GEF-H1 functions in apical constriction and cell intercalations and is essential for vertebrate neural tube closure

Journal of Cell Science

Volumn 127, Issue 11, 2014, Pages 2542-2553

  Itoh, Keiji ^a   Ossipova, Olga ^a   Sokol, Sergei Y ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apical constriction; Cell intercalation; Epiboly; Lfc; Morphogenesis; Myosin II; Neural tube closure; Rho GTPases; Xenopus

Indexed keywords

F ACTIN; GAMMA TUBULIN; MORPHOLINO OLIGONUCLEOTIDE; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; MYOSIN LIGHT CHAIN; PLASMID DNA; RHO GUANINE NUCLEOTIDE BINDING PROTEIN; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR GEF H1; SERUM RESPONSE FACTOR; TRANSCRIPTION FACTOR SOX2; UNCLASSIFIED DRUG; WNT PROTEIN; ACTIN; GEF-H1 PROTEIN, XENOPUS; RAB PROTEIN; RAB11 PROTEIN; RHO KINASE; TUBULIN; XENOPUS PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CELL INTERCALATION; CELL SHAPE; CELL STRUCTURE; CELLULAR, SUBCELLULAR AND MOLECULAR BIOLOGICAL PHENOMENA AND FUNCTIONS; CONTROLLED STUDY; ECTODERM; EMBRYO; EMBRYO CULTURE; EMBRYO DEVELOPMENT; GAIN OF FUNCTION MUTATION; GASTRULATION; LIGATION; MORPHOGENESIS; NERVOUS TISSUE; NEURAL TUBE; NEURAL TUBE DEFECT; NEUROECTODERM; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; WESTERN BLOTTING; WNT SIGNALING PATHWAY; XENOPUS LAEVIS; ANIMAL; CELL COMMUNICATION; CELL CULTURE; CELL SURFACE; GENETICS; METABOLISM; NONMAMMALIAN EMBRYO; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN TRANSPORT; XENOPUS;

ACTINS; ANIMALS; CELL COMMUNICATION; CELL SURFACE EXTENSIONS; CELLS, CULTURED; CONSTRICTION; EMBRYO, NONMAMMALIAN; MORPHOGENESIS; MORPHOLINOS; MYOSIN TYPE II; NEURAL TUBE; PHOSPHORYLATION; PROTEIN TRANSPORT; RAB GTP-BINDING PROTEINS; RHO GUANINE NUCLEOTIDE EXCHANGE FACTORS; RHO-ASSOCIATED KINASES; TUBULIN; XENOPUS; XENOPUS PROTEINS;

EID: 84901779215     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.146811     Document Type: Article

References (91)

