Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions
Abstract
To test the hypothesis that agrin mediates motor neuron-induced aggregation of acetylcholine receptors (AChRs) in skeletal muscle fibers and to determine whether the agrin active in this process is released by motor neurons, we raised polyclonal antibodies to purified ray agrin that blocked its receptor aggregating activity. When the antibodies were applied to chick motor neuron--chick myotube cocultures, they inhibited the formation of AChR aggregates at and near neuromuscular contacts, demonstrating that agrin plays a role in the induction of the aggregates. Rat motor neurons, like chick motor neurons, induce AChR aggregates on chick myotubes. This effect was not inhibited by our antibodies, indicating that, although the antibodies inhibited the activity of chick agrin, they did not have a similar effect on rat agrin. We conclude that agrin released by rat motor neurons induced the chick myotubes to aggregate AChRs.
Integrity signals
Registry
Cites
Statistics
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?
Neuronal-specific Agrn isoforms containing the Z exons (32 and 33) are the most potent in promoting AChR aggregation.
“Neuronal-specific Agrn isoforms containing the Z exons (32 and 33) are the most potent in promoting AChR aggregation74–77.”
From The neurogenetics of alternative splicing (2016) · cites this paper as [75]
Cites
Isolation of pure IgG1, IgG2a and IgG2b immunoglobulins from mouse serum using protein A-Sepharose
Ey, P. L., Prowse, S. J., & Jenkin, C. R. (1978) · Immunochemistry · doi:10.1016/0161-5890(78)90070-6 · Cited by 2,673 · see citing works
The Agrin HypothesisPreprint
McMahan, U. J. (1990) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1990.055.01.041 · Cited by 643 · see citing works
Self-citationIdentification of agrin, a synaptic organizing protein from Torpedo electric organ.
Nitkin, R. M., Smith, M. A., Magill, C., Fallon, J. R., Yao, Y. M., Wallace, B. G., & McMahan, U. J. (1987) · The Journal of cell biology · doi:10.1083/jcb.105.6.2471 · Cited by 469 · see citing works
Self-citationSynapse formation between dissociated nerve and muscle cells in low density cell cultures
Fischbach, G. D. (1972) · Developmental Biology · doi:10.1016/0012-1606(72)90023-1 · Cited by 458 · see citing works
Burden, S. J., Sargent, P. B., & McMahan, U. J. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.82.2.412 · Cited by 355 · see citing works
Self-citationFrank, E., & Fischbach, G. D. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.83.1.143 · Cited by 347 · see citing works
Structure and expression of a rat agrin
Rupp, F., Payan, D. G., Magill, C., Cowan, D. M., & Scheller, R. H. (1991) · Neuron · doi:10.1016/0896-6273(91)90177-2 · Cited by 306 · see citing works
The agrin gene codes for a family of basal lamina proteins that differ in function and distribution
Rüegg, M. A., Tsim, K. W. K., Horton, S. E., Kröger, S., Escher, G., Gensch, E. M., & McMahan, U. J. (1992) · Neuron · doi:10.1016/0896-6273(92)90090-z · Cited by 254 · see citing works
Self-citationDevelopment of Acetylcholine Receptor Clusters on Cultured Muscle Cells
Sytkowski, A. J., Vogel, Z., & Nirenberg, M. W. (1973) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.70.1.270 · Cited by 231 · see citing works
cDNA that encodes active agrin
Tsim, K. W. K., Rüegg, M. A., Escher, G., Kröger, S., & McMahan, U. J. (1992) · Neuron · doi:10.1016/0896-6273(92)90089-v · Cited by 200 · see citing works
Self-citationAgrin-like molecules at synaptic sites in normal, denervated, and damaged skeletal muscles.
Reist, N. E., Magill, C., & McMahan, U. J. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.6.2457 · Cited by 173 · see citing works
Self-citationSchnaar, R. L., & Schaffner, A. (1981) · Journal of Neuroscience · doi:10.1523/jneurosci.01-02-00204.1981 · Cited by 158 · see citing works
Dohrmann, U., Edgar, D., Sendtner, M., & Thoenen, H. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90089-8 · Cited by 154 · see citing works
McMahan, U. J., & Slater, C. R. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.4.1453 · Cited by 135 · see citing works
Self-citationMotor neurons contain agrin-like molecules.
