Rho GTPase controls Drosophila salivary gland lumen size through regulation of the actin cytoskeleton and Moesin

Development

Volumn 138, Issue 24, 2011, Pages 5415-5427

  Xu, Na ^a,b   Bagumian, Gaiana ^b   Galiano, Michael ^b   Myat, Monn Monn ^b  

^a Weill Cornell Medical Center   (United States)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Actin; Drosophila; Lumen; Rho GTPase; Salivary gland; Tube

Indexed keywords

ACTIN; COFILIN; F ACTIN; MOESIN; RHO GUANINE NUCLEOTIDE BINDING PROTEIN;

ACTIN POLYMERIZATION; ARTICLE; BASOLATERAL MEMBRANE; CELL SHAPE; CELL STRUCTURE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; CYTOSKELETON; DOWN REGULATION; DROSOPHILA; EMBRYO; ENDOCYTOSIS; ENZYME ACTIVITY; MESODERM; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; SALIVARY GLAND; WILD TYPE;

ACTIN CYTOSKELETON; ACTIN DEPOLYMERIZING FACTORS; ACTINS; ANIMALS; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; MICROFILAMENT PROTEINS; MUTATION; ORGAN SIZE; RHO GTP-BINDING PROTEINS; SALIVARY GLANDS;

EID: 81755181896     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.069831     Document Type: Article

References (63)