1. Aijaz, S., D'Atri, F., Citi, S., Balda, M. S. and Matter, K. (2005). Binding of GEFH1 to the tight junction-associated adaptor cingulin results in inhibition of Rho signaling and G1/S phase transition. Dev. Cell 8, 777-786.
2. 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.
3. Benais-Pont, G., Punn, A., Flores-Maldonado, C., Eckert, J., Raposo, G., Fleming, T. P., Cereijido, M., Balda, M. S. and Matter, K. (2003). Identification of a tight junction-associated guanine nucleotide exchange factor that activates Rho and regulates paracellular permeability. J. Cell Biol. 160, 729-740.
4. Birkenfeld, J., Nalbant, P., Bohl, B. P., Pertz, O., Hahn, K. M. and Bokoch, G. M. (2007). GEF-H1 modulates localized RhoA activation during cytokinesis under the control of mitotic kinases. Dev. Cell 12, 699-712.
5. Birkenfeld, J., Nalbant, P., Yoon, S. H. and Bokoch, G. M. (2008). Cellular functions of GEF-H1, a microtubule-regulated Rho-GEF: is altered GEF-H1 activity a crucial determinant of disease pathogenesis? Trends Cell Biol. 18, 210-219.
6. Birukova, A. A., Adyshev, D., Gorshkov, B., Bokoch, G. M., Birukov, K. G. and Verin, A. D. (2006). GEF-H1 is involved in agonist-induced human pulmonary endothelial barrier dysfunction. Am. J. Physiol. 290, L540-L548.
7. Busche, S., Descot, A., Julien, S., Genth, H. and Posern, G. (2008). Epithelial cell-cell contacts regulate SRF-mediated transcription via Rac-actin-MAL signalling. J. Cell Sci. 121, 1025-1035.
8. Chang, Y. C., Nalbant, P., Birkenfeld, J., Chang, Z. F. and Bokoch, G. M. (2008). GEF-H1 couples nocodazole-induced microtubule disassembly to cell contractility via RhoA. Mol. Biol. Cell 19, 2147-2153.
9. Choi, S. C. and Sokol, S. Y. (2009). The involvement of lethal giant larvae and Wnt signaling in bottle cell formation in Xenopus embryos. Dev. Biol. 336, 68-75.
10. Chu, C. W., Gerstenzang, E., Ossipova, O. and Sokol, S. Y. (2013). Lulu regulates Shroom-induced apical constriction during neural tube closure. PLoS ONE 8, e81854.
11. Colas, J. F. and Schoenwolf, G. C. (2001). Towards a cellular and molecular understanding of neurulation. Dev. Dyn. 221, 117-145.
12. Davidson, L. A. and Keller, R. E. (1999). Neural tube closure in Xenopus laevis involves medial migration, directed protrusive activity, cell intercalation and convergent extension. Development 126, 4547-4556.
13. De Robertis, E. M. and Kuroda, H. (2004). Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu. Rev. Cell Dev. Biol. 20, 285-308.
14. Dollar, G. L., Weber, U., Mlodzik, M. and Sokol, S. Y. (2005). Regulation of lethal giant larvae by dishevelled. Nature 437, 1376-1380.
15. Ekker, S. C. (2000). Morphants: a new systematic vertebrate functional genomics approach. Yeast 17, 302-306.
16. Elul, T., Koehl, M. A. and Keller, R. (1997). Cellular mechanism underlying neural convergent extension in Xenopus laevis embryos. Dev. Biol. 191, 243-258.
17. Fan, M. J., Grüning, W., Walz, G. and Sokol, S. Y. (1998). Wnt signaling and transcriptional control of Siamois in Xenopus embryos. Proc. Natl. Acad. Sci. USA 95, 5626-5631.
18. Glaven, J. A., Whitehead, I., Bagrodia, S., Kay, R. and Cerione, R. A. (1999). The Dbl-related protein, Lfc, localizes to microtubules and mediates the activation of Rac signaling pathways in cells. J. Biol. Chem. 274, 2279-2285.
19. Gray, R. S., Roszko, I. and Solnica-Krezel, L. (2011). Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell 21, 120-133.
20. Guillemot, L., Paschoud, S., Jond, L., Foglia, A. and Citi, S. (2008). Paracingulin regulates the activity of Rac1 and RhoA GTPases by recruiting Tiam1 and GEF-H1 to epithelial junctions. Mol. Biol. Cell 19, 4442-4453.
21. 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.
22. 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.
23. Häcker, 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.
24. 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.
25. Hall, A. (2005). Rho GTPases and the control of cell behaviour. Biochem. Soc. Trans. 33, 891-895.
26. Harland, R. M. (1991). In situ hybridization: an improved whole-mount method for Xenopus embryos. Methods Cell Biol. 36, 685-695.
27. Harris, M. J. and Juriloff, D. M. (2010). An update to the list of mouse mutants with neural tube closure defects and advances toward a complete genetic perspective of neural tube closure. Birth Defects Res. A Clin. Mol. Teratol. 88, 653-669.
