Differential reelin-induced enhancement of NMDA and AMPA receptor activity in the adult hippocampus
Open accessAbstract
The developmental lamination of the hippocampus and other cortical structures requires a signaling cascade initiated by reelin and its receptors, apoER2 (apolipoprotein E receptor 2) and VLDLR (very-low-density lipoprotein receptor). However, the functional significance of continued reelin expression in the postnatal brain remains poorly understood. Here, we show that reelin application to adult mice hippocampal slices leads to enhanced glutamatergic transmission mediated by NMDA receptors (NMDARs) and AMPA receptors (AMPARs) through distinct mechanisms. Application of recombinant reelin enhanced NMDAR-mediated currents through postsynaptic mechanisms, as revealed by the variance-mean analysis of synaptic NMDAR currents, assessment of spontaneous miniature events, and the levels of NMDAR subunits at synaptic surface. In comparison, nonstationary fluctuation analysis of miniature AMPAR currents and quantification of synaptic surface proteins revealed that reelin-induced enhancement of AMPAR responses was mediated by increased AMPAR numbers. Reelin enhancement of synaptic NMDAR currents was abolished when receptor-associated protein (RAP) or the Src inhibitor 4-amino-5-(4-methylphenyl)-7-(t-butyl)pyrazolo[3,4-d]-pyrimidine (PP1) was bath applied and was abrogated by including PP1 in the recording electrodes. In comparison, including RAP or an inactive PP1 analog PP3 in the recording electrode was without effect. Interestingly, the increased AMPAR response after reelin application was not blocked by PP1 but was blocked by the phosphoinositide-3' kinase (PI3K) inhibitors wortmannin and LY294002 [2-(4-morpholinyl)-8-phenyl-1(4H)-benzopyran-4-one hydrochloride]. Furthermore, reelin-induced, PI3K-dependent AMPAR surface insertion was also observed in cultured hippocampal neurons. Together, these results reveal a differential functional coupling of reelin signaling with NMDAR and AMPAR function and define a novel mechanism for controlling synaptic strength and plasticity in the adult hippocampus.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
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?
Reelin enhances hippocampal synaptic plasticity by altering the composition of NMDA receptor subunits and promoting surface clustering of AMPA receptors.
“Reelin is also known to enhance hippocampal synaptic plasticity (Pujadas et al., 2010; Weeber et al., 2002) by altering the composition of NMDA receptor subunits and promoting surface clustering of AMPA receptors (Qiu et al., 2006) (Figure 3B).”
From Adult neurogenesis, glia, and the extracellular matrix (2019) · cites this paper as Qiu et al., 2006
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Discovery of a Novel, Potent, and Src Family-selective Tyrosine Kinase Inhibitor
Hanke, J. H., Gardner, J. P., Dow, R. L., Changelian, P. S., Brissette, W. H., Weringer, E. J., Pollok, B. A., & Connelly, P. A. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.2.695 · Cited by 1,939 · see citing works
A protein related to extracellular matrix proteins deleted in the mouse mutant reeler
D'Arcangelo, G., G. Miao, G., Chen, S.-C., Scares, H. D., Morgan, J. I., & Curran, T. (1995) · Nature · doi:10.1038/374719a0 · Cited by 1,748 · see citing works
Hayashi, Y., Shi, S.-H., Esteban, J. A., Piccini, A., Poncer, J.-C., & Malinow, R. (2000) · Science · doi:10.1126/science.287.5461.2262 · Cited by 1,524 · see citing works
Rapid Spine Delivery and Redistribution of AMPA Receptors After Synaptic NMDA Receptor Activation
Shi, S.-H., Hayashi, Y., Petralia, R. S., Zaman, S. H., Wenthold, R. J., Svoboda, K., & Malinow, R. (1999) · Science · doi:10.1126/science.284.5421.1811 · Cited by 1,276 · see citing works
Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., & Herz, J. (1999) · Cell · doi:10.1016/s0092-8674(00)80782-5 · Cited by 1,261 · see citing works
Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity
Lee, H.-K., Barbarosie, M., Kameyama, K., Bear, M. F., & Huganir, R. L. (2000) · Nature · doi:10.1038/35016089 · Cited by 1,116 · see citing works
Regulatory phosphorylation of AMPA-type glutamate receptors by CaM-KII during long-term potentiation
Barria, A., Muller, D., Derkach, V., Griffith, L. C., & Soderling, T. R. (1997) · Science · doi:10.1126/science.276.5321.2042 · Cited by 1,049 · see citing works
Hiesberger, T., Trommsdorff, M., Howell, B. W., Goffinet, A., Mumby, M. C., Cooper, J. A., & Herz, J. (1999) · Neuron · doi:10.1016/s0896-6273(00)80861-2 · Cited by 916 · see citing works
Reelin Is a Ligand for Lipoprotein Receptors
D'Arcangelo, G., Homayouni, R., Keshvara, L., Rice, D. S., Sheldon, M., & Curran, T. (1999) · Neuron · doi:10.1016/s0896-6273(00)80860-0 · Cited by 808 · cited 1× · see citing works
“The developmental lamination of the hippocampus and other cortical structures requires a signaling cascade initiated by reelin and its receptors, apoER2 (apolipoprotein E receptor 2) and VLDLR (very-low-density lipoprotein receptor).”
