Drosophila E-cadherin and its binding partner Armadillo/ β-catenin are required for axonal pathway choices in the developing larval brain

Developmental Biology

Volumn 332, Issue 2, 2009, Pages 371-382

  Fung, Siaumin ^a   Wang, Fay ^a   Spindler, Shana R ^a   Hartenstein, Volker ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Brain; DE cadherin; Drosophila; Lineage; Pathfinding

Indexed keywords

BETA CATENIN; UVOMORULIN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL CLONE; CELL DIVISION; CELL STRUCTURE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; IMMUNOREACTIVITY; LARVA; NERVE GROWTH; NEUROBLAST; NEUROPIL; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; WILD TYPE;

EID: 67650951125     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2009.06.005     Document Type: Article

References (45)

1. Ashburner M. Drosophila, A Laboratory Manual. New York (1989), Cold Sprint Harbor Laboratory Press
2. Bello B.C., Izergina N., Caussinus E., and Reichert H. Amplification of neural stem cell proliferation by intermediate progenitor cells in Drosophila brain development. Neural. Dev. 19 3 (2008) 5
3. Buff E., Carmena A., Gisselbrecht S., Jimenez F., and Michelson A.M. Signalling by the Drosophila epidermal growth factor receptor is required for the specification and diversification of embryonic muscle progenitors. Development 125 (1998) 2075-2086
4. Chang T., Younossi-Hartenstein A., and Hartenstein V. Development of neural lineages derived from the sine oculis positive eye field of Drosophila. Arthropod. Struct. Dev. 32 (2003) 303-317
5. Dumstrei K., Wang F., Shy D., Tepass U., and Hartenstein V. Interaction between EGFR signaling and DE-cadherin during nervous system morphogenesis. Development 129 (2002) 3983-3994
6. Dumstrei K., Wang F., and Hartenstein V. Role of DE-cadherin in neuroblast proliferation, neural morphogenesis, and axon tract formation in Drosophila larval brain development. J. Neurosci. 23 (2003) 3325-3335
7. Dumstrei K., Wang F., Nassif C., and Hartenstein V. Early development of the Drosophila brain: V. Pattern of postembryonic neuronal lineages expressing DE-cadherin. J. Comp. Neurol. 455 (2003) 451-462
8. Elul T.M., Kimes N.E., Kohwi M., and Reichardt L.F. N-and C-terminal domains of beta-catenin, respectively, are required to initiate and shape axon arbors of retinal ganglion cells in vivo. J. Neurosci. 23 (2003) 6567-6575
9. Fung S., Wang F., Chase M., Godt D., and Hartenstein V. The expression domains the cadherins in the Drosophila larval brain. J. Comp. Neur. 506 (2008) 469-488
10. Fujita S.C., Zipursky S.L., Benzer S., Ferrus A., and Shotwell S.L. Monoclonal antibodies against the Drosophila nervous system. Proc. Natl. Acad. Sci. U. S. A. 79 (1982) 7929-7933
11. Hassan B.A., Bermingham N.A., He Y., Sun Y., Jan Y.N., Zoghbi H.Y., and Bellen H.J. atonal regulates neurite arborization but does not act as a proneural gene in the Drosophila brain. Neuron 25 (2000) 549-561
12. Hayashi T., and Carthew R.W. Surface mechanics mediate pattern formation in the developing retina. Nature 431 (2004) 647-652
13. Hill E., Broadbent I.D., Chothia C., and Pettitt J. Cadherin superfamily proteins in Caenorhabditis elegans and Drosophila melanogaster. J. Mol. Biol. 305 (2001) 1011-1024
14. Hirano S., Suzuki S.T., and Redies C. The cadherin superfamily in neural development: diversity, function and interaction with other molecules. Front. Biosci. 8 (2003) d306-d355
15. Hortsch M., Patel N.H., Bieber A.J., Traquina Z.R., and Goodman C.S. Drosophila neurotactin, a surface glycoprotein with homology to serine esterases, is dynamically expressed during embryogenesis. Development 110 (1990) 1327-1340
16. Hummel T., and Zipursky S.L. Afferent induction of olfactory glomeruli requires N-cadherin. Neuron 42 (2004) 77-88
17. Iwai Y., Usui T., Hirano S., Steward R., Takeichi M., and Uemura T. Axon patterning requires DN-cadherin, a novel neuronal adhesion receptor, in the Drosophila embryonic CNS. Neuron 19 (1997) 77-89
18. Iwai Y., Hirota Y., Ozaki K., Okano H., Takeichi M., and Uemura T. DN-cadherin is required for spatial arrangement of nerve terminals and ultrastructural organization of synapses. Mol. Cell. Neurosci. 19 (2002) 375-388
19. Lee T., and Luo L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22 (1999) 451-461
