Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation

Molecular Biology of the Cell

Volumn 19, Issue 5, 2008, Pages 2289-2299

  Kinoshita, Nagatoki ^a   Sasai, Noriaki ^a   Misaki, Kazuyo ^a   Yonemura, Shigenobu ^a  

^a RIKEN Center for Biosystems Dynamics Research   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II; PROTEIN; PROTEIN PCP; RHO FACTOR; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; WNT PROTEIN;

ARTICLE; CELL STRUCTURE; CHICK EMBRYO; CONTROLLED STUDY; EMBRYO; MORPHOGENESIS; NEURAL TUBE; NEURAL TUBE DEFECT; NEUROECTODERM; NEURULATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN SYNTHESIS INHIBITION; SIGNAL TRANSDUCTION;

ACTOMYOSIN; ANIMALS; CELL ADHESION; CELL POLARITY; CELL SHAPE; CHICK EMBRYO; EMBRYO, NONMAMMALIAN; ENZYME ACTIVATION; MYOSIN TYPE II; NEURAL PLATE; NEURAL TUBE; NEURULATION; PROTEIN TRANSPORT; RHO GTP-BINDING PROTEINS; WNT PROTEINS; XENOPUS;

EID: 48249120719     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E07-12-1286     Document Type: Article

References (45)

