Echinoid regulates Flamingo endocytosis to control ommatidial rotation in the Drosophila eye

Development

Volumn 137, Issue 5, 2010, Pages 745-754

  Ho, Yu Huei ^a   Lien, Mong Ting ^a   Lin, Chiao Ming ^a   Wei, Shu Yi ^a   Chang, Li Hsun ^a   Hsu, Jui Chou ^a,b  

^a NATIONAL TSING HUA UNIVERSITY   (Taiwan)

^b NATIONAL CHIAO TUNG UNIVERSITY   (Taiwan)

Author keywords

Adherensjunction; Cell adhesion; DE cadherin (Shotgun); Drosophila; Echinoid; Endocytosis; Flamingo (Starry night); Frizzled; Planar cell polarity

Indexed keywords

CELL ADHESION MOLECULE; CLATHRIN; ECHINOID PROTEIN; FLAMINGO PROTEIN; TRANSCRIPTION FACTOR AP 2; UNCLASSIFIED DRUG;

ANIMAL TISSUE; ARTICLE; CELL MEMBRANE; CONTROLLED STUDY; ENDOCYTOSIS; EYE DEVELOPMENT; HISTOLOGY; IMMUNOHISTOCHEMISTRY; INSECT GENETICS; INTERNALIZATION; NONHUMAN; PHOTORECEPTOR; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CADHERINS; CELL ADHESION MOLECULES; CELL POLARITY; DROSOPHILA; DROSOPHILA PROTEINS; ENDOCYTOSIS; EYE; RECEPTOR, EPIDERMAL GROWTH FACTOR; RECEPTORS, INVERTEBRATE PEPTIDE; REPRESSOR PROTEINS;

ECHINOIDA;

EID: 76449094876     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.040238     Document Type: Article

References (56)

