Cited by 1,532Nerve injury and regenerationNeuroscience and Neuropharmacology ResearchAxon Guidance and Neuronal Signaling

The DOI matches its Crossref record; 401 of the 403 references it cites were found in a registry or an index.

DEVELOPMENT OF THE VERTEBRATE NEUROMUSCULAR JUNCTION

Sanes, Joshua R., Lichtman, Jeff W.·1999·Annual Review of Neuroscience

DOI 10.1146/annurev.neuro.22.1.389

Open this paper in CoChat — free account

Abstract

▪ Abstract We describe the formation, maturation, elimination, maintenance, and regeneration of vertebrate neuromuscular junctions (NMJs), the best studied of all synapses. The NMJ forms in a series of steps that involve the exchange of signals among its three cellular components—nerve terminal, muscle fiber, and Schwann cell. Although essentially any motor axon can form NMJs with any muscle fiber, an additional set of cues biases synapse formation in favor of appropriate partners. The NMJ is functional at birth but undergoes numerous alterations postnatally. One step in maturation is the elimination of excess inputs, a competitive process in which the muscle is an intermediary. Once elimination is complete, the NMJ is maintained stably in a dynamic equilibrium that can be perturbed to initiate remodeling. NMJs regenerate following damage to nerve or muscle, but this process differs in fundamental ways from embryonic synaptogenesis. Finally, we consider the extent to which the NMJ is a suitable model for development of neuron-neuron synapses.

Integrity signals

Registry

Crossref · 10.1146/annurev.neuro.22.1.389

Cites

401 of 401 references verified0 citation errors · 0 not checkable

Statistics

Recomputing p-values needs the paper’s full text.

Claims the paper makes

This paper’s full text isn’t openly available, so its claims and self-check weren’t run. The registry and citation checks still apply.

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?