1. Bertet, C., Sulak, L., and Lecuit, T. (2004). Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 429, 667-671.
2. Brouns, M. R., Matheson, S. F., Hu, K. Q., Delalle, I., Caviness, V. S., Silver, J., Bronson, R. T., and Settleman, J. (2000). The adhesion signaling molecule p190 RhoGAP is required for morphogenetic processes in neural development. Development (Cambridge, England) 127, 4891-4903.
3. Chen, F. et al. (2000). Cdc42 is required for PIP(2)-induced actin polymerization and early development but not for cell viability. Curr. Biol. 10, 758-765.
4. Ciruna, B., Jenny, A., Lee, D., Mlodzik, M., and Schier, A. F. (2006). Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439, 220-224.
5. Djiane, A., Riou, J., Umbhauer, M., Boucaut, J., and Shi, D. (2000). Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development (Cambridge, England) 127, 3091-3100.
6. Habas, R., Dawid, I. B., and He, X. (2003). Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17, 295-309.
7. Habas, R., Kato, Y., and He, X. (2001). Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107, 843-854.
8. Haigo, S. L., Hildebrand, J. D., Harland, R. M., and Wallingford, J. B. (2003). Shroom induces apical constriction and is required for hingepoint formation during neural tube closure. Curr. Biol. 13, 2125-2137.
9. Harada, A., Katoh, H., and Negishi, M. (2005). Direct interaction of Rnd1 with FRS2 beta regulates Rnd1-induced down-regulation of RhoA activity and is involved in fibroblast growth factor-induced neurite outgrowth in PC12 cells. J. Biol. Chem. 280, 18418-18424.
10. Harden, N., Ricos, M., Ong, Y. M., Chia, W., and Lim, L. (1999). Participation of small GTPases in dorsal closure of the Drosophila embryo: distinct roles for Rho subfamily proteins in epithelial morphogenesis. J. Cell Sci. 112(Pt 3), 273-284.
11. Hildebrand, J. D. (2005). Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 118, 5191-5203.
12. Hildebrand, J. D., and Soriano, P. (1999). Shroom, a PDZ domain-containing actin-binding protein, is required for neural tube morphogenesis in mice. Cell 99, 485-497.
13. Jaffe, A. B., and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
14. Kikuchi, A., Yamamoto, H., and Kishida, S. (2006). Multiplicity of the interactions of Wnt proteins and their receptors. Cell Signal. 19, 659-671.
15. Kobayashi, D., Kobayashi, M., Matsumoto, K., Ogura, T., Nakafuku, M., and Shimamura, K. (2002). Early subdivisions in the neural plate define distinct competence for inductive signals. Development (Cambridge, England) 129, 83-93.
16. Kumagai, N., Morii, N., Fujisawa, K., Nemoto, Y., and Narumiya, S. (1993). ADP-ribosylation of rho p21 inhibits lysophosphatidic acid-induced protein tyrosine phosphorylation and phosphatidylinositol 3-kinase activation in cultured Swiss 3T3 cells. J. Biol. Chem. 268, 24535-24538.
17. Lanier, L. M., Gates, M. A., Witke, W., Menzies, A. S., Wehman, A. M., Macklis, J. D., Kwiatkowski, D., Soriano, P., and Gertler, F. B. (1999). Mena is required for neurulation and commissure formation. Neuron 22, 313-325.
18. Mizuseki, K., Kishi, M., Matsui, M., Nakanishi, S., and Sasai, Y. (1998). Xenopus Zic-related-1 and Sox-2, two factors induced by chordin, have distinct activities in the initiation of neural induction. Development (Cambridge, England) 125, 579-587.
19. Nagai, T., Ibata, K., Park, E. S., Kubota, M., Mikoshiba, K., and Miyawaki, A. (2002). A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications. Nat. Biotechnol. 20, 87-90.
20. Niwa, H., Yamamura, K., and Miyazaki, J. (1991). Efficient selection for high-expression transfectants with a novel eukaryotic vector. Gene 108, 193-199.
21. Park, J., Kim, J. S., Jung, K. C., Lee, H. J., Kim, J. I., Kim, J., Lee, J. Y., Park, J. B., and Choi, S. Y. (2003). Exoenzyme Tat-C3 inhibits association of zymosan particles, phagocytosis, adhesion, and complement binding in macrophage cells. Mol. Cell 16, 216-223.
22. Reid, T., Furuyashiki, T., Ishizaki, T., Watanabe, G., Watanabe, N., Fujisawa, K., Morii, N., Madaule, P., and Narumiya, S. (1996). Rhotekin, a new putative target for Rho bearing homology to a serine/threonine kinase, PKN, and rhophilin in the rho-binding domain. J. Biol. Chem. 271, 13556-13560.
23. Schoenwolf, G. C., Folsom, D., and Moe, A. (1988). A reexamination of the role of microfilaments in neurulation in the chick embryo. Anat. Rec. 220, 87-102.
24. Shimizu, Y., Thumkeo, D., Keel, J., Ishizaki, T., Oshima, H., Oshima, M., Noda, Y., Matsumura, F., Taketo, M. M., and Narumiya, S. (2005). ROCK-I regulates closure of the eyelids and ventral body wall by inducing assembly of actomyosin bundles. J. Cell Biol. 168, 941-953.
25. Smith, J. L., and Schoenwolf, G. C. (1997). Neurulation: coming to closure. Trends Neurosci. 20, 510-517.
26. Sokol, S. Y. (1996). Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol. 6, 1456-1467.
27. Sugihara, K. et al. (1998). Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17, 3427-3433.
28. Sundin, O., and Eichele, G. (1992). An early marker of axial pattern in the chick embryo and its respecification by retinoic acid. Development (Cambridge, England) 114, 841-852.
29. Suzuki, T., Futaki, S., Niwa, M., Tanaka, S., Ueda, K., and Sugiura, Y. (2002). Possible existence of common internalization mechanisms among arginine-rich peptides. J. Biol. Chem. 277, 2437-2443.
30. Tada, M., Concha, M. L., and Heisenberg, C. P. (2002). Non-canonical Wnt signalling and regulation of gastrulation movements. Semin. Cell Dev. Biol. 13, 251-260.
31. Tada, M., and Smith, J. C. (2000). Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development (Cambridge, England) 127, 2227-2238.
32. Takai, Y., Sasaki, T., Tanaka, K., and Nakanishi, H. (1995). Rho as a regulator of the cytoskeleton. Trends Biochem. Sci. 20, 227-231.
33. Theriault, B. L., Shepherd, T. G., Mujoomdar, M. L., and Nachtigal, M. W. (2007). BMP4 induces EMT and Rho GTPase activation in human ovarian cancer cells. Carcinogenesis. 28, 1153-1162.
34. Van Aelst, L., and D'Souza-Schorey, C. (1997). Rho GTPases and signaling networks. Genes Dev. 11, 2295-2322.
35. Veeman, M. T., Axelrod, J. D., and Moon, R. T. (2003). A second canon. Functions and mechanisms of beta-catenin-independent Wnt signaling. Dev. Cell 5, 367-377.
36. Wallingford, J. B., and Harland, R. M. (2002). Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development (Cambridge, England) 129, 5815-5825.
37. Wang, J., Hamblet, N. S., Mark, S., Dickinson, M. E., Brinkman, B. C., Segil, N., Fraser, S. E., Chen, P., Wallingford, J. B., and Wynshaw-Boris, A. (2006). Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development (Cambridge, England) 133, 1767-1778.
38. Wei, L., Roberts, W., Wang, L., Yamada, M., Zhang, S., Zhao, Z., Rivkees, S. A., Schwartz, R. J., and Imanaka-Yoshida, K. (2001). Rho kinases play an obligatory role in vertebrate embryonic organogenesis. Development (Cambridge, England) 128, 2953-2962.
39. 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.
40. Wu, M., Chen, D. F., Sasaoka, T., and Tonegawa, S. (1996). Neural tube defects and abnormal brain development in F52-deficient mice. Proc. Natl. Acad. Sci. USA 93, 2110-2115.
41. Xu, W., Baribault, H., and Adamson, E. D. (1998). Vinculin knockout results in heart and brain defects during embryonic development. Development (Cambridge, England) 125, 327-337.
42. Ybot-Gonzalez, P., Savery, D., Gerrelli, D., Signore, M., Mitchell, C. E., Faux, C. H., Greene, N. D., and Copp, A. J. (2007). Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development (Cambridge, England) 134, 789-799.
43. Yonemura, S., Hirao-Minakuchi, K., and Nishimura, Y. (2004). Rho localization in cells and tissues. Exp. Cell Res. 295, 300-314.
44. Zhang, Y., Sawada, T., Jing, X., Yokote, H., Yan, X., and Sakaguchi, K. (2007). Regulation of ephexin1, a guanine nucleotide exchange factor of Rho family GTPases, by fibroblast growth factor receptor-mediated tyrosine phosphorylation. J. Biol. Chem. 282, 31103-31112.
45. Zhao, Z. S., and Manser, E. (2005). PAK and other Rho-associated kinases - effectors with surprisingly diverse mechanisms of regulation. Biochem. J. 386, 201-214.