Fasciclin II and beaten path modulate intercellular adhesion in Drosophila larval visual organ development

Development

Volumn 126, Issue 2, 1999, Pages 261-272

  Holmes, Amy L ^a,b   Heilig, Joseph S ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Bolwig's Organ; Drosophila; Intercellular adhesion; Neuronal development; Sensory organ

Indexed keywords

FASCICLIN II;

ARTICLE; CELL ADHESION; CELL SECRETION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EYE DEVELOPMENT; GENE EXPRESSION; GROWTH INHIBITION; LARVAL DEVELOPMENT; MOTONEURON; NERVE CELL DIFFERENTIATION; NONHUMAN; OPTIC LOBE; ORGANOGENESIS; PHENOTYPE; PRIORITY JOURNAL; SENSE ORGAN;

ANIMALS; CELL ADHESION; CELL ADHESION MOLECULES; CELL ADHESION MOLECULES, NEURONAL; DROSOPHILA; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, HELMINTH; IN SITU HYBRIDIZATION; LARVA; MUTATION; NERVE TISSUE PROTEINS; OPTIC LOBE; PHENOTYPE; PHOTORECEPTORS, INVERTEBRATE;

ARACHNIDA; HEXAPODA; INSECTA;

EID: 0032913762     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (75)

1. Bastiani, M. J., Harrelson, A. L., Snow, P. M. and Goodman, C. S. (1987) Expression of Fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell 48, 745-755.
2. Bastiani, M. J., du Lac, S. and Goodman, C. S. (1986). Guidance of neuronal growth cones in the grasshopper embryo. I. Recognition of a specific axonal pathway by the pCC neuron. J. Neurosci. 6, 3518-3531.
3. Bastiani, M. J., Raper, J. A. and Goodman, C. S. (1984). Pathfinding by neuronal growth cones in grasshopper embryos. III. Selective affinity of the G growth cone for the P cells within the A/P fascicle. J. Neurosci. 4, 2311-2328.
4. Bazan, J. F., Goodman, C. S. (1997). Modular structure of the Drosophila Beat protein. Curr. Biol. 7, R338-R339.
5. Bieber, A. J., Snow, P. M., Hortsch, M., Patel, N. H., Jacobs, J. R., Traquina, Z. R., Schilling, J. and Goodman, C. S. (1989). Drosophila Neuroglian: A member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell 59, 447-460.
6. Bier, E., Vaessin, H., Shepard, S., Lee, K., McCall, K., Barbel, S., Ackerman, L., Carretto, R., Uemura, T., Grell, E., Jan, L. Y. and Jan, Y. N. (1989). Searching for pattern and mutation in the Drosophila genome with a P-lacZ vector. Genes Dev. 3, 1273-1287.
7. Bonhoeffer, I. and Huf, J. (1985). Position-dependent properties of retinal axons and their growth cones. Nature 315, 409-410.
8. Brunner, A. and O'Kane, C. J. (1997). The Fascination of the Drosophila NMJ. Trends Genet. 13, 85-87.
9. Campos-Ortega, J. A. and Hartenstein, V. (1997). The Embryonic Development of Drosophila melanogaster. Springer-Verlag, Berlin.
10. Castelli-Gair, J. E., Greig, S., Micklem, G. and Akam, M. E. (1994) Dissecting the temporal requirements for homeotic gene function. Development 120, 1983-1995.
11. Chiba, A. and Keshishian, H. (1996). Neuronal pathfinding and recognition: Roles of cell adhesion molecules. Dev. Biol. 180, 424-432.
12. Colamarino, S. A. and Tessier-Lavigne, M. (1995). The axonal chemoattractant netrin-1 is also a chemorepellent for trochlear motor axons. Cell 81, 621-629.
13. Cremer, H., Lange, R., Christopy, A., Plomann, M., Vopper, G., Roes, J., Brown, R., Baldwin, S., Kreamer, P., Scheff, S., Bathels, D., Rajewsky, K. and Willie, W. (1994). Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning. Nature 367, 455-459.
14. Davis, F. W., Schuster, C. M. and Goodman, C. S. (1997). Genetic analysis of the mechanisms controlling target selection: Target-derived Fasciclin II regulates the pattern of synapse formation. Neuron 19, 561-573.
15. Doe, C. Q., Bastiani, M. J. and Goodman, C. S. (1986). Guidance of neuronal growth cones in the grasshopper embryo. IV. Temporal delay experiments. J. Neurosci. 6, 3552-3563.
