absence of membrane trafficking. BioTechniques. 50 (4), pp. 255-257. https://doi.org/10.2144/000113651

Analysis of the potential role of GluA4 carboxyl-terminus in PDZ interactions.
Coleman, S.K., Cai, C., Kalkkinen, N., Korpi, E.R. and Keinänen, K. 2010. Analysis of the potential role of GluA4 carboxyl-terminus in PDZ interactions. PLoS ONE. 5 (1) e8715. https://doi.org/10.1371/journal.pone.0008715

Ligand-binding domain determines endoplasmic reticulum exit of AMPA receptors.
Coleman, S.K., Möykkynen, T., Hinkkuri, S., Vaahtera, L., Korpi, E.R., Pentikäinen, O.T. and Keinänen, K. 2010. Ligand-binding domain determines endoplasmic reticulum exit of AMPA receptors. Journal of Biological Chemistry. 285 (46), pp. P36032-36039. https://doi.org/10.1074/jbc.m110.156943

Agonist occupancy is essential for forward trafficking of AMPA receptors.
Coleman, S.K., Möykkynen, T., Jouppila, A., Koskelainen, S., Rivera, C., Korpi, E.R. and Keinänen, K. 2009. Agonist occupancy is essential for forward trafficking of AMPA receptors. Journal of Neuroscience. 29 (2), pp. 303-312. https://doi.org/10.1523/jneurosci.3953-08.2009

Dynamic visualization of membrane-inserted fraction of pHluorin-tagged channels using repetitive acidification technique.
Khiroug, S.S., Pryazhnikov, E., Coleman, S.K., Jeromin, A., Keinänen, K. and Khiroug, L. 2009. Dynamic visualization of membrane-inserted fraction of pHluorin-tagged channels using repetitive acidification technique. BMC Neuroscience. 10 141. https://doi.org/10.1186/1471-2202-10-141

Ethanol increases desensitization of recombinant GluR-D AMPA receptor and TARP combinations
Tommi P. Möykkynen, Coleman, S.K., Kari Keinänen, David M. Lovinger and Esa R. Korpi 2009. Ethanol increases desensitization of recombinant GluR-D AMPA receptor and TARP combinations. Alcohol. 43 (4), pp. 277-284. https://doi.org/10.1016/j.alcohol.2009.04.005

KCC2 interacts with the dendritic cytoskeleton to promote spine development.
Li, H., Khirug, S., Cai, C., Ludwig, A., Blaesse, P., Kolikova, J., Afzalov, R., Coleman, S.K., Lauri, S., Airaksinen, M.S., Keinänen, K., Khiroug, L., Saarma, M., Kaila, K. and Rivera, C. 2007. KCC2 interacts with the dendritic cytoskeleton to promote spine development. Neuron. 56 (6), pp. P1019-1033. https://doi.org/10.1016/j.neuron.2007.10.039

Isoform-specific early trafficking of AMPA receptor flip and flop variants
Coleman, S.K., Möykkynen, T., Cai, C., von Ossowski, L., Kuismanen, E., Korpi, E.R. and Keinänen, K. 2006. Isoform-specific early trafficking of AMPA receptor flip and flop variants. Journal of Neuroscience. 26 (43), pp. 11220-11229. https://doi.org/10.1523/jneurosci.2301-06.2006

Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein.
Coleman, SK.., Cai, C., Mottershead, D.G., Haapalahti, J.P. and Keinänen, K. 2003. Surface expression of GluR-D AMPA receptor is dependent on an interaction between its C-terminal domain and a 4.1 protein. Journal of Neuroscience. 23 (3), pp. 798-806. https://doi.org/10.1523/jneurosci.23-03-00798.2003

Characterization of the functional role of the N-glycans in the AMPA receptor ligand-binding domain
Arja Pasternack, Sarah K. Coleman, James Féthière, Dean R. Madden, Jean-Pierre LeCaer, Jean Rossier, Michael Pasternack and Kari Keinänen 2003. Characterization of the functional role of the N-glycans in the AMPA receptor ligand-binding domain. Journal of Neurochemistry. 84 (5), pp. 1184-1192. https://doi.org/10.1046/j.1471-4159.2003.01611.x

Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif.
Cai, C., Coleman, S.K., Niemi, K. and Keinänen, K. 2002. Selective binding of synapse-associated protein 97 to GluR-A alpha-amino-5-hydroxy-3-methyl-4-isoxazole propionate receptor subunit is determined by a novel sequence motif. Journal of Biological Chemistry. 277 (35), pp. P31484-31490. https://doi.org/10.1074/jbc.m204354200

Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain.
Pasternack, A., Coleman, S.K., Jouppila, A., Mottershead, D.G., Lindfors, M., Pasternack, M. and Keinänen, K. 2002. Alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor channels lacking the N-terminal domain. Journal of Biological Chemistry. 277 (51), pp. P49662-49667. https://doi.org/10.1074/jbc.m208349200

Subunit Composition of Kv1 Channels in Human CNS
Coleman, S.K., Newcombe, J., Pryke, J. and Dolly, J.O. 1999. Subunit Composition of Kv1 Channels in Human CNS. Journal of Neurochemistry. 73 (2), pp. 849-858. https://doi.org/10.1046/j.1471-4159.1999.0730849.x

Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule.
Chazot, P.L., Coleman, S.K., Cik, M. and Stephenson, F.A. 1994. Molecular characterization of N-methyl-D-aspartate receptors expressed in mammalian cells yields evidence for the coexistence of three subunit types within a discrete receptor molecule. Journal of Biological Chemistry. 269 (39), pp. 24403-24409. https://doi.org/10.1016/s0021-9258(19)51098-5

Permalink - https://westminsterresearch.westminster.ac.uk/item/9w897/molecular-mechanisms-controlling-synaptic-recruitment-of-glua4-subunit-containing-ampareceptors


Share this

Usage statistics

128 total views
298 total downloads
These values cover views and downloads from WestminsterResearch and are for the period from September 2nd 2018, when this repository was created.