The DOI matches its Crossref record; 13 of the 13 references it cites were found in a registry or an index.
PRRT1 regulates basal and plasticity-induced AMPA receptor trafficking
Abstract
AMPA-type glutamate receptors (AMPAR) are one of the principal mediators of fast excitatory synaptic transmission in the brain. These receptors associate with multiple integral membrane proteins which influence their trafficking and channel properties. Proline-rich transmembrane protein 1 (PRRT1) is a membrane protein and an understudied component of native AMPAR complexes. In order to understand the regulation of AMPARs by PRRT1, we have performed electrophysiological and biochemical investigations on acute hippocampal slices derived from PRRT1 knockout mice. Our results show that PRRT1 controls the levels of AMPARs at the cell surface, though it is dispensable for synaptic transmission. PRRT1 has differential effects on the stability of AMPAR GluA1 subunit phosphorylated at S845 and at S831, two residues at which the phosphorylation status has major influences on receptor trafficking. Furthermore, PRRT1 is required for NMDA receptor-dependent long-term depression (LTD) and proper NMDA-induced AMPAR trafficking. These findings position PRRT1 as an important regulator of AMPAR stabilization and trafficking in different subcellular pools under basal conditions and during synaptic plasticity.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Mice lacking SynDIG4 are impaired in single tetanus-induced LTP and NMDAR-dependent LTD.
“Mice lacking SynDIG4 have reduced surface expression of GluA1 and GluA2 and are impaired in single tetanus-induced long-term potentiation and NMDA receptor (NMDAR)-dependent long-term depression.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Total levels of AMPARs are unchanged in SynDIG4 KO mice.
“In SynDIG4 knockout (KO) mice, while total levels of AMPARs are unchanged, surface expression of GluA1 and GluA2 was significantly decreased (Troyano-Rodriguez et al., 2019).”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Both NMDAR-dependent LTD and single tetanus-induced LTP are impaired in SynDIG4 deficient neurons while baseline synaptic transmission is intact.
“Intriguingly, both NMDAR-dependent LTD (Troyano-Rodriguez et al., 2019) and single tetanus-induced LTP (Matt et al., 2018), which require calcium-permeable AMPARs (Sanderson et al., 2016), which are mostly GluA1 homomers, are impaired in SynDIG4 deficient neurons while baseline synaptic transmission is intact.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Mice lacking SynDIG4 have reduced surface expression of GluA1 and GluA2.
“Mice lacking SynDIG4 have reduced surface expression of GluA1 and GluA2 and are impaired in single tetanus-induced long-term potentiation and NMDA receptor (NMDAR)-dependent long-term depression.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Previous work showed decreased surface expression of GluA1 and GluA2 in SynDIG4 KO neurons.
“Previous work showed decreased surface expression of GluA1 and GluA2 (Troyano-Rodriguez et al., 2019) and reduced density of extrasynaptic GluA1 and GluA2 puncta in SynDIG4 KO neurons (Matt et al., 2018).”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
SynDIG4 functions as an auxiliary factor of AMPARs and plays a critical role in excitatory synaptic plasticity and hippocampal-dependent learning and memory.
“The transmembrane protein Synapse Differentiation Induced Gene 4 (SynDIG4) functions as an auxiliary factor of AMPA receptors (AMPARs) and plays a critical role in excitatory synaptic plasticity as well as hippocampal-dependent learning and memory.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
SynDIG4 KO neurons display deficits in LTD and single-tetanus LTP, both of which require GluA1.
“SynDIG4 KO neurons display deficits in LTD (Troyano-Rodriguez et al., 2019) and single-tetanus LTP (Matt et al., 2018), both of which require GluA1.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Baseline synaptic transmission is intact in SynDIG4 KO neurons.
“Furthermore, NMDA receptor (NMDAR)-dependent long-term depression (LTD) (Troyano-Rodriguez et al., 2019) and single tetanus-induced long-term potentiation (LTP) (Matt et al., 2018) are impaired in SynDIG4 KO neurons while baseline synaptic transmission is intact.”
