Spatially defined Dsh-Lgl interaction contributes to directional tissue morphogenesis

Journal of Cell Science

Volumn 123, Issue 18, 2010, Pages 3157-3165

  Kaplan, Nicole A ^a   Tolwinski, Nicholas S ^a  

^a MEMORIAL SLOAN KETTERING CANCER CENTER   (United States)

Author keywords

catenin; Armadillo; Dsh; Lethal giant larvae; Polarity; Wnt

Indexed keywords

ACTIN; ALPHA CATENIN; CELL PROTEIN; DISHEVELLED PROTEIN; MYOSIN; PROTEIN KINASE C; PROTEIN LGL; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL POLARITY; CELL SHAPE; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EMBRYO DEVELOPMENT; EPIDERMIS; EPITHELIUM CELL; FEMALE; GENE INTERACTION; LOSS OF FUNCTION MUTATION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL POLARITY; DROSOPHILA; DROSOPHILA PROTEINS; EPIDERMIS; FEMALE; MALE; MORPHOGENESIS; PHOSPHOPROTEINS; PROTEIN BINDING; PROTEIN TRANSPORT; TUMOR SUPPRESSOR PROTEINS;

ARMADILLO;

EID: 77956928326     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.069898     Document Type: Article

References (61)

1. 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. (Pubitemid 28406962)
2. Bellaiche, Y., Radovic, A., Woods, D. F., Hough, C. D., Parmentier, M. L., O'[Kane, C. J., Bryant, P. J. and Schweisguth, F. (2001). The Partner of Inscuteable/Discs-large complex is required to establish planar polarity during asymmetric cell division in Drosophila. Cell 106, 355-366.
3. Bertet, C., Sulak, L. and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
4. Bilder, D., Schober, M. and Perrimon, N. (2003). Integrated activity of PDZ protein complexes regulates epithelial polarity. Nat. Cell Biol. 5, 53-58. (Pubitemid 36054329)
5. Bischof, J., Maeda, R. K., Hediger, M., Karch, F. and Basler, K. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl. Acad. Sci. USA 104, 3312-3317.
6. 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.
7. Blankenship, J. T., Fuller, M. T. and Zallen, J. A. (2007). The Drosophila homolog of the Exo84 exocyst subunit promotes apical epithelial identity. J. Cell Sci. 120, 3099-3110.
8. Chou, T. B. and Perrimon, N. (1992). Use of a yeast site-specific recombinase to produce female germline chimeras in Drosophila. Genetics 131, 643-653.
9. Colosimo, P. F. and Tolwinski, N. S. (2006). Wnt, Hedgehog and junctional Armadillo/beta-catenin establish planar polarity in the Drosophila embryo. PLoS ONE 1, e9.
10. Colosimo, P. F., Liu, X., Kaplan, N. A. and Tolwinski, N. S. (2010). GSK3beta affects apical-basal polarity and cell-cell adhesion by regulating aPKC levels. Dev. Dyn. 239, 115-125.
11. Courbard, J. R., Djiane, A., Wu, J. and Mlodzik, M. (2009). The apical/basal-polarity determinant Scribble cooperates with the PCP core factor Stbm/Vang and functions as one of its effectors. Dev. Biol. 333, 67-77.
12. Djiane, A., Yogev, S. and Mlodzik, M. (2005). The apical determinants aPKC and dPatj regulate Frizzled-dependent planar cell polarity in the Drosophila eye. Cell 121, 621-631. (Pubitemid 40720014)
13. Dollar, G. L., Weber, U., Mlodzik, M. and Sokol, S. Y. (2005). Regulation of Lethal giant larvae by Dishevelled. Nature 437, 1376-1380.
14. Etienne-Manneville, S. and Hall, A. (2003). Cdc42 regulates GSK-3beta and adenomatous polyposis coli to control cell polarity. Nature 421, 753-756.
15. Etienne-Manneville, S., Manneville, J. B., Nicholls, S., Ferenczi, M. A. and Hall, A. (2005). Cdc42 and Par6-PKCzeta regulate the spatially localized association of Dlg1 and APC to control cell polarization. J. Cell Biol. 170, 895-901. (Pubitemid 41306289)
