Girdin-mediated interactions between cadherin and the actin cytoskeleton are required for epithelial morphogenesis in Drosophila

Development (Cambridge)

Volumn 142, Issue 10, 2015, Pages 1777-1784

  Houssin, Elise ^a   Tepass, Ulrich ^b   Laprise, Patrick ^a  

^a LAVAL UNIVERSITY   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

Armadillo; Cell cell adhesion; Drosophila melanogaster; E cadherin; Epithelial morphogenesis; Epithelial tissues; Girdin; GIV

Indexed keywords

ADAPTOR PROTEIN; ALPHA CATENIN; CADHERIN; CATENIN; CYTOSKELETON PROTEIN; GIRDIN; UNCLASSIFIED DRUG; ACTIN; DROSOPHILA PROTEIN;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CELL ADHESION; CELL FUNCTION; CELL JUNCTION; CELL MIGRATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EPITHELIUM; EPITHELIUM CELL; GENE MUTATION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; ANIMAL; METABOLISM; PHYSIOLOGY;

ARMADILLO; DROSOPHILA MELANOGASTER; GREAT ISLAND VIRUS;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CADHERINS; CYTOSKELETAL PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; MORPHOGENESIS;

EID: 84929222948     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.122002     Document Type: Article

References (41)

1. Asai, M., Asai, N., Murata, A., Yokota, H., Ohmori, K., Mii, S., Enomoto, A., Murakumo, Y. and Takahashi, M. (2012). Similar phenotypes of Girdin germ-line and conditional knockout mice indicate a crucial role for Girdin in the nestin lineage. Biochem. Biophys. Res. Commun. 426, 533-538.
2. Bellen, H. J., Levis, R. W., Liao, G., He, Y., Carlson, J. W., Tsang, G., Evans- Holm, M., Hiesinger, P. R., Schulze, K. L., Rubin, G. M. et al. (2004). The BDGP gene disruption project: single transposon insertions associated with 40% of Drosophila genes. Genetics 167, 761-781.
3. Bellen, H. J., Levis, R. W., He, Y., Carlson, J. W., Evans-Holm, M., Bae, E., Kim, J., Metaxakis, A., Savakis, C., Schulze, K. L. et al. (2011). The Drosophila gene disruption project: progress using transposons with distinctive site specificities. Genetics 188, 731-743.
4. Chou, T. B. and Perrimon, N. (1996). The autosomal FLP-DFS technique for generating germline mosaics in Drosophila melanogaster. Genetics 144, 1673-1679.
5. David, D. J., Tishkina, A. and Harris, T. J. (2010). The PAR complex regulates pulsed actomyosin contractions during amnioserosa apical constriction in Drosophila. Development 137, 1645-1655.
6. Desai, R., Sarpal, R., Ishiyama, N., Pellikka, M., Ikura, M. and Tepass, U. (2013). Monomeric alpha-catenin links cadherin to the actin cytoskeleton. Nat. Cell Biol. 15, 261-273.
7. Enomoto, A., Murakami, H., Asai, N., Morone, N., Watanabe, T., Kawai, K., Murakumo, Y., Usukura, J., Kaibuchi, K. and Takahashi, M. (2005). Akt/PKB regulates actin organization and cell motility via Girdin/APE. Dev. Cell 9, 389-402.
8. Enomoto, A., Ping, J. and Takahashi, M. (2006). Girdin, a novel actin-binding protein, and its family of proteins possess versatile functions in the Akt and Wnt signaling pathways. Ann. N. Y. Acad. Sci. 1086, 169-184.
9. Enomoto, A., Asai, N., Namba, T., Wang, Y., Kato, T., Tanaka, M., Tatsumi, H., Taya, S., Tsuboi, D., Kuroda, K. et al. (2009). Roles of disrupted-inschizophrenia 1-interacting protein girdin in postnatal development of the dentate gyrus. Neuron 63, 774-787.
