The frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2

Development (Cambridge)

Volumn 140, Issue 5, 2013, Pages 1045-1054

  Warrington, Samantha J ^a   Strutt, Helen ^a   Strutt, David ^a  

^a UNIVERSITY OF SHEFFIELD   (United Kingdom)

Author keywords

E cadherin; Morphogenesis; Planar polarity

Indexed keywords

FRIZZLED PROTEIN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; UVOMORULIN;

ARTICLE; CELL POLARITY; CONTROLLED STUDY; ENDOTRACHEAL TUBE; ENZYME ACTIVITY; EPIDERMIS; FORELIMB; INSECT DEVELOPMENT; MORPHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; BODY PATTERNING; CADHERINS; CELL POLARITY; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; FRIZZLED RECEPTORS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOLYSIS; RHO GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; TRACHEA;

EID: 84873721893     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.088724     Document Type: Article

References (51)

1. Affolter, M., Zeller, R. and Caussinus, E. (2009). Tissue remodelling through branching morphogenesis. Nat. Rev. Mol. Cell Biol. 10, 831-842.
2. Aigouy, B., Farhadifar, R., Staple, D. B., Sagner, A., Röper, J.-C., Jülicher, F. and Eaton, S. (2010). Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773-786.
3. Baer, M. M., Bilstein, A., Caussinus, E., Csiszar, A., Affolter, M. and Leptin, M. (2010). The role of apoptosis in shaping the tracheal system in the Drosophila embryo. Mech. Dev. 127, 28-35.
4. Bardet, P. L., Kolahgar, G., Mynett, A., Miguel-Aliaga, I., Briscoe, J., Meier, P. and Vincent, J. P. (2008). A fluorescent reporter of caspase activity for live imaging. Proc. Natl. Acad. Sci. USA 105, 13901-13905.
5. Bastock, R. and Strutt, D. (2007). The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development 134, 3055-3064.
6. Bertet, C. and Lecuit, T. (2009). Planar polarity and short-range polarization in Drosophila embryos. Semin. Cell Dev. Biol. 20, 1006-1013.
7. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
8. Blankenship, J. T., Backovic, S. T., Sanny, J. S., Weitz, O. and Zallen, J. A. (2006). Multicellular rosette formation links planar cell polarity to tissue morphogenesis. Dev. Cell 11, 459-470.
9. Chihara, T., Kato, K., Taniguchi, M., Ng, J. and Hayashi, S. (2003). Rac promotes epithelial cell rearrangement during tracheal tubulogenesis in Drosophila. Development 130, 1419-1428.
10. Chung, S., Vining, M. S., Bradley, P. L., Chan, C. C., Wharton, K. A., Jr and Andrew, D. J. (2009). Serrano (sano) functions with the planar cell polarity genes to control tracheal tube length. PLoS Genet. 5, e1000746.
11. Classen, A. K., Anderson, K. I., Marois, E. and Eaton, S. (2005). Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817.
12. Förster, D. and Luschnig, S. (2012). Src42A-dependent polarized cell shape changes mediate epithelial tube elongation in Drosophila. Nat. Cell Biol. 14, 526-534.
13. Goodrich, L. V. and Strutt, D. (2011). Principles of planar polarity in animal development. Development 138, 1877-1892.
14. Gray, R. S., Roszko, I. and Solnica-Krezel, L. (2011). Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell 21, 120-133.
15. Grosshans, J., Wenzl, C., Herz, H. M., Bartoszewski, S., Schnorrer, F., Vogt, N., Schwarz, H. and Müller, H. A. (2005). RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 132, 1009-1020.
16. Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L. and Dickson, B. J. (2002). Rac function and regulation during Drosophila development. Nature 416, 438-442.
17. Huang, J., Zhou, W., Dong, W., Watson, A. M. and Hong, Y. (2009). From the cover: directed, efficient, and versatile modifications of the Drosophila genome by genomic engineering. Proc. Natl. Acad. Sci. USA 106, 8284-8289.
18. Irvine, K. D. and Wieschaus, E. (1994). Cell intercalation during Drosophila germband extension and its regulation by pair-rule segmentation genes. Development 120, 827-841.
19. Jaźwińska, A., Ribeiro, C. and Affolter, M. (2003). Epithelial tube morphogenesis during Drosophila tracheal development requires Piopio, a luminal ZP protein. Nat. Cell Biol. 5, 895-901.
20. Keller, R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954.
21. Lee, S. and Kolodziej, P. A. (2002). The plakin Short Stop and the RhoA GTPase are required for E-cadherin-dependent apical surface remodeling during tracheal tube fusion. Development 129, 1509-1520.
22. Levayer, R., Pelissier-Monier, A. and Lecuit, T. (2011). Spatial regulation of Dia and Myosin-II by RhoGEF2 controls initiation of E-cadherin endocytosis during epithelial morphogenesis. Nat. Cell Biol. 13, 529-540.
23. Mirkovic, I. and Mlodzik, M. (2006). Cooperative activities of drosophila DEcadherin and DN-cadherin regulate the cell motility process of ommatidial rotation. Development 133, 3283-3293.
