Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis

Development

Volumn 135, Issue 6, 2008, Pages 1005-1018

  Homem, Catarina C F ^a   Peifer, Mark ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

Drosophila; Formins; Myosin; RhoGEF2

Indexed keywords

ACTIN RELATED PROTEIN; CELL PROTEIN; DIA PROTEIN; DIAPHANOUS RELATED FORMINS PROTEIN; DRF PROTEIN; RHO FACTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL JUNCTION; CELL MATURATION; CELL POLARITY; CELL SHAPE; CYTOKINESIS; DROSOPHILA; EMBRYO; EMBRYO PATTERN FORMATION; GENE FUNCTION; GENE INTERACTION; GENETIC GAIN; MICROTUBULE ASSEMBLY; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REGULATORY MECHANISM;

ACTINS; ADHERENS JUNCTIONS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CARRIER PROTEINS; CELL SHAPE; DROSOPHILA; DROSOPHILA PROTEINS; EPIDERMIS; FEMALE; MALE; MODELS, BIOLOGICAL; MORPHOGENESIS; MUTATION; MYOSINS; PHENOTYPE; RHO GTP-BINDING PROTEINS;

EID: 42549102235     PISSN: 09501991     EISSN: None     Source Type: Journal    
DOI: 10.1242/dev.016337     Document Type: Article

References (55)

