Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the drosophila embryonic CNS

Neuron

Volumn 19, Issue 1, 1997, Pages 77-89

  Iwai, Youichi ^a   Usui, Tadao ^a   Hirano, Shinji ^a,c   Steward, Ruth ^b   Takeichi, Masatoshi ^a   Uemura, Tadashi ^a  

^a KYOTO UNIVERSITY   (Japan)

^b RUTGERS UNIVERSITY   (United States)

^c DOHENY EYE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CADHERIN; CATENIN; CELL RECEPTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL AGGREGATION; CELL INTERACTION; CELL MIGRATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; GENE EXPRESSION; GENE MUTATION; GROWTH CONE; NERVE GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL;

EID: 0030861051     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0896-6273(00)80349-9     Document Type: Article

References (85)

1. Bixby, J.L., and Zhang, R. (1990). Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J. Cell Biol. 110, 1253-1260.
2. Brand, A.M., and Perrimon, N. (1993). Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
3. Bunch, T.A., Grinblat, Y., and Goldstein, L.S.B. (1988). Characterization and use of the Drosophila metallothionein promotor in cultured Drosophila melanogaster cells. Nucleic Acids Res. 16, 1043-1061.
4. Campbell, G., Goring, H., Lin, T., Spana, E., Anderson, S., Doe, C.Q., and Tomlinson, A. (1994). RK2, a glial-specifichomeodomain protein required for embryonic nerve cord condensation and viability in Drosophila. Development 120, 2957-2966.
5. Chan, S.S.-Y., Zheng, H., Su, M.-W., Wilk, R., Killeen, M.T., Hedgecock, E.M., and Culotti, J.G. (1996). UNC-40, a C. elegans homolog of DCC (deleted in colorectal cancer), is required in motile cells responding to UNC-6 netrin cues. Cell 87, 187-195.
6. Clark, H.F., Brentrup, D., Schneitz, K., Bieber, A., Goodman, C., and Noll, M. (1995). Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev. 9, 1530-1542.
7. Cox, R.T., Kirkpatrick, C., and Reifer, M. (1996). Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J. Cell Biol. 134, 133-148.
8. Detrick, R.J., Dickey, D., and Kintner, C. (1990). The effects of N-cadherin misexpression on morphogenesis in Xenopus embryos. Neuron 4, 493-506.
9. Doherty, P., and Walsh, F.S. (1996). CAM-FGF receptor interactions: a model for axonal growth. Mol. Cell. Neurosci. 8, 99-111.
10. Dusband, J.-L., Volberg, T., Sabanay, I., Thiery, J.-P., and Geiger, B. (1988). Spatial and temporal distribution of the adherens-junction-associated adhesion molecule A-CAM during avian embryogenesis. Development 103, 325-344.
11. Edwards, J.S., Swales, L.S., and Bate, M. (1993). The differentiation between neuroglia and connective tissue sheath in insect ganglia revisited: the neural lamella and perineurial sheath cells are absent in a mesodermless mutant of Drosophila. J. Comp. Neurol. 333, 301-308.
12. Fannon, A.M., and Colman, D.R. (1996). A model for central synaptic junctional complex formation based on the differential adhesive specificities of the cadherins. Neuron 17, 423-434.
13. Fujimori, T., Miyatani, S., and Takeichi, M. (1990). Ectopic expression of N-cadherin perturb histogenesis in Xenopus embryos. Development 110, 97-104.
14. Fujita, S.C., Zipursky, S.L., Benzer, S., Ferrus, A., and Shotwell, S.L. (1982). Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. USA 79, 7929-7933.
15. Goodman, C.S. (1996). Mechanisms and molecules that control growth cone guidance. Annu. Rev. Neurosci. 19, 341-377.
16. Goodman, C.S., and Doe, C.Q. (1993). Embryonic development of the Drosophila central nervous system. In The Development of Drosophila melanogaster, M. Bate and A. M. Arias, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 1131-1206.
17. 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.
18. Halter, D.A., Urban, J., Rickert, C., Ner, S.S., Ito, K., Travers, A.A., and Technau, G.M. (1995). The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121, 317-332.
