UNC-11, a Caenorhabditis elegans AP180 homologue, regulates the size and protein composition of synaptic vesicles

Molecular Biology of the Cell

Volumn 10, Issue 7, 1999, Pages 2343-2360

  Nonet, Michael L ^a   Holgado, Andrea M ^b   Brewer, Faraha ^b   Serpe, Craig J ^b   Norbeck, Betty A ^b   Holleran, Julianne ^b   Wei, Liping ^a   Hartwieg, Erika ^c   Jorgensen, Erik M ^d   Alfonso, Aixa ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^c HOWARD HUGHES MEDICAL INSTITUTE   (United States)

^d UNIVERSITY OF UTAH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTOR PROTEIN; CLATHRIN; MUTANT PROTEIN; SYNAPTOBREVIN; SYNAPTOTAGMIN;

ANIMAL CELL; ARTICLE; BIOGENESIS; CAENORHABDITIS ELEGANS; ENDOCYTOSIS; EXOCYTOSIS; GENE EXPRESSION REGULATION; MAMMAL CELL; MOLECULAR CLONING; MUTANT; NERVE CELL; NERVE ENDING; NEUROTRANSMITTER RELEASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIKARYON; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; TISSUE DISTRIBUTION;

ANIMALIA; CAENORHABDITIS ELEGANS; MAMMALIA;

EID: 0032853429     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.10.7.2343     Document Type: Article

References (73)

