A retrograde signal is involved in activity-dependent remodeling at a C. elegans neuromuscular junction

Development

Volumn 127, Issue 6, 2000, Pages 1253-1266

  Zhao, Hongjuan ^a   Nonet, And Michael L ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Activity; C. elegans; Neuromuscular junction; Retrograde signal; Synaptic plasticity; Synaptogenesis

Indexed keywords

ACETYLCHOLINE; CHOLINE ACETYLTRANSFERASE; CHOLINERGIC RECEPTOR; POTASSIUM CHANNEL;

ANIMAL TISSUE; ARTICLE; CAENORHABDITIS ELEGANS; CHOLINERGIC NERVE; CONTROLLED STUDY; LARVA; MUTANT; NEUROMUSCULAR SYNAPSE; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION; SYNAPTOGENESIS; SYNAPTOSOME; TEMPERATURE SENSITIVE MUTANT;

ACETYLCHOLINE; ANIMALS; CAENORHABDITIS ELEGANS; CHOLINE O-ACETYLTRANSFERASE; GENES, HELMINTH; LARVA; MOTOR NEURONS; MUTATION; NEUROMUSCULAR JUNCTION; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION;

ANIMALIA; CAENORHABDITIS ELEGANS;

EID: 0034112232     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (86)

1. Aguinaldo, A. M., Turbeville, J. M., Linford, L. S., Rivera, M. C., Garey, J. R., Raff, R. A. and Lake, J. A. (1997). Evidence for a clade of nematodes, arthropods and other moulting animals. Nature 387, 489-493.
2. Aigner, L., Arber, S., Kapfhammer, J. P., Laux, T., Schneider, C., Botteri, F., Brenner, H. R. and Caroni, P. (1995). Overexpression of the neural growth-associated protein GAP-43 induces nerve sprouting in the adult nervous system of transgenic mice. Cell 83, 269-278.
3. Alfonso, A., Grundahl, K., Duerr, J. S., Han, H. P. and Rand, J. B. (1993). The Caenorhabditis elegans unc-17 gene: a putative vesicular acetylcholine transporter. Science 261, 617-619.
4. Alfonso, A., Grundahl, K., McManus, J. R. and Rand, J. B. (1994). Cloning and characterization of the choline acetyltransferase structural gene (cha-1) from C. elegans. J. Neurosci. 14, 2290-2300.
5. Antebi, A., Norris, C. R., Hedgecock, E. M. and Garriga, G. (1997). Cell and growth cone migrations. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer and J. R. Priess), pp. 583-609. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
6. Bailey, C. H. and Chen, M. (1983). Morphological basis of long-term habituation and sensitization in Aplysia. Science 220, 91-93.
7. Balice-Gordon, R. J. and Lichtman, J. W. (1994). Long-term synapse loss induced by focal blockade of postsynaptic receptors. Nature 372, 519-524.
8. Bargmann, C. I. and Mori, I. (1997). Chemotaxis and thermotaxis. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess), pp. 717-737. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
9. Broadie, K. and Bate, M. (1993). Activity-dependent development of the neuromuscular synapse during Drosophila embryogenesis. Neuron 11, 607-619.
10. Broadie, K., Prokop, A., Bellen, H. J., O'Kane, C. J., Schulze, K. L. and Sweeney, S. T. (1995). Syntaxin and synaptobrevin function downstream of vesicle docking in Drosophila. Neuron 15, 663-673.
11. Brown, M. C., Holland, R. L. and Hopkins, W. G. (1981). Motor nerve sprouting. Annu. Rev. Neurosci. 4, 17-42.
12. Budnik, V., Zhong, Y. and Wu, C. F. (1990). Morphological plasticity of motor axons in Drosophila mutants with altered excitability. J. Neurosci. 10, 3754-3768.
13. Caroni, P. (1993). Activity-sensitive signaling by muscle-derived insulin-like growth factors in the developing and regenerating neuromuscular system. Ann. N. Y. Acad. Sci. 692, 209-222.
