Presynaptic neuronal pentraxin receptor organizes excitatory and inhibitory synapses
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Three neuronal pentraxins are expressed in brain, the membrane-bound “neuronal pentraxin receptor” (NPR) and the secreted proteins NP1 and NARP (i.e., NP2). Neuronal pentraxins bind to AMPARs at excitatory synapses and play important, well-documented roles in the activity-dependent regulation of neural circuits via this binding activity. However, it is unknown whether neuronal pentraxins perform roles in synapses beyond modulating postsynaptic AMPAR-dependent plasticity, and whether they may even act in inhibitory synapses. Here, we show that NPR expressed in non-neuronal cells potently induces formation of both excitatory and inhibitory postsynaptic specializations in cocultured hippocampal neurons. Knockdown of NPR in hippocampal neurons, conversely, dramatically decreased assembly and function of both excitatory and inhibitory postsynaptic specializations. Overexpression of NPR rescued the NPR knockdown phenotype but did not in itself change synapse numbers or properties. However, the NPR knockdown decreased the levels of NARP, whereas NPR overexpression produced a dramatic increase in the levels of NP1 and NARP, suggesting that NPR recruits and stabilizes NP1 and NARP on the presynaptic plasma membrane. Mechanistically, NPR acted in excitatory synapse assembly by binding to the N-terminal domain of AMPARs; antagonists of AMPA and GABA receptors selectively inhibited NPR-induced heterologous excitatory and inhibitory synapse assembly, respectively, but did not affect neurexin-1β-induced synapse assembly as a control. Our data suggest that neuronal pentraxins act as signaling complexes that function as general trans-synaptic organizers of both excitatory and inhibitory synapses by a mechanism that depends, at least in part, on the activity of the neurotransmitter receptors at these synapses. SIGNIFICANCE STATEMENT Neuronal pentraxins comprise three neuronal proteins, neuronal pentraxin receptor (NPR) which is a type-II transmembrane protein on the neuronal surface, and secreted neuronal pentraxin-1 and NARP. The general functions of neuronal pentraxins at synapses have not been explored, except for their basic AMPAR binding properties. Here, we examined the functional role of NPR at synapses because it is the only neuronal pentraxin that is anchored to the neuronal cell-surface membrane. We find that NPR is a potent inducer of both excitatory and inhibitory heterologous synapses, and that knockdown of NPR in cultured neurons decreases the density of both excitatory and inhibitory synapses. Our data suggest that NPR performs a general, previously unrecognized function as a universal organizer of synapses.
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Neuronal pentraxins are involved in synapse formation and plasticity.
“Neuronal pentraxins have been found to be involved in synapse formation and plasticity [37, 38]”
The three NPTXs interact, directly or indirectly, with the N-terminal extracellular domain of AMPAR subunits (GluA1, GluA2, GluA3, and GluA4), via their conserved pentraxin domain.
“The three NPTXs interact, directly or indirectly, with the N-terminal extracellular domain of AMPAR subunits (GluA1, GluA2, GluA3 and GluA4), via their conserved pentraxin domain (Chang et al. 2010; Cho et al. 2008; Lee et al. 2017; Sia et al. 2007; Suzuki et al. 2020).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Lee et al. 2017
A potential role of NPTXR as universal organizer of both excitatory and inhibitory synapses was observed in in vitro studies.
“A potential role of NPTXR as universal organizer of both excitatory and inhibitory synapses was observed in in vitro studies (Lee et al. 2017).”
From Neuronal pentraxins as biomarkers of synaptic activity: from physiological functions to pathological changes in neurodegeneration (2022) · cites this paper as Lee et al. 2017
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High-Efficiency Transformation of Mammalian Cells by Plasmid DNA
Chen, C., & Okayama, H. (1987) · Molecular and Cellular Biology · doi:10.1128/mcb.7.8.2745 · Cited by 5,374 · see citing works
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 · see citing works
Definition of the readily releasable pool of vesicles at hippocampal synapses.
Rosenmund, C., & Stevens, C. (1996) · Neuron · doi:10.1016/s0896-6273(00)80146-4 · Cited by 1,084 · see citing works
Neuroligin Expressed in Nonneuronal Cells Triggers Presynaptic Development in Contacting Axons
Scheiffele, P., Fan, J., Choih, J., Fetter, R., & Serafini, T. (2000) · Cell · doi:10.1016/s0092-8674(00)80877-6 · Cited by 1,060 · see citing works
Neurexins Induce Differentiation of GABA and Glutamate Postsynaptic Specializations via Neuroligins
Graf, E. R., Zhang, X., Jin, S., Linhoff, M. W., & Craig, A. M. (2004) · Cell · doi:10.1016/j.cell.2004.11.035 · Cited by 989 · see citing works
Neuroligins Determine Synapse Maturation and Function
Varoqueaux, F., Aramuni, G., Rawson, R. L., Mohrmann, R., Missler, M., Gottmann, K., Zhang, W., Südhof, T. C., & Brose, N. (2006) · Neuron · doi:10.1016/j.neuron.2006.09.003 · Cited by 818 · see citing works
Self-citationα-Neurexins couple Ca2+ channels to synaptic vesicle exocytosis
Missler, M., Zhang, W., Rohlmann, A., Kattenstroth, G., Hammer, R. E., Gottmann, K., & Südhof, T. C. (2003) · Nature · doi:10.1038/nature01755 · Cited by 699 · see citing works
Self-citationNeurexins: Synaptic Cell Surface Proteins Related to the α-Latrotoxin Receptor and Laminin
Ushkaryov, Y. A., Petrenko, A. G., Geppert, M., & Südhof, T. C. (1992) · Science · doi:10.1126/science.1621094 · Cited by 682 · see citing works
Self-citationChubykin, A. A., Atasoy, D., Etherton, M. R., Brose, N., Kavalali, E. T., Gibson, J. R., & Südhof, T. C. (2007) · Neuron · doi:10.1016/j.neuron.2007.05.029 · Cited by 594 · see citing works
Self-citationSynaptic clustering of AMPA receptors by the extracellular immediate-early gene product narp.