1 retracted

Depolarization-transcription signals in skeletal muscle use calcium flux through L channels, but bypass the sarcoplasmic reticulum
Huang, C., Flucher, B. E., Schmidt, M. M., Stroud, S. K., & Schmidt, J. (1994) · Neuron · doi:10.1016/0896-6273(94)90467-7 · Cited by 43
Retracted
The Molecular Biology of Axon Guidance
Tessier‐Lavigne, M., & Goodman, C. S. (1996) · Science · doi:10.1126/science.274.5290.1123 · Cited by 3,311
The synaptic vesicle cycle: a cascade of protein–protein interactions
Südhof, T. C. (1995) · Nature · doi:10.1038/375645a0 · Cited by 1,991
Molecular diversity of myofibrillar proteins: gene regulation and functional significance
Schiaffino, S., & Reggiani, C. (1996) · Physiological Reviews · doi:10.1152/physrev.1996.76.2.371 · Cited by 1,545
Nerve, Muscle and Synapse
Katz, B. (1966) · Medical Entomology and Zoology · Cited by 1,410
Multiple essential functions of neuregulin in development
Meyer, D., & Birchmeier, C. (1995) · Nature · doi:10.1038/378386a0 · Cited by 1,273
Molecular and cellular biology of cholinesterases
Massoulié, J., Pezzementi, L., Bon, S., Krejci, E., & Vallette, F.-M. (1993) · Progress in Neurobiology · doi:10.1016/0301-0082(93)90040-y · Cited by 1,214
THE EPHRINS AND EPH RECEPTORS IN NEURAL DEVELOPMENT
Flanagan, J. G., & Vanderhaeghen, P. (1998) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.21.1.309 · Cited by 1,091
Molecular distinction between fetal and adult forms of muscle acetylcholine receptor
Mishina, M., Takai, T., Imoto, K., Noda, M., Takahashi, T., Numa, S., Methfessel, C., & Sakmann, B. J. (1986) · Nature · doi:10.1038/321406a0 · Cited by 1,000
Defective neuromuscular synaptogenesis in agrin-deficient mutant mice.
Gautam, M., Noakes, P., Moscoso, L. M., Rupp, F., Scheller, R., Merlie, J., & Sanes, J. (1996) · Cell · doi:10.1016/s0092-8674(00)81253-2 · Cited by 941
Self-citation
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 920
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
Self-citation
Elimination of synapses in the developing nervous system
Purves, D., & Lichtman, J. W. (1980) · Science · doi:10.1126/science.7414326 · Cited by 808
Self-citation
Synaptic Efficacy Enhanced by Glial Cells in Vitro
Pfrieger, F. W., & Barres, B. A. (1997) · Science · doi:10.1126/science.277.5332.1684 · Cited by 793
Polyneuronal innervation of skeletal muscle in new‐born rats and its elimination during maturation.
Brown, M. C., Jansen, J., & van Essen, D. V. (1976) · Journal of Physiology · doi:10.1113/jphysiol.1976.sp011565 · Cited by 789
Control of acetylcholine receptors in skeletal muscle
Fambrough, D. M. (1979) · Physiological Reviews · doi:10.1152/physrev.1979.59.1.165 · Cited by 775
Severe neuropathies in mice with targeted mutations in the ErbB3 receptor
Riethmacher, D., Sonnenberg-Riethmacher, E., Brinkmann, V., Yamaai, T., Lewin, G. R., & Birchmeier, C. (1997) · Nature · doi:10.1038/39593 · Cited by 729
Diversity and Pattern in the Developing Spinal Cord
Tanabe, Y., & Jessell, T. M. (1996) · Science · doi:10.1126/science.274.5290.1115 · Cited by 718
Neuromuscular transmission in new‐born rats
Redfern, P. (1970) · The Journal of Physiology · doi:10.1113/jphysiol.1970.sp009187 · Cited by 711
Agrin acts via a MuSK receptor complex.
Glass, D., Bowen, D., Stitt, T., Radziejewski, C., Bruno, J., Ryan, T. E., Gies, D., Shah, S., Mattsson, K., Burden, S., et al. (1996) · Cell · doi:10.1016/s0092-8674(00)81252-0 · Cited by 673
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
Skeletal and Cardiac Myopathies in Mice Lacking Utrophin and Dystrophin: A Model for Duchenne Muscular Dystrophy
Grady, R. M., Teng, H., Nichol, M. C., Cunningham, J. M., Wilkinson, R. S., & Sanes, J. R. (1997) · Cell · doi:10.1016/s0092-8674(00)80533-4 · Cited by 639
Self-citation
Mammalian Skeletal Muscle Fiber Type Transitions
Pette, D., & Staron, R. S. (1997) · International review of cytology · doi:10.1016/s0074-7696(08)61622-8 · Cited by 633
ARIA, a protein that stimulates acetylcholine receptor synthesis, is a member of the neu ligand family
Falls, D. L. (1993) · Cell · doi:10.1016/0092-8674(93)90407-h · Cited by 602
Peripheral nerve regeneration
Idé, C. (1996) · Neuroscience Research · doi:10.1016/0168-0102(96)01042-5 · Cited by 599
Reinnervation of muscle fiber basal lamina after removal of myofibers. Differentiation of regenerating axons at original synaptic sites.
Sanes, J. R., Marshall, L. M., & McMahan, U. J. (1978) · The Journal of Cell Biology · doi:10.1083/jcb.78.1.176 · Cited by 578
Self-citation
A laminin-like adhesive protein concentrated in the synaptic cleft of the neuromuscular junction
Hunter, D. D., Shah, V., Merlie, J., & Sanes, J. (1989) · Nature · doi:10.1038/338229a0 · Cited by 559
Self-citation
Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice
Gautam, M., Noakes, P. G., Mudd, J. L., Nichol, M. C., Chu, G. C., Sanes, J. R., & Merlie, J. P. (1995) · Nature · doi:10.1038/377232a0 · Cited by 545
Self-citation
Expression of nerve growth factor receptors by Schwann cells of axotomized peripheral nerves: ultrastructural location, suppression by axonal contact, and binding properties
Taniuchi, M., Clark, H., Schweitzer, J. B., & Johnson, E. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-02-00664.1988 · Cited by 542
Motor Nerve Sprouting
Brown, M. C., Holland, R. L., & Hopkins, W. G. (1981) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.04.030181.000313 · Cited by 528
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
Release of acetylcholine at voluntary motor nerve endings
Dale, H. H., Feldberg, W. S., & Vogt, M. (1936) · The Journal of Physiology · doi:10.1113/jphysiol.1936.sp003371 · Cited by 492
Aberrant differentiation of neuromuscular junctions in mice lacking s-laminin/laminin β2
Noakes, P., Gautam, M., Mudd, J., Sanes, J., & Merlie, J. (1995) · Nature · doi:10.1038/374258a0 · Cited by 474
Self-citation
Identification 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
Calcitonin gene-related peptide regulates muscle acetylcholine receptor synthesis
New, H. V., & Mudge, A. W. (1986) · Nature · doi:10.1038/323809a0 · Cited by 465
Nerve‐induced and spontaneous redistribution of acetylcholine receptors on cultured muscle cells.
Anderson, M. J., & Cohen, M. W. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp011880 · Cited by 460
Distribution and Function of Laminins in the Neuromuscular System of Developing, Adult, and Mutant Mice
Patton, B., Miner, J., Chiu, A. Y., & Sanes, J. (1997) · Journal of Cell Biology · doi:10.1083/jcb.139.6.1507 · Cited by 452
Self-citation
The MyoD family of transcription factors and skeletal myogenesis
Rudnicki, M. A., & Jaenisch, R. (1995) · BioEssays · doi:10.1002/bies.950170306 · Cited by 450
Neu differentiation factor is a neuron-glia signal and regulates survival, proliferation, and maturation of rat schwann cell precursors