From Loss of SynDIG4/PRRT1 alters distribution of AMPA receptors in Rab4- and Rab11-positive endosomes and impairs basal AMPA receptor recycling (2025) · cites this paper as Troyano-Rodriguez et al., 2019
Citations
Cites
Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms
Chen, L., Chetkovich, D. M., Petralia, R. S., Sweeney, N. T., Kawasaki, Y., Wenthold, R. J., Bredt, D. S., & Nicoll, R. A. (2000) · Nature · doi:10.1038/35050030 · Cited by 1,111
PKA phosphorylation of AMPA receptor subunits controls synaptic trafficking underlying plasticity
Esteban, J. A., Shi, S.-H., Wilson, C., Nuriya, M., Huganir, R. L., & Malinow, R. (2003) · Nature Neuroscience · doi:10.1038/nn997 · Cited by 894
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
Regulation of AMPA receptor endocytosis by a signaling mechanism shared with LTD
Beattie, E. C., Carroll, R. C., Yu, X., Morishita, W., Yasuda, H., von Zastrow, M., & Malenka, R. C. (2000) · Nature Neuroscience · doi:10.1038/81823 · Cited by 745
Recycling Endosomes Supply AMPA Receptors for LTP
Park, M., Penick, E. C., Edwards, J. G., Kauer, J. A., & Ehlers, M. D. (2004) · Science · doi:10.1126/science.1102026 · Cited by 730
Regulation of AMPA receptor trafficking and synaptic plasticity
Anggono, V., & Huganir, R. L. (2012) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2011.12.006 · Cited by 588
Hippocampal LTP and contextual learning require surface diffusion of AMPA receptors
Penn, A. C., Zhang, C. L., Georges, F., Royer, L., Breillat, C., Hosy, E., Petersen, J. D., Humeau, Y., & Choquet, D. (2017) · Nature · doi:10.1038/nature23658 · Cited by 324
Man, H.-Y., Sekine-Aizawa, Y., & Huganir, R. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0611698104 · Cited by 311
Lee, H.-K., Takamiya, K., He, K., Song, L., & Huganir, R. L. (2010) · Journal of Neurophysiology · doi:10.1152/jn.00835.2009 · Cited by 261
Postsynaptic synaptotagmins mediate AMPA receptor exocytosis during LTP
Wu, D., Bacaj, T., Morishita, W., Goswami, D., Arendt, K. L., Xu, W., Chen, L., Malenka, R. C., & Südhof, T. C. (2017) · Nature · doi:10.1038/nature21720 · Cited by 195
Postsynaptic Complexin Controls AMPA Receptor Exocytosis during LTP
Ahmad, M., Polepalli, J. S., Goswami, D., Yang, X., Kaeser-Woo, Y. J., Südhof, T. C., & Malenka, R. C. (2012) · Neuron · doi:10.1016/j.neuron.2011.11.020 · Cited by 133
Self-citationPICK1 loss of function occludes homeostatic synaptic scaling
Anggono, V., Clem, R. L., & Huganir, R. L. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.5633-10.2011 · Cited by 111
Guntupalli, S., Jang, S. E., Zhu, T., Huganir, R. L., Widagdo, J., & Anggono, V. (2017) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.774554 · Cited by 70
Flagged first, then by citations
Research works printed but not linked: 43
- Bacaj, 2015, Synaptic function of Rab 11Fip5: selective requirement for hippocampal long-term depression, J. Neurosci., 35, 7460, 10.1523/JNEUROSCI.1581-14.2015 · DOI
- Barria, 1997, Identification of the Ca2+/calmodulin-dependent protein kinase II regulatory phosphorylation site in the alpha-amino-3-hydroxyl-5-methyl-4-isoxazole-propionate-type glutamate receptor, J. Biol. Chem., 272, 32727, 10.1074/jbc.272.52.32727 · DOI
- Chen, 2014, Interaction proteomics reveals brain region-specific AMPA receptor complexes, J. Proteome Res., 13, 5695, 10.1021/pr500697b · DOI · Paper page
- Citri, 2010, Calcium binding to PICK1 is essential for the intracellular retention of AMPA receptors underlying long-term depression, J. Neurosci., 30, 16437, 10.1523/JNEUROSCI.4478-10.2010 · DOI