BackgroundSrc kinases: a hub for NMDA receptor regulation
Salter, M. W., & Kalia, L. V. (2004) · Nature reviews. Neuroscience · doi:10.1038/nrn1368 · Cited by 767 · see citing works
Neuronal position in the developing brain is regulated by mouse disabled-1
Howell, B. W., Hawkes, R., Soriano, P., & Cooper, J. A. (1997) · Nature · doi:10.1038/39607 · Cited by 692 · see citing works
Regulation of NMDA receptors by tyrosine kinases and phosphatases
Wang, Y. T., & Salter, M. W. (1994) · Nature · doi:10.1038/369233a0 · Cited by 666 · see citing works
Control of GluR1 AMPA receptor function by cAMP-dependent protein kinase
Banke, T. G., Bowie, D., Lee, H.-K., Huganir, R. L., Schousboe, A., & Traynelis, S. F. (2000) · The Journal of Neuroscience · doi:10.1523/jneurosci.20-01-00089.2000 · Cited by 652 · see citing works
Reelin and ApoE receptors cooperate to enhance hippocampal synaptic plasticity and learning
Weeber, E. J., Beffert, U., Jones, C., Christian, J. M., Förster, E., Sweatt, J. D., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205147200 · Cited by 623 · see citing works
Self-citationNMDA Channel Regulation by Channel-Associated Protein Tyrosine Kinase Src
Yu, X., Askalan, R., Keil, G. J., & Salter, M. W. (1997) · Science · doi:10.1126/science.275.5300.674 · Cited by 608 · see citing works
Jaworski, J., Spangler, S. A., Seeburg, D. P., Hoogenraad, C. C., & Sheng, M. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.2270-05.2005 · Cited by 577 · see citing works
Herz, J., Goldstein, J. L., Strickland, D. K., Ho, Y. K., & Brown, M. S. (1991) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)54845-6 · Cited by 576 · see citing works
Alcántara, S., Ruiz, M., D’Arcangelo, G., Ezan, F., de Lecea, L., Curran, T., Sotelo, C., & Soriano, E. (1998) · The Journal of Neuroscience · doi:10.1523/jneurosci.18-19-07779.1998 · Cited by 568 · see citing works
Trommsdorff, M., Borg, J., Margolis, B. L., & Herz, J. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.50.33556 · Cited by 540 · see citing works
Modulation of AMPA receptor unitary conductance by synaptic activity
Benke, T. A., Lüthi, A., Isaac, J. T. R., & Collingridge, G. L. (1998) · Nature · doi:10.1038/31709 · Cited by 533 · see citing works
Reelin Is a Secreted Glycoprotein Recognized by the CR-50 Monoclonal Antibody
D’Arcangelo, G., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., & Curran, T. (1997) · The Journal of Neuroscience · doi:10.1523/jneurosci.17-01-00023.1997 · Cited by 515 · see citing works
Beffert, U., Weeber, E. J., Durudas, A., Qiu, S., Masiulis, I., Sweatt, J. D., Li, W.-P., Adelmann, G., Frotscher, M., Hammer, R. E., et al. (2005) · Neuron · doi:10.1016/j.neuron.2005.07.007 · Cited by 497 · see citing works
Self-citationPostsynaptic induction and presynaptic expression of hippocampal long-term depression.