Dong, Z., Brennan, A., Liu, N., Yarden, Y., Lefkowitz, G. K., Mirsky, R., & Jessen, K. R. (1995) · Neuron · doi:10.1016/0896-6273(95)90147-7 · Cited by 445
Schwann cell processes guide regeneration of peripheral axons
Son, Y., & Thompson, W. J. (1995) · Neuron · doi:10.1016/0896-6273(95)90246-5 · Cited by 444
Functional colocalization of calcium and calcium-gated potassium channels in control of transmitter release
Robitaille, R., García, M. L., Kaczorowski, G. J., & Chariton, M. P. (1993) · Neuron · doi:10.1016/0896-6273(93)90076-4 · Cited by 443
Spontaneous release of transmitter from growth cones of embryonic neurones
Young, S. H., & Poo, M. (1983) · Nature · doi:10.1038/305634a0 · Cited by 440
Review: Fine structure of synaptogenesis in the vertebrate central nervous system
Vaughn, J. E. (1989) · Synapse · doi:10.1002/syn.890030312 · Cited by 434
Receptor tyrosine kinase specific for the skeletal muscle lineage: Expression in embryonic muscle, at the neuromuscular junction, and after injury
Valenzuela, D. M., Stitt, T. N., DiStefano, P. S., Rojas, E., Mattsson, K., Compton, D. L., Nuñez, L., Park, J. S., Stark, J. L., Gies, D. R., et al. (1995) · Neuron · doi:10.1016/0896-6273(95)90146-9 · Cited by 418
Collagen IV alpha 3, alpha 4, and alpha 5 chains in rodent basal laminae: sequence, distribution, association with laminins, and developmental switches.
Miner, J. H., & Sanes, J. R. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.127.3.879 · Cited by 411
Self-citation
Heterogeneity in the Molecular Composition of Excitatory Postsynaptic Sites during Development of Hippocampal Neurons in Culture
Rao, A., Kim, E., Sheng, M., & Craig, A. M. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01217.1998 · Cited by 399
Myogenic cell lineages
Stockdale, F. E. (1992) · Developmental Biology · doi:10.1016/0012-1606(92)90068-r · Cited by 388
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
Developmental Regulation Of Nicotinic Acetylcholine Receptors
Schuetze, S. M., & Role, L. W. (1987) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.10.030187.002155 · Cited by 364
Acetylcholine release from growth cones detected with patches of acetylcholine receptor-rich membranes
Hume, R. I., Role, L. W., & Fischbach, G. D. (1983) · Nature · doi:10.1038/305632a0 · Cited by 356
Acetylcholine receptors in regenerating muscle accumulate at original synaptic sites in the absence of the nerve.
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
Concentration of acetylcholine receptor mRNA in synaptic regions of adult muscle fibres
Merlie, J. P., & Sanes, J. R. (1985) · Nature · doi:10.1038/317066a0 · Cited by 350
Self-citation
Synaptic vesicle biogenesis, docking, and fusion: a molecular description
Calakos, N., & Scheller, R. H. (1996) · Physiological Reviews · doi:10.1152/physrev.1996.76.1.1 · Cited by 348
Early events in neuromuscular junction formation in vitro: induction of acetylcholine receptor clusters in the postsynaptic membrane and morphology of newly formed synapses.
Frank, E., & Fischbach, G. D. (1979) · The Journal of Cell Biology · doi:10.1083/jcb.83.1.143 · Cited by 347
Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles.
Covault, J., & Sanes, J. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.13.4544 · Cited by 346
Self-citation
The Drosophila Neuromuscular Junction: A Model System for Studying Synaptic Development and Function
Keshishian, H., Broadie, K. S., Chibá, A., & Bate, M. (1996) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.19.030196.002553 · Cited by 339
Expression of several adhesive macromolecules (N-CAM, L1, J1, NILE, uvomorulin, laminin, fibronectin, and a heparan sulfate proteoglycan) in embryonic, adult, and denervated adult skeletal muscle
Sanes, J., Schachner, M., & Covault, J. (1986) · Journal of Cell Biology · doi:10.1083/jcb.102.2.420 · Cited by 328
Self-citation
Myogenin and MyoD join a family of skeletal muscle genes regulated by electrical activity.
Eftimie, R., Brenner, H. R., & Buonanno, A. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.4.1349 · Cited by 323
Axonal Interactions Regulate Schwann Cell Apoptosis in Developing Peripheral Nerve: Neuregulin Receptors and the Role of Neuregulins
Grinspan, J. B., Marchionni, M. A., Reeves, M. F., Coulaloglou, M. J., & Scherer, S. S. (1996) · Journal of Neuroscience · doi:10.1523/jneurosci.16-19-06107.1996 · Cited by 316
Nerve sprouting in muscle is induced and guided by processes extended by schwann cells
Son, Y., & Thompson, W. J. (1995) · Neuron · doi:10.1016/0896-6273(95)90247-3 · Cited by 312
Calcitonin gene-related peptide, a peptide present in spinal cord motoneurons, increases the number of acetylcholine receptors in primary cultures of chick embryo myotubes
Fontaine, B., Klarsfeld, A., Hökfelt, T. G. M., & Changeux, J. (1986) · Neuroscience Letters · doi:10.1016/0304-3940(86)90257-0 · Cited by 310
THE FINE STRUCTURE OF MOTOR ENDPLATE MORPHOGENESIS
Kelly, A. M., & Zacks, S. I. (1969) · The Journal of Cell Biology · doi:10.1083/jcb.42.1.154 · Cited by 309
Identification and purification of an agrin receptor from torpedo postsynaptic membranes: A heteromeric complex related to the dystroglycans
Bowe, M. A., Deyst, K. A., Leszyk, J., & Fallon, J. R. (1994) · Neuron · doi:10.1016/0896-6273(94)90324-7 · Cited by 307
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
Distribution of N-CAM in synaptic and extrasynaptic portions of developing and adult skeletal muscle.
Covault, J., & Sanes, J. R. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.102.3.716 · Cited by 306
Self-citation
The ability of agrin to cluster AChRs depends on alternative splicing and on cell surface proteoglycans
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
In vivo visualization of pre- and postsynaptic changes during synapse elimination in reinnervated mouse muscle
Rich, M., & Lichtman, J. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01781.1989 · Cited by 294
Self-citation
Long-term synapse loss induced by focal blockade of postsynaptlc receptors
Balice‐Gordon, R. J., & Lichtman, J. W. (1994) · Nature · doi:10.1038/372519a0 · Cited by 287
Self-citation
Distribution of Na+ channels and ankyrin in neuromuscular junctions is complementary to that of acetylcholine receptors and the 43 kd protein
Flucher, B. E., & Daniels, M. P. (1989) · Neuron · doi:10.1016/0896-6273(89)90029-9 · Cited by 284
Agrin Is a Heparan Sulfate Proteoglycan
Tsen, G., Halfter, W. M., Kröger, S., & Cole, G. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.7.3392 · Cited by 279
ARIA: A Neuromuscular Junction Neuregulin
Fischbach, G. D., & Rosen, K. M. (1997) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.20.1.429 · Cited by 278
Neuregulins are concentrated at nerve-muscle synapses and activate ACh–receptor gene expression