- Clem, 2010, PICK1 regulates incorporation of calcium-permeable AMPA receptors during cortical synaptic strengthening, J. Neurosci., 30, 6360, 10.1523/JNEUROSCI.6276-09.2010 · DOI
- Diering, 2014, PKA-GluA1 coupling via AKAP5 controls AMPA receptor phosphorylation and cell-surface targeting during bidirectional homeostatic plasticity, Neuron, 84, 790, 10.1016/j.neuron.2014.09.024 · DOI · Paper page
- Diering, 2016, Extensive phosphorylation of AMPA receptors in neurons, Proc. Natl. Acad. Sci. U. S. A., 113, E4920, 10.1073/pnas.1610631113 · DOI
- Ehlers, 2000, Reinsertion or degradation of AMPA receptors determined by activity-dependent endocytic sorting, Neuron, 28, 511, 10.1016/S0896-6273(00)00129-X · DOI · Paper page
- Fernandez-Monreal, 2012, The balance between receptor recycling and trafficking toward lysosomes determines synaptic strength during long-term depression, J. Neurosci., 32, 13200, 10.1523/JNEUROSCI.0061-12.2012 · DOI
- Garcia-Alvarez, 2015, STIM2 regulates PKA-dependent phosphorylation and trafficking of AMPARs, Mol. Biol. Cell, 26, 1141, 10.1091/mbc.E14-07-1222 · DOI
- Gu, 2016, GSG1L suppresses AMPA receptor-mediated synaptic transmission and uniquely modulates AMPA receptor kinetics in hippocampal neurons, Nat. Commun., 7, 10.1038/ncomms10873 · DOI
- He, 2009, Stabilization of Ca2+-permeable AMPA receptors at perisynaptic sites by GluR1-S845 phosphorylation, Proc. Natl. Acad. Sci. U. S. A., 106, 20033, 10.1073/pnas.0910338106 · DOI
- Henley, 2016, Synaptic AMPA receptor composition in development, plasticity and disease, Nat. Rev. Neurosci., 17, 337, 10.1038/nrn.2016.37 · DOI
- Holman, 2007, Differential redistribution of native AMPA receptor complexes following LTD induction in acute hippocampal slices, Neuropharmacology, 52, 92, 10.1016/j.neuropharm.2006.05.022 · DOI
- Huganir, 2013, AMPARs and synaptic plasticity: the last 25 years, Neuron, 80, 704, 10.1016/j.neuron.2013.10.025 · DOI · Paper page
- Jackson, 2011, The expanding social network of ionotropic glutamate receptors: TARPs and other transmembrane auxiliary subunits, Neuron, 70, 178, 10.1016/j.neuron.2011.04.007 · DOI · Paper page
- Jurado, 2013, LTP requires a unique postsynaptic SNARE fusion machinery, Neuron, 77, 542, 10.1016/j.neuron.2012.11.029 · DOI · Paper page
- Kalashnikova, 2010, SynDIG1: an activity-regulated, AMPA- receptor-interacting transmembrane protein that regulates excitatory synapse development, Neuron, 65, 80, 10.1016/j.neuron.2009.12.021 · DOI
- Kato, 2010, Hippocampal AMPA receptor gating controlled by both TARP and cornichon proteins, Neuron, 68, 1082, 10.1016/j.neuron.2010.11.026 · DOI
- Kirk, 2016, Distribution of the SynDIG4/proline-rich transmembrane protein 1 in rat brain, J. Comp. Neurol., 524, 2266, 10.1002/cne.23945 · DOI · Paper page
- Ladd-Acosta, 2013, Common DNA methylation alterations in multiple brain regions in autism, Mol. Psychiatry, 19, 862, 10.1038/mp.2013.114 · DOI
- Lee, 1998, NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus, Neuron, 21, 1151, 10.1016/S0896-6273(00)80632-7 · DOI · Paper page
- Lee, 2000, Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity, Nature, 405, 955, 10.1038/35016089 · DOI · Paper page
- Lee, 2003, Phosphorylation of the AMPA receptor GluR1 subunit is required for synaptic plasticity and retention of spatial memory, Cell, 112, 631, 10.1016/S0092-8674(03)00122-3 · DOI · Paper page
- Malenka, 2004, LTP and LTD: an embarrassment of riches, Neuron, 44, 5, 10.1016/j.neuron.2004.09.012 · DOI · Paper page
- Mammen, 1997, Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II, J. Biol. Chem., 272, 32528, 10.1074/jbc.272.51.32528 · DOI · Paper page