Bolshakov, V., & Siegelbaum, S. (1994) · Science · doi:10.1126/science.7909958 · Cited by 489 · see citing works
A role for Cajal–Retzius cells and reelin in the development of hippocampal connections
Del Río, J. A., Heimrich, B., Borrell, V., Förster, E., Drakew, A., Alcántara, S., Nakajima, K., Miyata, T., Ogawa, M., Mikoshiba, K., et al. (1997) · Nature · doi:10.1038/385070a0 · Cited by 472 · see citing works
Reelin-induced tryosine phosphorylation of Disabled 1 during neuronal positioning
Howell, B. W., Herrick, T. M., & Cooper, J. A. (1999) · Genes & Development · doi:10.1101/gad.13.6.643 · Cited by 411 · see citing works
Pesold, C., Impagnatiello, F., Pisu, M. G., Uzunov, D. P., Costa, E., Guidotti, A., & Caruncho, H. J. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.6.3221 · Cited by 391 · see citing works
Reelin promotes hippocampal dendrite development through the VLDLR/ApoER2-Dab1 pathway
Niu, S., Renfro, A., Quattrocchi, C. C., Sheldon, M., & D'Arcangelo, G. (2004) · Neuron · doi:10.1016/s0896-6273(03)00819-5 · Cited by 375 · see citing works
Howell, B. W., Lanier, L. M., Frank, R., Gertler, F. B., & Cooper, J. A. (1999) · Molecular and Cellular Biology · doi:10.1128/mcb.19.7.5179 · Cited by 371 · see citing works
Reelin Activates Src Family Tyrosine Kinases in Neurons
Bock, H. H., & Herz, J. (2003) · Current Biology · doi:10.1016/s0960-9822(02)01403-3 · Cited by 355 · see citing works
LTP leads to rapid surface expression of NMDA but not AMPA receptors in adult rat CA1
Grosshans, D. R., Clayton, D. A., Coultrap, S. J., & Browning, M. D. (2001) · Nature Neuroscience · doi:10.1038/nn779 · Cited by 354 · see citing works
Man, H., Wang, Q., Lu, W.-Y., Ju, W. H., Ahmadian, G., Liu, L., D’Souza, S. A., Wong, T. P., Taghibiglou, C., Lu, J., et al. (2003) · Neuron · doi:10.1016/s0896-6273(03)00228-9 · Cited by 345 · see citing works
Src Activation in the Induction of Long-Term Potentiation in CA1 Hippocampal Neurons
Lu, Y. M., Roder, J., Davidow, J. S., & Salter, M. W. (1998) · Science · doi:10.1126/science.279.5355.1363 · Cited by 328 · see citing works
Chung, H. J., Huang, Y., Lau, L., & Huganir, R. L. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.0546-04.2004 · Cited by 315 · see citing works
Reelin-mediated Signaling Locally Regulates Protein Kinase B/Akt and Glycogen Synthase Kinase 3β
Beffert, U., Morfini, G., Bock, H. H., Reyna, H., Brady, S. T., & Herz, J. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m209205200 · Cited by 306 · see citing works
Reelin modulates NMDA receptor activity in cortical neurons
Chen, Y., Beffert, U., Ertunc, M., Tang, T.-S., Kavalali, E. T., Bezprozvanny, I., & Herz, J. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1951-05.2005 · Cited by 299 · see citing works
Ahmadian, G., Ju, W., Liu, L., Wyszynski, M., Lee, S. H., Dunah, A. W., Taghibiglou, C., Wang, Y., Lu, J., Wong, T. P., et al. (2004) · The EMBO Journal · doi:10.1038/sj.emboj.7600126 · Cited by 296 · see citing works
Role of Tissue Plasminogen Activator Receptor LRP in Hippocampal Long-Term Potentiation
Zhuo, M., Holtzman, D. M., Li, Y., Osaka, H., DeMaro, J., Jacquin, M. F., & Bu, G. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-02-00542.2000 · Cited by 279 · see citing works
Differential Tyrosine Phosphorylation of N-Methyl-D-aspartate Receptor Subunits
Lau, L., & Huganir, R. L. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.34.20036 · Cited by 276 · see citing works