14. Caroni, P. and Grandes, P. (1990). Nerve sprouting in innervated adult skeletal muscle induced by exposure to elevated levels of insulin-like growth factors. J. Cell Biol. 110, 1307-1317.
15. Cline, H. T. and Constantine-Paton, M. (1990). NMDA receptor agonist and antagonists alter retinal ganglion cell arbor structure in the developing frog retinotectal projection. J. Neurosci. 10, 1197-1216.
16. Coburn, C. M., Mori, I., Ohshima, Y. and Bargmann, C. I. (1998). A cyclic nucleotide-gated channel inhibits sensory axon outgrowth in larval and adult Caenorhabditis elegans: a distinct pathway for maintenance of sensory axon structure. Development 125, 249-258.
17. Covault, J. and Sanes, J. R. (1985). Neural cell adhesion molecule (N-CAM) accumulates in denervated and paralyzed skeletal muscles. Proc. Natl. Acad. Sci. USA 82, 4544-4548.
18. Davis, G. W., DiAntonio, A., Petersen, S. A. and Goodman, C. S. (1998). Postsynaptic PKA controls quantal size and reveals a retrograde signal that regulates presynaptic transmitter release in Drosophila. Neuron 20, 305-315.
19. Davis, G. W. and Goodman, C. S. (1998). Genetic analysis of synaptic development and plasticity: homeostatic regulation of synaptic efficacy. Curr. Opin. Neurobiol. 8, 149-156.
20. 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., Smith, C., DiStefano, P. S., Glass, D. J., Burden, S. J. and Yancopoulos, G. D. (1996). The receptor tyrosine kinase MuSK is required for neuromuscular junction formation in vivo. Cell 85, 501-512.
21. Driscoll, M. and Kaplan, J. (1997). Mechanosensation. In C. elegans II (ed.
22. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess), pp. 645-677. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
23. Duchen, L. W. and Strich, S. J. (1968). The effects of botulinum toxin on the pattern of innervation of skeletal muscle in the mouse. Q. J. Exp. Physiol. Cogn. Med. Sci. 53, 84-89.
24. Duerr, J. S., Frisby, D. L., Gaskin, J. G., Duke, A., Asermely, K., Huddleston, D., Eiden, L. E. and Rand, J. B. (1999). The cat-1 gene of C. elegans encodes a vesicular monoamine transporter required for specific monoamine-dependent behaviors. J. Neurosci. 19, 72-84.
25. Fisher, C. L. and Pei, G. K. (1997). Modification of a PCR-based site-directed mutagenesis method. Biotechniques 23, 570-1, 574.
26. Fleming, J. T., Squire, M. D., Barnes, T. M., Tornoe, C., Matsuda, K., Ahnn, J., Fire, A., Sulston, J. E., Barnard, E. A., Sattelle, D. B. and Lewis, J. A. (1997). Caenorhabditis elegans levamisole resistance genes lev-1, unc-29, and unc-38 encode functional nicotinic acetylcholine receptor subunits. J. Neurosci. 17, 5843-5857.
27. Gautam, M., Noakes, P. G., Moscoso, L., Rupp, F., Scheller, R. H., Merlie, J. P. and Sanes, J. R. (1996). Detective neuromuscular synaptogenesis in agrin-deficient mutant mice. Cell 85, 525-535.
28. Gautam, M., Noakes, P. G., Mudd, J., Nichol, M., Chu, G. C., Sanes, J. R. and Merlie, J. P. (1995). Failure of postsynaptic specialization to develop at neuromuscular junctions of rapsyn-deficient mice. Nature 377, 232-236.
29. Gengyo-Ando, K., Kamiya, Y., Yamakawa, A., Kodaira, K., Nishiwaki, K., Miwa, J., Hori, I. and Hosono, R. (1993). The C. elegans unc-18 gene encodes a protein expressed in motor neurons. Neuron 11, 703-711.
30. Geppert, M., Bolshakov, V. Y., Siegelbaum, S. A., Takei, K., De Camilli, P., Hammer, R. E. and Südhof, T. C. (1994). The role of Rab3A in neurotransmitter release. Nature 369, 493-497.