- Matt, 2018, SynDIG4/Prrt1 is required for excitatory synapse development and plasticity underlying cognitive function, Cell Rep., 22, 2246, 10.1016/j.celrep.2018.02.026 · DOI · Paper page
- Oh, 2006, Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation, J. Biol. Chem., 281, 752, 10.1074/jbc.M509677200 · DOI
- Otmakhov, 2004, Forskolin-induced LTP in the CA1 hippocampal region is NMDA receptor dependent, J. Neurophysiol., 91, 1955, 10.1152/jn.00941.2003 · DOI
- Purkey, 2018, AKAP150 palmitoylation regulates synaptic incorporation of Ca(2+)-permeable AMPA receptors to control LTP, Cell Rep., 25, 974, 10.1016/j.celrep.2018.09.085 · DOI
- Roche, 1996, Characterization of multiple phosphorylation sites on the AMPA receptor GluR1 subunit, Neuron, 16, 1179, 10.1016/S0896-6273(00)80144-0 · DOI · Paper page
- Rouach, 2005, TARP gamma-8 controls hippocampal AMPA receptor number, distribution and synaptic plasticity, Nat. Neurosci., 8, 1525, 10.1038/nn1551 · DOI
- Sallman Almen, 2012, The dispanins: a novel gene family of ancient origin that contains 14 human members, PLoS One, 7, 10.1371/journal.pone.0031961 · DOI
- Sanderson, 2016, NMDA receptor-dependent LTD requires transient synaptic incorporation of Ca(2)(+)-permeable AMPARs mediated by AKAP150-anchored PKA and calcineurin, Neuron, 89, 1000, 10.1016/j.neuron.2016.01.043 · DOI · Paper page
- Schwenk, 2012, High-resolution proteomics unravel architecture and molecular diversity of native AMPA receptor complexes, Neuron, 74, 621, 10.1016/j.neuron.2012.03.034 · DOI · Paper page
- Schwenk, 2014, Regional diversity and developmental dynamics of the AMPA-receptor proteome in the mammalian brain, Neuron, 84, 41, 10.1016/j.neuron.2014.08.044 · DOI
- Shanks, 2012, Differences in AMPA and kainate receptor interactomes facilitate identification of AMPA receptor auxiliary subunit GSG1L, Cell Rep., 1, 590, 10.1016/j.celrep.2012.05.004 · DOI · Paper page
- Soler-Llavina, 2011, The neurexin ligands, neuroligins and leucine-rich repeat transmembrane proteins, perform convergent and divergent synaptic functions in vivo, Proc. Natl. Acad. Sci. U. S. A., 108, 16502, 10.1073/pnas.1114028108 · DOI
- Tomita, 2005, Bidirectional synaptic plasticity regulated by phosphorylation of stargazin-like TARPs, Neuron, 45, 269, 10.1016/j.neuron.2005.01.009 · DOI · Paper page
- Tomita, 2005, Stargazin modulates AMPA receptor gating and trafficking by distinct domains, Nature, 435, 1052, 10.1038/nature03624 · DOI · Paper page
- van Eijk, 2015, Identification of schizophrenia-associated loci by combining DNA methylation and gene expression data from whole blood, Eur. J. Hum. Genet., 23, 1106, 10.1038/ejhg.2014.245 · DOI
- von Engelhardt, 2010, CKAMP44: a brain-specific protein attenuating short-term synaptic plasticity in the dentate gyrus, Science, 327, 1518, 10.1126/science.1184178 · DOI
- Yap, 2017, STIM2 regulates AMPA receptor trafficking and plasticity at hippocampal synapses, Neurobiol. Learn. Mem., 138, 54, 10.1016/j.nlm.2016.08.007 · DOI
Cited by
Sorted by citations
He, C.-W., & Díaz, E. (2025) · Frontiers in Pharmacology · doi:10.3389/fphar.2025.1568908 · Cited by 3
Metadata
- Authors
- Troyano-Rodriguez, E., Mann, S., Ullah, R., & Ahmad, M.
- Venue
- Molecular and Cellular Neuroscience
- Publisher
- Elsevier BV
- Published
- 2019-07
- Volume
- 98
- Pages
- 155-163
- ISSN
- 1044-7431
- Cited by
- 35
- References
- 13
- Language
- en
- Funders
- Oklahoma Center for the Advancement of Science and Technology (HR16-116)
- College of Medicine Alumni Association Fund
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review