Golden goal collaborates with flamingo in conferring synaptic-layer specificity in the visual system

Nature Neuroscience

Volumn 14, Issue 3, 2011, Pages 314-323

  Hakeda Suzuki, Satoko ^a   Berger Müller, Sandra ^a   Tomasi, Tatiana ^a   Usui, Tadao ^b   Horiuchi, Shin Ya ^b   Uemura, Tadashi ^b,c   Suzuki, Takashi ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

^b KYOTO UNIVERSITY   (Japan)

^c JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FLAMINGO PROTEIN; GOLD GOAL PROTEIN; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; CELL CONTACT; CONTROLLED STUDY; CYTOPLASM; NERVE CELL DIFFERENTIATION; NERVE FIBER; PHOTORECEPTOR; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; STRUCTURE ACTIVITY RELATION; SYNAPSE; VISUAL SYSTEM;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; AXONS; CADHERINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE PROTEINS; NEURAL PATHWAYS; PHENOTYPE; PHOTORECEPTOR CELLS, INVERTEBRATE; RECEPTORS, CELL SURFACE; SYNAPSES;

EID: 79952008315     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2756     Document Type: Article

References (47)

1. Luo, L. & Flanagan, J.G. Development of continuous and discrete neural maps. Neuron 56, 284-300 (2007).
2. Huberman, A.D., Clandinin, T.R. & Baier, H. Molecular and cellular mechanisms of lamina-specific axon targeting. Cold Spring Harb. Perspect. Biol. 2, a001743 (2010).
3. Sanes, J.R. & Zipursky, S.L. Design principles of insect and vertebrate visual systems. Neuron 66, 15-36 (2010).
4. Sanes, J.R. & Yamagata, M. Many paths to synaptic specificity. Annu. Rev. Cell Dev. Biol. 25, 161-195 (2009).
5. Yamagata, M. & Sanes, J.R. Dscam and Sidekick proteins direct lamina-specific synaptic connections in vertebrate retina. Nature 451, 465-469 (2008).
6. Yamagata, M., Weiner, J.A. & Sanes, J.R. Sidekicks: synaptic adhesion molecules that promote lamina-specific connectivity in the retina. Cell 110, 649-660 (2002).
7. Ting, C.Y. & Lee, C.H. Visual circuit development in Drosophila. Curr. Opin. Neurobiol. 17, 65-72 (2007).
8. Mast, J.D., Prakash, S., Chen, P.L. & Clandinin, T.R. The mechanisms and molecules that connect photoreceptor axons to their targets in Drosophila. Semin. Cell Dev. Biol. 17, 42-49 (2006).
9. Astigarraga, S., Hofmeyer, K. & Treisman, J.E. Missed connections: photoreceptor axon seeks target neuron for synaptogenesis. Curr. Opin. Genet. Dev. 20, 400-407 (2010).
10. Lee, C.H., Herman, T., Clandinin, T.R., Lee, R. & Zipursky, S.L. N-cadherin regulates target specificity in the Drosophila visual system. Neuron 30, 437-450 (2001).
11. Berger, J. et al. Systematic identification of genes that regulate neuronal wiring in the Drosophila visual system. PLoS Genet. 4, e1000085 (2008).
12. Maurel-Zaffran, C., Suzuki, T., Gahmon, G., Treisman, J.E. & Dickson, B.J. Cellautonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32, 225-235 (2001).
13. Clandinin, T.R. et al. Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32, 237-248 (2001).
14. Garrity, P.A. et al. Retinal axon target selection in Drosophila is regulated by a receptor protein tyrosine phosphatase. Neuron 22, 707-717 (1999).
15. Newsome, T.P., Asling, B. & Dickson, B.J. Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860 (2000).
16. Shinza-Kameda, M., Takasu, E., Sakurai, K., Hayashi, S. & Nose, A. Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 49, 205-213 (2006).
17. Shishido, E., Takeichi, M. & Nose, A. Drosophila synapse formation: regulation by transmembrane protein with Leu-rich repeats, CAPRICIOUS. Science 280, 2118-2121 (1998).
18. Tomasi, T., Hakeda-Suzuki, S., Ohler, S., Schleiffer, A. & Suzuki, T. The transmembrane protein Golden goal regulates R8 photoreceptor axon-axon and axon-target interactions. Neuron 57, 691-704 (2008).
19. Lee, R.C. et al. The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat. Neurosci. 6, 557-563 (2003).