31. Hall, D. H. and Hedgecock, E. M. (1991). Kinesin-related gene unc-104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65, 837-847.
32. Hall, D. H. and Russell, R. L. (1991). The posterior nervous system of the nematode Caenorhabditis elegans: serial reconstruction of identified neurons and complete pattern of synaptic interactions. J. Neurosci. 11, 1-22.
33. Hallam, S. J. and Jin, Y. (1998). lin-14 regulates the timing of synaptic remodelling in Caenorhabditis elegans. Nature 395, 78-82.
34. Harish, O. E. and Poo, M. M. (1992). Retrograde modulation at developing neuromuscular synapses: involvement of G protein and arachidonic acid cascade. Neuron 9, 1201-1209.
35. Hedgecock, E. M., Culotti, J. G. and Hall, D. H. (1990). The unc-5, unc-6, and unc-40 genes guide circumferential migrations of pioneer axons and mesodermal cells on the epidermis in C. elegans. Neuron 4, 61-85.
36. Holland, R. L. and Brown, M. C. (1980). Postsynaptic transmission block can cause terminal sprouting of a motor nerve. Science 207, 649-651.
37. Hopkins, W. G., Brown, M. C. and Keynes, R. J. (1985). Postnatal growth of motor nerve terminals in muscles of the mouse. J. Neurocytol. 14, 525-540.
38. Hubel, D. H. and Wiesel, T. N. (1970). The period of susceptibility to the physiological effects of unilateral eye closure in kittens. J. Physiol. (Lond) 206, 419-436.
39. Jarecki, J. and Keshishian, H. (1995). Role of neural activity during synaptogenesis in Drosophila. J. Neurosci. 15, 8177-8190.
40. Jin, Y., Jorgensen, E., Hartwieg, E. and Horvitz, H. R. (1999). The C. elegans gene unc-25 encodes glutamic acid decarboxylase and is required for synaptic transmission but not synaptic development. J. Neurosci. 19, 539-548.
41. Johnstone, D. B., Wei, A., Butler, A., Salkoff, L. and Thomas, J. H. (1997). Behavioral defects in C. elegans egl-36 mutants result from potassium channels shifted in voltage-dependence of activation. Neuron 19, 151-164.
42. Jorgensen, E. M. and Nonet, M. L. (1995). Neuromuscular junctions in the nematode C. elegans. Sem. Dev. Biol. 6, 207-220.
43. Katz, L. C. and Shatz, C. J. (1996). Synaptic activity and the construction of cortical circuits. Science 274, 1133-1138.
44. Keshishian, H., Broadie, K., Chiba, A. and Bate, M. (1996). The Drosophila neuromuscular junction: a model system for studying synaptic development and function. Annu. Rev. Neurosci. 19, 545-575.
45. Keshishian, H., Chiba, A., Chang, T. N., Halfon, M. S., Harkins, E. W., Jarecki, J., Wang, L., Anderson, M., Cash, S., Halpern, M. E., et al. (1993). Cellular mechanisms governing synaptic development in Drosophila melanogaster. J. Neurobiol. 24, 757-787.
46. Lee, R. Y. N., Sawin, E. R., Chalfie, M., Horvitz, H. R. and Avery, L. (1999). EAT-4, a homolog of a mammalina sodium-dependent inorganic phosphate cotransporter, is necessary for glutamatergic neurotransmission in Caenorhabditis elegans. J. Neurosci. 19, 159-167.
47. Lnenicka, G. A., Hong, S. J., Combatti, M. and LePage, S. (1991). Activity-dependent development of synaptic varicosities at crayfish motor terminals. J. Neurosci. 11, 1040-1048.
48. Lnenicka, G. A. and Murphey, R. K. (1989). The refinement of invertebrate synapses during development. J. Neurobiol. 20, 339-355.