16. Drescher, U., Krenoser, C., Handwerker, C., Loschinger, J., Noda, M. and Bonhoeffer, F. (1995). In Vitro guidance of retinal ganglion cell axons by RAGS, a 25 kDa tectal protein related to ligands for Eph receptor tyrosine kinases. Cell 82, 359-370.
17. du Lac, S., Bastiani, M. J. and Goodman, C. S. (1986). Guidance of neuronal growth cones in the grasshopper embryo. II. Recognition of a specific axonal pathway by the aCC neuron. J. Neurosci. 6, 3532-3541.
18. Fambrough, D. and Goodman, C. S. (1996). The Drosophila beaten path gene encodes a novel secreted protein that regulates defasciculation at motor axon choice points. Cell 87, 1049-1058.
19. Franco, B., Guioli, S., Pragliola, A., Incerti, B., Bardoni, B., Tonlorenzi, R., Carrozzo, R., Maestrini, E., Pieretti, M., Taillon-Miller, P., Brown, C.J., Willard, H. F., Lawrence, C., Persico, M. G., Camerinao, G. and Ballabio, A. (1991). A gene deleted in Kallmann's syndrome shares homology with neural cell adhesion and axonal path-finding molecules. Nature 353, 529-535.
20. Garrity, P. A. and Zipursky, S. L. (1996). Neuronal target recognition. Cell 83, 177-185.
21. Gaul, U., Seifert, E., Schuh, R. and Jäckle, H. (1987). Analysis of Krüppel protein distribution during early Drosophila development reveals posttranscriptional regulation. Cell 50, 639-646.
22. Goodman, C. S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19, 341-377.
23. Goodman, C. S. and Shatz, C. J. (1993). Developmental mechanisms that generate precise patterns of neuronal connectivity. Cell/Neuron (Suppl.) 72/10, 77-98.
24. Green, P., Hartenstein, A. Y. and Hartenstein, V. (1993). The embryonic development of the Drosophila visual system. Cell Tissue Res. 273, 583-598.
25. Grenningloh, G., Bieber, A. J., Rehm, E. J., Snow, P. M., Traquina, Z. R., Hortsch, M., Patel, N. H. and Goodman, C. S. (1990) Molecular genetics of neuronal recognition in Drosophila: Evolulion and function of immunoglohulin superfamily cell adhesion molecules. Cold Spring Harbor Symp. Quant. Biol. 55, 327-340.
26. Grenningloh, G., Rehm, E. J. and Goodman, C. S. (1991). Genetic analysis of growth cone guidance in Drosophila: Fasciclin II functions as a neuronal recognition molecule. Cell 67, 45-57.
27. Hardelin, J.-P., Levilliers, J., del Castillo, I., Cohen-Salmon, M., Legous, R., Blanchard, S., Compain, S., Bouloux, P., Kirk, J., Moraine, C., Chaussain, J.-L., Weissenbach, J. and Petit, C. (1992). X chromosome-linked Kallmann syndrome: Stop mutations validate the candidate gene. Proc. Natl. Acad. Sci. USA 89, 8190-8194.
28. Harrelson, A. L. and Goodman, C. S. (1988). Growth cone guidance in insects: Fasciclin II is a member of the immunoglobulin superfamily. Science 242, 700-708.
29. Harris, R., Sabatelli, L. M. and Seeger, M. A. (1996). Guidance cues at the Drosophila CNS midline: Identification and characterization of two Drosophila Netrin/UNC-6 homologs. Neuron 17, 217-228.
30. Holmes, A. L., Raper, R. N. and Heilig, J. S. (1998). Genetic analysis of Drosophila larval optic nerve development. Genetics 148, 1189-1201.
31. Kania, A., Salzberg, A., Bhat, M., D'Evelyn, D., He, Y., Kiss, I. and Bellen, H. J. (1995). P-element mutations affecting embryonic peripheral nervous system development in Drosophila melanogaster. Genetics 139, 1663-1678.
32. Kidd, T., Brose, K., Mitchell, K. J., Fetter, R. D., Tessier-Lavigne, M., Goodman, C. S. and Tear, G. (1998). Roundabout controls axon crossing of the CNS midline and defines a novel subfamily of evolutionarily conserved guidance receptors. Cell 92, 205-215.
33. Kolodkin, A. L. (1996). Growth cones and the cues that repel them. Trends Neurosci. 19, 507-513.
34. Kolodkin, A. L., Matthes, D. J. and Goodman, C. S. (1993). The semaphorin genes encode a family of transmembrane and secreted growth cone guidance molecules. Cell 75, 1389-1399.
