Respective roles of the DRL receptor and its ligand WNT5 in Drosophila mushroom body development

Development

Volumn 134, Issue 17, 2007, Pages 3089-3097

  Grillenzoni, Nicola ^a   Flandre, Adrien ^a   Lasbleiz, Christelle ^a   Dural, Jean Maurice ^a  

^a INSTITUTE OF HUMAN GENETICS   (France)

Author keywords

Brain development; Derailed (linotte); Developmental genetics; Drosophila; Mushroom body; Receptor tyrosine kinase; Ryk ortholog; Wnt5 signaling

Indexed keywords

DERAILED RECEPTOR TYROSINE KINASE; LIGAND; PROTEIN TYROSINE KINASE; UNCLASSIFIED DRUG; WNT PROTEIN; WNT5 PROTEIN;

ARTICLE; BRAIN DEVELOPMENT; CELL TYPE; CENTRAL NERVOUS SYSTEM; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GLIA CELL; IMAGE PROCESSING; IMMUNOHISTOCHEMISTRY; MICROSCOPY; MOLECULAR CLONING; NERVE CELL; NERVE FIBER GROWTH; NONHUMAN; PHYSICAL DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN INTERACTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CLONE CELLS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; MUSHROOM BODIES; PROTO-ONCOGENE PROTEINS; RECEPTOR PROTEIN-TYROSINE KINASES; WNT PROTEINS;

BASIDIOMYCOTA;

EID: 34848850420     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.02876     Document Type: Article

References (40)