O’Brien, R. J., Xu, D., Petralia, R. S., Steward, O., Huganir, R. L., & Worley, P. (1999) · Neuron · doi:10.1016/s0896-6273(00)80782-5 · Cited by 471 · see citing works
Schwenk, J., Harmel, N., Brechet, A., Zolles, G., Berkefeld, H., Müller, C. S., Bildl, W., Baehrens, D., Hüber, B., Kulik, A., et al. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.034 · Cited by 433 · see citing works
Postsynaptic assembly induced by neurexin-neuroligin interaction and neurotransmitter
Nam, C. I., & Chen, L. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0502038102 · Cited by 322 · see citing works
Narp regulates homeostatic scaling of excitatory synapses on parvalbumin-expressing interneurons
Chang, M. C., Park, J. M., Pelkey, K. A., Grabenstatter, H. L., Xu, D., Linden, D. J., Sutula, T. P., McBain, C. J., & Worley, P. F. (2010) · Nature Neuroscience · doi:10.1038/nn.2621 · Cited by 316 · see citing works
Tsui, C., Copeland, N., Gilbert, D., Jenkins, N., Barnes, C., & Worley, P. (1996) · The Journal of Neuroscience · doi:10.1523/jneurosci.16-08-02463.1996 · Cited by 315 · see citing works
Regional Diversity and Developmental Dynamics of the AMPA-Receptor Proteome in the Mammalian Brain
Schwenk, J., Baehrens, D., Haupt, A., Bildl, W., Boudkkazi, S., Roeper, J., Fakler, B., & Schulte, U. (2014) · Neuron · doi:10.1016/j.neuron.2014.08.044 · Cited by 270 · see citing works
Xu, D., Hopf, C., Reddy, R., Cho, R. W., Guo, L., Lanahan, A., Petralia, R. S., Wenthold, R. J., O'Brien, R. J., & Worley, P. (2003) · Neuron · doi:10.1016/s0896-6273(03)00463-x · Cited by 265 · see citing works
Pelkey, K. A., Barksdale, E., Craig, M. T., Yuan, X., Sukumaran, M., Vargish, G. A., Mitchell, R. M., Wyeth, M. S., Petralia, R. S., Chittajallu, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.020 · Cited by 245 · see citing works
Maximov, A., & Südhof, T. C. (2005) · Neuron · doi:10.1016/j.neuron.2005.09.006 · Cited by 238 · see citing works
Self-citationSia, G.-M., Béïque, J.-C., Rumbaugh, G., Cho, R., Worley, P. F., & Huganir, R. L. (2007) · Neuron · doi:10.1016/j.neuron.2007.06.020 · Cited by 201 · see citing works
Knackstedt, L. A., Moussawi, K., LaLumiere, R. T., Schwendt, M., Klugmann, M., & Kalivas, P. W. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.1244-10.2010 · Cited by 197 · see citing works
Neurexins Physically and Functionally Interact with GABAA Receptors
Zhang, C., Atasoy, D., Araç, D., Yang, X., Fucillo, M. V., Robison, A. J., Ko, J., Brünger, A. T., & Südhof, T. C. (2010) · Neuron · doi:10.1016/j.neuron.2010.04.008 · Cited by 187 · see citing works
Self-citationDissection of Synapse Induction by Neuroligins
Chubykin, A. A., Liu, X., Comoletti, D., Tsigelny, I. F., Taylor, P., & Südhof, T. C. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m410723200 · Cited by 185 · see citing works
Self-citationNeuronal Pentraxins Mediate Synaptic Refinement in the Developing Visual System
Bjartmar, L., Huberman, A. D., Ullian, E. M., Renteria, R. C., Liu, X., Xu, W., Prezioso, J., Susman, M. W., Stellwagen, D., Stokes, C. C., et al. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4212-05.2006 · Cited by 179 · see citing works
Neuronal pentraxin, a secreted protein with homology to acute phase proteins of the immune system
Schlimgen, A. K., Helms, J. A., Vogel, H. S., & Perin, M. S. (1995) · Neuron · doi:10.1016/0896-6273(95)90308-9 · Cited by 163 · see citing works
O'Brien, R., Xu, D., Mi, R., Tang, X., Hopf, C., & Worley, P. (2002) · The Journal of Neuroscience · doi:10.1523/jneurosci.22-11-04487.2002 · Cited by 160 · see citing works
Biochemical Interactions of the Neuronal Pentraxins
Kirkpatrick, L., Matzuk, M. M., Dodds, D. C., & Perin, M. S. (2000) · Journal of Biological Chemistry · doi:10.1074/jbc.m002254200 · Cited by 149 · see citing works
Cho, R. W., Park, J. M., Wolff, S. B. E., Xu, D., Hopf, C., Kim, J.-A., Reddy, R. C., Petralia, R. S., Perin, M. S., Linden, D. J., et al. (2008) · Neuron · doi:10.1016/j.neuron.2008.01.010 · Cited by 125 · see citing works
Obligatory Role for the Immediate Early Gene NARP in Critical Period Plasticity
Gu, Y., Huang, S., Chang, M., Worley, P. F., Kirkwood, A., & Quinlan, E. M. (2013) · Neuron · doi:10.1016/j.neuron.2013.05.016 · Cited by 117 · see citing works
