A putative tyrosine phosphorylation site of the cell surface receptor golden goal is involved in synaptic layer selection in the visual system

Development

Volumn 139, Issue 4, 2012, Pages 760-771

  Mann, Klaudiusz ^a   Wang, Mengzhe ^a   Luu, Si Hong ^a   Ohler, Stephan ^a   Hakeda Suzuki, Satoko ^a   Suzuki, Takashi ^a  

^a MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

Axon guidance; Drosophila; Gogo; Tyrosine phosphorylation

Indexed keywords

CELL SURFACE PROTEIN; CELL SURFACE RECEPTOR; GOLDEN GOAL PROTEIN; INSULIN RECEPTOR; TRIPEPTIDE; TYROSINE; TYROSINYLTYROSINYLASPARTIC ACID; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DEPHOSPHORYLATION; DROSOPHILA; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; SYNAPSE; SYNAPTIC LAYER SELECTION; VISUAL SYSTEM;

AMINO ACID SEQUENCE; ANIMALS; AXONS; DROSOPHILA MELANOGASTER; EYE PROTEINS; HUMANS; PHOSPHORYLATION; PHOTORECEPTOR CELLS; RECEPTORS, CELL SURFACE; SEQUENCE ALIGNMENT; SYNAPSES; TYROSINE; VISUAL PATHWAYS;

EID: 84862955080     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.074104     Document Type: Article

References (39)