10. Franke, J. D., Montague, R. A. and Kiehart, D. P. (2005). Nonmuscle myosin II generates forces that transmit tension and drive contraction in multiple tissues during dorsal closure. Curr. Biol. 15, 2208-2221.
11. Friedl, P. and Gilmour, D. (2009). Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10, 445-457.
12. Gamblin, C. L., Hardy, E. J.-L., Chartier, F. J.-M., Bisson, N. and Laprise, P. (2014). A bidirectional antagonism between aPKC and Yurt regulates epithelial cell polarity. J. Cell Biol. 204, 487-495.
13. Ghosh, P., Garcia-Marcos, M., Bornheimer, S. J. and Farquhar, M. G. (2008). Activation of Galphai3 triggers cell migration via regulation of GIV. J. Cell Biol. 182, 381-393.
14. Groth, A. C., Fish, M., Nusse, R. and Calos, M. P. (2004). Construction of transgenic Drosophila by using the site-specific integrase from phage phiC31. Genetics 166, 1775-1782.
15. Harden, N. (2002). Signaling pathways directing the movement and fusion of epithelial sheets: lessons from dorsal closure in Drosophila. Differentiation 70, 181-203.
16. Harris, T. J. C. and Peifer, M. (2004). Adherens junction-dependent and -independent steps in the establishment of epithelial cell polarity in Drosophila. J. Cell Biol. 167, 135-147.
17. Harris, T. J. C. and Tepass, U. (2010). Adherens junctions: from molecules to morphogenesis. Nat. Rev. Mol. Cell Biol. 11, 502-514.
18. Jiang, P., Enomoto, A., Jijiwa, M., Kato, T., Hasegawa, T., Ishida, M., Sato, T., Asai, N., Murakumo, Y. and Takahashi, M. (2008). An actin-binding protein Girdin regulates the motility of breast cancer cells. Cancer Res. 68, 1310-1318.
19. Kiehart, D. P., Galbraith, C. G., Edwards, K. A., Rickoll, W. L. and Montague, R. A. (2000). Multiple forces contribute to cell sheet morphogenesis for dorsal closure in Drosophila. J. Cell Biol. 149, 471-490.
20. Kitamura, T., Asai, N., Enomoto, A., Maeda, K., Kato, T., Ishida, M., Jiang, P., Watanabe, T., Usukura, J., Kondo, T. et al. (2008). Regulation of VEGFmediated angiogenesis by the Akt/PKB substrate Girdin. Nat. Cell Biol. 10, 329-337.
21. Kowalczyk, A. P. and Nanes, B. A. (2012). Adherens junction turnover: regulating adhesion through cadherin endocytosis, degradation, and recycling. Subcell. Biochem. 60, 197-222.
22. Laprise, P., Chailler, P., Houde, M., Beaulieu, J.-F., Boucher, M.-J. and Rivard, N. (2002). Phosphatidylinositol 3-kinase controls human intestinal epithelial cell differentiation by promoting adherens junction assembly and p38 MAPK activation. J. Biol. Chem. 277, 8226-8234.
23. Matsushita, E., Asai, N., Enomoto, A., Kawamoto, Y., Kato, T., Mii, S., Maeda, K., Shibata, R., Hattori, S., Hagikura, M. et al. (2011). Protective role of Gipie, a Girdin family protein, in endoplasmic reticulum stress responses in endothelial cells. Mol. Biol. Cell 22, 736-747.
24. McGill, M. A., McKinley, R. F. A. and Harris, T. J. C. (2009). Independent cadherincatenin and Bazooka clusters interact to assemble adherens junctions. J. Cell Biol. 185, 787-796.
25. Morais-de-Sá, E., Mirouse, V. and St Johnston, D. (2010). aPKC phosphorylation of Bazooka defines the apical/lateral border in Drosophila epithelial cells. Cell 141, 509-523.