19. Hammond, C., and Helenius, A. (1994). Quality control in the secretory pathway: retention of a misfolded viral membrane glycoprotein involves cycling between the ER, intermediate compartment, and Golgi apparatus. J. Cell Biol. 126, 41-52.
20. 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 homolog. Neuron 17, 217-228.
21. Hatta, K., and Takeichi, M. (1986). Expression of N-cadherin adhesion molecules associated with early morphogenetic events in chick development. Nature 320, 447-449.
22. Hatta, K., Takagi, S., Fujisawa, H., and Takeichi, M. (1987). Spatial and temporal expression pattern of N-cadherin cell adhesion molecules correlated with morphogenetic processes of chicken embryos. Dev. Biol. 120, 215-227.
23. Higashijima, S., Shishido, E., Matsuzaki, M., and Saigo, K. (1996). eagle, a member of the steroid receptor gene superfamily, is expressed in a subset of neuroblasts and regulates the fate of their putative progeny in the Drosophila CNS. Development 122, 527-536.
24. Hirano, S., Kimoto, N., Shimoyama, Y., Hirohashi, S., and Takeichi, M. (1992). Identification of a neural a-catenin as a key regulator of cadherin function and multicellular organization. Cell 70, 293-301.
25. Hiromi, Y., Kuroiwa, A., and Gehring, W.J. (1985). Control elements of the Drosophila segmentation gene fushi tarazu. Cell 43, 603-613.
26. Hoshino, M., Suzuki, E., Nabeshima, Y.-I., and Hama, C. (1996). Hikaru genki protein is secreted into synaptic clefts from an early stage of synapse formation in Drosophila. Development 122, 589-597.
27. Hosoya, T., Takizawa, K., Nitta, K., and Hotta, Y. (1995). glial cells missing: a binary switch between neuronal and glial determination in Drosophila. Cell 82, 1025-1036.
28. Huber, O., Bierkamp, C., and Kemler, R. (1996). Cadherins and catenins in development. Curr. Opin. Cell Biol. 8, 685-691.
29. Jan, L.Y., and Jan, Y.N. (1982). Antibodies to horseradish peroxidase as specific neuronal markers in Drosophila and grasshopper embryos. Proc. Natl. Acad. Sci. USA 79, 2700-2704.
30. Jan, Y.N., and Jan, L.Y. (1993). The peripheral nervous system. In The Development of Drosophila melanogaster, M. Bate and A.M. Arias, eds. (Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press), pp. 1207-1244.
31. Jokerst, R.S., Weeks, J.R., Zehring, W.A., and Greenleaf, A.L. (1989). Analysis of the gene encoding the largest subunit of RNA polymerase II in Drosophila. Mol. Gen. Genet. 215, 266-275.
32. Jones, B.W., Fetter, R.D., Tear, G., and Goodman, C.S. (1995). glial cells missing: a genetic switch that controls glial versus neuronal fate. Cell 82, 1013-1023.
33. Kawanishi, J., Kato, J., Sasaki, K., Fujii, S., Watanabe, N., and Niitsu, Y. (1994). Loss of E-cadherin-dependent cell-cell adhesion due to mutation of the β-catenin gene in a human cancer cell line, HSC-39. Mol. Cell. Biol. 15, 1175-1181.
34. Keino-Masu, K., Masu, M., Hinck, L., Leonardo, E.D., and Tessier-Lavigne, M. (1996). Deleted in colorectal cancer (DCC) encodes a netrin receptor. Cell 87, 175-185.
35. Keynes, R., and Cook, M.W.G. (1995). Axon guidance molecules. Cell 83, 161-169.
36. Klaes, A., Menne, T., Stollewerk, A., Schoiz, H., and Klämbt, C. (1994). The Ets transcription factors encoded by the Drosophila gene pointed direct glial cell differentiation in the embryonic CNS. Cell 78, 149-160.
37. 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 immunoglobulin subfamily and is required for CNS and motor axon guidance. Cell 87, 197-204.
38. 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.
39. Lindsley, D.L., and Zimm, G.G. (1992). The Genome of Drosophila melanogaster. (New York: Academic Press, Inc.).
40. Lundgren, S.E., Callahan, C.A., Thor, S., and Thomas, J.B. (1995). Control of neuronal pathway selection by the Drosophila LIM homeodomain gene apterous. Development 121, 1769-1773.
41. Luo, L., Liao, Y.J., Jan, L.Y., and Jan, Y.N. (1994). Distinct morphogenetic functions of similar small GTPases: Drosophila Drad1 is involved in axonal outgrowth and myoblast fusion. Genes Dev. 8, 1787-1802.