Jo, S. A., Zhu, X., Marchionni, M. A., & Burden, S. J. (1995) · Nature · doi:10.1038/373158a0 · Cited by 277
In vivo observations of pre- and postsynaptic changes during the transition from multiple to single innervation at developing neuromuscular junctions
Balice‐Gordon, R. J., & Lichtman, J. W. (1993) · Journal of Neuroscience · doi:10.1523/jneurosci.13-02-00834.1993 · Cited by 276
Self-citation
Schwann cell apoptosis at developing neuromuscular junctions is regulated by glial growth factor
Trachtenberg, J. T., & Thompson, W. J. (1996) · Nature · doi:10.1038/379174a0 · Cited by 276
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
Maintenance of Acetylcholine Receptor Number by Neuregulins at the Neuromuscular Junction in Vivo
Sandrock, A. W., Dryer, S. E., Rosen, K. M., Gozani, S. N., Kramer, R., Theill, L. E., & Fischbach, G. D. (1997) · Science · doi:10.1126/science.276.5312.599 · Cited by 274
Neurotrophic Survival Molecules for Motoneurons: An Embarrassment of Riches
Oppenheim, R. W. (1996) · Neuron · doi:10.1016/s0896-6273(00)80151-8 · Cited by 272
The distribution of α‐bungarotoxin binding sites on mammalian skeletal muscle developing in vivo
Bevan, S., & Steinbach, J. H. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp011808 · Cited by 271
Visualization of neuromuscular junctions over periods of several months in living mice
Lichtman, J. W., Magrassi, L., & Purves, D. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-04-01215.1987 · Cited by 268
Self-citation
Lineage, arrangement, and death of clonally related motoneurons in chick spinal cord
Leber, S., Breedlove, S., & Sanes, J. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-07-02451.1990 · Cited by 262
Self-citation
Alterations in Synaptic Strength Preceding Axon Withdrawal
Colman, H., Nabekura, J., & Lichtman, J. W. (1997) · Science · doi:10.1126/science.275.5298.356 · Cited by 261
Self-citation
Hyperinnervation of Neuromuscular Junctions Caused by GDNF Overexpression in Muscle
Nguyen, Q. T., Parsadanian, A. S., Snider, W. D., & Lichtman, J. W. (1998) · Science · doi:10.1126/science.279.5357.1725 · Cited by 258
Self-citation
Neuregulin-β induces expression of an NMDA-receptor subunit
Ozaki, M., Sasner, M., Yano, R., Lu, H. S., & Buonanno, A. (1997) · Nature · doi:10.1038/37795 · Cited by 257
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
Agrin induces phosphorylation of the nicotinic acetylcholine receptor
Wallace, B. G., Zhican, Q., & Richard, H. L. (1991) · Neuron · doi:10.1016/0896-6273(91)90227-q · Cited by 253
Development of the myotomal neuromuscular junction in Xenopus laevis: An electrophysiological and fine-structural study
Kullberg, R. W., Lentz, T. L., & Cohen, M. W. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90113-0 · Cited by 252
Components of Torpedo electric organ and muscle that cause aggregation of acetylcholine receptors on cultured muscle cells.
Godfrey, E. W., Nitkin, R. M., Wallace, B. G., Rubin, L. L., & McMahan, U. J. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.2.615 · Cited by 251
Induction of acetylcholine receptors on cultured skeletal muscle by a factor extracted from brain and spinal cord.
Jessell, T. M., Siegel, R. E., & Fischbach, G. D. (1979) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.76.10.5397 · Cited by 247
Schwann cell development, differentiation and myelination
Mirsky, R., & Jessen, K. R. (1996) · Current Opinion in Neurobiology · doi:10.1016/s0959-4388(96)80013-4 · Cited by 243
Rapsyn Is Required for MuSK Signaling and Recruits Synaptic Components to a MuSK-Containing Scaffold
Apel, E. D., Glass, D. J., Moscoso, L. M., Yancopoulos, G. D., & Sanes, J. R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80303-7 · Cited by 243
Self-citation
Calcitonin gene-related peptide and muscle activity regulate acetylcholine receptor alpha-subunit mRNA levels by distinct intracellular pathways.
Fontaine, B., Klarsfeld, A., & Changeux, J. (1987) · The Journal of Cell Biology · doi:10.1083/jcb.105.3.1337 · Cited by 243
The postsynaptic 43k protein clusters muscle nicotinic acetylcholine receptors in xenopus oocytes
Froehner, S. C., Luetje, C. W., Scotland, P., & Patrick, J. (1990) · Neuron · doi:10.1016/0896-6273(90)90079-u · Cited by 241
Schwann cells induce and guide sprouting and reinnervation of neuromuscular junctions
Son, Y., Trachtenberg, J. T., & Thompson, W. J. (1996) · Trends in Neurosciences · doi:10.1016/s0166-2236(96)10032-1 · Cited by 241
Role of Neurotrophins in Synapse Development and Plasticity
Lu, B., & Figurov, A. (1997) · Reviews in the Neurosciences · doi:10.1515/revneuro.1997.8.1.1 · Cited by 241
Two adjacent MyoD1-binding sites regulate expression of the acetylcholine receptor α-subunit gene
Piette, J., Bessereau, J., Huchet, M., & Changeux, J. P. (1990) · Nature · doi:10.1038/345353a0 · Cited by 240
Agrin released by motor neurons induces the aggregation of acetylcholine receptors at neuromuscular junctions
Reist, N. E., Werle, M. J., & McMahan, U. J. (1992) · Neuron · doi:10.1016/0896-6273(92)90200-w · Cited by 237
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
In vivo visualization of the growth of pre- and postsynaptic elements of neuromuscular junctions in the mouse
Balice‐Gordon, R. J., & Lichtman, J. W. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-03-00894.1990 · Cited by 229
Self-citation
Acetylcholine receptor α-, β-, γ-, and δ-subunit mRNA levels are regulated by muscle activity
Goldman, D. J., Brenner, H. R., & Heinemann, S. F. (1988) · Neuron · doi:10.1016/0896-6273(88)90081-5 · Cited by 229
Pathway selection by embryonic chick motoneurons in an experimentally altered environment
Lance-Jones, C. C., & Landmesser, L. T. (1981) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1981.0080 · Cited by 228
Nicotinic acetylcholine receptors in vertebrate muscle: Properties, distribution and neural control
Salpeter, M. (1985) · Progress in Neurobiology · doi:10.1016/0301-0082(85)90018-8 · Cited by 227
Alternative Splicing of Agrin Alters Its Binding to Heparin, Dystroglycan, and the Putative Agrin Receptor
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
Retrograde Signaling in the Development and Modification of Synapses
Fitzsimonds, R. M., & Poo, M. (1998) · Physiological Reviews · doi:10.1152/physrev.1998.78.1.143 · Cited by 223
Neuregulins in Development
Lemke, G. (1996) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1996.0019 · Cited by 223
Immunological evidence for a change in subunits of the acetylcholine receptor in developing and denervated rat muscle
Gu, Y., & Hall, Z. W. (1988) · Neuron · doi:10.1016/0896-6273(88)90195-x · Cited by 221
Postsynaptic Abnormalities at the Neuromuscular Junctions of Utrophin-deficient Mice