Calmodulin Controls Synaptic Strength via Presynaptic Activation of Calmodulin Kinase II
Pang, Z. P., Cao, P., Xu, W., & Südhof, T. C. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.3129-09.2010 · Cited by 106 · see citing works
Self-citationHomo- and Heterodimerization of Synapsins
Hosaka, M., & Südhof, T. C. (1999) · Journal of Biological Chemistry · doi:10.1074/jbc.274.24.16747 · Cited by 103 · see citing works
Self-citationNeuronal Pentraxins Mediate Silent Synapse Conversion in the Developing Visual System
Koch, S. M., & Ullian, E. M. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4893-09.2010 · Cited by 55 · see citing works
The amino-terminal domain of glutamate receptor δ2 triggers presynaptic differentiation
Uemura, T., & Mishina, M. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2008.10.170 · Cited by 49 · see citing works
Elbaz, I., Lerer‐Goldshtein, T., Okamoto, H., & Appelbaum, L. (2014) · The FASEB Journal · doi:10.1096/fj.14-258350 · Cited by 23 · see citing works
Vamping: Stereology-based automated quantification of fluorescent puncta size and density
Dumitriu, D., Berger, S., HAMO, C. E., Hara, Y., Bailey, M., Hamo, A., Grossman, Y. S., Janssen, W. G. M., & Morrison, J. H. (2012) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2012.05.031 · Cited by 21 · see citing works
Localized disruption of Narp in medial prefrontal cortex blocks reinforcer devaluation performancePreprint
Johnson, A. W., Han, S. B., Blouin, A. M., Saini, J. K., Worley, P. F., During, M. J., Holland, P. C., Baraban, J. M., & Reti, I. M. (2010) · Learning & Memory · doi:10.1101/lm.1937210 · Cited by 19 · see citing works
Role of medial prefrontal cortex Narp in the extinction of morphine conditioned place preferencePreprint
Blouin, A. M., Han, S. B., Pearce, A. M., Cheng, K., Lee, J. J., Johnson, A. W., Wang, C., During, M. J., Holland, P. C., Shaham, Y., et al. (2013) · Learning & Memory · doi:10.1101/lm.028621.112 · Cited by 16 · see citing works
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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
Structure, 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
Towards an Understanding of Synapse Formation
Südhof, T. C. (2018) · Neuron · doi:10.1016/j.neuron.2018.09.040 · Cited by 698 · see citing works
Self-citationThe roles of perineuronal nets and the perinodal extracellular matrix in neuronal function
Fawcett, J. W., Oohashi, T., & Pizzorusso, T. (2019) · Nature Reviews Neuroscience · doi:10.1038/s41583-019-0196-3 · Cited by 589 · see citing works
Structural and Functional Architecture of AMPA-Type Glutamate Receptors and Their Auxiliary Proteins
Greger, I. H., Watson, J. F., & Cull-Candy, S. G. (2017) · Neuron · doi:10.1016/j.neuron.2017.04.009 · Cited by 392 · see citing works
The cell biology of synapse formation
Südhof, T. C. (2021) · Journal of Cell Biology · doi:10.1083/jcb.202103052 · Cited by 358 · see citing works
Self-citationTranscellular Nanoalignment of Synaptic Function
Biederer, T., Kaeser, P. S., & Blanpied, T. A. (2017) · Neuron · doi:10.1016/j.neuron.2017.10.006 · Cited by 352 · see citing works
NPTX2 and cognitive dysfunction in Alzheimer’s Disease
Xiao, M.-F., Xu, D., Craig, M. T., Pelkey, K. A., Chien, C.-C., Shi, Y., Zhang, J., Resnick, S., Pletnikova, O., Salmon, D., et al. (2017) · eLife · doi:10.7554/elife.23798 · Cited by 316 · see citing works
Goetzl, E. J., Abner, E. L., Jicha, G. A., Kapogiannis, D., & Schwartz, J. B. (2018) · The FASEB Journal · doi:10.1096/fj.201700731r · Cited by 219 · see citing works
Farhy-Tselnicker, I., van Casteren, A. C. M., Lee, A., Chang, V. T., Aricescu, A. R., & Allen, N. J. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.053 · Cited by 199 · see citing works
Fluid Biomarkers for Synaptic Dysfunction and Loss
Camporesi, E., Nilsson, J., Brinkmalm, A., Becker, B., Ashton, N. J., Blennow, K., & Zetterberg, H. (2020) · Biomarker Insights · doi:10.1177/1177271920950319 · Cited by 165 · see citing works
Functional organization of postsynaptic glutamate receptors
Scheefhals, N., & MacGillavry, H. D. (2018) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2018.05.002 · Cited by 151 · see citing works