1. Ahle, S., and Ungewickell, E. (1986). Purification and properties of a new clathrin assembly protein. EMBO J. 5, 3143-3149.
2. Albertson, D.G. (1984). Formation of the first cleavage spindle in nematode embryos. Dev. Biol. 101, 61-72.
3. 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.
4. Artalejo, C.R., Henley, J.R., McNiven, M.A., and Palfrey, H.C. (1995). Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP and dynamin, but not clathrin. Proc. Natl. Acad. Sci. USA 92, 8328-8332.
5. Avery, L. (1993a). Motor neuron M3 controls pharyngeal muscle relaxation timing in Caenorhabditis elegans. J. Exp. Biol. 175, 283-297.
6. Avery, L. (1993b). The genetics of feeding in Caenorhabditis elegans. Genetics 133, 897-917.
7. Barstead, R.J., and Waterston, R.H. (1989). The basal component of the nematode dense-body is vinculin. J. Biol. Chem. 264, 10177-10185.
8. Barton, M.K., and Kimble, J. (1990). fog-1, a regulatory gene required for specification of spermatogenesis in the germ line of Caenorhabditis elegans. Genetics 125, 29-39.
9. Beck, K.A., and Keen, J.H. (1991). Interaction of phosphoinositide cycle intermediates with the plasma membrane-associated clathrin assembly protein AP-2. J. Biol. Chem. 266, 4442-4447.
10. Bennett, M.K., Calakos, N., Kreiner, T., and Scheller, R.H. (1992). Synaptic vesicle membrane proteins interact to form a multimeric complex. J. Cell Biol. 116, 761-775.
11. Blumenthal, T. (1995). Trans-splicing and polycistronic transcription in Caenorhabditis elegans. Trends Genet. 11, 132-136.
12. Brenner, S. (1974). The genetics of Caenorhabditis elegans. Genetics 77, 71-94.
13. 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.
14. elegans Sequencing Consortium. (1998). Genome sequence of the nematode C. elegans: a plaform for investigating biology. Science 282, 2012-2018.
15. Cremona, O., and De Camilli, P. (1997). Synaptic vesicle endocytosis. Curr. Opin. Neurobiol. 7, 323-330.
16. Dreyling, M.H., Martinez-Climent, J.A., Zheng, M., Mao, J., Rowley, J.D., and Bohlander, S.K. (1996). The t(10;11)(p13;q14) in the U937 cell line results in the fusion of the AF10 gene and CALM, encoding a new member of the AP-3 clathrin assembly protein family. Proc. Natl. Acad. Sci. USA 93, 4804-4809.
17. 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.
18. Faundez, V., Horng, J.T., and Kelly, R.B. (1998). A function for the AP3 coat complex in synaptic vesicle formation from endosomes. Cell 93, 423-432.
19. Fesce, R., Grohovaz, F., Valtorta, F., and Meldolesi, J. (1994). Neurotransmitter release: fusion or 'kiss-and-run'? Trends Cell Biol. 4, 1-4.
20. Gaidarov, I., Chen, Q., Falck, J.R., Reddy, K.K., and Keen, J.H. (1996). A functional phosphatidylinositol 3,4,5-trisphosphate/phosphoinositide binding domain in the clathrin adaptor AP-2 alpha subunit. Implications for the endocytic pathway. J. Biol. Chem. 271, 20922-20929.
21. Gaidarov, I., Krupnick, J.G., Falck, J.R., Benovic, J.L., and Keen, J.H. (1999). Arrestin function in G protein-coupled receptor endocytosis requires phosphoinositide binding. EMBO J. 18, 871-881.
22. Gonzalez-Gaitan, M., and Jackle, H. (1997). Role of Drosophila alphaadaptin in presynaptic vesicle recycling. Cell 88, 767-776.
23. Hall, D.H., and Hedgecock, E.M. (1991). Kinesin-related gene unc104 is required for axonal transport of synaptic vesicles in C. elegans. Cell 65, 837-847.
24. Hanson, P.I., Roth, R., Morisaki, H., Jahn, R., and Heuser, J.E, (1997). Structure and conformational changes in NSF and its membrane receptor complexes visualized by quick-freeze/deep-etch electron microscopy. Cell 90, 523-535.
25. Hao, W., Tan, Z., Prasad, K., Reddy, K.K., Chen, J., Prestwich, G.D., Falck, J.R., Shears, S.B., and Lafer, E.M. (1997). Regulation of AP-3 function by inositides. Identification of phosphatidylinositol 3,4,5-trisphosphate as a potent ligand. J. Biol. Chem. 272, 6393-6398.
26. Hosono, R., and Kamiya, Y. (1991). Additional genes result in an elevation of acetylcholine levels by mutations in Caenorhabditis elegans. Neurosci. Lett. 128, 243-244.