49. Maruyama, I. N. and Brenner, S. (1991). A phorbol ester/diacylglycerol-binding protein encoded by the unc-13 gene of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 88, 5729-5733.
50. McIntire, S. L., Jorgensen, E., Kaplan, J. and Horvitz, H. R. (1993). The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337-341.
51. Mello, C. and Fire, A. (1995). DNA transformation. In Caenorhabditis elegans: Modern analysis of an organism, vol. 48 (ed. H. F. Epstein and D. C. Shakes), pp. 451-482. Academic Press, San Diego.
52. Mello, C. C., Kramer, J. M., Stinchcomb, D. and Ambros, V. (1991). Efficient gene transfer in C. elegans: extrachromosomal maintenance and integration of transforming sequences. EMBO J. 10, 3959-3970.
53. Miller, D. M. I. and Niemeyer, C. J. (1995). Expression of the unc-4 homeoprotein in Caenorhabditis elegans motor neurons specifies presynaptic input. Development 121, 2877-2886.
54. Mushegian, A. R., Garey, J. R., Martin, J. and Liu, L. X. (1998). Large-scale taxonomic profiling of eukaryotic model organisms: a comparison of orthologous proteins encoded by the human, fly, nematode, and yeast genomes. Genome Res. 8, 590-598.
55. Nguyen, Q. T. and Lichtman, J. W. (1996). Mechanism of synapse disassembly at the developing neuromuscular junction. Curr. Opin. Neurobiol. 6, 104-112.
56. Nonet, M. L. (1999). Visualisation of synaptic specializations in live C. elegans using synaptic vesicle-GFP protein fusions. J. Neurosci. Methods 89, 33-40.
57. Nonet, M. L., Grundahl, K., Meyer, B. J. and Rand, J. B. (1993). Synaptic function is impaired but not eliminated in C. elegans mutants lacking synaptotagmin. Cell 73, 1291-1305.
58. Nonet, M. L., Saifee, O., Zhao, H., Rand, J. B. and Wei, L. (1998). Synaptic transmission deficits in C. elegans synaptobrevin mutants. J. Neurosci. 18, 70-80.
59. Nonet, M. L., Staunton, J., Kilgard, M. P., Fergestad, T., Hartweig, E., Horvitz, H. R., Jorgensen, E. and Meyer, B. J. (1997). C. elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17, 8021-8073.
60. Okkema, P. G., Harrison, S. W., Plunger, V., Aryana, A. and Fire, A. (1993). Sequence requirements tor myosin gene expression and regulation in Caenorhabditis elegans. Genetics 135, 385-404.
61. Peckol, E. L., Zallen, J. A., Yarrow, J. C. and Bargmann, C. I. (1999). Sensory activity affects sensory axon development in C. elegans. Development 126, 1891-1902.
62. Petersen, S. A., Fetter, R. D., Noordermeer, J. N., Goodman, C. S. and DiAntonio, A. (1997). Genetic analysis of glutamate receptors in Drosophila reveals a retrograde signal regulating presynaptic transmitter release. Neuron 19, 1237-1248.
63. Piehl, F., Hammarberg, H., Hokfelt, T. and Cullheim, S. (1998). Regulatory effects of trophic factors on expression and distribution of CGRP and GAP-43 in rat motoneurons. J. Neurosci. Res. 51, 1-14.
64. Plunkett, J. A., Simmons, R. B. and Walthall, W. W. (1996). Dynamic interactions between nerve and muscle in Caenorhabditis elegans. Dev. Biol. 175, 154-165.
65. Raizen, D. M., Lee, R. Y. N. and Avery, L. (1995). Interacting genes required for pharyngeal excitation by motor neuron MC in Caenorhabditis elegans. Genetics 141, 1365-1382.
66. Rand, J. B. (1989). Genetic analysis of the cha-I-unc-17 gene complex in Caenorhabditis. Genetics 122,73-80.
67. Rand, J. B. and Nonet, M. L. (1997a). Neurotransmitter assignments for specific neurons. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess), pp. 1049-1052. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