Zhou, J., Wade, S. D., Graykowski, D., Xiao, M.-F., Zhao, B., Giannini, L. A. A., Hanson, J. E., van Swieten, J. C., Sheng, M., Worley, P. F., et al. (2023) · Science Translational Medicine · doi:10.1126/scitranslmed.adf0141 · Cited by 152 · see citing works
Galasko, D., Xiao, M., Xu, D., Smirnov, D., Salmon, D. P., Dewit, N., Vanbrabant, J., Jacobs, D., Vanderstichele, H., Vanmechelen, E., et al. (2019) · Alzheimer's & Dementia: Translational Research & Clinical Interventions · doi:10.1016/j.trci.2019.11.002 · Cited by 133 · see citing works
Longitudinal CSF proteomics identifies NPTX2 as a prognostic biomarker of Alzheimer's disease
Libiger, O., Shaw, L. M., Watson, M. H., Nairn, A. C., Umaña, K. L., Biarnes, M. C., Canet‐Avilés, R. M., Jack, C. R., Breton, Y., Cortes, L., et al. (2021) · Alzheimer's & Dementia · doi:10.1002/alz.12353 · Cited by 108 · see citing works
Two Classes of Secreted Synaptic Organizers in the Central Nervous System
Yuzaki, M. (2018) · Annual Review of Physiology · doi:10.1146/annurev-physiol-021317-121322 · Cited by 125 · see citing works
A synthetic synaptic organizer protein restores glutamatergic neuronal circuits
Suzuki, K., Elegheert, J., Song, I., Sasakura, H., Senkov, O., Matsuda, K., Kakegawa, W., Clayton, A. J., Chang, V. T.-C., Ferrer-Ferrer, M., et al. (2020) · Science · doi:10.1126/science.abb4853 · Cited by 123 · see citing works
Cell adhesion and matricellular support by astrocytes of the tripartite synapse
Hillen, A. E. J., Burbach, J. P. H., & Hol, E. M. (2018) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2018.02.002 · Cited by 108 · see citing works
Gómez de San José, N., Massa, F., Halbgebauer, S., Oeckl, P., Steinacker, P., & Otto, M. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-021-02411-2 · Cited by 112 · see citing works
Siedlecki‐Wullich, D., Català-Solsona, J., Fábregas, C., Hernández, I., Clarimón, J., Lleó, A., Boada, M., Saura, C. A., Rodrı́guez-Álvarez, J., & Miñano-Molina, A. J. (2019) · Alzheimer s Research & Therapy · doi:10.1186/s13195-019-0501-4 · Cited by 118 · see citing works
Subunit-specific role for the amino-terminal domain of AMPA receptors in synaptic targeting
Díaz-Alonso, J., Sun, Y. J., Granger, A. J., Levy, J. M., Blankenship, S. M., & Nicoll, R. A. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1707472114 · Cited by 89 · see citing works
Cerebrospinal fluid biomarker panel for synaptic dysfunction in Alzheimer's disease
Nilsson, J., Gobom, J., Sjödin, S., Brinkmalm, G., Ashton, N. J., Svensson, J., Johansson, P., Portelius, E., Zetterberg, H., Blennow, K., et al. (2021) · Alzheimer's & Dementia: Diagnosis, Assessment & Disease Monitoring · doi:10.1002/dad2.12179 · Cited by 82 · see citing works
Nilsson, J., Binette, A. P., Palmqvist, S., Brum, W. S., Janelidze, S., Ashton, N. J., Spotorno, N., Stomrud, E., Gobom, J., Zetterberg, H., et al. (2024) · Brain · doi:10.1093/brain/awae032 · Cited by 82 · see citing works
The Basic Characteristics of the Pentraxin Family and Their Functions in Tumor Progression
Wang, Z., Wang, X., Zou, H., Dai, Z., Feng, S., Zhang, M., Xiao, G., Liu, Z., & Cheng, Q. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01757 · Cited by 73 · see citing works
AMPA receptor trafficking and LTP: Carboxy-termini, amino-termini and TARPs
Díaz-Alonso, J., & Nicoll, R. A. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108710 · Cited by 66 · see citing works
Fossati, G., Pozzi, D., Canzi, A., Mirabella, F., Valentino, S., Morini, R., Ghirardini, E., Filipello, F., Moretti, M., Gotti, C., et al. (2018) · The EMBO Journal · doi:10.15252/embj.201899529 · Cited by 65 · see citing works
Kanda, M., Shimizu, D., Sawaki, K., Nakamura, S., Umeda, S., Miwa, T., Tanaka, H., Tanaka, C., Hayashi, M., Iguchi, Y., et al. (2020) · Molecular Cancer · doi:10.1186/s12943-020-01251-0 · Cited by 67 · see citing works
Nilsson, J., Cousins, K. A. Q., Gobom, J., Portelius, E., Chen‐Plotkin, A. S., Shaw, L. M. J., Grossman, M., Irwin, D. J., Trojanowski, J. Q., Zetterberg, H., et al. (2022) · Alzheimer s & Dementia · doi:10.1002/alz.12809 · Cited by 61 · see citing works