Deconinck, A. E., Potter, A. C., Tinsley, J. M., Wood, S. J., Vater, R., Young, C., Metzinger, L., Vincent, A. C., Slater, C. R., & Davies, K. E. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.4.883 · Cited by 218
Terminal Schwann cells elaborate extensive processes following denervation of the motor endplate
Reynolds, M. L., & Woolf, C. J. (1992) · Journal of Neurocytology · doi:10.1007/bf01206897 · Cited by 216
Subtle Neuromuscular Defects in Utrophin-deficient Mice
Grady, R. M., Merlie, J. P., & Sanes, J. R. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.136.4.871 · Cited by 215
Self-citation
Acetylcholine receptor gene expression at the developing neuromuscular junction.
Duclert, A., & Changeux, J. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.2.339 · Cited by 212
The perinatal reorganization of the innervation of skeletal muscle in mammals
JANSEN, J., & Fladby, T. (1990) · Progress in Neurobiology · doi:10.1016/0301-0082(90)90025-c · Cited by 212
RNA splicing regulates agrin-mediated acetylcholine receptor clustering activity on cultured myotubes
Ferns, M., Hoch, W., Campanelli, J. T., Rupp, F., Hall, Z. W., & Scheller, R. H. (1992) · Neuron · doi:10.1016/0896-6273(92)90129-2 · Cited by 212
Sprouting and degeneration of mammalian motor axons in normal and de-afferentated skeletal muscle
Barker, D. J. P., & Ip, M. C. (1966) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1966.0008 · Cited by 208
Rapsyn may function as a link between the acetylcholine receptor and the agrin-binding dystrophin-associated glycoprotein complex
Apel, E. D., Roberds, S. L., Campbell, K. P., & Merlie, J. P. (1995) · Neuron · doi:10.1016/0896-6273(95)90069-1 · Cited by 206
ACh Receptor-Rich Membrane Domains Organized in Fibroblasts by Recombinant 43-Kilodalton Protein
Phillips, W. D., Kopta, C. I., Blount, P., Gardner, P. D., Steinbach, J. H., & Merlie, J. P. (1991) · Science · doi:10.1126/science.1703661 · Cited by 202
Development of the neuromuscular junction in the chick embryo: The number, distribution, and stability of acetylcholine receptors
Burden, S. J. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90218-4 · Cited by 199
Crosslinking of proteins in acetylcholine receptor-rich membranes: Association between the β-subunit and the 43 kd subsynaptic protein
Burden, S. J., Depalma, R. L., & Gottesman, G. S. (1983) · Cell · doi:10.1016/0092-8674(83)90101-0 · Cited by 199
Maturation of the Acetylcholine Receptor in Skeletal Muscle: Regulation of the AChR γ-to-ϵ Switch
Missias, A. C., Chu, G. C., Klocke, B. J., Sanes, J. R., & Merlie, J. P. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0253 · Cited by 197
Self-citation
Development of the Neuromuscular Junction: Inductive Interactions Between Cells
Dennis, M. J. (1981) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.04.030181.000355 · Cited by 197
Denervation supersensitivity in skeletal muscle: analysis with a cloned cDNA probe.
Merlie, J. P., Isenberg, K. E., Russell, S. D., & Sanes, J. R. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.99.1.332 · Cited by 190
Self-citation
Initial events in the formation of neuromuscular synapse: rapid induction of acetylcholine release from embryonic neuron.
Xie, Z. P., & Poo, M. (1986) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.83.18.7069 · Cited by 188
Selective expression of an acetylcholine receptor–lacZ transgene in synaptic nuclei of adult muscle fibers
Sanes, J. R., Johnson, Y. R., Kotzbauer, P. T., Mudd, J. L., Hanley, T. A., Marttnou, J.-C., & Merlie, J. P. (1991) · Development · doi:10.1242/dev.113.4.1181 · Cited by 187
Self-citation
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
Fibroblasts that proliferate near denervated synaptic sites in skeletal muscle synthesize the adhesive molecules tenascin(J1), N-CAM, fibronectin, and a heparan sulfate proteoglycan.
Gatchalian, C. L., Schachner, M., & Sanes, J. R. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.5.1873 · Cited by 185
Self-citation
Purification and characterization of a polypeptide from chick brain that promotes the accumulation of acetylcholine receptors in chick myotubes.
Usdin, T. B., & Fischbach, G. D. (1986) · The Journal of Cell Biology · doi:10.1083/jcb.103.2.493 · Cited by 185
The Role of Agrin in Synapse Formation
Bowe, M. A., & Fallon, J. R. (1995) · Annual Review of Neuroscience · doi:10.1146/annurev.ne.18.030195.002303 · Cited by 181
Neuregulin receptors, erbB3 and erbB4, are localized at neuromuscular synapses.
Zhu, X., Lai, C., Thomas, S. Μ., & Burden, S. J. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00272.x · Cited by 178
The contribution of postsynaptic folds to the safety factor for neuromuscular transmission in rat fast‐ and slow‐twitch muscles.
Wood, S. J., & Slater, C. R. (1997) · The Journal of Physiology · doi:10.1113/jphysiol.1997.sp022007 · Cited by 175
Agrin Binds to the Nerve–Muscle Basal Lamina via Laminin
Denzer, A. J., Brandenberger, R., Gesemann, M., Chiquet, M., & Rüegg, M. A. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.137.3.671 · Cited by 174
Synapse-Associated Expression of an Acetylcholine Receptor-Inducing Protein, ARIA/Heregulin, and Its Putative Receptors, ErbB2 and ErbB3, in Developing Mammalian Muscle
Moscoso, L. M., Chu, G. C., Gautam, M., Noakes, P. G., Merlie, J. P., & Sanes, J. R. (1995) · Developmental Biology · doi:10.1006/dbio.1995.0012 · Cited by 173
Self-citation
The Mammalian Gene of Acetylcholinesterase-associated Collagen
Krejci, É., Thomine, S., Boschetti, N., Legay, C., Sketelj, J., & Massoulié, J. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.36.22840 · Cited by 173
Synaptic Integrins in Developing, Adult, and Mutant Muscle: Selective Association of α1, α7A, and α7B Integrins with the Neuromuscular Junction
Martin, P. T., Kaufman, S. J., Kramer, R. H., & Sanes, J. R. (1996) · Developmental Biology · doi:10.1006/dbio.1996.0057 · Cited by 171
Self-citation
Muscle-specific trk-related receptor with a kringle domain defines a distinct class of receptor tyrosine kinases.
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
Degeneration and Regeneration of the Nervous System
G., J. G. (1929) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.s1-9.36.378 · Cited by 168
Synapse elimination in neonatal rat muscle is sensitive to pattern of muscle use
Thompson, W. J. (1983) · Nature · doi:10.1038/302614a0 · Cited by 165
Induction of motor neuron sprouting in vivo by ciliary neurotrophic factor and basic fibroblast growth factor
Gurney, M., Yamamoto, H., & Kwon, Y. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-08-03241.1992 · Cited by 164
Agrin-induced specializations contain cytoplasmic, membrane, and extracellular matrix-associated components of the postsynaptic apparatus
Wallace, B. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-04-01294.1989 · Cited by 163