Magill-Solc, C., & McMahan, U. J. (1988) · The Journal of Cell Biology · doi:10.1083/jcb.107.5.1825 · Cited by 130 · see citing works
Self-citationOn the mechanism of acetylcholine receptor accumulation at newly formed synapses on chick myotubes
Role, L. W., Matossian, V., O’Brien, R., & Fischbach, G. D. (1985) · Journal of Neuroscience · doi:10.1523/jneurosci.05-08-02197.1985 · Cited by 109 · see citing works
Fallon, J. R., & Gelfman, C. E. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.4.1527 · Cited by 104 · see citing works
Miles, K., Anthony, D. T., Rubin, L. L., Greengard, P., & Huganir, R. L. (1987) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.84.18.6591 · Cited by 93 · see citing works
McMahan, U. J., & Wallace, B. G. (1989) · Developmental Neuroscience · doi:10.1159/000111903 · Cited by 83 · see citing works
Self-citationSynthesis and Transport of Agrin-Like Molecules in Motor Neurons
Magill-Solc, C., & McMahan, U. J. (1990) · Journal of Experimental Biology · doi:10.1242/jeb.153.1.1 · Cited by 72 · see citing works
Self-citationde la Porte, S., Vallette, F. M., Grassi, J. J., Vigny, M., & Koenig, J. (1986) · Developmental Biology · doi:10.1016/0012-1606(86)90044-8 · Cited by 30 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
DEVELOPMENT OF THE VERTEBRATE NEUROMUSCULAR JUNCTION
Sanes, J. R., & Lichtman, J. W. (1999) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.22.1.389 · Cited by 1,532 · see citing works
Cellular signaling by neural cell adhesion molecules of the immunoglobulin superfamily
Crossin, K. L., & Krushel, L. A. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200006)218:2 · Cited by 283 · see citing works
Defective Neuromuscular Synaptogenesis in Agrin-Deficient Mutant Mice
Gautam, M., Noakes, P. G., Moscoso, L. M., Rupp, F., Scheller, R. H., Merlie, J. P., & Sanes, J. R. (1996) · Cell · doi:10.1016/s0092-8674(00)81253-2 · Cited by 933 · see citing works
The Receptor Tyrosine Kinase MuSK Is Required for Neuromuscular Junction Formation In Vivo
DeChiara, T. M., Bowen, D. C., Valenzuela, D. M., Simmons, M. V., Poueymirou, W. T., Thomas, S., Kinetz, E., Compton, D. L., Rojas, E., Park, J. S., et al. (1996) · Cell · doi:10.1016/s0092-8674(00)81251-9 · Cited by 912 · see citing works
Synaptic structure and development: The neuromuscular junction
Hall, Z. W., & Sanes, J. R. (1993) · Cell · doi:10.1016/s0092-8674(05)80031-5 · Cited by 834 · see citing works
Menorca, R. M. G., Fussell, T. S., & Elfar, J. C. (2013) · Hand Clinics · doi:10.1016/j.hcl.2013.04.002 · Cited by 729 · see citing works
Agrin Acts via a MuSK Receptor Complex
Glass, D. J., Bowen, D. C., Stitt, T. N., Radziejewski, C. H., Bruno, J., RYAN, T. E., Gies, D. R., Shah, S., Mattsson, K., Burden, S. J., et al. (1996) · Cell · doi:10.1016/s0092-8674(00)81252-0 · Cited by 662 · see citing works
LRP4 serves as a coreceptor of Agrin
Zhang, B., Luo, S., Wang, Q., Suzuki, T., Xiong, W. C., & Mei, L. (2008) · Neuron · doi:10.1016/j.neuron.2008.10.006 · Cited by 525 · see citing works
To build a synapse: signaling pathways in neuromuscular junction assembly
Wu, H., Xiong, W., & Mei, L. (2010) · Development · doi:10.1242/dev.038711 · Cited by 519 · see citing works
Dystroglycan-α, a dystrophin-associated glycoprotein, is a functional agrin receptor
Gee, S., Montanaro, F., Lindenbaum, M., & Carbonetto, S. (1994) · Cell · doi:10.1016/0092-8674(94)90052-3 · Cited by 512 · see citing works
Ion Channels in Excitable Membranes
Ruppersberg, J. P. (1996) · Springer eBooks · doi:10.1007/978-3-642-60946-6_13 · Cited by 450 · see citing works