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Hruška-Plocháň, M., Wiersma, V. I., Betz, K. M., Mallona, I., Ronchi, S., Maniecka, Z., Hock, E., Tantardini, E., Laferrière, F., Sahadevan, S., et al. (2024) · Nature · doi:10.1038/s41586-024-07042-7 · Cited by 72 · see citing works
Mackmull, M., Nagel, L., Sesterhenn, F., Muntel, J., Großbach, J., Stalder, P., Bruderer, R., Reiter, L., van de Berg, W. D. J., de Souza, N., et al. (2022) · Nature Structural & Molecular Biology · doi:10.1038/s41594-022-00837-0 · Cited by 53 · see citing works
Begcevic, I., Tsolaki, M., Brinc, D., Brown, M., Martinez-Morillo, E., Lazarou, I., Kozori, M., Tagaraki, F., Nenopoulou, S., Gkioka, M., et al. (2018) · F1000Research · doi:10.12688/f1000research.15095.1 · Cited by 51 · see citing works
Moreno‐Rodríguez, M., Perez, S. E., Nadeem, M., Malek‐Ahmadi, M. H., & Mufson, E. J. (2020) · Journal of Neuroinflammation · doi:10.1186/s12974-020-1723-x · Cited by 52 · see citing works
Spatiotemporal patterns of gene expression around implanted silicon electrode arrays
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van Oostrum, M., Campbell, B. F. N., Seng, C., Müller, M., Dieck, S. T., Hammer, J., Pedrioli, P. G. A., Földy, C., Tyagarajan, S. K., & Wollscheid, B. (2020) · Nature Communications · doi:10.1038/s41467-020-18494-6 · Cited by 47 · see citing works
The Role of Neuronal Pentraxin 2 (NP2) in Regulating Glutamatergic Signaling and Neuropathology
Chapman, G., Shanmugalingam, U., & Smith, P. D. (2020) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2019.00575 · Cited by 48 · see citing works
Poulsen, L. L. C., Plá, I., Sánchez, A., Grøndahl, M. L., Marko‐Varga, G., Andersen, C. Y., Englund, A. L. M., & Malm, J. (2019) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2019.110522 · Cited by 47 · see citing works
Jiang, X., Sando, R. C., & Südhof, T. C. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2000173118 · Cited by 47 · see citing works
Self-citationde Bartolomeis, A., Buonaguro, E. F., Latte, G., Rossi, R., Marmo, F., Iasevoli, F., & Tomasetti, C. (2017) · Frontiers in Behavioral Neuroscience · doi:10.3389/fnbeh.2017.00240 · Cited by 44 · see citing works
Barschke, P., Oeckl, P., Steinacker, P., Al Shweiki, M. R., Weishaupt, J. H., Landwehrmeyer, G. B., Anderl-Straub, S., Weydt, P., Diehl-Schmid, J., Danek, A., et al. (2020) · Journal of Neurology, Neurosurgery & Psychiatry · doi:10.1136/jnnp-2019-322476 · Cited by 45 · see citing works
Jiang, W., Wei, M., Liu, M., Pan, Y., Cao, D., Yang, X., & Zhang, C. (2017) · Journal of Neuroscience · doi:10.1523/jneurosci.0729-17.2017 · Cited by 45 · see citing works
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The interplay between electrical and chemical synaptogenesis
Jabeen, S., & Thirumalai, V. (2018) · Journal of Neurophysiology · doi:10.1152/jn.00398.2018 · Cited by 41 · see citing works
Lim, B., Sando, S. B., Grøntvedt, G. R., Bråthen, G., & Diamandis, E. P. (2020) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2020.03.013 · Cited by 39 · see citing works
Extracellular matrix and synapse formation
Yang, L., Wei, M., Xing, B., & Zhang, C. (2022) · Bioscience Reports · doi:10.1042/bsr20212411 · Cited by 40 · see citing works
Self-citationAlamro, H., Bajić, V., Mačvanin, M., Isenović, E. R., Gojobori, T., Essack, M., & Gao, X. (2023) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.1084656 · Cited by 39 · see citing works
AMPA receptor anchoring at CA1 synapses is determined by N-terminal domain and TARP γ8 interactions
Watson, J. F., Pinggera, A., Ho, H., & Greger, I. H. (2021) · Nature Communications · doi:10.1038/s41467-021-25281-4 · Cited by 38 · see citing works
Wang, Z., Jin, T., Le, Q., Liu, C., Wang, X., Wang, F., & Ma, L. (2019) · Biological Psychiatry · doi:10.1016/j.biopsych.2019.10.009 · Cited by 37 · see citing works
Bolsewig, K., Hok-A-Hin, Y. S., Sepe, F. N., Boonkamp, L., Jacobs, D., Bellomo, G., Paoletti, F. P., Vanmechelen, E., Teunissen, C. E., Parnetti, L., et al. (2022) · Journal of Alzheimer's Disease · doi:10.3233/jad-220318 · Cited by 36 · see citing works
Sanfilippo, P., Kim, A. J., Bhukel, A., Yoo, J., Mirshahidi, P. S., Pandey, V., Bevir, H., Yuen, A., Mirshahidi, P. S., Guo, P., et al. (2024) · Neuron · doi:10.1016/j.neuron.2023.12.014 · Cited by 36 · see citing works