42. Mahoney, P.A., Weber, U., Onofrechuk, P., Biessmann, H., Bryant, P.J., and Goodman, C.S. (1991). The fat tumor suppressor gene in Drosophila encodes a novel member of the cad herin gene superfamily. Cell 67, 853-868.
43. Matsunaga, M., Hatta, K., Nagafuchi, A., and Takeichi, M. (1988). Guidance of optic nerve fibers by N-cadherin adhesion molecules. Nature 334, 62-64.
44. Matsunami, H., and Takeichi, M. (1995). Fetal brain subdivisions defined by R-and E-cadherin expressions: evidence for the role of cadherin activity in region-specific, cell-cell adhesion. Dev. Biol. 172, 466-478.
45. McCrea, P.D., Turck, C.W., and Gumbiner, B. (1991). A homolog of the armadillo protein in Drosophila (Plakoglobin) associated with E-cadherin. Science 254, 1359-1361.
46. Meinertzhagen, I.A., and O'Neil, S.D. (1991). Synaptic organization of columnar elements in the lamina of the wild type in Drosophila melanogaster. J. Comp. Neurol. 305, 232-263.
47. 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 commissural axons and peripheral motor axons. Neuron 17, 203-215.
48. Miyatani, S., Shimamura, K., Hatta, M., Nagafuchi, A., Nose, A., Matsunaga, M., Hatta, K., and Takeichi, M. (1989). Neural cadherin: role in selective cell-cell adhesion. Science 245, 631-635.
49. Nagafuchi, A., Shirayoshi, Y., Okazaki, K., Yasuda, K., and Takeichi, M. (1987). Transformation of cell adhesion properties by exogenously introduced E-cadherin cDNA. Nature 329, 341-343.
50. Nagafuchi, A., Takeichi, M., and Tsukita, S. (1991). The 102 kd cadherin-associated protein: similarity to vinculin and posttranscriptional regulation of expression. Cell 65, 849-857.
51. Nagafuchi, A., Ishihara, S., and Tsukita, S. (1994). The roles of catenins in the cadherin-mediated cell adhesion: functional analysis of E-cadherin-α catenin fusion molecules. J. Cell Biol. 127, 235-245.
52. Nagar, B., Overduin, M., Ikura, M., and Rini, J.M. (1996). Structural basis of calcium-induced E-cadherin rigidification and dimerization. Nature 380, 360-364.
53. Oda, H., Uemura, T., Shiomi, K., Nagafuchi, A., Tsukita, S., and Takeichi, M. (1993). Identification of a Drosophila homologue of α-catenin and its association with the armadillo protein. J. Cell Biol. 121, 1133-1140.
54. Oda, H., Uemura, T., Harada, Y., Iwai, Y., and Takeichi, M. (1994). A Drosophila homolog of cadherin associated with Armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165, 716-726.
55. O'Kane, C., and Gehring, W. (1987). Detection in situ of genomic regulatory elements in Drosophila. Proc. Natl. Acad. Sci. USA 84, 9123-9127.
56. Oyama, T., Kanai, Y., Ochiai, A., Akimoto, S., Oda, T., Yanagihara, T., Nagafuchi, A., Tsukita, S., Shibamoto, S., Ito, F., Takeichi, M., Matsuda, H., and Hirohashi, S. (1995). Atruncated β-catenin disrupts the interaction between E-cadherin and a-catenin: a cause of loss of intercellular adhesiveness in human cancer cell lines. Cancer Res. 54, 6282-6287.
57. Pai, L.-M., Kirkpatrick, C., Blanton, J., Oda, H., Takeichi, M., and Reifer, M. (1996). Drosophila α-catenin and E-cadherin bind to distinct regions of Drosophila Armadillo. J. Biol. Chem. 271, 32411-32420.
58. Patel, N.H., 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.
59. Pearson, W.R., and Lipman, D.J. (1988). Improved tools for biological sequence comparison. Proc. Nat. Acad. Sci. USA 85, 2444-2448.
60. Peifer, M. (1993). The product of the Drosophila segment polarity gene armadillo is part of a multi-protein complex resembling the vertebrate adherens junction. J. Cell Sci. 105, 993-1000.
61. Radice, G.L., Rayburn, H., Matsunami, H., Knudsen, K.A., Takeichi, M., and Hynes, R.O. (1997). Developmental defects in mouse embryos lacking N-cadherin. Dev. Biol. 181, 64-78.
62. Ranscht, B. (1994). Cadherins and catenins: interactions and functions in embryonic development. Curr. Opin. Cell Biol. 6, 740-746.
63. Redies, C. (1995). Cadherin expression in the developing vertebrate CNS: from neuromeres to brain nuclei and neural circuits. Exp. Cell Res. 220, 243-256.