Traynelis, S. F., Silver, R. A., & Cull-Candy, S. G. (1993) · Neuron · doi:10.1016/0896-6273(93)90184-s · Cited by 267 · see citing works
Sanna, P. P., Cammalleri, M., Berton, F., Simpson, C., Lütjens, R., Bloom, F. E., & Francesconi, W. G. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-09-03359.2002 · Cited by 250 · see citing works
Reelin expression and glycosylation patterns are altered in Alzheimer’s disease
Botella-López, A., Burgaya, F., Gavín, R., García-Ayllón, M. S., Gómez-Tortosa, E., Peña-Casanova, J., Ureña, J. M., Del Río, J. A., Blesa, R., Soriano, E., et al. (2006) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0601279103 · Cited by 221 · see citing works
Interaction of reelin signaling and Lis1 in brain development
Assadi, A. H., Zhang, G., Beffert, U., McNeil, R. S., Renfro, A., Niu, S., Quattrocchi, C. C., Antalffy, B. A., Sheldon, M., Armstrong, D. D., et al. (2003) · Nature Genetics · doi:10.1038/ng1257 · Cited by 219 · see citing works
Opazo, P., Watabe, A. M., Grant, S. G. N., & O'Dell, T. J. (2003) · The Journal of Neuroscience · doi:10.1523/jneurosci.23-09-03679.2003 · Cited by 215 · see citing works
Activation of a Dab1/CrkL/C3G/Rap1 Pathway in Reelin-Stimulated Neurons
Ballif, B. A., Arnaud, L., Arthur, W. T., Guris, D. L., Imamoto, A., & Cooper, J. A. (2004) · Current Biology · doi:10.1016/j.cub.2004.03.038 · Cited by 208 · see citing works
Absence of Fyn and Src Causes a Reeler-Like Phenotype
Kuo, G., Arnaud, L., Kronstad-O'Brien, P., & Cooper, J. A. (2005) · Journal of Neuroscience · doi:10.1523/jneurosci.1656-05.2005 · Cited by 200 · see citing works
Tyrosine phosphorylation and regulation of the AMPA receptor by SRC family tyrosine kinases
Hayashi, T., & Huganir, R. L. (2004) · The Journal of Neuroscience · doi:10.1523/jneurosci.0799-04.2004 · Cited by 177 · see citing works
Regulation of Protein Tyrosine Kinase Signaling by Substrate Degradation during Brain Development
Arnaud, L., Ballif, B. A., & Cooper, J. A. (2003) · Molecular and Cellular Biology · doi:10.1128/mcb.23.24.9293-9302.2003 · Cited by 164 · see citing works
Calmodulin Activates Phosphatidylinositol 3-Kinase
Joyal, J. L., Burks, D. J., Pons, S., Matter, W. F., Vlahos, C. J., White, M. F., & Sacks, D. B. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.45.28183 · Cited by 163 · see citing works
Frerking, M. E., Schmitz, D., Zhou, Q., Johansen, J. P., & Nicoll, R. A. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-09-02958.2001 · Cited by 163 · see citing works
Kelly, A. M., & Lynch, M. A. (2000) · Neuropharmacology · doi:10.1016/s0028-3908(99)00169-0 · Cited by 144 · see citing works
Ramos‐Moreno, T., Galazo, M. J., Porrero, C., Martínez‐Cerdeño, V., & Clascá, F. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04567.x · Cited by 129 · see citing works
Sinagra, M., Verrier, D., Frankova, D., Korwek, K. M., Blahos, J., Weeber, E. J., Manzoni, O. J., & Chavis, P. (2005) · The Journal of Neuroscience · doi:10.1523/jneurosci.1757-05.2005 · Cited by 128 · see citing works
Self-citationReelin is a positional signal for the lamination of dentate granule cells
Zhao, S., Chai, X., Förster, E., & Frotscher, M. (2004) · Development · doi:10.1242/dev.01387 · Cited by 127 · see citing works
Activation of Metabotropic Glutamate Receptor 1 Accelerates NMDA Receptor Trafficking
Lan, J.-Y., Skeberdis, V. A., Jover, T., Zheng, X., Bennett, M. V. L., & Zukin, R. S. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-16-06058.2001 · Cited by 115 · see citing works