Ju, L.-S., Yang, J., Zhu, T., Liu, P., & Yang, J. (2022) · BMC Psychiatry · doi:10.1186/s12888-022-03838-x · Cited by 34 · see citing works
Ramesh, V., Liu, F., Minto, M. S., Chan, U., & West, A. E. (2023) · eLife · doi:10.7554/elife.86273 · Cited by 36 · see citing works
Boudkkazi, S., Schwenk, J., Nakaya, N., Bréchet, A., Kollewe, A., Harada, H., Bildl, W., Kulik, Á., Dong, L., Sultana, A., et al. (2023) · Neuron · doi:10.1016/j.neuron.2023.07.013 · Cited by 32 · see citing works
Neuronal pentraxin 1: A synaptic-derived plasma biomarker in Alzheimer's disease
Ma, Q., Teng, E., Zuo, X., Jones, M. R., Teter, B., Zhao, E. Y., Zhu, C., Bilousova, T. V., Gylys, K. H., Apostolova, L. G., et al. (2018) · Neurobiology of Disease · doi:10.1016/j.nbd.2018.02.014 · Cited by 32 · see citing works
Compartment-Specific Neurexin Nanodomains Orchestrate Tripartite Synapse AssemblyPreprint
Trotter, J. H., Dargaei, Z., Sclip, A., Essayan-Perez, S., Liakath‐Ali, K., Raju, K., Nabet, A., Liu, X., Wöhr, M., & Südhof, T. C. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.21.262097 · Cited by 33 · see citing works
Self-citationAssociation between serum NPTX2 and cognitive function in patients with vascular dementia
Shao, K., Shan, S., Ru, W., & Ma, C. (2020) · Brain and Behavior · doi:10.1002/brb3.1779 · Cited by 25 · see citing works
Plasticity of postsynaptic nanostructure
Droogers, W. J., & MacGillavry, H. D. (2023) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2023.103819 · Cited by 27 · see citing works
Differential nanoscale organization of excitatory synapses onto excitatory vs. inhibitory neurons
Dharmasri, P. A., Levy, A. D., & Blanpied, T. A. (2024) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2315379121 · Cited by 25 · see citing works
Molecular signatures of cortical expansion in the human foetal brain
Ball, G., Oldham, S., Kyriakopoulou, V., Williams, L. Z. J., Karolis, V. R., Price, A. N., Hutter, J. M., Seal, M. L., Alexander‐Bloch, A. F., Hajnal, J. V., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54034-2 · Cited by 27 · see citing works
Biology of AMPA receptor interacting proteins - From biogenesis to synaptic plasticity
Matthews, P. M., Pinggera, A., Kampjut, D., & Greger, I. H. (2021) · Neuropharmacology · doi:10.1016/j.neuropharm.2021.108709 · Cited by 25 · see citing works
Revealing NOTCH-dependencies in synaptic targets associated with Alzheimer's disease
Perna, A., Marathe, S. V., Dreos, R., Falquet, L., Akarsu, H., & Auber, L. A. (2021) · Molecular and Cellular Neuroscience · doi:10.1016/j.mcn.2021.103657 · Cited by 25 · see citing works
Gulyássy, P., Völgyi, K., Tóth, V., Györffy, B. A., Puska, G., Simor, A., Juhász, G. D., Drahos, L., & Kékesi, K. A. (2022) · Molecular Neurobiology · doi:10.1007/s12035-021-02699-x · Cited by 26 · see citing works
Lim, B., Tsolaki, M., Soosaipillai, A., Brown, M., Zilakaki, M., Tagaraki, F., Fotiou, D., Koutsouraki, E., Grosi, E., Prassas, I., et al. (2019) · Clinical Chemistry and Laboratory Medicine (CCLM) · doi:10.1515/cclm-2019-0428 · Cited by 25 · see citing works
Dulewicz, M., Kulczyńska-Przybik, A., Słowik, A., Borawska, R., & Mroczko, B. (2021) · Journal of Clinical Medicine · doi:10.3390/jcm10194575 · Cited by 22 · see citing works
Shantaraman, A., Dammer, E. B., Ugochukwu, O., Duong, D. M., Yin, L., Carter, E. K., Gearing, M., Chen‐Plotkin, A. S., Lee, E. B., Trojanowski, J. Q., et al. (2024) · Molecular Neurodegeneration · doi:10.1186/s13024-024-00749-1 · Cited by 22 · see citing works
Photoaffinity Probes for the Identification of Sequence-Specific Glycosaminoglycan-Binding Proteins
Joffrin, A. M., & Hsieh‐Wilson, L. C. (2020) · Journal of the American Chemical Society · doi:10.1021/jacs.0c06046 · Cited by 22 · see citing works
Wang, R., Man, Y., Zhou, M., Zhu, Y., Wang, L., & Yang, J. (2021) · Neuroreport · doi:10.1097/wnr.0000000000001584 · Cited by 20 · see citing works
AMPA receptors in Alzheimer disease: Pathological changes and potential therapeutic targets
Ning, L., Shen, R., Xie, B., Jiang, Y., Geng, X., & Dong, W. (2024) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/nlae093 · Cited by 19 · see citing works