Synaptic transmission: A bidirectional and self-modifiable form of cell-cell communication
Jessell, T. M., & Kandel, E. R. (1993) · Cell · doi:10.1016/s0092-8674(05)80025-x · Cited by 370 · see citing works
A role for dystrophin-associated glycoproteins and utrophin in agrin-induced AChR clustering
Campanelll, J. T., Roberds, S. L., Campbell, K. P., & Scheller, R. H. (1994) · Cell · doi:10.1016/0092-8674(94)90051-5 · Cited by 369 · see citing works
The neurogenetics of alternative splicing
Vuong, C. K., Black, D. L., & Zheng, S. (2016) · Nature Reviews Neuroscience · doi:10.1038/nrn.2016.27 · Cited by 340 · see citing works
Bowe, M. A., Deyst, K. A., Leszyk, J., & Fallon, J. R. (1994) · Neuron · doi:10.1016/0896-6273(94)90324-7 · Cited by 307 · see citing works
Ferns, M., Campanelli, J. T., Hoch, W., Scheller, R. H., & Hall, Z. W. (1993) · Neuron · doi:10.1016/0896-6273(93)90153-i · Cited by 306 · see citing works
Neuronal differentiation factors/cytokines and synaptic plasticity
Patterson, P. H., & Nawa, H. (1993) · Cell · doi:10.1016/s0092-8674(05)80032-7 · Cited by 288 · see citing works
Dystroglycan binds nerve and muscle agrin
Sugiyama, J. E., Bowen, D. C., & Hall, Z. W. (1994) · Neuron · doi:10.1016/0896-6273(94)90462-6 · Cited by 274 · see citing works
The agrin gene codes for a family of basal lamina proteins that differ in function and distribution
Rüegg, M. A., Tsim, K. W. K., Horton, S. E., Kröger, S., Escher, G., Gensch, E. M., & McMahan, U. J. (1992) · Neuron · doi:10.1016/0896-6273(92)90090-z · Cited by 254 · see citing works
Self-citationThe C.elegans ric‐3 gene is required for maturation of nicotinic acetylcholine receptors
Halevi, S., McKay, J., Palfreyman, M. T., Yassin, L., Eshel, M., Jørgensen, E. M., & Treinin, M. (2002) · The EMBO Journal · doi:10.1093/emboj/21.5.1012 · Cited by 251 · see citing works
Littleton, J. T., Bellen, H. J., & Perin, M. S. (1993) · Development · doi:10.1242/dev.118.4.1077 · Cited by 250 · see citing works
Craig, A. M., Blackstone, C. D., Huganir, R. L., & Banker, G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.26.12373 · Cited by 237 · see citing works
Acetylcholine receptor-aggregating activity of agrin isoforms and mapping of the active site.
Gesemann, M., Denzer, A. J., & Ruegg, M. A. (1995) · The Journal of cell biology · doi:10.1083/jcb.128.4.625 · Cited by 236 · see citing works
Gesemann, M., Cavalli, V., Denzer, A. J., Brancaccio, A., Schumacher, B., & Rüegg, M. A. (1996) · Neuron · doi:10.1016/s0896-6273(00)80096-3 · Cited by 227 · see citing works
Agrin promotes synaptic differentiation by counteracting an inhibitory effect of neurotransmitter
Misgeld, T., Kummer, T. T., Lichtman, J. W., & Sanes, J. R. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0504806102 · Cited by 218 · see citing works
Agrin orchestrates synaptic differentiation at the vertebrate neuromuscular junction
Rüegg, M. A., & Bixby, J. L. (1998) · Trends in Neurosciences · doi:10.1016/s0166-2236(97)01154-5 · Cited by 189 · see citing works
The formation of neuromuscular synapsesPreprint
Burden, S. J. (1998) · Genes & Development · doi:10.1101/gad.12.2.133 · Cited by 188 · see citing works
Developmental regulation of highly active alternatively spliced forms of agrin
Hoch, W., Ferns, M., Campanelli, J. T., Hall, Z. W., & Scheller, R. H. (1993) · Neuron · doi:10.1016/0896-6273(93)90152-h · Cited by 187 · see citing works
Regulation of Ion Channel Distribution at Synapses
Froehner, S. C. (1993) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.16.030193.002023 · Cited by 178 · see citing works