1. Adachi, Y., Hauck, B., Clements, J., Kawauchi, H., Kurusu, M., Totani, Y., Kang, Y. Y., Eggert, T., Walldorf, U., Furukubo-Tokunaga, K. et al. (2003). Conserved cis-regulatory modules mediate complex neural expression patterns of the eyeless gene in the Drosophila brain. Mech. Dev. 120, 1113-1126.
2. Bonkowsky, J. L. and Thomas, J. B. (1999). Cell-type specific modular regulation of derailed in the Drosophila nervous system. Mech. Dev. 82, 181-184.
3. Bonkowsky, J. L., Yoshikawa, S., O'Keefe, D. D., Scully, A. L. and Thomas, J. B. (1999). Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature 402, 540-544.
4. Callahan, C. A., Muralidhar, M. G., Lundgren, S. E., Scully, A. L. and Thomas, J. B. (1995). Control of neuronal pathway selection by a Drosophila receptor protein-tyrosine kinase family member. Nature 376, 171-174.
5. Callahan, C. A., Bonkovsky, J. L., Scully, A. L. and Thomas, J. B. (1996). derailed is required for muscle attachment site selection in Drosophila. Development 122, 2761-2767.
6. Connolly, J. B., Roberts, I. J., Armstrong, J. D., Kaiser, K., Forte, M., Tully, T. and O'Kane, C. J. (1996). Associative learning disrupted by impaired Gs signaling in Drosophila mushroom bodies. Science 274, 2104-2107.
7. de Belle, J. S. and Heisenberg, M. (1994). Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263, 692-695.
8. Dura, J. M., Preat, T. and Tully, T. (1993). Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9, 1-14.
9. Dura, J. M., Taillebourg, E. and Preat, T. (1995). The Drosophila learning and memory gene linotte encodes a putative receptor tyrosine kinase homologous to the human RYK gene product. FEBS Lett. 370, 250-254.
10. Ferveur, J. F., Stortkuhl, K. F., Stocker, R. F. and Greenspan, R. J. (1995). Genetic feminization of brain structures and changed sexual orientation in male Drosophila. Science 267, 902-905.
11. Fradkin, L. G., van Schie, M., Wouda, R. R., de Jong, A., Kamphorst, J. T., Radjkoemar-Bansraj, M. and Noordermeer, J. N. (2004). The Drosophila Wnt5 protein mediates selective axon fasciculation in the embryonic central nervous system. Dev. Biol. 272, 362-375.
12. Fradkin, L. G., Garriga, G., Salinas, P. C., Thomas, J. B., Yu, X. and Zou, Y. (2005). Wnt signaling in neural circuit development. J. Neurosci. 25, 10376-10378.
13. Halford, M. M., Oates, A. C., Hibbs, M. L., Wilks, A. F. and Stacker, S. A. (1999), Genomic structure and expression of the mouse growth factor receptor related to tyrosine kinases (Ryk). J. Biol. Chem. 274, 7379-7390.
14. Heisenberg, M., Borst, A., Wagner, S. and Byers, D. (1985). Drosophila mushroom body mutants are deficient in olfactory learning. J. Neurogenet. 2, 1-30.
15. Hitier, R., France Simon, A., Savarit, F. and Preat, T. (2000). no-bridge and linotte act jointly at the interhemispheric junction to build up the adult central brain of Drosophila melanogaster. Mech. Dev. 99, 93-100.
16. Hovens, C. M., Stacker, S. A., Andres, A. C., Harpur, A. G., Ziemiecki, A. and Wilks, A. F. (1992). RYK, a receptor tyrosine kinase-related molecule with unusual kinase domain motifs. Proc. Natl. Acad. Sci. USA 89, 11818-11822.
17. Ito, K., Suzuki, K., Estes, P., Ramaswami, M., Yamamoto, D. and Strausfeld, N. J. (1998). The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn. Mem. 5, 52-77.
18. Keeble, T. R., Halford, M. M., Seaman, C., Kee, N., Macheda, M., Anderson, R. B., Stacker, S. A. and Cooper, H. M. (2006). The Wnt receptor Ryk is required for Wnt5a-mediated axon guidance on the contralateral side of the corpus callosum. J. Neurosci. 26, 5840-5848.
19. Kurusu, M., Awasaki, T., Masuda-Nakagawa, L. M., Kawauchi, H., Ito, K. and Furukubo-Tokunaga, K. (2002). Embryonic and larval development of the Drosophila mushroom bodies: concentric layer subdivisions and the role of fasciclin II. Development 129, 409-419.
20. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
21. Lee, T., Lee, A. and Luo, L. (1999). Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126, 4065-4076.
22. Lee, T., Winter, C., Marticke, S. S., Lee, A. and Luo, L. (2000). Essential roles of Drosophila RhoA in the regulation of neuroblast proliferation and dendritic but not axonal morphogenesis. Neuron 25, 307-316.
23. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
24. Lu, W., Yamamoto, V., Ortega, B. and Baltimore, D. (2004). Mammalian Ryk is a Wnt coreceptor required for stimulation of neurite outgrowth. Cell 119, 97-108.
25. Moreau-Fauvarque, C., Taillebourg, E., Boissoneau, E., Mesnard, J. and Dura, J. M. (1998). The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech. Dev. 78, 47-61.
26. Moreau-Fauvarque, C., Taillebourg, E., Preat, T. and Dura, J. M. (2002). Mutation of linotte causes behavioral defects independently of pigeon in Drosophila. NeuroReport 13, 2309-2312.
27. Ng, J., Nardine, T., Harms, M., Tzu, J., Goldstein, A., Sun, Y., Dietzl, G., Dickson, B. J. and Luo, L. (2002). Rac GTPases control axon growth, guidance and branching. Nature 416, 442-447.
28. Nicolai, M., Lasbleiz, C. and Dura, J. M. (2003). Gain-of-function screen identifies a role of the Src64 oncogene in Drosophila mushroom body development. J. Neurobiol. 57, 291-302.
29. Noveen, A., Daniel, A. and Hartenstein, V. (2000). Early development of the Drosophila mushroom body: the roles of eyeless and dachshund. Development 127, 3475-3488.
30. Patel, N. H. (1994). Imaging neuronal subsets and other cell types in whole-mount Drosophila embryos and larvae using antibody probes. Methods Cell Biol. 44, 445-487.
31. Reuter, J. E., Nardine, T. M., Penton, A., Billuart, P., Scott, E. K., Usui, T., Uemura, T. and Luo, L. (2003). A mosaic genetic screen for genes necessary for Drosophila mushroom body neuronal morphogenesis. Development 130, 1203-1213.
32. Simon, A. F., Boquet, I., Synguelakis, M. and Preat, T. (1998). The Drosophila putative kinase linotte (derailed) prevents central brain axons from converging on a newly described interhemispheric ring. Mech. Dev. 76, 45-55.
33. Srahna, M., Leyssen, M., Choi, C. M., Fradkin, L. G., Noordermeer, J. N. and Hassan, B. A. (2006). A signaling network for patterning of neuronal connectivity in the Drosophila brain. PLoS Biol. 4, e348.
34. Strausfeld, N. J., Sinakevitch, I. and Vilinsky, I. (2003). The mushroom bodies of Drosophila melanogaster: an immunocytological and golgi study of Kenyon cell organization in the calyces and lobes. Microsc. Res. Tech. 62, 151-169.
35. Taillebourg, E., Moreau-Fauvarque, C., Delaval, K. and Dura, J. M. (2005). In vivo evidence for a regulatory role of the kinase activity of the linotte/derailed receptor tyrosine kinase, a Drosophila Ryk ortholog. Dev. Genes Evol. 215, 158-163.
36. Tettamanti, M., Armstrong, J. D., Endo, K., Yang, M. Y., Furukubo-Tokunaga, K., Kaiser, K. and Reichert, H. (1997). Early development of the Drosophila mushroom bodies, brain centres for associative learning and memory. Dev. Genes Evol. 207, 242-252.
37. Wang, J., Zugates, C. T., Liang, I. H., Lee, C. H. and Lee, T. (2002). Drosophila Dscam is required for divergent segregation of sister branches and suppresses ectopic bifurcation of axons. Neuron 33, 559-571.
38. Yang, M. Y., Armstrong, J. D., Vilinsky, I., Strausfeld, N. J. and Kaiser K. (1995). Subdivision of the Drosophila mushroom bodies by enhancer-trap expression patterns. Neuron 15, 45-54.
39. Yoshikawa, S., McKinnon, R. D., Kokel, M. and Thomas, J. B. (2003). Wnt-mediated axon guidance via the Drosophila Derailed receptor. Nature 422, 583-588.
40. Zars, T., Fischer, M., Schulz, R. and Heisenberg, M. (2000). Localization of a short-term memory in Drosophila. Science 288, 672-675.