Carmel, M., Michaelovsky, E., Weinberger, R., Frisch, A., Mekori‐Domachevsky, E., Gothelf, D., & Weizman, A. (2020) · The World Journal of Biological Psychiatry · doi:10.1080/15622975.2020.1747113 · Cited by 19 · see citing works
Lee, J. S., Sun, Y., Soares, A. R., Fai, C., Picciotto, M. R., & Guo, J. U. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.08.032 · Cited by 19 · see citing works
Liu, J., Wang, M., Sun, L., Pan, N. C., Zhang, C., Zhang, J., Zuo, Z., He, S., Wu, Q., & Wang, X. (2020) · Protein & Cell · doi:10.1007/s13238-020-00720-y · Cited by 18 · see citing works
Self-citationActivity-dependent diffusion trapping of AMPA receptors as a key step for expression of early LTP
Nowacka, A., Getz, A. M., Bessa‐Neto, D., & Choquet, D. (2024) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2023.0220 · Cited by 19 · see citing works
Podvin, S., Jones, A. C., Liu, Q., Aulston, B. D., Mosier, C., Ames, J., Winston, C. N., Lietz, C. B., Jiang, Z., O’Donoghue, A. J., et al. (2021) · ACS Omega · doi:10.1021/acsomega.1c00660 · Cited by 16 · see citing works
Hao, Y., Liu, H., Zeng, X.-T., Wang, Y., Zeng, W.-X., Qian, K., Li, L., Chi, M.-X., Gao, S., Hu, Z., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-37137-0 · Cited by 16 · see citing works
Microglia and Astrocytes in Postnatal Neural Circuit Formation
Duffy, A., & Eyo, U. B. (2024) · Glia · doi:10.1002/glia.24650 · Cited by 15 · see citing works
Drulis‐Fajdasz, D., Gostomska‐Pampuch, K., Duda, P., Wiśniewski, J. R., & Rakus, D. (2021) · Cells · doi:10.3390/cells10082021 · Cited by 14 · see citing works
Sumino, A., Sumikama, T., Zhao, Y., Flechsig, H., Umeda, K., Kodera, N., Konno, H., Hattori, M., & Shibata, M. (2024) · ACS Nano · doi:10.1021/acsnano.4c06295 · Cited by 14 · see citing works
Trans-synaptic interactions of ionotropic glutamate receptors
Fossati, M., & Charrier, C. (2020) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2020.09.001 · Cited by 14 · see citing works
Swaro, A., Bristow, B. N., Anwer, M., Zhang, A. A., Kraus, L., Gandhi, R. K., Erwin, S. R., Stach, T. R., Sullivan, K. E., Fan, J., et al. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115795 · Cited by 13 · see citing works
RNA-Sequencing-Based Transcriptomic Score with Prognostic and Theranostic Values in Multiple Myeloma
Alaterre, E., Vikova, V., Kassambara, A., Bruyer, A., Robert, N., Requirand, G., Bret, C., Herbaux, C., Vincent, L., Cartron, G., et al. (2021) · Journal of Personalized Medicine · doi:10.3390/jpm11100988 · Cited by 12 · see citing works
Saunders, T. S., Gadd, D. A., Spires‐Jones, T. L., King, D., Ritchie, C. W., & Terrera, G. M. (2022) · European Journal of Neuroscience · doi:10.1111/ejn.15656 · Cited by 12 · see citing works
Warpechowski, M., Warpechowski, J. J., Kulczyńska‐Przybik, A., & Mroczko, B. (2022) · Medical Science Monitor · doi:10.12659/msm.938826 · Cited by 11 · see citing works
Engineered adhesion molecules drive synapse organization
Hale, W. D., Südhof, T. C., & Huganir, R. L. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2215905120 · Cited by 11 · see citing works
Self-citationPedrero-Prieto, C. M., Frontiñán-Rubio, J., Alcain, F. J., Durán‐Prado, M., Peinado, J. R., & Rabanal‐Ruiz, Y. (2021) · Diagnostics · doi:10.3390/diagnostics11091655 · Cited by 12 · see citing works
Zhang, X., Wu, M., Cheng, L., Cao, W., Liu, Z., Yang, S., & Kim, M. S. (2024) · Molecular Psychiatry · doi:10.1038/s41380-024-02756-6 · Cited by 11 · see citing works
Human neural networks with sparse TDP-43 pathology reveal NPTX2 misregulation in ALS/FTLDPreprint
Hruška-Plocháň, M., Betz, K. M., Ronchi, S., Wiersma, V. I., Maniecka, Z., Hock, E., Laferrière, F., Sahadevan, S., Hoop, V., Delvendahl, I., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.08.471089 · Cited by 10 · see citing works
Lim, B., Fowler, C., Li, Q.-X., Rowe, C., Dhiman, K., Gupta, V. B., Masters, C. L., Doecke, J. D., Martins, R. N., Collins, S., et al. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.135078 · Cited by 10 · see citing works
Tuning synapse strength by nanocolumn plasticity
Xu, N., Chen, S.-Y., & Tang, A. (2025) · Trends in Neurosciences · doi:10.1016/j.tins.2024.12.009 · Cited by 10 · see citing works
Do pentraxin 3 and neural pentraxin 2 have different facet function in hepatocellular carcinoma?