64. Redies, C., and Takeichi, M. (1996). Cadherins in the developing central nervous system: an adhesive code for segmental and functional subdivisions. Dev. Biol. 180, 413-423.
65. Riehl, R., Johnson, K., Bradley, R., Grunwald, G.B., Cornel, E., Lifenbaum, A., and Holt, C.E. (1996). Cadherin function is required for axon outgrowth in retinal ganglion cells in vivo. Neuron 17, 837-848.
66. Sasaki, M., Kleinman, H.K., Huber, H., Deutzmann, R., and Yamada, Y. (1988). Laminin, amultidomain protein. The A chain has a unique globular domain and homology with the basement membrane proteoglycan and the laminin B chains. J. Biol. Chem. 263, 16536-16544.
67. Schneider, T., Reiter, C., Eule, E., Bader, B., Lichte, B., Nie, Z., Schimansky, T., Ramos, R.G.P., and Fischbach, K.-F. (1995). Restricted expression of the irreC-rst protein is required for normal axonal projections of columnar visual neurons. Neuron 15, 259-271.
68. Seeger, M., Tear, G., Ferres-Marco, D., and Goodman, C.S. (1993). Mutations affecting growth coneguidance in Drosophila: genes necessary for guidance toward or away from the midline. Neuron 10, 409-426.
69. Shapiro, I., Fannon, A.M., Kwong, P.D., Thompson, A., Lehmann, M.S., Grubel, G., Legrand, J.F., Als-Nielsen, J., Colman, D.R., and Hendrickson, W.A. (1995). Structural basis of cell-cell adhesion by cadherins. Nature 374, 327.
70. Sone, M., Hoshino, M., Suzuki, E., Kuroda, S., Kaibuchi, K., Kakagoshi, H., Saigo, K., Nabeshima, Y.-I., and Hama, C. (1997). Still life, a protein in synaptic terminals of Drosophila homologous to GDP-GTP exchangers. Science 275, 543-547.
71. Spradling, A.C., Stern, D.M., Kiss, I., Roote, J., Laverty, T., and Rubin, G.M. (1995). Gene disruptions using P transposable elements: an integral component of the Drosophila genome project. Proc. Natl. Acad. Sci. USA 92, 10824-10830.
72. Steward, R., and Nüsslein-Volhard, C. (1986). The genetics of the dorsal-bicaudal-Dregion of Drosophila melanogaster. Genetics 113, 665-678.
73. Takeichi, M. (1991). Cadherin cell adhesion receptors as a morphogenetic regulator. Science 251, 1451-1455.
74. Takeichi, M. (1995). Morphogenetic roles of classic cadherins. Curr. Opin. Cell Biol. 7, 619-627.
75. Tanaka-Matakatsu, M., Uemura, T., Oda, H., Takeichi, M., and Hayashi, S. (1996). Cadherin-mediated cell adhesion and cell motility in Drosophila trachea regulated by the transcription factor Escargot. Development 122, 3697-3705.
76. Tepass, U., and Hartenstein, V. (1994). The development of cellular junctions in the Drosophila embryo. Dev. Biol. 161, 563-596.
77. Tepass, U., Gruszynski-DeFeo, E., Haag, T.A., Omatyar, L., Torok, T., and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neuroectoderm and other morphogenetically activeepithelia. Genes Dev. 10, 672-685.
78. Tessier-Lavigne, M., and Goodman, C.S. (1996). The molecular biology of axon guidance. Science 274, 1123-1133.
79. Thisse, C., and Thisse, B. (1992). Dorsoventral development of the Drosophila embryo is controlled by a cascade of transcriptional regulators. Dev. Suppl. 173-181.
80. Uchida, N., Honjo, Y., Jonson, K.R., Wheelock, M., and Takeichi, M. (1996). The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J. Cell Biol. 135, 767-779.
81. Uemura, T., Oda, H., Kraut, R., Hayashi, S., Kataoka, Y., and Takeichi, M. (1996). Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 10, 659-671.
82. Ushkaryov, Y.A., Petrenko, A.G., Geppert, M., and Südhof, T.C. (1992). Neurexins: synaptic cell surface proteins related to the α-latrotoxin receptor and laminin. Science 257, 50-56.
83. 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.
84. Xiong, W.-C., Okano, H., Patel, N.H., Blendy, J.A., and Montell, C. (1994). repoencodes aglial-specific homeo domain protein required in the Drosophila nervous system. Genes Dev. 8, 981-994.
85. Zinn, K., McAllister, L., and Goodman, C.S. (1988). Sequence analysis and neuronal expression of fasciclin I in grasshopper and Drosophila. Cell. 53, 577-587.