20. Lee C.H., Herman T., Clandinin T.R., Lee R., and Zipursky S.L. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30 (2001) 437-450
21. Murase S., Mosser E., and Schuman E.M. Depolarization drives beta-catenin into neuronal spines promoting changes in synaptic structure and function. Neuron 35 (2002) 91-105
22. Nassif C., Noveen A., and Hartenstein V. Early development of the Drosophila brain: III. The pattern of neuropile founder tracts during the larval period. J. Comp. Neurol. 455 (2003) 417-434
23. Nollet F., Kools P., and van Roy F. Phylogenetic analysis of the cadherin superfamily allows identification of six major subfamilies besides several solitary members. J. Mol. Biol. 299 (2000) 551-572
24. Oda H., Uemura T., Shiomi K., Nagafuchi A., Tsukita S., and Takeichi M. Identification of a Drosophila homologue of alpha-catenin and its association with the armadillo protein. J. Cell. Biol. 121 (1993) 1133-1140
25. Oda H., Uemura T., Harada Y., Iwai Y., and Takeichi M. A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165 (1994) 716-726
26. Pereanu W., and Hartenstein V. Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 26 (2006) 5534-5553
27. Pereanu, W., Jennett, A., Younossi-Hartenstein, A., Hartenstein, V. (submitted for publication). A development-based compartmentalization of the Drosophila central brain.
28. Prakash S., Caldwell J.C., Eberl D.F., and Clandinin T.R. Drosophila N-cadherin mediates an attractive interaction between photoreceptor axons and their targets. Nat. Neurosci. 8 (2005) 443-450
29. Rasin M.R., Gazula V.R., Breunig J.J., Kwan K.Y., Johnson M.B., Liu-Chen S., Li H.S., Jan L.Y., Jan Y.N., Rakic P., et al. Numb and Numbl are required for maintenance of cadherin-based adhesion and polarity of neural progenitors. Nat. Neurosci. 10 (2007) 819-827
30. Redies C. Cadherins in the central nervous system. Prog. Neurobiol. 61 (2000) 611-648
31. Sanes J.R., and Yamagata M. Formation of lamina-specific synaptic connections. Curr. Opin. Neurobiol. 9 (1999) 79-87
32. Shimizu T., Yabe T., Muraoka O., Yonemura S., Aramaki S., Hatta K., Bae Y.K., Nojima H., and Hibi M. E-cadherin is required for gastrulation cell movements in zebrafish. Mech. Dev. 122 (2005) 747-763
33. Tepass U., Gruszynski-DeFeo E., Haag T.A., Omatyar L., Torok T., and Hartenstein V. Shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10 (1996) 672-685
34. Tepass U., Truong K., Godt D., Ikura M., and Peifer M. Cadherins in embryonic and neural morphogenesis. Nat. Rev. Mol. Cell. Biol. 1 (2000) 91-100
35. Thoumine O., Lambert M., Mege R.M., and Choquet D. Regulation of N-cadherin dynamics at neuronal contacts by ligand binding and cytoskeletal coupling. Mol. Biol. Cell. 17 (2006) 862-875
36. Togashi H., Abe K., Mizoguchi A., Takaoka K., Chisaka O., and Takeichi M. Cadherin regulates dendritic spine morphogenesis. Neuron 35 (2002) 77-89
37. Townes P.L., and Holtfreter J. Directed movement and selective adhesion of embryonic amphibian cells. J. Exp. Zool. 128 (1955) 53-120
38. Urbach R., and Technau G.M. Molecular markers for identified neuroblasts in the developing brain of Drosophila. Development 130 (2003) 3621-3637
39. Wang F., Dumstrei K., Haag T., and Hartenstein V. The role of DE-cadherin during cellularization, germ layer formation and early neurogenesis in the Drosophila embryo. Dev. Biol. 270 (2004) 350-363
40. Williams E.J., Williams G., Howell F.V., Skaper S.D., Walsh F.S., and Doherty P. Identification of an N-cadherin motif that can interact with the fibroblast growth factor receptor and is required for axonal growth. J. Biol. Chem. 276 (2001) 43879-43886
41. Yagi T., and Takeichi M. Cadherin superfamily genes: functions, genomic organization, and neurologic diversity. Genes. Dev. 14 (2000) 1169-1180
42. Yap A.S., and Kovacs E.M. Direct cadherin-activated cell signaling: a view from the plasma membrane. J. Cell. Biol. 160 (2003) 11-16
43. Younossi-Hartenstein A., Nassif C., Green P., and Hartenstein V. Early neurogenesis of the Drosophila brain. J. Comp. Neurol. 370 (1996) 313-329
44. Yu X., and Malenka R.C. Multiple functions for the cadherin/catenin complex during neuronal development. Neuropharmacology 47 (2004) 779-786
45. Zhu H., and Luo L. Diverse functions of N-cadherin in dendritic and axonal terminal arborization of olfactory projection neurons. Neuron 42 (2004) 63-75