Cabiati, M., Gaggini, M., SIMONE, P. D., & Ry, S. D. (2021) · Clinical and Experimental Medicine · doi:10.1007/s10238-021-00714-y · Cited by 9 · see citing works
Zhao, J., Hou, S.-J., Zhao, J., Yu, H., & Duan, S.-R. (2023) · Translational Neuroscience · doi:10.1515/tnsci-2022-0298 · Cited by 8 · see citing works
Emerging evidence of context-dependent synapse elimination by phagocytes in the CNS
Shen, F.-S., Liu, C., Sun, H.-Z., Chen, X., Xue, Y., & Chen, L. (2024) · Journal of Leukocyte Biology · doi:10.1093/jleuko/qiae098 · Cited by 8 · see citing works
Heinrich, I. A., Freitas, A. E., Wolin, I. A. V., Nascimento, A. P. M., Walz, R., Rodrigues, A. L. S., & Leal, R. B. (2021) · Metabolic Brain Disease · doi:10.1007/s11011-021-00675-x · Cited by 8 · see citing works
Fluid markers of synapse degeneration in synucleinopathies
Cervantes González, A., & Belbin, O. (2022) · Journal of Neural Transmission · doi:10.1007/s00702-022-02467-8 · Cited by 7 · see citing works
Palomino, P. A. P., Black, K. C., & Ressl, S. (2023) · Biochemical Society Transactions · doi:10.1042/bst20220439 · Cited by 7 · see citing works
Blanco, I., Deasy, S., Amontree, M., Gabriel, M., Caccavano, A., Vicini, S., Glasgow, E., & Conant, K. (2025) · Molecular Psychiatry · doi:10.1038/s41380-025-03007-y · Cited by 4 · see citing works
Dynamic extracellular interactions with AMPA receptors
Goldschmidt, H. L., Barber, C. N., Renuse, S., Cutler, J. A., Kreimer, S. D., Bygrave, A. M., Meyers, D. J., Hale, W. D., Pandey, A., & Huganir, R. L. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2517436122 · Cited by 7 · see citing works
Membrane trafficking of synaptic adhesion molecules
Bogaciu, C. A., & Rizzoli, S. O. (2024) · The Journal of Physiology · doi:10.1113/jp286401 · Cited by 7 · see citing works
Wei, M., Wang, M., Wang, J., Su, F., Wang, Y., Sun, M., Wang, S., Liu, M., Wang, H., Lu, M., et al. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.00829 · Cited by 7 · see citing works
Self-citationGómez, G., Shi, L., Fohner, A. E., Chen, J., Yang, Y., Fornage, M., Duggan, M. R., Peng, Z., Daya, G. N., Tin, A., et al. (2024) · medRxiv · doi:10.1101/2024.10.07.24314972 · Cited by 7 · see citing works
Reig-Viader, R., del Castillo-Berges, D., Burgas-Pau, A., Arco-Alonso, D., Zerpa-Rios, O., Ramos-Vicente, D., Picañol, J., Castellanos, A., Soto, D., Roher, N., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-65490-9 · Cited by 6 · see citing works
- Authors
- Lee, S.-J., Wei, M., Zhang, C., Maxeiner, S., Pak, C., Calado Botelho, S., Trotter, J., Sterky, F. H., & Südhof, T. C.
- Affiliations
- Stanford Medicine (US)
- Peking University (CN)
- Howard Hughes Medical Institute (US)
- ORCID
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2016-12-16
- Volume
- 37
- Issue
- 5
- Pages
- 1062-1080
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC5296791
- OpenAlex
- W2562584466
- Cited by
- 146
- References
- 36
- Citations by year
- 2026: 9 · 2025: 12 · 2024: 28 · 2023: 13 · 2022: 18 · 2021: 21 · 2020: 21 · 2019: 6 · 2018: 9 · 2017: 9
- FWCI
- 4.49
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institute of Mental Health (R01MH052804, R37MH052804)
- Eunice Kennedy Shriver National Institute of Child Health and Human Development (F32HD078051)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Immunology and Microbiology › Immunology › Biomarkers in Disease Mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- NARP, excitatory synapses, inhibitory synapses, AMPA receptors, GABA receptors, trans-synaptic signaling, postsynaptic specialization, hippocampal neurons, synaptic plasticity, presynaptic plasma membrane
- MeSH terms
- Pentraxins, Animals, C-Reactive Protein, Hippocampus, Humans, Nerve Tissue Proteins, Neurons, Receptors, Cell Surface, Synapses, Receptors, AMPA, Patch-Clamp Techniques, Excitatory Amino Acid Antagonists, GABA Antagonists, Coculture Techniques, Excitatory Postsynaptic Potentials, RNA, Small Interfering, Mice, Gene Knockdown Techniques, HEK293 Cells
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