26. Muller, H. A. and Wieschaus, E. (1996). armadillo, bazooka, and stardust are critical for early stages in formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149-163.
27. Ohara, K., Enomoto, A., Kato, T., Hashimoto, T., Isotani-Sakakibara, M., Asai, N., Ishida-Takagishi, M., Weng, L., Nakayama, M., Watanabe, T. et al. (2012). Involvement of Girdin in the determination of cell polarity during cell migration. PLoS ONE 7, e36681.
28. Ooshio, T., Fujita, N., Yamada, A., Sato, T., Kitagawa, Y., Okamoto, R., Nakata, S., Miki, A., Irie, K. and Takai, Y. (2007). Cooperative roles of Par-3 and afadin in the formation of adherens and tight junctions. J. Cell Sci. 120, 2352-2365.
29. Pellikka, M., Tanentzapf, G., Pinto, M., Smith, C., McGlade, C. J., Ready, D. F. and Tepass, U. (2002). Crumbs, the Drosophila homologue of human CRB1/RP12, is essential for photoreceptor morphogenesis. Nature 416, 143-149.
30. Puseenam, A., Yoshioka, Y., Nagai, R., Hashimoto, R., Suyari, O., Itoh, M., Enomoto, A., Takahashi, M. and Yamaguchi, M. (2009). A novel Drosophila Girdin-like protein is involved in Akt pathway control of cell size. Exp. Cell Res. 315, 3370-3380.
31. Simpson, F., Martin, S., Evans, T. M., Kerr, M., James, D. E., Parton, R. G., Teasdale, R. D. and Wicking, C. (2005). A novel hook-related protein family and the characterization of hook-related protein 1. Traffic 6, 442-458.
32. Solon, J., Kaya-Copur, A., Colombelli, J. and Brunner, D. (2009). Pulsed forces timed by a ratchet-like mechanism drive directed tissue movement during dorsal closure. Cell 137, 1331-1342.
33. 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.
34. Tepass, U., Gruszynski-DeFeo, E., Haag, T. A., Omatyar, L., Torok, T. and Hartenstein, V. (1996). shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 10, 672-685.
35. Thibault, S. T., Singer, M. A., Miyazaki, W. Y., Milash, B., Dompe, N. A., Singh, C. M., Buchholz, R., Demsky, M., Fawcett, R., Francis-Lang, H. L. et al. (2004). A complementary transposon tool kit for Drosophila melanogaster using P and piggyBac. Nat. Genet. 36, 283-287.
36. Uemura, T., Oda, H., Kraut, R., Hayashi, S., Kotaoka, Y. and Takeichi, M. (1996). Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 11, 659-671.
37. Wang, Y., Kaneko, N., Asai, N., Enomoto, A., Isotani-Sakakibara, M., Kato, T., Asai, M., Murakumo, Y., Ota, H., Hikita, T. et al. (2011). Girdin is an intrinsic regulator of neuroblast chain migration in the rostral migratory stream of the postnatal brain. J. Neurosci. 31, 8109-8122.
38. Weng, L., Enomoto, A., Ishida-Takagishi, M., Asai, N. and Takahashi, M. (2010). Girding for migratory cues: roles of the Akt substrate Girdin in cancer progression and angiogenesis. Cancer Sci. 101, 836-842.
39. Weng, L., Enomoto, A., Miyoshi, H., Takahashi, K., Asai, N., Morone, N., Jiang, P., An, J., Kato, T., Kuroda, K. et al. (2014). Regulation of cargo-selective endocytosis by dynamin 2 GTPase-activating protein girdin. EMBO J. 33, 2098-2112.
40. Xue, B., Krishnamurthy, K., Allred, D. C. and Muthuswamy, S. K. (2013). Loss of Par3 promotes breast cancer metastasis by compromising cell-cell cohesion. Nat. Cell Biol. 15, 189-200.
41. Young, P. E., Richman, A. M., Ketchum, A. S. and Kiehart, D. P. (1993). Morphogenesis in Drosophila requires nonmuscle myosin heavy chain function. Genes Dev. 7, 29-41.