1. Adler, P. N., Charlton, J. and Liu, J. (1998). Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering Frizzled signaling. Development 125, 959-968.
2. Ahmed, A., Chandra, S., Magarinos, M. and Vaessin, H. (2003). Echinoid mutants exhibit neurogenic phenotypes and show synergistic interactions with the Notch signaling pathway. Development 130, 6295-6304.
3. Axelrod, J. D., Miller, J. R., Shulman, J. M., Moon, R. T. and Perrimon, N. (1998). Differential recruitment of Dishevelled provides signaling specificity in the planar cell polarity and Wingless signaling pathways. Genes Dev. 12, 2610-2622.
4. Bai, J., Chiu, W., Wang, J., Tzeng, T., Perrimon, N. and Hsu, J. (2001). The cell adhesion molecule Echinoid defines a new pathway that antagonizes the Drosophila EGF receptor signaling pathway. Development 128, 591-601.
5. Bastock, R. and Strutt, D. (2007). The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development 134, 3055-3064.
6. Brown, K. E. and Freeman, M. (2003). Egfr signalling defines a protective function for ommatidial orientation in the Drosophila eye. Development 130, 5401-5412.
7. Brown, K. E., Baonza, A. and Freeman, M. (2006). Epithelial cell adhesion in the developing Drosophila retina is regulated by Atonal and the EGF receptor pathway. Dev. Biol. 300, 710-721.
8. Chae, J., Kim, M. J., Goo, J. H., Collier, S., Gubb, D., Charlton, J., Adler, P. N. and Park, W. J. (1999). The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126, 5421-5429.
9. Chang, W. L., Liou, W., Pen, H. C., Chou, H. Y., Chang, Y. W., Li, W. H., Chiang, W. and Pai, L. M. (2008). The gradient of Gurken, a long-range morphogen, is directly regulated by Cbl-mediated endocytosis. Development 135, 1923-1933.
10. Chen, M. S., Obar, R. A., Schroeder, C. C., Austin, T. W., Poodry, C. A., Wadsworth, S. C. and Vallee, R. B. (1991). Multiple forms of dynamin are encoded by shibire, a Drosophila gene involved in endocytosis. Nature 351, 583-586.
11. Cooper, M. T. and Bray, S. J. (1999). Frizzled regulation of Notch signalling polarizes cell fate in the Drosophila eye. Nature 397, 526-530.
12. Das, G., Reynolds-Kenneally, J. and Mlodzik, M. (2002). The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye. Dev. Cell 2, 655-666.
13. Entchev, E. V., Schwabedissen, A. and Gonzalez-Gaitan, M. (2000). Gradient formation of the TGF-beta homolog Dpp. Cell 103, 981-991.
14. Escudero, L. M., Wei, S. Y., Chiu, W. H., Modolell, J. and Hsu, J. C. (2003). Echinoid synergizes with the Notch signaling pathway in Drosophila mesothorax bristle patterning. Development 130, 6305-6316.
15. Fanto, M. and Mlodzik, M. (1999). Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397, 523-526.
16. Fetting, J. L., Spencer, S. A. and Wolff, T. (2009). The cell adhesion molecules Echinoid and Friend of Echinoid coordinate cell adhesion and cell signaling to regulate the fidelity of ommatidial rotation in the Drosophila eye. Development 136, 3323-3333.
17. Fiehler, R. W. and Wolff, T. (2007). Drosophila myosin II, Zipper, is essential for ommatidial rotation. Dev. Biol. 310, 348-362.
18. Fiehler, R. W. and Wolff, T. (2008). Nemo is required in a subset of photoreceptors to regulate the speed of ommatidial rotation. Dev. Biol. 313, 533-544.
19. Freeman, M. (1996). Reiterative use of the EGF receptor triggers differentiation of all cell types in the Drosophila eye. Cell 87, 651-660.
20. Gaengel, K. and Mlodzik, M. (2003). Egfr signaling regulates ommatidial rotation and cell motility in the Drosophila eye via MAPK/Pnt signaling and the Ras effector Canoe/AF6. Development 130, 5413-5423.
21. Hacohen, N., Kramer, S., Sutherland, D., Hiromi, Y. and Krasnow, M. A. (1998). sprouty encodes a novel antagonist of FGF signaling that patterns apical branching of the Drosophila airways. Cell 92, 253-263.
22. Hayashi, T. and Carthew, R. W. (2004). Surface mechanics mediate pattern formation in the developing retina. Nature 431, 647-652.
23. Hicke, L. and Dunn, R. (2003). Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu. Rev. Cell Dev. Biol. 19, 141-172.
24. Islam, R., Wei, S. Y., Chiu, W. H., Hortsch, M. and Hsu, J. C. (2003). Neuroglian activates Echinoid to antagonize the Drosophila EGF receptor signaling pathway. Development 130, 2051-2059.
25. Ito, K., Awano, W., Suzuki, K., Hiromi, Y. and Yamamoto, D. (1997). The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurones and glial cells. Development 124, 761-771.
26. Kimura, H., Usui, T., Tsubouchi, A. and Uemura, T. (2006). Potential dual molecular interaction of the Drosophila 7-pass transmembrane cadherin Flamingo in dendritic morphogenesis. J. Cell Sci. 119, 1118-1129.
27. Klein, T. J. and Mlodzik, M. (2005). Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell Dev. Biol. 21, 155-176.