27. Hunt, J.M., Bommert, K., Charlton, M.P., Kistner, A., Habermann, E., Augustine, G.J., and Betz, H. (1994). A postdocking role for synaptobrevin in synaptic vesicle fusion. Neuron 12, 1269-1279.
28. Innis, M.A., Gelfand, D.H., Sninsky, J.J., and White, T.J. (1990). PCR Protocols: A Guide to Methods and Applications, San Diego, Acadmic Press, 482.
29. Kohtz, D.S., and Puszkin, S. (1988). A neuronal protein (NP185) associated with clathrin-coated vesicles. Characterization of NP185 with monoclonal antibodies. J. Biol. Chem. 263, 7418-7425.
30. Kramer, J.M., French, R.P., Park, E.C., and Johnson, J.J. (1990). The Caenorhabditis elegans rol-6 gene, which interacts with the sqt-1 collagen gene to determine organismal morphology, encodes a collagen. Mol. Cell. Biol. 10, 2081-2089.
31. Li, H., Avery, L., Denk, W., and Hess, G. (1997). Identification of chemical synapses in the pharynx of Caenorhabditis elegans. Proc. Natl. Acad. Sci. USA 94, 5912-5916.
32. Matthews, G. (1996). Neurotransmitter release. Annu. Rev. Neurosci. 19, 219-233.
33. McIntire, S.L., Garriga, G., White, J., Jacobson, D., and Horvitz, H.R. (1992). Genes necessary for directed axonal elongation or fasciculation in C. elegans. Neuron 8, 307-322.
34. McIntire, S.L., Jorgensen, E., Kaplan, J., and Horvitz, H.R. (1993). The GABAergic nervous system of Caenorhabditis elegans. Nature 364, 337-341.
35. 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.
36. Miller, K.G., Alfonso, A., Nguyen, M., Crowell, J.A., Johnson, C.D., and Rand, J.B. (1996). A genetic selection for Caenorhabditis elegans synaptic transmission mutants. Proc. Natl. Acad. Sci. USA 93, 12593-12598.
37. Morris, S.A., Schroder, S., Plessmann, U., Weber, K., and Ungewickell, E. (1993). Clathrin assembly protein AP180: primary structure, domain organization and identification of a clathrin binding site. EMBO J. 12, 667-675.
38. Nguyen, M., Alfonso, A., Johnson, C.D., and Rand, J.B. (1995). Caenorhabditis elegans mutants resistant to inhibitors of acetylcholinesterase. Genetics 140, 527-535.
39. Nonet, M.L. (1999). Visualization of synaptic specializations in live C. elegans using synaptic vesicle-GFP protein fusions. J. Neurosci. Methods (in press).
40. 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.
41. Nonet, M.L., and Meyer, B.J. (1991). Early aspects of Caenorhabditis elegans sex determination and dosage compensation are regulated by a zinc-finger protein. Nature 351, 65-68.
42. 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.
43. 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.
44. Norris, F.A., Ungewickell, E., and Majerus, P.W. (1995). Inositol hexakisphosphate binds to clathrin assembly protein 3 (AP-3/ AP180) and inhibits clathrin cage assembly in vitro. J. Biol. Chem. 270, 214-217.
45. Palfrey, H.C., and Artalejo, C.R. (1998). Vesicle recycling revisited: rapid endocytosis may be the first step. Neuroscience 83, 969-989.
46. Poodry, C., and Edgar, L. (1979). Reversible alteration in the neuromuscular junctions of Droscphila melanogaster bearing a temperature-sensitive mutation. shibire. J. Cell Biol. 81, 520-527.
47. Puszkin, S., Perry, D., Li, S., and Hanson, V. (1992). Neuronal protein NP185 is developmentally regulated, initially expressed during synaptogenesis, and localized in synaptic terminals. Mol. Neurobiol. 6, 253-283.
48. Raizen, D.M., and Avery, L. (1994). Electrical activity and behavior in the pharynx of Caenorhabditis elegans. Neuron 12, 483-495.
49. 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.
50. Rand, J.B., and Nonet, M.L. (1997). Synaptic transmission. In: C. elegans II, ed. D.L. Riddle, T. Blumenthal, B.J. Meyer, and J.R. Priess, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, 611-644.
51. Rapoport, I., Miyazaki, M., Boll, W., Duckworth, B., Cantley, L.C., Shoelson, S., and Kirchhausen, T. (1997). Regulatory interactions in the recognition of endocytic sorting signals by AP-2 complexes. EMBO J. 16, 2240-2250.
52. Rosenzweig, B., Liao, L.W., and Hirsh, D. (1983). Sequence of the C. elegans transposable element, Tc1. Nucleic Acids Res. 11, 4201-4209.
53. 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.