68. Rand, J. B. and Nonet, M. L. (1997b). Synaptic transmission. In C. elegans II (ed. D. L. Riddle, T. Blumenthal, B. J. Meyer, and J. R. Priess), pp. 611-644. Cold Spring Harbor Laboratory Press, Cold Spring Harbor.
69. Rand, J. B. and Russell, R. L. (1984). Choline acetyltransferase-deficient mutants of the nematode Caenorhabditis elegans. Genetics 106, 227-248.
70. Richmond, J. E., Davis, W. S. and Jorgensen, E. M. (1999). UNC-13 is required for synaptic vesicle fusion in C. elegans. Mat. Neurosci. 2, 959-964.
71. Richmond, J. E. and Jorgensen, E. M. (1999). One GABA and two acetylcholine receptors function at the C. elegans neuromuscular junction. Nat. Neurosci. 2, 791-797.
72. Rongo, C. and Kaplan, J. M. (1999). CaMKII regulates the density of central glutamatergic synapses in vivo. Nature 402, 195-199.
73. Saifee, O., Wei, L. P. and Nonet, M. L. (1998). The C. elegans unc-64 gene-encodes a syntaxin which interacts with genetically with synaptobrevin. Mol. Biol. Cell 9, 1235-1252.
74. Sala, C., Andreose, J. S., Fumagalli, G. and Lomo, T. (1995). Calcitonin gene-related peptide: possible role in formation and maintenance of neuromuscular junctions. J. Neurosci. 15, 520-528.
75. Schulze, K. L., Broadie, K., Perin, M. S. and Bellen, H. J. (1995). Genetic and electrophysioloical studies of Drosophila syntaxin-1A demonstrate its role in nonneuronalsecretion and neurotransmission. Cell 80, 311-320.
76. Schuster, C. M., Davis, G. W., Fetter, R. D. and Goodman, C. S. (1996a). Genetic dissection of structural and functional components of synaptic plasticity. I. Fasciclin II controls synaptic stabilization and growth. Neuron 17, 641-654.
77. Schuster, C. M., Davis, G. W., Fetter, R. D. and Goodman, C. S. (1996b). Genetic dissection of structural and functional components of synaptic plasticity. II. Fasciclin II controls presynaptic structural plasticity. Neuron 17, 655-667.
78. Sidow, A. and Thomas, W. K. (1994). A molecular evolutionary framework for eukaryotic model organisms. Curr. Biol. 4, 596-603.
79. Stryker, M. P. and Harris, W. A. (1986). Binocular impulse blockade prevents the formation of ocular dominance columns in cat visual cortex. J. Neurosci. 6, 2117-2133.
80. Sulston, J. and Hodgkin, J. (1988). Methods. In The nematode Caenorhabditis elegans (ed. W. B. Wood), pp. 587-606. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
81. Sulston, J. E. and Horvitz, H. R. (1977). Post-embryonic cell lineages of the nematode Caenorhabditis elegans. Dev. Biol. 56, 110-156.
82. Thompson, W. and Jansen, J. K. (1977). The extent of sprouting of remaining motor units in partly denervated immature and adult rat soleus muscle. Neuroscience 2, 523-535.
83. Way, J. C. and Chalfie, M. (1989). The mec-3 gene of Caenorhabditis elegans requires its own product for maintained expression and is expressed in three neuronal cell types. Genes Dev. 3, 1823-1833.
84. White, J. G., Albertson, D. G. and Anness, M. A. (1978). Connectivity changes in a class of motoneurone during the development of a nematode. Nature 271, 764-766.
85. White, J. G., Southgate, E., Thomson, J. N. and Brenner, S. (1986). The structure of the nervous system of Caenorhabditis elegans. Phil. Trans. R. Soc. Lond. B 314, 1-340.
86. Zhong, Y., Budnik, V. and Wu, C. F. (1992). Synaptic plasticity in Drosophila memory and hyperexcitable mutants: role of cAMP cascade. J. Neurosci. 12, 644-651.