Binding of purified Reelin to ApoER2 and VLDLR mediates tyrosine phosphorylation of Disabled-1
Benhayon, D., Magdaleno, S. M., & Curran, T. (2003) · Molecular Brain Research · doi:10.1016/s0169-328x(03)00032-9 · Cited by 110 · see citing works
Involvement of the Secretory Pathway for AMPA Receptors in NMDA-Induced Potentiation in Hippocampus
Broutman, G., & Baudry, M. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-01-00027.2001 · Cited by 99 · see citing works
Reelin‐expressing neurons in the postnatal and adult human hippocampal formation
Ábrahám, H., & Meyer, G. (2003) · Hippocampus · doi:10.1002/hipo.10125 · Cited by 93 · see citing works
Nimpf, J. (2000) · Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids · doi:10.1016/s1388-1981(00)00155-4 · Cited by 90 · see citing works
Src is necessary and sufficient for human airway smooth muscle cell proliferation and migration
Krymskaya, V. P., Goncharova, E. A., Ammit, A. J., et al. (2004) · The FASEB Journal · doi:10.1096/fj.04-2869fje · Cited by 90 · see citing works
Apolipoprotein E Receptor 2 Interactions with the N-Methyl-D-aspartate Receptor
Hoe, H., Pocivavsek, A., Chakraborty, G., Fu, Z., Vicini, S., Ehlers, M., & Rebeck, G. W. (2005) · Journal of Biological Chemistry · doi:10.1074/jbc.m509380200 · Cited by 89 · see citing works
Lei, G., Xue, S., Chéry, N., et al. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf292 · Cited by 78 · see citing works
Abnormal laminar position and dendrite development of interneurons in the reeler forebrain
Yabut, O., Renfro, A., Niu, S., Swann, J. W., Marín, Ó., & D’Arcangelo, G. (2006) · Brain Research · doi:10.1016/j.brainres.2005.09.070 · Cited by 68 · see citing works
Apoer2: a reelin receptor to remember
D’Arcangelo, G. (2005) · Neuron · doi:10.1016/j.neuron.2005.08.001 · Cited by 62 · see citing works
Qiu, S., Korwek, K. M., & Weeber, E. J. (2005) · Neurobiology of Learning and Memory · doi:10.1016/j.nlm.2005.08.009 · Cited by 61 · see citing works
Self-citationShah, B. H., Neithardt, A. B., Chu, D. B., et al. (2005) · Journal of Cellular Physiology · doi:10.1002/jcp.20423 · Cited by 57 · see citing works
Ultrastructural localization of reelin in the cortex in post-mortem human brain
Roberts, R. C., Xu, L., Roche, J. K., & Kirkpatrick, B. W. (2004) · The Journal of Comparative Neurology · doi:10.1002/cne.20408 · Cited by 56 · see citing works
Goffinet, A. M. (1995) · Nature · doi:10.1038/374675a0 · Cited by 38 · see citing works
Baxter, A. W., & Wyllie, D. J. A. (2006) · Journal of Neuroscience · doi:10.1523/jneurosci.4101-05.2006 · Cited by 30 · see citing works
Yabut, O., Renfro, A., Niu, S., Swann, J. W., Marín, Ó., & D’Arcangelo, G. (2005) · Molecular Brain Research · doi:10.1016/j.molbrainres.2005.09.015 · Cited by 4 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Apolipoprotein E and Apolipoprotein E Receptors: Normal Biology and Roles in Alzheimer Disease
Holtzman, D. M., Herz, J., & Bu, G. (2012) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a006312 · Cited by 782 · see citing works
The dual role of the extracellular matrix in synaptic plasticity and homeostasis
Dityatev, A., Schachner, M., & Sonderegger, P. (2010) · Nature Reviews Neuroscience · doi:10.1038/nrn2898 · Cited by 559 · see citing works
Liu, Q., Trotter, J., Zhang, J., Peters, M. M., Cheng, H., Bao, J., Han, X., Weeber, E. J., & Bu, G. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.4067-10.2010 · Cited by 268 · see citing works