Jennings, C. G. B., Dyer, S. M., & Burden, S. J. (1993) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.90.7.2895 · Cited by 168 · see citing works
Wagner, K. R., Cohen, J. B., & Huganir, R. L. (1993) · Neuron · doi:10.1016/0896-6273(93)90338-r · Cited by 159 · see citing works
Myotoxic phospholipases A2 and the regeneration of skeletal muscles
Harris, J. B. (2003) · Toxicon · doi:10.1016/j.toxicon.2003.11.011 · Cited by 150 · see citing works
Agrin isoforms and their role in synaptogenesis
McMahan, U. J., Horton, S. E., Werle, M. J., Honig, L. S., Kröger, S., Rüegg, M. A., & Escher, G. (1992) · Current Opinion in Cell Biology · doi:10.1016/0955-0674(92)90113-q · Cited by 147 · see citing works
Self-citationBerthier, C., & Blaineau, S. (1997) · Biology of the Cell · doi:10.1016/s0248-4900(97)89313-6 · Cited by 131 · see citing works
Agrin-Induced Postsynaptic-like Apparatus in Skeletal Muscle Fibersin Vivo
Cohen, I., Rimer, M., Lømo, T., & McMahan, U. J. (1997) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1997.0623 · Cited by 130 · see citing works
Self-citationDenzer, A. J., Gesemann, M., Schumacher, B., & Rüegg, M. A. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.6.1547 · Cited by 129 · see citing works
α3Na+/K+-ATPase Is a Neuronal Receptor for Agrin
Hilgenberg, L. G. W., Su, H., Gu, H., O’Dowd, D. K., & Smith, M. A. (2006) · Cell · doi:10.1016/j.cell.2006.01.052 · Cited by 126 · see citing works
Innervation directs receptor synthesis and localization in Drosophila embryo synaptogenesis
Broadie, K. S., & Bate, M. (1993) · Nature · doi:10.1038/361350a0 · Cited by 125 · see citing works
Functions of agrin and agrin-related proteins
Patthy, L., & Nikolics, K. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90021-d · Cited by 118 · see citing works
Integrins mediate adhesion to agrin and modulate agrin signaling
Martin, P. T., & Sanes, J. R. (1997) · Development · doi:10.1242/dev.124.19.3909 · Cited by 117 · see citing works
Baghy, K. (2015) · World Journal of Gastroenterology · doi:10.3748/wjg.v22.i1.379 · Cited by 113 · see citing works
Sakuma, M., Górski, G. K., Sheu, S., Lee, S. J., Barrett, L. B., Singh, B., Omura, T., Latrémolière, A., & Woolf, C. J. (2015) · European Journal of Neuroscience · doi:10.1111/ejn.13059 · Cited by 114 · see citing works
Association of muscle‐specific kinase MuSK with the acetylcholine receptor in mammalian muscle
Fuhrer, C., Sugiyama, J. E., Taylor, R. G., & Hall, Z. W. (1997) · The EMBO Journal · doi:10.1093/emboj/16.16.4951 · Cited by 109 · see citing works
Structural domains of agrin required for clustering of nicotinic acetylcholine receptors.
Hoch, W., Campanelli, J. T., Harrison, S. D., & Scheller, R. H. (1994) · The EMBO Journal · doi:10.1002/j.1460-2075.1994.tb06575.x · Cited by 109 · see citing works
Activation of Matrix Metalloproteinase-3 and Agrin Cleavage in Cerebral Ischemia/Reperfusion
Solé, S., Petegnief, V., Gorina, R., Chamorro, Á., & Planas, A. M. (2004) · Journal of Neuropathology & Experimental Neurology · doi:10.1093/jnen/63.4.338 · Cited by 107 · see citing works
Thoby‐Brisson, M., & Simmers, J. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-06-02212.1998 · Cited by 105 · see citing works
DiMario, J. X., & Stockdale, F. E. (1997) · Developmental Biology · doi:10.1006/dbio.1997.8619 · Cited by 102 · see citing works
Building synapses: agrin and dystroglycan stick together
Fallon, J. R., & Hall, Z. W. (1994) · Trends in Neurosciences · doi:10.1016/0166-2236(94)90135-x · Cited by 100 · see citing works
Staurosporine inhibits agrin-induced acetylcholine receptor phosphorylation and aggregation.