1. Alonso, A., Sasin, J., Bottini, N., Friedberg, I., Osterman, A., Godzik, A., Hunter, T., Dixon, J. and Mustelin, T. (2004). Protein tyrosine phosphatases in the human genome. Cell 117, 699-711.
2. Bashaw, G. J., Kidd, T., Murray, D., Pawson, T. and Goodman, C. S. (2000). Repulsive axon guidance: Abelson and Enabled play opposing roles downstream of the roundabout receptor. Cell 101, 703-715.
3. Bazigou, E., Apitz, H., Johansson, J., Loren, C. E., Hirst, E. M., Chen, P. L., Palmer, R. H. and Salecker, I. (2007). Anterograde Jelly belly and Alk receptor tyrosine kinase signaling mediates retinal axon targeting in Drosophila. Cell 128, 961-975.
4. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
5. Bonner, J. and O'Connor, T. P. (2001). The permissive cue laminin is essential for growth cone turning in vivo. J. Neurosci. 21, 9782-9791.
6. 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.
7. Clandinin, T. R. and Zipursky, S. L. (2002). Making connections in the fly visual system. Neuron 35, 827-841.
8. Clandinin, T. R., Lee, C. H., Herman, T., Lee, R. C., Yang, A. Y., Ovasapyan, S. and Zipursky, S. L. (2001). Drosophila LAR regulates R1-R6 and R7 target specificity in the visual system. Neuron 32, 237-248.
9. Dickson, B. J. (2001). Rho GTPases in growth cone guidance. Curr. Opin. Neurobiol. 11, 103-110.
10. Fang, X., Yu, S. X., Lu, Y., Bast, R. C., Jr, Woodgett, J. R. and Mills, G. B. (2000). Phosphorylation and inactivation of glycogen synthase kinase 3 by protein kinase A. Proc. Natl. Acad. Sci. USA 97, 11960-11965.
11. Fernandez, R., Tabarini, D., Azpiazu, N., Frasch, M. and Schlessinger, J. (1995). The Drosophila insulin receptor homolog: a gene essential for embryonic development encodes two receptor isoforms with different signaling potential. EMBO J. 14, 3373-3384.
12. Garrity, P. A., Rao, Y., Salecker, I., McGlade, J., Pawson, T. and Zipursky, S. L. (1996). Drosophila photoreceptor axon guidance and targeting requires the dreadlocks SH2/SH3 adapter protein. Cell 85, 639-650.
13. Gronke, S., Clarke, D. F., Broughton, S., Andrews, T. D. and Partridge, L. (2010). Molecular evolution and functional characterization of Drosophila insulin-like peptides. PLoS Genet. 6, e1000857.
14. Hakeda-Suzuki, S., Berger-Muller, S., Tomasi, T., Usui, T., Horiuchi, S. Y., Uemura, T. and Suzuki, T. (2011). Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nat. Neurosci. 14, 314-323.
15. Henkemeyer, M., Orioli, D., Henderson, J. T., Saxton, T. M., Roder, J., Pawson, T. and Klein, R. (1996). Nuk controls pathfinding of commissural axons in the mammalian central nervous system. Cell 86, 35-46.
16. Hing, H., Xiao, J., Harden, N., Lim, L. and Zipursky, S. L. (1999). Pak functions downstream of Dock to regulate photoreceptor axon guidance in Drosophila. Cell 97, 853-863.
17. Johansen, J. W. and Ingebritsen, T. S. (1986). Phosphorylation and inactivation of protein phosphatase 1 by pp60v-src. Proc. Natl. Acad. Sci. USA 83, 207-211.
18. Knoll, B. and Drescher, U. (2004). Src family kinases are involved in EphA receptor-mediated retinal axon guidance. J. Neurosci. 24, 6248-6257.
19. Lee, R. C., Clandinin, T. R., Lee, C. H., Chen, P. L., Meinertzhagen, I. A. and Zipursky, S. L. (2003). The protocadherin Flamingo is required for axon target selection in the Drosophila visual system. Nat. Neurosci. 6, 557-563.
20. Lin, A. N., Barnes, S. and Wallace, R. W. (1990). Phosphorylation by protein kinase C inactivates an inositol 1,4,5-trisphosphate 3-kinase purified from human platelets. Biochem. Biophys. Res. Commun. 170, 1371-1376.
21. Liu, G., Beggs, H., Jurgensen, C., Park, H. T., Tang, H., Gorski, J., Jones, K. R., Reichardt, L. F., Wu, J. and Rao, Y. (2004). Netrin requires focal adhesion kinase and Src family kinases for axon outgrowth and attraction. Nat. Neurosci. 7, 1222-1232.
22. Longo, N., Shuster, R. C., Griffin, L. D., Langley, S. D. and Elsas, L. J. (1992). Activation of insulin receptor signaling by a single amino acid substitution in the transmembrane domain. J. Biol. Chem. 267, 12416-12419.
23. Maher, P. A. and Pasquale, E. B. (1988). Tyrosine phosphorylated proteins in different tissues during chick embryo development. J. Cell Biol. 106, 1747-1755.
24. Maurel-Zaffran, C., Suzuki, T., Gahmon, G., Treisman, J. E. and Dickson, B. J. (2001). Cell-autonomous and -nonautonomous functions of LAR in R7 photoreceptor axon targeting. Neuron 32, 225-235.
25. Newsome, T. P., Asling, B. and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
26. Ohler, S., Hakeda-Suzuki, S. and Suzuki, T. (2011). Hts, the Drosophila homologue of Adducin, physically interacts with the transmembrane receptor Golden goal to guide photoreceptor axons. Dev. Dyn. 240, 135-148.
27. Rulifson, E. J., Kim, S. K. and Nusse, R. (2002). Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296, 1118-1120.
28. Sanes, J. R. and Zipursky, S. L. (2010). Design principles of insect and vertebrate visual systems. Neuron 66, 15-36.
29. Saucedo, L. J. and Edgar, B. A. (2007). Filling out the Hippo pathway. Nat. Rev. Mol. Cell Biol. 8, 613-621.
30. Senti, K. A., Usui, T., Boucke, K., Greber, U., Uemura, T. and Dickson, B. J. (2003). Flamingo regulates R8 axon-axon and axon-target interactions in the Drosophila visual system. Curr. Biol. 13, 828-832.
31. Shinza-Kameda, M., Takasu, E., Sakurai, K., Hayashi, S. and Nose, A. (2006). Regulation of layer-specific targeting by reciprocal expression of a cell adhesion molecule, capricious. Neuron 49, 205-213.
32. Song, J., Wu, L., Chen, Z., Kohanski, R. A. and Pick, L. (2003). Axons guided by insulin receptor in Drosophila visual system. Science 300, 502-505.
33. Tarrant, M. K. and Cole, P. A. (2009). The chemical biology of protein phosphorylation. Annu. Rev. Biochem. 78, 797-825.
34. Ting, C. Y., Yonekura, S., Chung, P., Hsu, S. N., Robertson, H. M., Chiba, A. and Lee, C. H. (2005). Drosophila N-cadherin functions in the first stage of the two-stage layer-selection process of R7 photoreceptor afferents. Development 132, 953-963.
35. Tomasi, T., Hakeda-Suzuki, S., Ohler, S., Schleiffer, A. and Suzuki, T. (2008). The transmembrane protein Golden goal regulates R8 photoreceptor axon-axon and axon-target interactions. Neuron 57, 691-704.
36. Wu, J. S. and Luo, L. (2006). A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat. Protoc. 1, 2110-2115.
37. Wu, Q., Zhang, Y., Xu, J. and Shen, P. (2005). Regulation of hunger-driven behaviors by neural ribosomal S6 kinase in Drosophila. Proc. Natl. Acad. Sci. USA 102, 13289-13294.
38. Xia, F., Li, J., Hickey, G. W., Tsurumi, A., Larson, K., Guo, D., Yan, S. J., Silver Morse, L. and Li, W. X. (2008). Raf activation is regulated by tyrosine 510 phosphorylation in Drosophila. PLoS Biol. 6, e128.
39. Zang, M., Gong, J., Luo, L., Zhou, J., Xiang, X., Huang, W., Huang, Q., Luo, X., Olbrot, M., Peng, Y. et al. (2008). Characterization of Ser338 phosphorylation for Raf-1 activation. J. Biol. Chem. 283, 31429-31437.