28. Lin, H. P., Chen, H. M., Wei, S. Y., Chen, L. Y., Chang, L. H., Sun, Y. J., Huang, S. Y. and Hsu, J. C. (2007). Cell adhesion molecule Echinoid associates with unconventional myosin VI/Jaguar motor to regulate cell morphology during dorsal closure in Drosophila. Dev. Biol. 311, 423-433.
29. Littleton, J. T. and Bellen, H. J. (1994). Genetic and phenotypic analysis of thirteen essential genes in cytological interval 22F1-2; 23B1-2 reveals novel genes required for neural development in Drosophila. Genetics 138, 111-123.
30. 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 cadherin gene superfamily. Cell 67, 853-868.
31. Mirkovic, I. and Mlodzik, M. (2006). Cooperative activities of drosophila DE-cadherin and DN-cadherin regulate the cell motility process of ommatidial rotation. Development 133, 3283-3293.
32. Mlodzik, M. (2002). Planar cell polarization: do the same mechanisms regulate Drosophila tissue polarity and vertebrate gastrulation? Trends Genet. 18, 564-571.
33. Newsome, T. P., Asling, B. and Dickson, B. J. (2000). Analysis of Drosophila photoreceptor axon guidance in eye-specific mosaics. Development 127, 851-860.
34. Oda, H. and Tsukita, S. (2001). Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 114, 493-501.
35. Rawlins, E. L., White, N. M. and Jarman, A. P. (2003a). Echinoid limits R8 photoreceptor specification by inhibiting inappropriate EGF receptor signalling within R8 equivalence groups. Development 130, 3715-3724.
36. Rawlins, E. L., Lovegrove, B. and Jarman, A. P. (2003b). Echinoid facilitates Notch pathway signalling during Drosophila neurogenesis through functional interaction with Delta. Development 130, 6475-6484.
37. Rawls, A. S. and Wolff, T. (2003). Strabismus requires Flamingo and Prickle function to regulate tissue polarity in the Drosophila eye. Development 130, 1877-1887.
38. Robinson, M. S. (2004). Adaptable adaptors for coated vesicles. Trends Cell Biol. 14, 167-174.
39. Sanson, B., White, P. and Vincent, J. P. (1996). Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 383, 627-630.
40. Seto, E. S., Bellen, H. J. and Lloyd, T. E. (2002). When cell biology meets development: endocytic regulation of signaling pathways. Genes Dev. 16, 1314-1336.
41. Spencer, S. A. and Cagan, R. L. (2003). Echinoid is essential for regulation of Egfr signaling and R8 formation during Drosophila eye development. Development 130, 3725-3733.
42. Stowers, R. S. and Schwarz, T. L. (1999). A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152, 1631-1639.
43. Strutt, D. (2003). Frizzled signalling and cell polarisation in Drosophila and vertebrates. Development 130, 4501-4513.
44. Strutt, D., Johnson, R., Cooper, K. and Bray, S. (2002). Asymmetric localization of Frizzled and the determination of Notch-dependent cell fate in the Drosophila eye. Curr. Biol. 12, 813-824.
45. Strutt, H. and Strutt, D. (2003). EGF signaling and ommatidial rotation in the Drosophila eye. Curr. Biol. 13, 1451-1457.
46. Strutt, H. and Strutt, D. (2008). Differential stability of Flamingo protein complexes underlies the establishment of planar polarity. Curr. Biol. 18, 1555-1564.
47. Strutt, H., Price, M. A. and Strutt, D. (2006). Planar polarity is positively regulated by casein kinase Iepsilon in Drosophila. Curr. Biol. 16, 1329-1336.
48. Tomlinson, A. and Struhl, G. (1999). Decoding vectorial information from a gradient: sequential roles of the receptors Frizzled and Notch in establishing planar polarity in the Drosophila eye. Development 126, 5725-5738.
49. Usui, T., Shima, Y., Shimada, Y., Hirano, S., Burgess, R. W., Schwarz, T. L., Takeichi, M. and Uemura, T. (1999). Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595.
50. van der Bliek, A. M. and Meyerowitz, E. M. (1991). Dynamin-like protein encoded by the Drosophila shibire gene associated with vesicular traffic. Nature 351, 411-414.
51. Waddell, S., Armstrong, J. D., Kitamoto, T., Kaiser, K. and Quinn, W. G. (2000). The amnesiac gene product is expressed in two neurons in the Drosophila brain that are critical for memory. Cell 103, 805-813.
52. Wei, S. Y., Escudero, L. M., Yu, F., Chang, L. H., Chen, L. Y., Ho, Y. H., Lin, C. M., Chou, C. S., Chia, W., Modolell, J. et al. (2005). Echinoid is a component of adherens junctions that cooperates with DE-cadherin to mediate cell adhesion. Dev. Cell 8, 493-504.
53. Wolff, T. and Ready, D. F. (1993). Pattern formation in Drosophila retina. In The Development of Drosophila melanogaster (ed. M. Bate and A. Martinez-Arias), pp. 1277-1325. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
54. Wucherpfennig, T., Wilsch-Brauninger, M. and Gonzalez-Gaitan, M. (2003). Role of Drosophila Rab5 during endosomal trafficking at the synapse and evoked neurotransmitter release. J. Cell Biol. 161, 609-624.
55. Yang, C. H., Axelrod, J. D. and Simon, M. A. (2002). Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108, 675-688.
56. Zheng, L., Zhang, J. and Carthew, R. W. (1995). frizzled regulates mirrorsymmetric pattern formation in the Drosophila eye. Development 121, 3045-3055.