Ultrastructural localization of the Mr 43,000 protein and the acetylcholine receptor in Torpedo postsynaptic membranes using monoclonal antibodies.
Sealock, R. W., Wray, B. E., & Froehner, S. C. (1984) · The Journal of Cell Biology · doi:10.1083/jcb.98.6.2239 · Cited by 163
Studies of nerve-muscle interactions in Xenopus cell culture: analysis of early synaptic currents
Evers, J., Laser, M., Sun, Y., Xie, Z., & Poo, M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01523.1989 · Cited by 161
Mechanism of nicotinic acetylcholine receptor cluster formation by rapsyn
Ramarao, M. K., & Cohen, J. B. (1998) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.95.7.4007 · Cited by 161
Induction by agrin of ectopic and functional postsynaptic-like membrane in innervated muscle
Jones, G., Meier, T., Lichtsteiner, M., Witzemann, V., Sakmann, B. J., & Brenner, H. R. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.6.2654 · Cited by 157
Acetylcholine receptor-inducing activity stimulates expression of the epsilon-subunit gene of the muscle acetylcholine receptor.
Martinou, J., Falls, D. L., Fischbach, G. D., & Merlie, J. P. (1991) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.88.17.7669 · Cited by 156
Activity regulates the levels of acetylcholine receptor alpha-subunit mRNA in cultured chicken myotubes.
Klarsfeld, A., & Changeux, J. (1985) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.82.13.4558 · Cited by 155
Postnatal maturation of nerve-muscle junctions in hindlimb muscles of the mouse
Slater, C. R. (1982) · Developmental Biology · doi:10.1016/0012-1606(82)90063-x · Cited by 154
Muscles of a different 'color'
Porter, J. D., & Baker, R. S. (1996) · Neurology · doi:10.1212/wnl.46.1.30 · Cited by 153
Developmental changes in acetylcholine receptor aggregates at rat skeletal neuromuscular junctions
Steinbach, J. H. (1981) · Developmental Biology · doi:10.1016/0012-1606(81)90394-8 · Cited by 153
Agrin-induced acetylcholine receptor clustering in mammalian muscle requires tyrosine phosphorylation.
Ferns, M., Deiner, M. S., & Hall, Z. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.132.5.937 · Cited by 151
Sprouting and remodelling at the nerve-muscle junction
Wernig, A., & Herrera, A. A. (1986) · Progress in Neurobiology · doi:10.1016/0301-0082(86)90023-7 · Cited by 149
The interaction between foreign and original motor nerves innervating the soleus muscle of rats.
Frank, E., Jansen, J. K. S., Lono, T., & Westgaard, R. H. (1975) · The Journal of Physiology · doi:10.1113/jphysiol.1975.sp010954 · Cited by 149
Implication of a multisubunit Ets‐related transcription factor in synaptic expression of the nicotinic acetylcholine receptor
Schaeffer, L., Duclert‐Savatier, N., Huchet, M., & Changeux, J. (1998) · The EMBO Journal · doi:10.1093/emboj/17.11.3078 · Cited by 149
A motoneuron-selective stop signal in the synaptic protein S-laminin.
Porter, B. E., Weis, J., & Sanes, J. (1995) · Neuron · doi:10.1016/0896-6273(95)90311-9 · Cited by 147
Self-citation
Development of innervation of skeletal muscle fibers in man: Relation to acetylcholine receptors
Hesselmans, L. F. G. M., Jennekens, F. G. I., van den Oord, C. J. M., Veldman, H., & Vincent, A. C. (1993) · The Anatomical Record · doi:10.1002/ar.1092360315 · Cited by 145
Proteolytic action of thrombin is required for electrical activity-dependent synapse reduction.
Liu, Y., Fields, R. D., Festoff, B. W., & Nelson, P. G. (1994) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.91.22.10300 · Cited by 145
Intrinsic neuronal determinants that promotes axonal sprouting and elongation
Caroni, P. (1997) · BioEssays · doi:10.1002/bies.950190906 · Cited by 145
Synaptic laminin prevents glial entry into the synaptic cleft
Patton, B. L., Chiu, A. Y., & Sanes, J. R. (1998) · Nature · doi:10.1038/31502 · Cited by 143
Self-citation
Reduction of multiaxonal innervation at the neuromuscular junction of the rat during development.
Rosenthal, J., & Taraskevich, P. S. (1977) · The Journal of Physiology · doi:10.1113/jphysiol.1977.sp011953 · Cited by 139
Regulation of muscle AChR α subunit gene expression by electrical activity: Involvement of protein kinase C and Ca 2+
Klarsfeld, A., Laufer, R., Fontaine, B., Devillers‐Thiéry, A., Dubreuil, C., & Changeux, J. (1989) · Neuron · doi:10.1016/0896-6273(89)90307-3 · Cited by 137
Dynamics of nerve-muscle interaction in developing and mature neuromuscular junctions
Grinnell, A. D. (1995) · Physiological Reviews · doi:10.1152/physrev.1995.75.4.789 · Cited by 137
Are Neurotrophins Synaptotrophins?
Snider, W. D., & Lichtman, J. W. (1996) · Molecular and Cellular Neuroscience · doi:10.1006/mcne.1996.0031 · Cited by 136
Self-citation
Synapse Elimination in the Central Nervous System: Functional Significance and Cellular Mechanisms
Lohof, A. M., Delhaye‐Bouchaud, N., & Mariani, J. (1996) · Reviews in the Neurosciences · doi:10.1515/revneuro.1996.7.2.85 · Cited by 135
Laminin-induced Acetylcholine Receptor Clustering: An Alternative Pathway
Sugiyama, J. E., Glass, D. J., Yancopoulos, G. D., & Hall, Z. W. (1997) · The Journal of Cell Biology · doi:10.1083/jcb.139.1.181 · Cited by 135
ErbB3 and ErbB2/neu mediate the effect of heregulin on acetylcholine receptor gene expression in muscle: differential expression at the endplate.
Altıok, N., Bessereau, J., & Changeux, J. (1995) · The EMBO Journal · doi:10.1002/j.1460-2075.1995.tb00100.x · Cited by 133
Physiological properties of motoneurons innervating different muscle unit types in rat gastrocnemius
Gardiner, P. F. (1993) · Journal of Neurophysiology · doi:10.1152/jn.1993.69.4.1160 · Cited by 133
Peripheral nerve regeneration
Idé, C. (1996) · Neuroscience Research · doi:10.1016/s0168-0102(96)01042-5 · Cited by 131
ARIA/HRG regulates AChR epsilon subunit gene expression at the neuromuscular synapse via activation of phosphatidylinositol 3-kinase and Ras/MAPK pathway.
Tansey, M. G., Chu, G. C., & Merlie, J. P. (1996) · The Journal of Cell Biology · doi:10.1083/jcb.134.2.465 · Cited by 131
Topographic mapping of motor pools onto skeletal muscles
Laskowski, M., & Sanes, J. (1987) · Journal of Neuroscience · doi:10.1523/jneurosci.07-01-00252.1987 · Cited by 130
Self-citation
Neural Agrin Induces Ectopic Postsynaptic Specializations in Innervated Muscle Fibers
Meier, T., Hauser, D. M., Chiquet, M., Landmann, L., Rüegg, M. A., & Brenner, H. R. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-17-06534.1997 · Cited by 130
ARIA can be released from extracellular matrix through cleavage of a heparin-binding domain.
Loeb, J. A., & Fischbach, G. D. (1995) · The Journal of Cell Biology · doi:10.1083/jcb.130.1.127 · Cited by 130
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
Differential Membrane Localization and Intermolecular Associations of α-Dystrobrevin Isoforms in Skeletal Muscle