16. Foe, V. E., Field, C. M. and Odell, G. M. (2000). Microtubules and mitotic cycle phase modulate spatiotemporal distributions of F-actin and myosin II in Drosophila syncytial blastoderm embryos. Development 127, 1767-1787.
17. Gateff, E. (1978). Malignant neoplasms of genetic origin in Drosophila melanogaster. Science 200, 1448-1459.
18. Gateff, E. and Schneiderman, H. A. (1974). Developmental capacities of benign and malignant neoplasms of Drosophila. Roux's Arch Dev. Biol. 176, 23-65.
19. 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.
20. Hartenstein, V. (1993). Atlas of Drosophila Development. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
21. Hatini, V. and DiNardo, S. (2001). Divide and conquer: pattern formation in Drosophila embryonic epidermis. Trends Genet. 17, 574-579. (Pubitemid 32918299)
22. Hirano, M., Neff, D. and Collier, S. (2009). Cell shape and epithelial patterning in the Drosophila embryonic epidermis. Fly (Austin) 3, 185-191.
23. Humbert, P., Russell, S. and Richardson, H. (2003). Dlg, Scribble and Lgl in cell polarity, cell proliferation and cancer. BioEssays 25, 542-553.
24. Humbert, P. O., Grzeschik, N. A., Brumby, A. M., Galea, R., Elsum, I. and Richardson, H. E. (2008). Control of tumourigenesis by the Scribble/Dlg/Lgl polarity module. Oncogene 27, 6888-6907.
25. Hutterer, A., Betschinger, J., Petronczki, M. and Knoblich, J. A. (2004). Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 6, 845-854.
26. Kaplan, N. A., Liu, X. and Tolwinski, N. S. (2009). Epithelial polarity: interactions between junctions and apical-basal machinery. Genetics 183, 897-904.
27. Kemphues, K. (2000). PARsing embryonic polarity. Cell 101, 345-348.
28. Laprise, P., Lau, K. M., Harris, K. P., Silva-Gagliardi, N. F., Paul, S. M., Beronja, S., Beitel, G. J., McGlade, C. J. and Tepass, U. (2009). Yurt, Coracle, Neurexin IV and the Na(+),K(+)-ATPase form a novel group of epithelial polarity proteins. Nature 459, 1141-1145.
29. Lawrence, P. A., Struhl, G. and Casal, J. (2007). Planar cell polarity: one or two pathways? Nat. Rev. Genet. 8, 555-563. (Pubitemid 46955212)
30. Lee, J. K., Brandin, E., Branton, D. and Goldstein, L. S. (1997). alpha-Spectrin is required for ovarian follicle monolayer integrity in Drosophila melanogaster. Development 124, 353-362.
31. Macara, I. G. (2004). Parsing the polarity code. Nat. Rev. Mol. Cell Biol. 5, 220-231.
32. Margolis, B. and Borg, J. P. (2005). Apicobasal polarity complexes. J. Cell Sci. 118, 5157-5159.
33. Mechler, B. M., McGinnis, W. and Gehring, W. J. (1985). Molecular cloning of lethal(2)giant larvae, a recessive oncogene of Drosophila melanogaster. EMBO J. 4, 1551-1557.
34. 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.
35. Na, J., Lykke-Andersen, K., Torres Padilla, M. E. and Zernicka-Goetz, M. (2007). Dishevelled proteins regulate cell adhesion in mouse blastocyst and serve to monitor changes in Wnt signaling. Dev. Biol. 302, 40-49. (Pubitemid 46096922)
36. Peifer, M., Pai, L. M. and Casey, M. (1994a). Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. Dev. Biol. 166, 543-556.
37. Peifer, M., Sweeton, D., Casey, M. and Wieschaus, E. (1994b). wingless signal and Zeste-white 3 kinase trigger opposing changes in the intracellular distribution of Armadillo. Development 120, 369-380.
38. Peng, C. Y., Manning, L., Albertson, R. and Doe, C. Q. (2000). The tumour-suppressor genes lgl and dlg regulate basal protein targeting in Drosophila neuroblasts. Nature 408, 596-600.