54. Salcini, A., Confalonieri, S., Doria, M., Santolini, E., Tassi, E., Minenkova, O., Cesareni, G., Pelicci, P., and Di Fiore, P. (1997). Binding specificity and in vivo targets of the EH domain, a novel proteinprotein interaction module. Genes Dev. 11, 2239-2249.
55. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Book Molecular Cloning: A Laboratory Manual, 2nd edition, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
56. Schiavo, G., Benfenati, F., Poulain, B., Rossetto, O., Polverino de Laureto, P., DasGupta, B.R., and Montecucco, C. (1992). Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin. Nature 359, 832-835.
57. Schmid, S.L. (1997). Clathrin-coated vesicle formation and protein sorting: an integrated process. Annu. Rev. Biochem. 66, 511-548.
58. Smith, D., and Fisher, P.A. (1984). Identification, developmental regulation, and response to heat shock of two antigenically related forms of a major nuclear envelope protein in Drosophila embryos: applications of an improved method for affinity purification of antibodies using polypeptides immobilized on nitrocellulose blots. J. Cell Biol. 99, 20-28.
59. Sollner, T., Bennett, M.K., Whiteheart, S.W., Scheller, R.H., and Rothman, J.E. (1993b). A protein assembly-disassembly pathway in vitro that may correspond to sequential steps of synaptic vesicle docking, activation, and fusion. Cell 75, 409-418.
60. Sollner, T., Whiteheart, S.W., Brunner, M., Erdjument-Bromage, H., Geromanos, S., Tempst, P., and Rothman, J.E, (1993a). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318-324.
61. Stenius, K., Janz, R., Sudhof, T.C., and Jahn, R. (1995). Structure of synaptogyrin (p29) defines novel synaptic vesicle protein. J Cell. Biol. 131, 1801-1809.
62. Sudhof, T.C. (1995). The synaptic vesicle cycle: a cascade of protein-protein interactions. Nature 375, 645-653.
63. Sulston, J., and Hodgkin, J. (1988). Methods. In: The Nematode Caenorhabditis elegans, ed. W.B. Wood, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory, 587-606.
64. Walch-Solimena, C., Blasi, J., Edelmann, L., Chapman, E.R., von Mollard, G.F., and Jahn, R. (1995). The t-SNAREs syntaxin 1 and SNAP-25 are present on organelles that participate in synaptic vesicle recycling. J. Cell Biol. 128, 637-645.
65. Wang, L.-H., Südhof, T.C., and Anderson, R.G.W. (1995). The appendage domain of α-adaptin is a high affinity binding site for dynamin. J. Biol. Chem. 260, 10079-10083.
66. Weber, T., Zemelman, B.V., McNew, J.A., Westermann, B., Gmachl, M., Parlati, F., Sollner, T.H., and Rothman, J.E. (1998). SNAREpins: minimal machinery for membrane fusion. Cell 92, 759-772.
67. Wendland, B., and Emr, S.D. (1998). Pan1p, yeast eps15, functions as a multivalent adaptor that coordinates protein-protein interactions essential for endocytosis. J. Cell Biol. 141, 71-84.
68. Ye, W., Ali, N., Bembenek, M.E., Shears, S.B., and Lafer, E.M. (1995). Inhibition of clathrin assembly by high affinity binding of specific inositol polyphosphates to the synapse-specific clathrin assembly protein AP-3. J. Biol. Chem. 270, 1564-1568.
69. Ye, W., and Lafer, E.M. (1995a). Bacterially expressed F1-20/AP-3 assembles clathrin into cages with a narrow size distribution: implications for the regulation of quantal size during neurotransmission. J. Neurosci. Res. 41, 15-26.
70. Ye, W., and Lafer, E.M. (1995b). Clathrin binding and assembly activities of expressed domains of the synapse-specific clathrin assembly protein AP-3. J. Biol. Chem. 270, 10933-10939.
71. Zhang, B., Koh, Y.H., Beckstead, R.B., Budnik, V., Ganetzky, B., and Bellen, H.J. (1998). Synaptic vesicle size and number are regulated by a clathrin adaptor protein required for endocytosis. Neuron 21, 1465-1475.
72. Zhang, J.Z., Davletov, B.A., Sudhof, T.C., and Anderson, R.G.W. (1994). Synaptotagmin I is a high affinity receptor for clathrin AP-2: implications for membrane recycling. Cell 78, 751-760.
73. Zhou, S., Tannery, N.H., Yang, J., Puszkin, S., and Lafer, E.M. (1993). The synapse-specific phosphoprotein F1-20 is identical to the clathrin assembly protein AP-3. J. Biol. Chem. 268, 12655-12662.