Peters, M. F., Puccio, H. M., Grady, R. M., Kramarcy, N. R., Kunkel, L. M., Sanes, J. R., Sealock, R. W., & Froehner, S. C. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.142.5.1269 · Cited by 130
Self-citation
Spatial restriction of AChR gene expression to subsynaptic nuclei
Simon, A. M., Höppe, P., & Burden, S. J. (1992) · Development · doi:10.1242/dev.114.3.545 · Cited by 129
Spatial and temporal expression of acetylcholine receptor RNAs in innervated and denervated rat soleus muscle
Goldman, D. J., & Staple, J. K. (1989) · Neuron · doi:10.1016/0896-6273(89)90035-4 · Cited by 129
An amino-terminal extension is required for the secretion of chick agrin and its binding to extracellular matrix.
Denzer, 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
Heregulin‐stimulated acetylcholine receptor gene expression in muscle: requirement for MAP kinase and evidence for a parallel inhibitory pathway independent of electrical activity
Altıok, N., Altiok, S., & Changeux, J. (1997) · The EMBO Journal · doi:10.1093/emboj/16.4.717 · Cited by 127
Multiple innervation of tonic endplates revealed by activity-dependent uptake of fluorescent probes
Lichtman, J., Wilkinson, R. S., & Rich, M. (1985) · Nature · doi:10.1038/314357a0 · Cited by 127
Self-citation
The formation of topographical maps in developing rat gastrocnemius muscle during synapse elimination.
Bennett, M. R., & Ho, S. S. (1988) · The Journal of Physiology · doi:10.1113/jphysiol.1988.sp016973 · Cited by 125
Regulation of the acetylcholine receptor ϵ subunit gene by recombinant ARIA: An in vitro model for transynaptic gene regulation
Chu, G. C., Moscoso, L. M., Sliwkowski, M. X., & Merlie, J. P. (1995) · Neuron · doi:10.1016/0896-6273(95)90289-9 · Cited by 125
Gradual loss of synaptic cartels precedes axon withdrawal at developing neuromuscular junctions
Balice‐Gordon, R. J., Chua, C. K., Nelson, C. C., & Lichtman, J. W. (1993) · Neuron · doi:10.1016/0896-6273(93)90110-d · Cited by 125
Self-citation
Activity and synapse elimination at the neuromuscular junction
Thompson, W. J. (1985) · Cellular and Molecular Neurobiology · doi:10.1007/bf00711091 · Cited by 125
Studies of nerve-muscle interactions in Xenopus cell culture: fine structure of early functional contacts
Buchanan, J., Sun, Y., & Poo, M. (1989) · Journal of Neuroscience · doi:10.1523/jneurosci.09-05-01540.1989 · Cited by 124
Neuromuscular junctions shrink and expand as muscle fiber size is manipulated: in vivo observations in the androgen-sensitive bulbocavernosus muscle of mice
Balice‐Gordon, R. J., Breedlove, S. M., Bernstein, S., & Lichtman, J. W. (1990) · Journal of Neuroscience · doi:10.1523/jneurosci.10-08-02660.1990 · Cited by 123
Self-citation
Laminin and α-Dystroglycan Mediate Acetylcholine Receptor Aggregation via a MuSK-Independent Pathway
Montanaro, F., Gee, S., Jacobson, C., Lindenbaum, M., Froehner, S. C., & Carbonetto, S. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01250.1998 · Cited by 121
Synergistic Effects of Schwann- and Muscle-Derived Factors on Motoneuron Survival Involve GDNF and Cardiotrophin-1 (CT-1)
Gorvel, V. A., Pollock, R. A., Philippe, J., Pennica, D., Henderson, C. E., & deLapeyrière, O. (1998) · Journal of Neuroscience · doi:10.1523/jneurosci.18-04-01440.1998 · Cited by 118
Agrin is a differentiation-inducing “stop signal” for motoneurons in vitro
Campagna, J. A., Rüegg, M. A., & Bixby, J. L. (1995) · Neuron · doi:10.1016/0896-6273(95)90014-4 · Cited by 117
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
Self-citation
A synapse-specific carbohydrate at the neuromuscular junction: association with both acetylcholinesterase and a glycolipid
Scott, L., Bacou, F., & Sanes, J. R. (1988) · Journal of Neuroscience · doi:10.1523/jneurosci.08-03-00932.1988 · Cited by 116
Self-citation
Agrin Can Mediate Acetylcholine Receptor Gene Expression in Muscle by Aggregation of Muscle-derived Neuregulins
Meier, T., Masciulli, F., Moore, C., Schoumacher, F., Eppenberger, U., Denzer, A. J., Jones, G., & Brenner, H. R. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.141.3.715 · Cited by 116
Induction of synaptic development in cultured muscle cells by basic fibroblast growth factor
Peng, H. B., Baker, L. P., & Chen, Q. (1991) · Neuron · doi:10.1016/0896-6273(91)90359-8 · Cited by 115
Role of muscle insulin-like growth factors in nerve sprouting: suppression of terminal sprouting in paralyzed muscle by IGF-binding protein 4.
Caroni, P., Schneider, C., Kiefer, M. C., & Zapf, J. (1994) · The Journal of Cell Biology · doi:10.1083/jcb.125.4.893 · Cited by 114
Synapse-specific and neuregulin-induced transcription require an Ets site that binds GABPα/GABPβPreprint
Fromm, L., & Burden, S. J. (1998) · Genes & Development · doi:10.1101/gad.12.19.3074 · Cited by 114
Development of basal lamina in synaptic and extrasynaptic portions of embryonic rat muscle
Chiu, A. Y., & Sanes, J. R. (1984) · Developmental Biology · doi:10.1016/0012-1606(84)90333-6 · Cited by 113
Self-citation
Skeletal muscle denervation activates acetylcholine receptor genes.
Tsay, H.-J., & Schmidt, J. (1989) · The Journal of Cell Biology · doi:10.1083/jcb.108.4.1523 · Cited by 113
β-Spectrin Is Colocalized with Both Voltage-gated Sodium Channels and AnkyrinG at the Adult Rat Neuromuscular Junction
Wood, S. J., & Slater, C. R. (1998) · The Journal of Cell Biology · doi:10.1083/jcb.140.3.675 · Cited by 112
Synaptic Segregation at the Developing Neuromuscular Junction
Gan, W., & Lichtman, J. W. (1998) · Science · doi:10.1126/science.282.5393.1508 · Cited by 111
Self-citation
The Neuromuscular Junction
Engel, A. G. (1985) · Journal of Neuropathology & Experimental Neurology · doi:10.1097/00005072-198501000-00010 · Cited by 111
Nerve Terminal Withdrawal from Rat Neuromuscular Junctions Induced by Neuregulin and Schwann Cells
Trachtenberg, J. T., & Thompson, W. J. (1997) · Journal of Neuroscience · doi:10.1523/jneurosci.17-16-06243.1997 · Cited by 111
The downregulation of growth-associated proteins in motoneurons at the onset of synapse elimination is controlled by muscle activity and IGF1
Caroni, P., & Becker, M. (1992) · Journal of Neuroscience · doi:10.1523/jneurosci.12-10-03849.1992 · Cited by 111
Localization of the inositol 1,4,5-trisphosphate receptor in synaptic terminals in the vertebrate retina
Peng, Y., Sharp, A. H., Snyder, S. H., & Yau, K. (1991) · Neuron · doi:10.1016/0896-6273(91)90055-5 · Cited by 110
Age changes in neuromuscular junction morphology and acetylcholine receptor distribution on rat skeletal muscle fibres.
Courtney, J., & Steinbach, J. H. (1981) · The Journal of Physiology · doi:10.1113/jphysiol.1981.sp013960 · Cited by 110
Control of ACh Sensitivity in Rat Muscle FibersPreprint
Lømo, T., & Westgaard, R. H. (1976) · Cold Spring Harbor Symposia on Quantitative Biology · doi:10.1101/sqb.1976.040.01.027 · Cited by 110
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