Self-citationAdult neurogenesis, glia, and the extracellular matrix
Cope, E. C., & Gould, E. (2019) · Cell Stem Cell · doi:10.1016/j.stem.2019.03.023 · Cited by 236 · see citing works
Groc, L., Choquet, D., Stephenson, F. A., Verrier, D., Manzoni, O. J., & Chavis, P. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.1772-07.2007 · Cited by 225 · see citing works
Reelin regulates postnatal neurogenesis and enhances spine hypertrophy and long-term potentiation
Pujadas, L., Gruart, A., Bosch, C., Delgado, L., Teixeira, C. M., Rossi, D., de Lecea, L., Martínez, A., Delgado-García, J. M., & Soriano, E. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.5284-09.2010 · Cited by 219 · see citing works
Retrieval-specific endocytosis of GluA2-AMPARs underlies adaptive reconsolidation of contextual fear
Rao-Ruiz, P., Rotaru, D. C., van der Loo, R. J., Mansvelder, H. D., Stiedl, O., Smit, A. B., & Spijker, S. (2011) · Nature Neuroscience · doi:10.1038/nn.2907 · Cited by 192 · see citing works
Reelin and neuropsychiatric disorders
Ishii, K., Kubo, K.-I., & Nakajima, K. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00229 · Cited by 185 · see citing works
Reelin supplementation enhances cognitive ability, synaptic plasticity, and dendritic spine density
Rogers, J. T., Rusiana, I., Trotter, J., Zhao, L., Donaldson, E., Pak, D. T. S., Babus, L. W., Peters, M., Banko, J. L., Chavis, P., et al. (2011) · Learning & Memory · doi:10.1101/lm.2153511 · Cited by 181 · see citing works
Self-citationLRP8-Reelin-regulated neuronal enhancer signature underlying learning and memory formation
Telese, F., Ma, Q., Perez, P. M., Notani, D., Oh, S., Li, W., Comoletti, D., Ohgi, K. A., Taylor, H., & Rosenfeld, M. G. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.033 · Cited by 166 · see citing works
Shaping Synapses by the Neural Extracellular Matrix
Ferrer-Ferrer, M., & Dityatev, A. (2018) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2018.00040 · Cited by 169 · see citing works
Reelin signaling antagonizes β-amyloid at the synapse
Durakoglugil, M. S., Chen, Y., White, C. L., Kavalali, E. T., & Herz, J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0908176106 · Cited by 153 · see citing works
Kocherhans, S., Madhusudan, A., Doehner, J., Breu, K. S., Nitsch, R. M., Fritschy, J.-M., & Knuesel, I. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.0418-10.2010 · Cited by 132 · see citing works
Pujadas, L., Rossi, D., Andrés, R., Teixeira, C. M., Serra-Vidal, B., Parcerisas, A., Maldonado, R., Giralt, E., Carulla, N., & Soriano, E. (2014) · Nature Communications · doi:10.1038/ncomms4443 · Cited by 129 · see citing works
Iafrati, J., Orejarena, M. J., Lassalle, O., Bouamrane, L., & Chavis, P. (2014) · Molecular Psychiatry · doi:10.1038/mp.2013.66 · Cited by 132 · see citing works
Bal, M., Leitz, J., Reese, A. L., Ramirez, D. M. O., Durakoglugil, M., Herz, J., Monteggia, L. M., & Kavalali, E. T. (2013) · Neuron · doi:10.1016/j.neuron.2013.08.024 · Cited by 131 · see citing works
Emerging topics in Reelin function
Förster, E., Bock, H. H., Herz, J., Chai, X., Frotscher, M., & Zhao, S. (2010) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2010.07222.x · Cited by 130 · see citing works
Reelin in the years: controlling neuronal migration and maturation in the mammalian brain
D'Arcangelo, G. (2014) · Advances in Neuroscience · doi:10.1155/2014/597395 · Cited by 120 · see citing works
Reelin secreted by GABAergic neurons regulates glutamate receptor homeostasis