Wallace, B. G. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.3.661 · Cited by 100 · see citing works
Activity-dependent current distributions in model neurons
Siegel, M., Marder, E., & Abbott, L. F. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.24.11308 · Cited by 91 · see citing works
Formation of the neuromuscular junction
Hoch, W. (1999) · European Journal of Biochemistry · doi:10.1046/j.1432-1327.1999.00765.x · Cited by 98 · see citing works
Wallace, B. G. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.128.6.1121 · Cited by 98 · see citing works
Roles of Rapsyn and Agrin in Interaction of Postsynaptic Proteins with Acetylcholine Receptors
Fuhrer, C., Gautam, M., Sugiyama, J. E., & Hall, Z. W. (1999) · Journal of Neuroscience · doi:10.1523/jneurosci.19-15-06405.1999 · Cited by 96 · see citing works
Localization and Regulation of MuSK at the Neuromuscular Junction
Bowen, D. C., Park, J. S., Bodine, S. C., Stark, J. L., Valenzuela, D. M., Stitt, T. N., Yancopoulos, G. D., Lindsay, R. M., Glass, D. J., & DiStefano, P. S. (1998) · Developmental Biology · doi:10.1006/dbio.1998.8936 · Cited by 95 · see citing works
Agrin Controls Synaptic Differentiation in Hippocampal Neurons
Böse, C., Qiu, D., Bergamaschi, A., Gravante, B., Bossi, M., Villa, A., Rupp, F., & Malgaroli, A. (2000) · Journal of Neuroscience · doi:10.1523/jneurosci.20-24-09086.2000 · Cited by 93 · see citing works
Functional Interaction of Src Family Kinases with the Acetylcholine Receptor in C2 Myotubes
Fuhrer, C., & Hall, Z. W. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.50.32474 · Cited by 92 · see citing works
Matrix metalloproteinases MMP‐2 and MMP‐9 in denervated muscle and injured nerve
Kherif, Dehaupas, Lafuma, Fardeau, M., & Alameddine (1998) · Neuropathology and Applied Neurobiology · doi:10.1046/j.1365-2990.1998.00118.x · Cited by 90 · see citing works
Stone, D., & Nikolics, K. (1995) · Journal of Neuroscience · doi:10.1523/jneurosci.15-10-06767.1995 · Cited by 90 · see citing works
The role of peripheral nerve ECM components in the tissue engineering nerve construction
Gao, X., Wang, Y., Chen, J., & Peng, J. C. (2013) · Reviews in the Neurosciences · doi:10.1515/revneuro-2013-0022 · Cited by 89 · see citing works
Reduced expression of nicotinic AChRs in myotubes from spinal muscular atrophy I patients
Arnold, A., Gueye, M., Guettier‐Sigrist, S., Courdier-Fruh, I., Coupin, G., Poindron, P., & Gies, J. (2004) · Laboratory Investigation · doi:10.1038/labinvest.3700163 · Cited by 88 · see citing works
Neumann, F. R., Bittcher, G., Annies, M., Schumacher, B., Kröger, S., & Rüegg, M. A. (2001) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.2000.0932 · Cited by 87 · see citing works
How many agrins does it take to make a synapse?
Ferns, M., & Hall, Z. W. (1992) · Cell · doi:10.1016/0092-8674(92)90525-h · Cited by 87 · see citing works
ARIA is concentrated in the synaptic basal lamina of the developing chick neuromuscular junction.