Research works printed but not linked: 10

Aframian D, 1988, Puerto Rico Health Sci. J., 7, 80
Bewick GS, 1996, J. Neurocytol., 25, 367
Brand-Saberi B, 1996, Int. J. Dev. Biol., 40, 411
Burgess RW, 1998, Neurosci. Abstr., 24, 1534
Ganju P, 1995, Oncogene, 11, 281
Laskowski MB, 1998, Neurosci. Abstr., 24, 791
Martin D, 1996, Am. J. Physiol., 271, R1422
Patton BL, 1995, Neurosci. Abstr., 20, 799
Serpinskaya AS, 1997, Neurosci. Abstr., 23, 33
Zhou H, 1998, Neurosci. Abstr., 24, 1534

Sorted by citations

Microglia Sculpt Postnatal Neural Circuits in an Activity and Complement-Dependent Manner
Schafer, D. P., Lehrman, E. K., Kautzman, A. G., Koyama, R., Mardinly, A. R., Yamasaki, R., Ransohoff, R. M., Greenberg, M. E., Barres, B. A., & Stevens, B. (2012) · Neuron · doi:10.1016/j.neuron.2012.03.026 · Cited by 4,089
“Microglia-Mediated Engulfment of RGC Inputs Is Regulated by Neural Activity Synaptic pruning is thought to result from competition between neighboring axons for postsynaptic territory based on differences in patterns or levels of activity (Hua and Smith, 2004; Katz and Shatz, 1996; Sanes and Lichtman, 1999).”
Receptors for Purines and Pyrimidines
Burnstock, G., & Verkhratsky, A. (2012) · Springer eBooks · doi:10.1007/978-3-642-28863-0_5 · Cited by 3,962
The Classical Complement Cascade Mediates CNS Synapse Elimination
Stevens, B., Allen, N. J., Vazquez, L. E., Howell, G. R., Christopherson, K. S., Nouri, N., Micheva, K. D., Mehalow, A. K., Huberman, A. D., Stafford, B., et al. (2007) · Cell · doi:10.1016/j.cell.2007.10.036 · Cited by 3,313
Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., & Sanes, J. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00084-2 · Cited by 3,042
Self-citation
Neurotrophin regulation of neural circuit development and function
Park, H., & Poo, M.-M. (2013) · Nature Reviews Neuroscience · doi:10.1038/nrn3379 · Cited by 2,060

See all 1,532

Authors: Sanes, J. R., & Lichtman, J. W.
Affiliations: Washington University in St. Louis (US)
ORCID: Sanes, Joshua R.
Lichtman, Jeff W.
Venue: Annual Review of Neuroscience
Publisher: Annual Reviews
Published: 1999-03
Volume: 22
Issue: 1
Pages: 389-442
ISSN: 0147-006X (ISSN-L)
1545-4126
DOI: 10.1146/annurev.neuro.22.1.389
OpenAlex: W2134505400
Cited by: 1,532
References: 403
Citations by year: 2026: 22 · 2025: 36 · 2024: 47 · 2023: 35 · 2022: 35 · 2021: 47 · 2020: 60 · 2019: 44 · 2018: 48 · 2017: 55 · 2016: 49 · 2015: 27 · 2014: 57 · 2013: 39 · 2012: 57
FWCI: 8.58
Type: journal article
Language: en
Open access: closed
Locations: Annual Review of Neuroscience (publishedVersion)
PubMed (publishedVersion)
Topics: Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Axon Guidance and Neuronal Signaling
Keywords: neuromuscular junction, synaptogenesis, synapse maturation, synaptic pruning, synapse maintenance, synaptic remodeling, neuromuscular junction regeneration, motor axons, muscle fibers, Schwann cells, vertebrate development
MeSH terms: Animals, Glycoproteins, Nerve Regeneration, Neuromuscular Junction, Synapses, Transcription, Genetic, Vertebrates, Signal Transduction, Presynaptic Terminals, Neuregulins

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

DEVELOPMENT OF THE VERTEBRATE NEUROMUSCULAR JUNCTION

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Citations

Cites

Cited by

Related

Metadata

Record

About these checks