Campo, C. G., Sinagra, M., Verrier, D., Manzoni, O. J., & Chavis, P. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005505 · Cited by 100 · see citing works
Cell-autonomous inactivation of the reelin pathway impairs adult neurogenesis in the hippocampus
Teixeira, C. M., Kron, M. M., Masachs, N., Zhang, H., Lagace, D. C., Martinez, A., Reillo, I., Duan, X., Bosch, C., Pujadas, L., et al. (2012) · The Journal of Neuroscience · doi:10.1523/jneurosci.1857-12.2012 · Cited by 97 · see citing works
Reelin-mediated signaling in neuropsychiatric and neurodegenerative diseases
Knuesel, I. (2010) · Progress in Neurobiology · doi:10.1016/j.pneurobio.2010.04.002 · Cited by 89 · see citing works
ApoE isoform-dependent changes in hippocampal synaptic function
Korwek, K. M., Trotter, J. H., LaDu, M. J., Sullivan, P. M., & Weeber, E. J. (2009) · Molecular Neurodegeneration · doi:10.1186/1750-1326-4-21 · Cited by 89 · see citing works
Self-citationBosch, C., Masachs, N., Exposito-Alonso, D., Martínez, A., Teixeira, C. M., Fernaud, I., Pujadas, L., Ulloa, F., Comella, J. X., DeFelipe, J., et al. (2016) · Cerebral Cortex · doi:10.1093/cercor/bhw216 · Cited by 70 · see citing works
Kadriu, B., Musazzi, L., Johnston, J. N., Kalynchuk, L. E., Caruncho, H. J., Popoli, M., & Zarate, C. A. (2021) · Drug Discovery Today · doi:10.1016/j.drudis.2021.07.027 · Cited by 62 · see citing works
Reelin proteolysis affects signaling related to normal synapse function and neurodegeneration
Lussier, A. L., Weeber, E. J., & Rebeck, G. W. (2016) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2016.00075 · Cited by 31 · see citing works
Self-citationLaminar distribution of neurotransmitter receptors in different reeler mouse brain regions
Cremer, C. M., Lübke, J. H. R., Palomero-Gallagher, N., & Zilles, K. (2011) · Brain Structure and Function · doi:10.1007/s00429-011-0303-3 · Cited by 17 · see citing works
- Authors
- Qiu, S., Zhao, L. F., Korwek, K. M., & Weeber, E. J.
- Affiliations
- Vanderbilt University Medical Center (US)
- Vanderbilt University (US)
- Venue
- The Journal of Neuroscience
- Publisher
- Society for Neuroscience
- Published
- 2006-12-13
- Volume
- 26
- Issue
- 50
- Pages
- 12943-12955
- ISSN
- 0270-6474 (ISSN-L)
- 1529-2401
- PMC
- PMC6674964
- OpenAlex
- W2040901919
- Cited by
- 186
- References
- 69
- Citations by year
- 2026: 5 · 2025: 8 · 2024: 9 · 2023: 11 · 2022: 9 · 2021: 8 · 2020: 14 · 2019: 9 · 2018: 3 · 2017: 7 · 2016: 17 · 2015: 9 · 2014: 12 · 2013: 10 · 2012: 11
- FWCI
- 2.53
- 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
- Vanderbilt University (HEK293)
- Vanderbilt University Medical Center
- National Institutes of Health (HEK293)
- National Institute on Aging (R01AG022574)
- Topics
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetics and Neurodevelopmental Disorders
- Keywords
- reelin, NMDA receptor, AMPA receptors, hippocampus, synaptic transmission, phosphoinositide 3-kinase signaling, Src family kinases, receptor-associated protein, synaptic plasticity, postnatal brain development, glutamatergic synapses
- MeSH terms
- Reelin Protein, Animals, Cell Line, Cells, Cultured, Female, Hippocampus, Humans, Male, Mice, Inbred C3H, Mice, Inbred C57BL, Nerve Tissue Proteins, Serine Endopeptidases, Signal Transduction, Cell Adhesion Molecules, Neuronal, Receptors, N-Methyl-D-Aspartate, Extracellular Matrix Proteins, Receptors, AMPA, src-Family Kinases, Excitatory Postsynaptic Potentials, Mice
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