35. Kolodziej, P. A., Jan, L. Y. and Jan, Y. N. (1995). Mutations that affect the length, fasciculation or ventral orientation of specific sensory axons in the Drosophila embryo. Neuron 15, 273-286.
36. Kolodziej, P. A., Timpe, L. C., Mitchell, K. J., Fried, S. R., Goodman, C. S., Jan, L. Y. and Jan, Y. N. (1996). frazzled encodes a Drosophila member of the DCC immunoglohulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
37. Legouis, R., Hardelin, J.-P., Levilliers, J., Claverie, J.-M., Compain, S., Wunderie. V., Millasseau, P., Paslier, D.L., Cohen, D., Caterina, D., Bougueleret, L., Delemarre-Van de Waal, H., Lutfalla, G., Weissenbach, J. and Petit, C. (1991). The candidate gene for the X-linked Kallmann syndrome encodes a protein related to adhesion molecules. Cell 67, 423-425.
38. Lehmann, R. and Tautz, D. (1994). In Situ hybridization to RNA. In Drosophila melanogaster: Practical Uses in Cell and Molecular Biology (ed. L. S. B. Goldstein and E. A. Fyrberg), pp. 575-598. San Diego, California: Academic Press.
39. Lin, D. M., Fetter, R. D., Kopczynski, C., Grenningloh, G. and Goodman, C. S. (1994). Genetic analysis of Fasciclin II in Drosophila: Defasciculation, refasciculation and altered fasciculation. Neuron 13, 1055-1069.
40. Lin, D. M. and Goodman, C. S. (1994). Ectopic and increased expression of Fasciclin II alters motoneuron growth cone guidance. Neuron 13, 507-523.
41. Lis, J. T., Simon, J. A. and Sutton, C. A. (1983). New heat shock puffs and β-Galactosidase activity resulting from transformation of Drosophila with an hsp70-lacZ hybrid gene. Cell 35, 403-410.
42. Luo, Y., Raible, D. and Raper, J. A. (1993). Collapsin: a protein in brain that induces the collapse and paralysis of neuronal growth cones. Cell 75, 217-227.
43. Martin, K. A., Poeck, B., Rothe, H., Ebens, A. J., Ballard, L. C. and Zipursky, S. L. (1995). Mutations disrupting neuronal connectivity in the Drosophila visual system. Neuron 14, 229-240.
44. Mitchell, K. J., Doyle, J. L., Serafini, T., Kennedy, T. E., Tessier-Lavigne, M., Goodman, C. S. and Dickson, B. J. (1996). Genetic analysis of netrin genes in Drosophila: Netrins guide CNS commisural axons and peripheral motor axons. Neuron 17, 203-215.
45. Mitchison, T. J. and Sedat, J. W. (1983). Localization of antigenic determinants in whole Drosophila embryos. Dev. Biol. 99, 261-264.
46. Moses, K., Ellis, M. C. and Rubin, G. M. (1989). The glass gene encodes a zinc-finger protein required by Drosophila photoreceptor cells. Nature 340, 531-536.
47. Moses, K. and Rubin, G. M. (1991). glass encodes a site-specific DNA-binding protein that is regulated in response to positional signals in the developing Drosophila eye. Genes Dev. 5, 583-593.
48. Mushegian, A. R. (1997). The Drosophila Beat protein is related to adhesion proteins that contain immunoglobulin domains. Curr. Biol. 7, R336-R338.
49. Nose, A., Mahajan, V. B. and Goodman, C. S. (1992). Connectin: A homophilic cell adhesion molecule expressed on a subset of muscles and the motoneurons that innervate them in Drosophila. Cell 70, 553-567.
50. Ono, K., Tomasiewicz, H., Magnuson, T. and Ruthishauser, U. (1994). N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13, 595-609.
51. Patel, N., Snow, P. M. and Goodman, C. S. (1987). Characterization and cloning of Fasciclin III: a glycoprotein expressed on a subset of neurons and axon pathways in Drosophila. Cell 48, 975-988.
52. Raper, J. A., Bastiani, M. J. and Goodman, C. S. (1983a). Guidance of neuronal growth cones: selective fasciculation in the grasshopper embryo. Cold Spring Harbor Symp. Quant. Biol. 48, 587-598.
53. Raper, J. A., Bastiani, M. J. and Goodman, C. S. (1983b). Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by the growth cones of sibling neurons. J. Neurosci. 3, 20-30.