1. Adam, J. C., Pringle, J. R. and Peifer, M. (2000). Evidence for functional differentiation among Drosophila septins in cytokinesis and cellularization. Mol. Biol. Cell 11, 3123-3135.
2. Afshar, K., Stuart, B. and Wasserman, S. A. (2000). Functional analysis of the Drosophila diaphanous FH protein in early embryonic development. Development 127, 1887-1897.
3. Barrett, K., Leptin, M. and Settleman, J. (1997). The Rho GTPase and a putative RhoGEF mediate a signaling pathway for the cell shape changes in Drosophila gastrulation. Cell 91, 905-915.
4. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
5. 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.
6. Bloor, J. W. and Klehart, D. P. (2002). Drosophila RhoA regulates the cytoskeleton and cell-cell adhesion in the developing epidermis. Development 129, 3173-3183.
7. Carramusa, L., Ballestrem, C., Zilberman, Y. and Bershaclsky, A. D. (2007). Mammalian diaphanous-related formin Dia1 controls the organization of E-cadherin-mediated cell-cell junctions. J. Cell Sci. 120, 3870-3882.
8. Castrillon, D. H. and Wasserman, S. A. (1994). diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 120, 3367-3377.
9. Cox, R. T., Kirkpatrick, C. and Pelfer, M. (1996). Armadillo is required for adherens junction assembly, cell polarity, and morphogenesis during Drosophila embryogenesis. J. Cell Biol. 134, 133-148.
10. D'Avino, P. P., Crispll, S., Polito, L. C. and Furia, M. (1995). The role of the BR-C locus on the expression of genes located at the ecclysone-regulated 3C puff of Drosophila melanogaster. Mech. Dev. 49, 161-171.
11. Dawes-Hoang, R. E., Parmar, K. M., Christiansen, A. E., Phelps, C. B., Brand, A. H. and Wieschaus, E. F. (2005). folded gastrulation, cell shape change and the control of myosin localization. Development 132, 4165-4178.
12. Dean, S. O., Rogers, S. L., Stuurman, N., Vale, R. D. and Spudich, J. A. (2005). Distinct pathways control recruitment and maintenance of myosin II at the cleavage furrow during cytokinesis. Proc. Natl. Acad. Sci. USA 102, 13473-13478.
13. Drees, F., Pokutta, S., Yamada, S., Nelson, W. J. and Weis, W. I. (2005). Catenin is a molecular switch that binds E-cadherin/ β-Catenin and regulates actin-filament assembly. Cell 123, 903-915.
14. Eisenmann, K. M., West, R. A., Hildebrand, D., Kitchen, S. M., Peng, J., Sigler, R., Zhang, J., Siminovitch, K. A. and Alberts, A. S. (2007). T cell responses in mammalian diaphanous-related formin mDia1 knock-out mice. J. Biol. Chem. 282, 25152-25158.
15. Faix, J. and Grosse, R. (2006). Staying in shape with formins. Dev Cell 10, 693-706.
16. Fox, D. T. and Pelfer, M. (2007). Abelson kinase (Abl) and RhoGEF2 regulate actin organization during cell constriction in Drosophila. Development 134, 567-578.
17. Franke, J. D., Montague, R. A. and Klehart, 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.
18. Grevengoed, E. E., Loureiro, J. J., Jesse, T. L. and Pelifer, M. (2001). Abelson kinase regulates epithelial morphogenesis in Drosophila. J. Cell Biol. 155, 1185-1198.
19. Grosshans, J., Wenzi, C., Herz, H. M., Bartoszewski, S., Schnorrer, F., Vogt, N., Schwarz, H. and Muller, 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.
20. Guillemin, K., Groppe, J., Ducker, K., Treisman, R., Hafen, E., Affolter, M. and Krasnow, M. A. (1996). The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122, 1353-1362.
21. Hacker, U. and Perrimon, N. (1998). DRhoGEF2 encodes a member of the Dbl family of oncogenes and controls cell shape changes during gastrulation in Drosophila. Genes Dev 12, 274-284.
22. Halblelb, J. M. and Nelson, W. J. (2006). Cadherins in development: cell adhesion, sorting, and tissue morphogenesis. Genes Dev. 20, 3199-3214.
23. Harris, T. J. and Peifer, M. (2007). aPKC controls microtubule organization to balance adherens junction symmetry and planar polarity during development. Dev. Cell 12, 727-738.
24. Kaltschmidt, J. A., Lawrence, N., Morel, V., Balayo, T., Fernandez, B. G., Pelissier, A., Jacinto, A. and Martinez Arias, A. (2002). Planar-polarity and actin dynamics in the epidermis of Drosophila. Nat. Cell Biol. 4, 937-944.
25. 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.
26. Kim, Y. S., Fritz, J. L., Seneviratne, A. K. and VanBerkum, M. F. (2002). Constitutively active myosin light chain kinase alters axon guidance decisions in Drosophila embryos. Dev. Biol. 249, 367-381.
27. Kitzing, T. M., Sahadevan, A. S., Brandt D. T., Knieling, H., Hannemann, S., Fackler, O. T., Grosshans, J. and Grosse, R. (2007). Positive feedback between Dia1, LARG, and RhoA regulates cell morphology and invasion. Genes Dev. 21, 1478-1483.
28. Kobielak, A., Pasolli, H. A. and Fuchs, E. (2004). Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat. Cell Biol. 6, 21-30.
29. Kovar, D. R. (2006). Molecular details of formin-mediated actin assembly. Curr. Opin. Cell Biol. 18, 11-17.