1. Andrew, D. and Ewald, A. (2010). Morphogenesis of epithelial tubes: insights into tube formation, elongation and elaboration. Dev. Biol. 341, 34-55
2. Apodaca, G. (2001). Endocytic traffic in polarized epithelial cells: role of the actin and microtubule cytoskeleton. Traffic 2, 149-159
3. Blair, A., Tomlinson, A., Pham, H., Gunsalus, K., Goldberg, M. and Laski, F. (2006). Twinstar, the Drosophila homolog of cofilin/ADF, is required for planar cell polarity patterning. Development 133, 1789-1797
4. Blake, K., Myette, G. and Jack, J. (1999). Ribbon, raw and zipper have distinct functions in reshaping the Drosophila cytoskeleton. Dev. Genes Evol. 9, 555-559.
5. Bradley, P. B. and Andrew, D. J. (2001). Ribbon encodes a novel BTB/POZ protein required for directed cell migration in Drosophila melanogaster. Development 128, 3001-3015
6. Bradley, P. L., Myat, M. M., Comeaux, C. A. and Andrew, D. J. (2003). Posterior migration of the salivary gland requires an intact visceral mesoderm and integrin function. Dev. Biol. 257, 249-262
7. Brown, B. and Song, W. (2001). The actin cytoskeleton is required for the trafficking of the b cell antigen receptor to the late endosomes. Traffic 2, 414-427.
8. Chandrasekaran, V. and Beckendorf, S. (2005). Tec29 controls actin remodeling and endoreplication during invagination of the Drosophila embryonic salivary glands. Development, 3515-3524
9. Chen, J., Godt, D., Gunsalus, K., Kiss, I., Goldberg, M. and Laski, F. (2001). Cofilin/ADF is required for cell motility during Drosophila ovary development and oogensis. Nat. Cell Biol. 3, 204-209
10. Cheshire, A., Kerman, B., Zipfel, W., Spector, A. and Andrew, D. (2008). Kinetic and mechanical analysis of live tube morphogenesis. Dev. Dyn. 237, 2874-2888
11. Cooley, L., Verheyen, E. and Ayers, K. (1992). Chickadee encodes a profilin required for intercellular cytoplasm transport during Drosophila oogenesis. Cell 69, 173-184
12. Davis, G., Koh, W. and Stratman, A. (2007). Mechanisms controlling human endothelial lumen formation and tube assembly in three-dimensional extracellular matrices. Birth Defects Res. C Embryo Today 81, 270-285
13. Fischer, J., Acosta, S., Kenny, A., Cater, C., Robinson, C. and Hook, J. (2004). Drosophila klarsicht has distinct subcellular localization domains for nuclear envelope and microtubule localization in the eye. Genetics 168, 1385-1393
14. Fischer-Vize, J. A. and Mosley, K. L. (1994). Marbles mutants: uncoupling cell determination and nuclear migration in the developing Drosophila eye. Development 120, 2609-2618
15. Fukata, Y., Kimura, K., Oshiro, N., Saya, H., Matsuura, Y. and Kaibuchi, K. (1998). Association of the myosin-binding subunit of myosin phosphatase and moesin: dual regulation of moesin phosphorylation by Rho-associated kinase and myosin phosphatase. J. Cell Biol. 141, 409-418
16. Guo, Y., Jangi, S. and Welte, M. (2005). Organelle-specific control of intracellular transport: distinctly targeted isoforms of the regulator Klar. Mol. Biol. Cell 16, 1406-1416
17. Halsell, S., Chu, B. and Kiehart, D. (2000). Genetic analysis demonstrates a direct link between Rho signaling and nonmuscle myosin function during Drosophila morphogenesis. Genetics 155, 1253-1265
18. Henderson, K. D. and Andrew, D. J. (2000). Regulation and function of Scr, exd, and hth in the Drosophila salivary gland. Dev. Biol. 217, 362-374
19. Hipfner, D., Keller, N. and Cohen, S. (2004). Slik Sterile-20 kinase regulates Moesin activity to promote epithelial integrity during tissue growth. Genes Dev. 18, 2243-2248
20. Jack, J. and Myette, G. (1997). The genes raw and ribbon are required for proper shape of tubular epithelial tissues in Drosophila. Genetics 147, 243-253
21. Jaffe, A., Kaji, N., Durgan, J. and Hall, A. (2008). Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J. Cell Biol. 183, 625-633
22. Jani, K. and Schöck, F. (2007). Zasp is required for the assembly of functional integrin adhesion sites. J. Cell Biol. 179, 1583-1597
23. Jung, A. C., Denholm, B., Skaer, H. and Affolter, M. (2005). Renal tubule development in Drosophila: a closer look at the cellular level. J. Am. Soc. Nephrol. 16, 322-328
24. Kerman, B., Chesire, A., Myat, M. and Andrew, D. (2008). Ribbon modulates apical membrane during tube elongation through Crumbs and Moesin. Dev. Biol. 320, 278-288
25. Kesavan, G., Sand, F., Greiner, T., Johansson, J, Kobberup, S., Wu, X., Brakebusch, C. and Semb, H. (2009). Cdc42-mediated tubulogenesis controls cell specification. Cell 139, 791-801
26. Kunda, P., Pelling, A., Liu, T. and Baum, B. (2008). Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 18, 91-101
27. Lu, H. and Bilder, D. (2005). Endocytic control of epithelial polarity and proliferation in Drosophila. Nat. Cell Biol. 7, 1232-1239
28. Lubarsky, B. and Krasnow, M. A. (2003). Tube morphogenesis: making and shaping biological tubes. Cell 112, 19-28
29. Maekawa, M., Ishizaki, T., Boku, S., Watanabe, N., Fujita, A., Iwamatsu, A., Obinata, T., Ohashi, K., Mizuno, K. and Narumiya, S. (1999). Signaling from Rho to the actin cytoskeleton through protein kinases ROCk and LIM-kinase. Science 285, 895-898
30. Magie, C. and Parkhurst, S. (2005). Rho1 regulates signaling events required for proper Drosohila embryonic development. Dev. Biol. 278, 144-154
31. Magie, C., Meyer, M., Gorsuch, M. and Parkhurst, S. (1999). Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126, 5353-5364
32. Martin-Belmonte, F. and Mostov, K. (2008). Regulation of cell polarity during epithelial morphogenesis. Curr. Opin. Cell Biol. 20, 227-234
33. Martin-Belmonte, F., Gassama, A., Datta, A., Yu, W., Rescher, U., Gerke, V. and Mostov, K. (2007). PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 128, 383-397