54. Raper, J. A., Bastiani, M. J. and Goodman, C. S. (1983c). Pathfinding by neuronal growth cones in grasshopper embryos. II. Selective fasciculation onto specific axonal pathways. J. Neurosci. 3, 31-41.
55. Raper, J. A., Bastiani, M. J. and Goodman, C. S. (1984). Pathfinding by neuronal growth cones in grasshopper embryos. IV. The effects of ablating the A and P axons upon the behavior of the G growth cone. J. Neurosci. 4, 2329-2345.
56. Rutishauser, U., Acheson, A., Hall, A. K., Mann, D. M. and Sunshine, J. (1988). The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 240, 53-57.
57. Rutishauser, U. and Landmesser, L. (1991). Polysialic acid on the surface of axons regulates patterns of normal and activity-dependent innervation. Trends Neurosci. 14, 528-532.
58. Salzberg, A., D'Evelyn, D., Schulze, K. L., Lee, J.-K., Strumpf, D., Tsai, L. and Bellen, H. J. (1994). Mutations affecting the pattern of the PNS in Drosophila reveal novel aspects of neuronal development. Neuron 13, 269-287.
59. Schmucker, D., Jäckle, H. and Gaul, U. (1997). Genetic analysis of the larval optic nerve projection in Drosophila. Development 124, 937-948.
60. Schmucker, D., Su, A. L., Beermann, A., Jäckle, H. and Jay, D. G. (1994). Chromophore-assisted laser inactivation of patched protein switches cell fate in the larval visual system in Drosophila. Proc. Natl. Acad. Sci. USA 91, 2664-2668.
61. Schmucker, D., Taubert, H. and Jäckle, H. (1992). Formation of the Drosophila larval photoreceptor organ and its neuronal differentiation require continuous Krüppel activity. Neuron 9, 1025-1039.
62. 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.
63. 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.
64. Seeger, M., Tear, G., Ferres-Marco, D. and Goodman, C. S. (1993). Mutations affecting growth cone guidance in Drosophila: Genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
65. Serafini, T., Kennedy, T. E., Galko, M. J., Mirzayan, C., Jessell, T. M. and Tessier-Lavigne, M. (1994). The Netrins define a family of axon outgrowth-promoting proteins homologous to C. elegans UNC-6. Cell 78, 409-424.
66. Simon, J. A., Sutton, C. A., Lobell, R. B., Glaser, R. L. and Lis, J. T. (1985) Determinants of heat shock-induced chromosome puffing. Cell 40, 805-817.
67. Snow, P. M., Zinn, K., Harrelson, A. L., McAllister, L., Schilling, J., Bastiani, M. J., Makk, G. and Goodman, C. S. (1988). Characterization and cloning of Fasciclin I and Fasciclin II glycoproteins in the grasshopper. Proc. Natl. Acad. Sci. USA 86, 5291-5295.
68. Tang, J., Landmesser, L. and Rutishauser, U. (1992). Polysialic acid influences specific pathtinding by avian motoneurons. Neuron 8, 1031-1044.
69. Tang, J., Rutishauser, U. and Landmesser, L. (1994). Polysialic acid regulates growth cone behavior during sorting of motor axons in the plexus region. Neuron 13, 405-414.
70. Tessier-Lavigne, M. and Goodman, C. S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
71. Thomas, U., Kim, E., Kuhlendahl, S., Koh, Y. H., Gundelfinger, E. D., Sheng, M., Garner, C. C. and Budnik, V. (1997). Synaptic clustering of the cell adhesion molecule Fasciclin II by Discs-large and its role in the regulation of presynaptic structure. Neuron 19, 787-799.
72. Thor, S. and Thomas, J. B. (1997). The Drosophila islet gene governs axon pathfinding and neurotransmitter identity. Neuron 18, 397-409.
73. Tomasiewicz, H., Ono, K., Yee, D., Thompson, C., Groidis, C., Rutishauser, U. and Magnuson, T. (1993). Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11, 1163-1174.
74. Van Vactor, D., Sink, H., Fambrough, D., Tsoo, R. and Goodman, C. S. (1993). Genes that control neuromuscular specificity in Drosophila. Cell 73, 1137-1153.
75. Zito, K., Fetter, R. D., Goodman, C. S. and Isacoff, E. Y. (1997). Synaptic clustering of Fasciclin II and Shaker: essential targeting sequences and role of Dlg. Neuron 19, 1007-1016.