30. Larsen, C. W., Hirst, E., Alexandre, C. and Vincent, J. P. (2003). Segment boundary formation in Drosophila embryos. Development 130, 5625-5635.
31. Lynch, E. D., Lee, M. K., Morrow, J. E., Welcsh, P. L., Leon, P. E. and King, M. C. (1997). Nonsyndromic deafness DFNA1 associated with mutation of a human homolog of the Drosophila gene diaphanous. Science 278, 1315-1318.
32. Magie, C. R., Meyer, M. R., Gorsuch, M. S. and Parkhurst, S. M. (1999). Mutations in the Rho1 small GTPase disrupt morphogenesis and segmentation during early Drosophila development. Development 126, 5353-5364.
33. Magie, C. R., Pinto-Santini, D. and Parkhurst, S. M. (2002). Rho1 interacts with p120(ctn) and alpha-catenin, and regulates cadherin- based adherens junction components in Drosophila. Development 129, 3771-3782.
34. Müller, H.-A. J. and Wieschaus, E. (1996). armadillo, bazooka, and stardust are critical for formation of the zonula adherens and maintenance of the polarized blastoderm epithelium in Drosophila. J. Cell Biol. 134, 149-165.
35. Peifer, M., McCrea, P. D., Green, K. J., Wieschaus, E. and Gumbiner, B. M. (1992). The vertebrate adhesive junction proteins beta-catenin and plakoglobin and the Drosophiia segment polarity gene armadillo form a multigene family with similar properties. J. Cell Biol. 118, 681-691.
36. Peng, J., Kitchen, S. M., West, R. A., Sigler, R., Eisenmann, K. M. and Alberts, A. S. (2007). Myeloproliferative defects following targeting of the Drf1 gene encoding the mammalian diaphanous related formin mDia1. Cancer Res. 67, 7565-7571.
37. Quinlan, M. P. and Hyatt, J. L. (1999). Establishment of the circumferential actin filament network is a prerequisite for localization of the cadherin-catenin complex in epithelial cells. Cell Growth Differ. 10, 839-854.
38. Rorth, P. (1998). Gal4 in the Drosophila female germline. Mech. Dev. 78, 113-118.
39. Sahai, E. and Marshall, C. J. (2002). ROCK and Dia have opposing effects on adherens junctions downstream of Rho. Nat. Cell Biol. 4, 408-415.
40. Schock, F. and Perrimon, N. (2002). Cellular processes associated with germ band retraction in Drosophila. Dev. Biol. 248, 29-39.
41. Schock, F. and Perrimon, N. (2003). Retraction of the Drosophila germ band requires cell-matrix interaction. Genes Dev. 17, 597-602.
42. Severson, A. F., Baillie, D. L. and Bowerman, B. (2002). A Formin Homology protein and a profilin are required for cytokinesis and Arp2/ 3-independent assembly of cortical microfilaments in C. elegans. Curr. Biol. 12, 2066-2075.
43. Shewan, A. M., Maddugoda, M., Kraemer, A., Stehbens, S. J., Verma, S., Kovacs, E. M. and Yap, A. S. (2005). Myosin 2 is a key rho kinase target necessary for the local concentration of E-cadherin at cell-cell contacts. Mol. Biol. Cell 16, 4531-4542.
44. Somogyi, K. and Rarth, P. (2004). Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev Cell 7, 85-93.
45. Swan, K. A., Severson, A. F., Carter, J. C., Martin, P. R., Schnabel, H., Schnabel, R. and Bowerman, B. (1998). cyk-1: a C. elegans FH gene required for a late step in embryonic cytokinesis. J. Cell Sci. 111, 2017-2027.
46. Tominaga, T., Sahai, E., Chardin, P., McCormick F., Courtneidge, S. A. and Alberts, A. S. (2000). Diaphanous-related formins bridge Rho GTPase and Src tyrosine kinase signaling. Mol. Cell 5, 13-25.
47. Verdier, V., Guang-Chao-Chen and Settleman, J. (2006a). Rho-kinase regulates tissue morphogenesis via non-muscle myosin and LIM-kinase during Drosophila development. BMC Dev Biol. 6, 38.
48. Verdier, V., Johndrow, J. E., Betson, M., Chen, G. C., Hughes, D. A., Parkhurst, S. M. and Settleman, J. (2006b). Drosophila Rho-kinase (DRok) is required for tissue morphogenesis in diverse compartments of the egg chamber during oogenesis. Dev Biol. 297, 417-432.
49. Wallar, B. J. and Alberts, A. S. (2003). The formins: active scaffolds that remodel the cytoskeleton. Trends Cell Biol. 13, 435-446.
50. Walters, J. W., Dilks, S. A. and Dinardo, S. (2006). Planar polarization of the denticle field in the Drosophila embryo: roles for Myosin II (Zipper) and Fringe. Dev. Biol. 297, 323-339.
51. Watanabe, N., Madaule, P., Reid, T., Ishizaki, T., Watanabe, G., Kakizuka, A., Salto, Y., Nakao, K., Jockusch, B. M. and Narumiya, S. (1997). p140mDia, a mammalian homolog of Drosophila diaphanous, is a target protein for Rho small GTPase and is a ligand for profilin. EMBO J. 16, 3044-3056.
52. Winter, C. G., Wang, B., Ballew, A., Royou, A., Karess, R., Axelrod, J. D. and Luo, L. (2001). Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105, 81-91.
53. Yamada, S. and Nelson, W. J. (2007). Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell cell adhesion. J. Cell Biol. 178, 517-527.
54. Zallen, J. A. (2007). Planar-polarity and tissue morphogenesis. Cell 129, 1051-1063.
55. Zallen, J. A. and Wieschaus, E. (2004). Patterned gene expression directs bipolar planar-polarity in Drosophila. Dev. Cell 6, 343-355.