Goodearl, A. D. J., Yee, A., Sandrock, A. W., Corfas, G., & Fischbach, G. D. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.6.1423 · Cited by 86 · see citing works
Deafferentation Causes Apoptosis in Cortical Sensory Neurons in the Adult Rat
Capurso, S. A., Calhoun, M. E., Sukhov, R. R., Mouton, P. R., Price, D. L., & Koliatsos, V. E. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-19-07372.1997 · Cited by 83 · see citing works
Mittaud, P., Marangi, P. A., Erb‐Vögtli, S., & Fuhrer, C. (2001) · Journal of Biological Chemistry · doi:10.1074/jbc.m007024200 · Cited by 83 · see citing works
Das, S., Browne, K. D., Laimo, F. A., Maggiore, J. C., Hilman, M. C., Kaisaier, H., Aguilar, C. A., Ali, Z. S., Mourkioti, F., & Cullen, D. K. (2020) · Communications Biology · doi:10.1038/s42003-020-1056-4 · Cited by 81 · see citing works
Agrin Binding to α-Dystroglycan
Hopf, C., & Hoch, W. (1996) · Journal of Biological Chemistry · doi:10.1074/jbc.271.9.5231 · Cited by 81 · see citing works
Role for a synapse-specific carbohydrate in agrin-induced clustering of acetylcholine receptors
Martin, P. T., & Sanes, J. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90218-x · Cited by 79 · see citing works
O'Toole, J. J., Deyst, K. A., Bowe, M. A., Nastuk, M. A., McKechnie, B. A., & Fallon, J. R. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.14.7369 · Cited by 78 · see citing works
Molecular and spatial landmarks of early mouse skin development
Jacob, T., Annusver, K., Czarnewski, P., Dalessandri, T., Kalk, C., Levron, C. L., Sanz, N. C., Kastriti, M. E., Mikkola, M. L., Rendl, M., et al. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.07.015 · Cited by 75 · see citing works
Liyanage, Y. S. H., Hoch, W., Beeson, D., & Vincent, A. C. (2001) · Muscle & Nerve · doi:10.1002/mus.1218 · Cited by 77 · see citing works
Neuromuscular Junctions as Key Contributors and Therapeutic Targets in Spinal Muscular Atrophy
Boido, M., & Vercelli, A. (2016) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2016.00006 · Cited by 76 · see citing works
Cohen, M. W., Jacobson, C., Yurchenco, P. D., Morris, G. E., & Carbonetto, S. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.5.1047 · Cited by 75 · see citing works
Expression of agrin in the developing and adult rat brain
Cohen, N. A., Kaufmann, W. E., Worley, P. F., & Rupp, F. (1997) · Neuroscience · doi:10.1016/s0306-4522(96)00345-4 · Cited by 74 · see citing works
Campanelli, J. T., Gayer, G. G., & Scheller, R. H. (1996) · Development · doi:10.1242/dev.122.5.1663 · Cited by 74 · see citing works
The Yin–Yang of Dendrite Morphology: Unity of Actin and Microtubules
Georges, P. C., Hadzimichalis, N. M., Sweet, E. S., & Firestein, B. L. (2008) · Molecular Neurobiology · doi:10.1007/s12035-008-8046-8 · Cited by 73 · see citing works
Basal lamina and the organization of neuromuscular synapses
Patton, B. L. (2003) · Journal of Neurocytology · doi:10.1023/b:neur.0000020630.74955.19 · Cited by 73 · see citing works
Barik, A., Zhang, B., Sohal, G. S., Xiong, W., & Mei, L. (2014) · Developmental Neurobiology · doi:10.1002/dneu.22190 · Cited by 70 · see citing works
Agrin and the molecular choreography of synapse formation
Nastuk, M. A., & Fallon, J. R. (1993) · Trends in Neurosciences · doi:10.1016/0166-2236(93)90020-m · Cited by 70 · see citing works
β1 Integrins in Muscle, But Not in Motor Neurons, Are Required for Skeletal Muscle Innervation
Schwander, M., Shirasaki, R., Pfaff, S. L., & Müller, U. (2004) · Journal of Neuroscience · doi:10.1523/jneurosci.1345-04.2004 · Cited by 68 · see citing works
Structural alterations at the neuromuscular junctions of matrix metalloproteinase 3 null mutant mice
VanSaun, M. N., Herrera, A. A., & Werle, M. J. (2003) · Journal of Neurocytology · doi:10.1023/b:neur.0000021907.68461.9c · Cited by 66 · see citing works
Self-citationThe role of the dystrophin glycoprotein complex on the neuromuscular system
Belhasan, D. C., & Akaaboune, M. (2020) · Neuroscience Letters · doi:10.1016/j.neulet.2020.134833 · Cited by 67 · see citing works
Rimer, M., Cohen, I., Lømo, T., Burden, S. J., & McMahan, U. J. (1998) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1998.0695 · Cited by 67 · see citing works
Self-citationDistribution of alpha-dystroglycan during embryonic nerve-muscle synaptogenesis.