39. Price, M. H., Roberts, D. M., McCartney, B. M., Jezuit, E. and Peifer, M. (2006). Cytoskeletal dynamics and cell signaling during planar polarity establishment in the Drosophila embryonic denticle. J. Cell Sci. 119, 403-415.
40. Reya, T. and Clevers, H. (2005). Wnt signalling in stem cells and cancer. Nature 434, 843-850. (Pubitemid 40558990)
41. Schlessinger, K., McManus, E. J. and Hall, A. (2007). Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J. Cell Biol. 178, 355-361.
42. Schlessinger, K., Hall, A. and Tolwinski, N. (2009). Wnt signaling pathways meet Rho GTPases. Genes Dev. 23, 265-277.
43. 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.
44. Simons, M. and Mlodzik, M. (2008). Planar cell polarity signaling: from fly development to human disease. Annu. Rev. Genet. 42, 517-540.
45. Sokol, S. (2000). A role for Wnts in morpho-genesis and tissue polarity. Nat. Cell Biol. 2, E124-E125.
46. Strand, D., Jakobs, R., Merdes, G., Neumann, B., Kalmes, A., Heid, H. W., Husmann, I. and Mechler, B. M. (1994). The Drosophila lethal(2)giant larvae tumor suppressor protein forms homo-oligomers and is associated with nonmuscle myosin II heavy chain. J. Cell Biol. 127, 1361-1373.
47. Strand, D., Unger, S., Corvi, R., Hartenstein, K., Schenkel, H., Kalmes, A., Merdes, G., Neumann, B., Krieg-Schneider, F., Coy, J. F. et al. (1995). A human homologue of the Drosophila tumour suppressor gene l(2)gl maps to 17p11.2-12 and codes for a cytoskeletal protein that associates with nonmuscle myosin II heavy chain. Oncogene 11, 291-301.
48. Tanentzapf, G. and Tepass, U. (2003). Interactions between the crumbs, lethal giant larvae and bazooka pathways in epithelial polarization. Nat. Cell Biol. 5, 46-52. (Pubitemid 36054328)
49. 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.
50. Tolwinski, N. S. and Wieschaus, E. (2001). Armadillo nuclear import is regulated by cytoplasmic anchor Axin and nuclear anchor dTCF/Pan. Development 128, 2107-2117.
51. Tolwinski, N. S. and Wieschaus, E. (2004a). A nuclear function for armadillo/beta-catenin. PLoS Biol. 2, E95.
52. Tolwinski, N. S. and Wieschaus, E. (2004b). Rethinking WNT signaling. Trends Genet. 20, 177-181.
53. Torban, E., Kor, C. and Gros, P. (2004). Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends Genet. 20, 570-577.
54. Tree, D. R., Ma, D. and Axelrod, J. D. (2002). A three-tiered mechanism for regulation of planar cell polarity. Semin. Cell Dev. Biol. 13, 217-224.
55. 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.
56. Wang, Y. (2009). Wnt/planar cell polarity signaling: a new paradigm for cancer therapy. Mol. Cancer Ther. 8, 2103-2109.
57. Wirtz-Peitz, F. and Knoblich, J. A. (2006). Lethal giant larvae take on a life of their own. Trends Cell. Biol. 16, 234-241.
58. Yamanaka, H. and Nishida, E. (2007). Wnt11 stimulation induces polarized accumulation of Dishevelled at apical adherens junctions through Frizzled7. Genes Cells 12, 961-967. (Pubitemid 47261990)
59. Zallen, J. A. (2007). Planar polarity and tissue morphogenesis. Cell 129, 1051-63.
60. Zallen, J. A. and Wieschaus, E. (2004). Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 6, 343-355.
61. Zhang, X., Zhu, J., Yang, G. Y., Wang, Q. J., Qian, L., Chen, Y. M., Chen, F., Tao, Y., Hu, H. S., Wang, T. et al. (2007). Dishevelled promotes axon differentiation by regulating atypical protein kinase C. Nat. Cell Biol. 9, 743-754.