20. Senti, K.A. et al. Flamingo regulates R8 axon-axon and axon-target interactions in the Drosophila visual system. Curr. Biol. 13, 828-832 (2003).
21. Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595 (1999).
22. Gao, F.B., Kohwi, M., Brenman, J.E., Jan, L.Y. & Jan, Y.N. Control of dendritic field formation in Drosophila: the roles of flamingo and competition between homologous neurons. Neuron 28, 91-101 (2000).
23. Chen, P.L. & Clandinin, T.R. The cadherin Flamingo mediates level-dependent interactions that guide photoreceptor target choice in Drosophila. Neuron 58, 26-33 (2008).
24. McGuire, S.E., Mao, Z. & Davis, R.L. Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci. STKE 2004, pl6 (2004).
25. Vladar, E.K., Antic, D. & Axelrod, J.D. Planar cell polarity signaling: the developing cell's compass. Cold Spring Harb. Perspect. Biol. 1, a002964 (2009).
26. Ting, C.Y. et al. Drosophila N-cadherin functions in the first stage of the two-stage layerselection process of R7 photoreceptor afferents. Development 132, 953-963 (2005).
27. Kimura, H., Usui, T., Tsubouchi, A. & Uemura, T. Potential dual molecular interaction of the Drosophila 7-pass transmembrane cadherin Flamingo in dendritic morphogenesis. J. Cell Sci. 119, 1118-1129 (2006).
28. Chen, W.S. et al. Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133, 1093-1105 (2008).
29. Strutt, H. & Strutt, D. Differential stability of flamingo protein complexes underlies the establishment of planar polarity. Curr. Biol. 18, 1555-1564 (2008).
30. Keleman, K. & Dickson, B.J. Short- and long-range repulsion by the Drosophila Unc5 netrin receptor. Neuron 32, 605-617 (2001).
31. Bazigou, E. et al. Anterograde Jelly belly and Alk receptor tyrosine kinase signaling mediates retinal axon targeting in Drosophila. Cell 128, 961-975 (2007).
32. Struhl, G. & Basler, K. Organizing activity of wingless protein in Drosophila. Cell 72, 527-540 (1993).
33. Saka, Y., Hagemann, A.I. & Smith, J.C. Visualizing protein interactions by bimolecular fluorescence complementation in Xenopus. Methods 45, 192-195 (2008).
34. Gajadhar, A. & Guha, A. A proximity ligation assay using transiently transfected, epitope-tagged proteins: application for in situ detection of dimerized receptor tyrosine kinases. Biotechniques 48, 145-152 (2010).
35. Shima, Y. et al. Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat. Neurosci. 10, 963-969 (2007).
36. Shima, Y., Kengaku, M., Hirano, T., Takeichi, M. & Uemura, T. Regulation of dendritic maintenance and growth by a mammalian 7-pass transmembrane cadherin. Dev. Cell 7, 205-216 (2004).
37. Grueber, W.B., Jan, L.Y. & Jan, Y.N. Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129, 2867-2878 (2002).
38. Nern, A., Zhu, Y. & Zipursky, S.L. Local N-cadherin interactions mediate distinct steps in the targeting of lamina neurons. Neuron 58, 34-41 (2008).
39. Takemura, S.Y., Lu, Z. & Meinertzhagen, I.A. Synaptic circuits of the Drosophila optic lobe: the input terminals to the medulla. J. Comp. Neurol. 509, 493-513 (2008).
40. Morante, J. & Desplan, C. The color-vision circuit in the medulla of Drosophila. Curr. Biol. 18, 553-565 (2008).
41. Fan, Y. et al. The egghead gene is required for compartmentalization in Drosophila optic lobe development. Dev. Biol. 287, 61-73 (2005).
42. Tree, D.R. et al. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381 (2002).
43. Clandinin, T.R. & Zipursky, S.L. Afferent growth cone interactions control synaptic specificity in the Drosophila visual system. Neuron 28, 427-436 (2000).
44. Strutt, D.I. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367-375 (2001).
45. Thibault, S.T. et al. A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287 (2004).
46. Lee, T. & Luo, L. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461 (1999).
47. Wu, J.S. & Luo, L. A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat. Protoc. 1, 2110-2115 (2006).