Cohen, M. W., Jacobson, C., Godfrey, E. W., Campbell, K. P., & Carbonetto, S. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.129.4.1093 · Cited by 67 · see citing works
Meier, T., Perez, G. M., & Wallace, B. G. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.131.2.441 · Cited by 66 · see citing works
Ji, R., Böse, C., Lesuisse, C., Qiu, D., Huang, J. C., Zhang, Q., & Rupp, F. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-23-09695.1998 · Cited by 64 · see citing works
Distribution of agrin mRNAs in the chick embryo nervous system
Ma, E., Morgan, R. G., & Godfrey, E. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-05-02943.1994 · Cited by 64 · see citing works
Mechanism of agrin‐induced acetylcholine receptor aggregation
Wallace, B. G. (1992) · Journal of Neurobiology · doi:10.1002/neu.480230512 · Cited by 61 · see citing works
Qu, Z., & Huganir, R. L. (1994) · Journal of Neuroscience · doi:10.1523/jneurosci.14-11-06834.1994 · Cited by 60 · see citing works
Dystrophin-associated proteins and synapse formation: Is α-dystroglycan the agrin receptor?
Sealock, R. W., & Froehner, S. C. (1994) · Cell · doi:10.1016/0092-8674(94)90045-0 · Cited by 59 · see citing works
γ-AChR/ϵ-AChR Switch at Agrin-Induced Postsynaptic-like Apparatus in Skeletal Muscle
Rimer, M., Mathiesen, I., Lømo, T., & McMahan, U. J. (1997) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1997.0622 · Cited by 57 · see citing works
Self-citationFunte, L. R., & Haydon, P. G. (1993) · Neuron · doi:10.1016/0896-6273(93)90055-v · Cited by 56 · see citing works
Portiér, G. L., Benders, A. A. G. M., Oosterhof, A., Veerkamp, J. H., & Kuppevelt, T. H. V. (1999) · In Vitro Cellular & Developmental Biology - Animal · doi:10.1007/s11626-999-0030-8 · Cited by 54 · see citing works
Muscle agrin: neural regulation and localization at nerve-induced acetylcholine receptor clusters
Lieth, E., & Fallon, J. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-06-02509.1993 · Cited by 53 · see citing works
Sun, Z., & Schacher, S. (1996) · Journal of Neurobiology · doi:10.1002/(sici)1097-4695(199602)29:2 · Cited by 8 · see citing works
Membrane traffic in polarized neurons
Bradke, F., & Dotti, C. G. (1998) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/s0167-4889(98)00060-3 · Cited by 53 · see citing works
Effects of Purified Recombinant Neural and Muscle Agrin on Skeletal Muscle Fibers in Vivo
Bezáková, G., Helm, P. J., Francolini, M., & Lømo, T. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.153.7.1441 · Cited by 52 · see citing works
Liou, J., & Fu, W. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-07-02459.1997 · Cited by 52 · see citing works
Soendenbroe, C., Bechshøft, C. J. L., Heisterberg, M. F., Jensen, S. M., Bomme, E., Schjerling, P., Karlsen, A., Kjær, M., Andersen, J. L., & Mackey, A. L. (2020) · Cells · doi:10.3390/cells9040893 · Cited by 51 · see citing works
Retrograde interactions during formation and elimination of neuromuscular synapses
Dan, Y., & Poo, M. (1994) · Current Opinion in Neurobiology · doi:10.1016/0959-4388(94)90037-x · Cited by 51 · see citing works
- Authors
- Reist, N. E., Werle, M. J., & McMahan, U. J.
- Affiliations
- Stanford Medicine (US)
- ORCID
- Reist, Noreen E.
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 1992-05
- Volume
- 8
- Issue
- 5
- Pages
- 865-868
- ISSN
- 0896-6273 (ISSN-L)
- OpenAlex
- W2068836997
- Cited by
- 237
- References
- 21
- Citations by year
- 2026: 3 · 2025: 5 · 2024: 3 · 2023: 2 · 2022: 6 · 2020: 7 · 2019: 5 · 2018: 2 · 2017: 2 · 2016: 5 · 2015: 4 · 2014: 3 · 2013: 7 · 2012: 5
- FWCI
- 8.60
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- Neuron (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nicotinic Acetylcholine Receptors Study
- Health Sciences › Medicine › Neurology › Myasthenia Gravis and Thymoma
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Keywords
- agrin, acetylcholine receptor aggregation, neuromuscular junction, motor neurons, polyclonal antibodies, skeletal muscle
- MeSH terms
- Animals, Antibodies, Cells, Cultured, Chickens, Motor Neurons, Nerve Tissue Proteins, Neuromuscular Junction, Receptors, Cholinergic, Agrin, Macromolecular Substances, Rats
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