24. Mirkovic, I., Gault, W. J., Rahnama, M., Jenny, A., Gaengel, K., Bessette, D., Gottardi, C. J., Verheyen, E. M. and Mlodzik, M. (2011). Nemo kinase phosphorylates β-catenin to promote ommatidial rotation and connects core PCP factors to E-cadherin-β-catenin. Nat. Struct. Mol. Biol. 18, 665-672.
25. Nelson, K. S., Khan, Z., Molnár, I., Mihály, J., Kaschube, M. and Beitel, G. J. (2012). Drosophila Src regulates anisotropic apical surface growth to control epithelial tube size. Nat. Cell Biol. 14, 518-525.
26. Nishimura, T., Honda, H. and Takeichi, M. (2012). Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149, 1084-1097.
27. 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.
28. Oda, H., Uemura, T., Harada, Y., Iwai, Y. and Takeichi, M. (1994). A Drosophila homolog of cadherin associated with armadillo and essential for embryonic cell-cell adhesion. Dev. Biol. 165, 716-726.
29. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994). wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369-380.
30. Pirraglia, C., Jattani, R. and Myat, M. M. (2006). Rac function in epithelial tube morphogenesis. Dev. Biol. 290, 435-446.
31. Rauzi, M., Lenne, P. F. and Lecuit, T. (2010). Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114.
32. Ribeiro, C., Neumann, M. and Affolter, M. (2004). Genetic control of cell intercalation during tracheal morphogenesis in Drosophila. Curr. Biol. 14, 2197-2207.
33. Saburi, S., Hester, I., Fischer, E., Pontoglio, M., Eremina, V., Gessler, M., Quaggin, S. E., Harrison, R., Mount, R. and McNeill, H. (2008). Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 40, 1010-1015.
34. Samakovlis, C., Hacohen, N., Manning, G., Sutherland, D. C., Guillemin, K. and Krasnow, M. A. (1996). Development of the Drosophila tracheal system occurs by a series of morphologically distinct but genetically coupled branching events. Development 122, 1395-1407.
35. Shaye, D. D., Casanova, J. and Llimargas, M. (2008). Modulation of intracellular trafficking regulates cell intercalation in the Drosophila trachea. Nat. Cell Biol. 10, 964-970.
36. Shindo, M., Wada, H., Kaido, M., Tateno, M., Aigaki, T., Tsuda, L. and Hayashi, S. (2008). Dual function of Src in the maintenance of adherens junctions during tracheal epithelial morphogenesis. Development 135, 1355-1364.
37. Simoes, S. M., Blankenship, J. T., Weitz, O., Farrell, D. L., Tamada, M., Fernandez-Gonzalez, R. and Zallen, J. A. (2010). Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 19, 377-388.
38. Simone, R. P. and DiNardo, S. (2010). Actomyosin contractility and Discs large contribute to junctional conversion in guiding cell alignment within the Drosophila embryonic epithelium. Development 137, 1385-1394.
39. Sommer, B., Oprins, A., Rabouille, C. and Munro, S. (2005). The exocyst component Sec5 is present on endocytic vesicles in the oocyte of Drosophila melanogaster. J. Cell Biol. 169, 953-963.
40. Strutt, D. I. (2001). Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367-375.
41. Strutt, H., Warrington, S. J. and Strutt, D. (2011). Dynamics of core planar polarity protein turnover and stable assembly into discrete membrane subdomains. Dev. Cell 20, 511-525.
42. Takahashi, M., Takahashi, F., Ui-Tei, K., Kojima, T. and Saigo, K. (2005). Requirements of genetic interactions between Src42A, armadillo and shotgun, a gene encoding E-cadherin, for normal development in Drosophila. Development 132, 2547-2559.
43. Tamada, M., Farrell, D. L. and Zallen, J. A. (2012). Abl regulates planar polarized junctional dynamics through β-catenin tyrosine phosphorylation. Dev. Cell 22, 309-319.
44. Tepass, U., Theres, C. and Knust, E. (1990). crumbs encodes an EGF-like protein expressed on apical membranes of Drosophila epithelial cells and required for organization of epithelia. Cell 61, 787-799.
45. Tree, D. R. P., Shulman, J. M., Rousset, R., Scott, M. P., Gubb, D. and Axelrod, J. D. (2002). Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381.
46. Ulrich, F., Krieg, M., Schötz, E. M., Link, V., Castanon, I., Schnabel, V., Taubenberger, A., Mueller, D., Puech, P. H. and Heisenberg, C. P. (2005). Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9, 555-564.
47. 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.
48. Uv, A., Cantera, R. and Samakovlis, C. (2003). Drosophila tracheal morphogenesis: intricate cellular solutions to basic plumbing problems. Trends Cell Biol. 13, 301-309.
49. Vichas, A. and Zallen, J. A. (2011). Translating cell polarity into tissue elongation. Semin. Cell Dev. Biol. 22, 858-864.
50. Wirtz-Peitz, F. and Zallen, J. A. (2009). Junctional trafficking and epithelial morphogenesis. Curr. Opin. Genet. Dev. 19, 350-356.
51. Zallen, J. A. and Wieschaus, E. (2004). Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 6, 343-355.