34. Matsui, T., Maeda, M., Doi, Y., Yonemura, S., Amano, M., Kaibuchi, K., Tsukita, S. and Tsukita, S. (1998). Rho-kinase phosphorylated COOH-terminal threonines of ezrin/radixin/moesin (ERM) proteins and regulates their head-to-tail association. J. Cell Biol. 140, 647-657
35. Maybeck, V. and Roper, K. (2009). A targeted gain-of-function screen identifies genes affecting salivary gland morphogenesis/tubulogenesis in Drosophila. Genetics 181, 543-565
36. Medina, E., Williams, J., Klipfell, E., Zarnescu, D., Thomas, G. and Bivic, A. L. (2002). Crumbs interacts with moesin and β Heavy-spectrin in the apical membrane skeleton of Drosophila. J. Cell Biol. 158, 941-951
37. Merrifield, C., Moss, S., Ballestrem, C., Imhof, B., Giese, G., Wunderlich, I. and Aimers, W. (1999). Endocytic vesicless move at the tips of actin tails in cultured mast cells. Nat. Cell Biol. 1, 72-74
38. Molnar, C. and de Celis, J. (2006). Independent roles of Drosophila Moesin in imaginal disc morphogenesis and hedgehog signalling. Mech. Dev. 123, 337-351.
39. Mosley-Bishop, K. L., Li, Q., Patterson, L. and Fischer, J. A. (1999). Molecular analysis of the klarsicht gene and its role in nuclear migration within differentiating cells of the Drosophila eye. Curr. Biol. 9, 1211-1220
40. Myat, M. M. and Andrew, D. J. (2002). Epithelial tube morphology is determined by the polarized growth and delivery of apical membrane. Cell 111, 879-891
41. Neisch, A., Speck, O., Stronach, B. and Fehon, R. (2010). Rho1 regulates apoptosis via activation of the JNK signaling pathway at the plasma membrane. J. Cell Biol. 189, 311-323
42. Ohshiro, N., Fukata, Y. and Kaibuchi, K. (1988). Phosphorylation of moesin by rho-associated kinase (Rho-kinase) plays a crucial role in the formation of microvilli-like structures. J. Biol. Chem. 273, 34663-34666
43. Pirraglia, C., Walters, J. and Myat, M. M. (2010). Pak1 control of E-cadherin endocytosis regulates salivary gland lumen size and shape. Development 137, 4177-4189
44. Qualmann, B. and Kessels, M. (2002). Endocytosis and the cytoskeleton. Int. Rev. Cytol. 220, 93-144
45. Rangarajan, R., Gong, Q. and Gaul, U. (1999). Migration and function of glia in the developing Drosophila eye. Development 126, 3285-3292
46. Reed, R., Womble, M., Dush, M., Tull, R., Bloom, S., Morckel, A., Devlin, E. and Nascone-Yoder, N. (2009). Morphogenesis of the primitive gut tube is generated by Rho/ROCK/myosin II-mediated endoderm rearrangements. Dev. Dyn. 238, 3111-3125
47. Reuter, R., Panganiban, G. E. F., Hoffman, F. M. and Scott, M. P. (1990). Homeotic genes regulate the spatial expression of putative growth factors in the visceral mesoderm of Drosophila embryos. Development 110, 1031-1040
48. Ridley, A. and Hall, A. (1992). The small GTP-binding protein rho regulates the assembly of focal adhesions and actin stress fibers in response to growth factors. Cell 70, 389-399
49. Roch, F., Polesello, C., Roubinet, C., Martin, M., Roy, C., Valenti, P., Carreno, S., Mangeat, P. and Payre, F. (2010). Differential roles of PtdIns(4,5)P2 and phosphorylation in moesin activation during Drosophila development. J. Cell Sci. 123, 2058-2067
50. Shim, K., Blake, K. J., Jack, J. and Krasnow, M. A. (2001). The Drosophila ribbon gene encodes a nuclear BTB domain protein that promotes epithelial migration and morphogenesis. Development 128, 4923-4933
51. Simoes, S., Denholm, B., Azevedo, D., Sotillos, S., Martin, P., Skaer, H., Hombria, J. and Jacinto, A. (2006). Compartmentalisation of Rho regulators directs cell invagination during tissue morphogenesis. Development 133, 4257-4267.
52. Speck, O., Hughes, S. C., Noren, N. K., Kulikauskas, R. M. and Fehon, R. G. (2003b). Moesin functions antagonistically to the Rho pathway to maintain epithelial integrity. Nature 421, 83-87
53. Strutt, D., Weber, U. and Mlodzik, M. (1997). The role of RhoA in tissue polarity and Frizzled signalling. Nature 387, 292-295
54. Suzuki, N., Buechner, M., Nishiwaki, K., Hall, D. H., Nakanishi, H., Takai, Y., HIsamoto, N. and Matsumoto, K. (2001). A putative GDP-GTP exchange factor is required for development of the excretory cell in Caenorhabditis elegans. EMBO Rep. 2, 530-535
55. Taunton, J., Rowning, B., Coughlin, M., Wu, M., Moon, R., Mitchison, T. and Larabell, C. (2000). Actin-dependent propulsion of endosomes and lysosomes by recruitment of N-WASP. J. Cell Biol. 148, 519-530
56. Tepass, U. and Knust, E. (1993). Crumbs and Stardust act in a genetic pathway that controls the organization of epithelia in Drosophila melanogaster. Dev. Biol.159, 311-326
57. 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
58. van Deurs, B., Holm, P., Kayser, L. and Sandvig, K. (1995). Delivery to lysosomes in the human carcinoma cell-line Hep-2 involves an actin filamentfacilitated fusion between mature endosomes and preexisting lysosomes. Eur. J. Cell Biol. 66, 309-323
59. Verheyen, E. and Cooley, L. (1994). Profilin mutations disrupt multiple actindependent processes during Drosophila development. Development 120, 717-728.
60. Vining, M. S., Bradley, P. L., Comeaux, C. A. and Andrew, D. J. (2005). Organ positioning in Drosophila requires complex tissue-tissue interactions. Dev. Biol. 287, 19-34
61. Xu, N., Keung, B. and Myat, M. (2008). Rho GTPase controls invagination and cohesive migration of the Drosophila salivary gland through Crumbs and Rhokinase. Dev. Biol. 321, 88-100
62. Yonemura, S., Matsui, T., Tsukita, S. and Tsukita, S. (2002). Rho-dependent and-independent activation mechanisms of ezrin/radixin/moesin proteins: an essential role for polyphosphoinositides in vivo. J. Cell Sci. 115, 2569-2580.
63. Zhang, L., Luo, L., Wan, P., Wu, J., Laski, F. and Chen, J. (2011). Regulation of cofilin phosphorylation and asymmetry in collective cell migration during morphogenesis. Development 138, 455-464.