28. Heasman, J., Kofron, M. and Wylie, C. (2000). Beta-catenin signaling activity dissected in the early Xenopus embryo: a novel antisense approach. Dev. Biol. 222, 124-134.
29. Heasman, S. J., Carlin, L. M., Cox, S., Ng, T. and Ridley, A. J. (2010). Coordinated RhoA signaling at the leading edge and uropod is required for Tcell transendothelial migration. J. Cell Biol. 190, 553-563.
30. Hildebrand, J. D. (2005). Shroom regulates epithelial cell shape via the apical positioning of an actomyosin network. J. Cell Sci. 118, 5191-5203.
31. 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.
32. Howard, J. E. and Smith, J. C. (1993). Analysis of gastrulation: different types of gastrulation movement are induced by different mesoderm-inducing factors in Xenopus laevis. Mech. Dev. 43, 37-48.
33. Itoh, K., Antipova, A., Ratcliffe, M. J. and Sokol, S. (2000). Interaction of dishevelled and Xenopus axin-related protein is required for wnt signal transduction. Mol. Cell. Biol. 20, 2228-2238.
34. Itoh, K., Brott, B. K., Bae, G. U., Ratcliffe, M. J. and Sokol, S. Y. (2005). Nuclear localization is required for Dishevelled function in Wnt/beta-catenin signaling. J. Biol. 4, 3.
35. Jaffe, A. B. and Hall, A. (2005). Rho GTPases: biochemistry and biology. Annu. Rev. Cell Dev. Biol. 21, 247-269.
36. Kashef, J., Köhler, A., Kuriyama, S., Alfandari, D., Mayor, R. and Wedlich, D. (2009). Cadherin-11 regulates protrusive activity in Xenopus cranial neural crest cells upstream of Trio and the small GTPases. Genes Dev. 23, 1393-1398.
37. Keller, R. E. (1980). The cellular basis of epiboly: an SEM study of deep-cell rearrangement during gastrulation in Xenopus laevis. J. Embryol. Exp. Morphol. 60, 201-234.
38. Keller, R. (1991). Early embryonic development of Xenopus laevis. Methods Cell Biol. 36, 61-113.
39. Keller, R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954.
40. Keller, R., Shih, J. and Sater, A. (1992a). The cellular basis of the convergence and extension of the Xenopus neural plate. Dev. Dyn. 193, 199-217.
41. Keller, R., Shih, J., Sater, A. K. and Moreno, C. (1992b). Planar induction of convergence and extension of the neural plate by the organizer of Xenopus. Dev. Dyn. 193, 218-234.
42. Kinoshita, N., Sasai, N., Misaki, K. and Yonemura, S. (2008). Apical accumulation of Rho in the neural plate is important for neural plate cell shape change and neural tube formation. Mol. Biol. Cell 19, 2289-2299.
43. Kölsch, V., Seher, T., Fernandez-Ballester, G. J., Serrano, L. and Leptin, M. (2007). Control of Drosophila gastrulation by apical localization of adherens junctions and RhoGEF2. Science 315, 384-386.
44. Krendel, M., Zenke, F. T. and Bokoch, G. M. (2002). Nucleotide exchange factor GEF-H1 mediates cross-talk between microtubules and the actin cytoskeleton. Nat. Cell Biol. 4, 294-301.
45. Kwan, K. M. and Kirschner, M. W. (2005). A microtubule-binding Rho-GEF controls cell morphology during convergent extension of Xenopus laevis. Development 132, 4599-4610.
46. Lecuit, T., Lenne, P. F. and Munro, E. (2011). Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 27, 157-184.
47. Lee, J. Y. and Harland, R. M. (2007). Actomyosin contractility and microtubules drive apical constriction in Xenopus bottle cells. Dev. Biol. 311, 40-52.
48. Lee, C., Scherr, H. M. and Wallingford, J. B. (2007a). Shroom family proteins regulate gamma-tubulin distribution and microtubule architecture during epithelial cell shape change. Development 134, 1431-1441.
49. Lee, J. D., Silva-Gagliardi, N. F., Tepass, U., McGlade, C. J. and Anderson, K. V. (2007b). The FERM protein Epb4.1l5 is required for organization of the neural plate and for the epithelial-mesenchymal transition at the primitive streak of the mouse embryo. Development 134, 2007-2016.
50. Makarova, O., Kamberov, E. and Margolis, B. (2000). Generation of deletion and point mutations with one primer in a single cloning step. Biotechniques 29, 970-972.
51. Marlow, F., Topczewski, J., Sepich, D. and Solnica-Krezel, L. (2002). Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12, 876-884.
52. Meiri, D., Marshall, C. B., Greeve, M. A., Kim, B., Balan, M., Suarez, F., Bakal, C., Wu, C., Larose, J., Fine, N. et al. (2012). Mechanistic insight into the microtubule and actin cytoskeleton coupling through dynein-dependent RhoGEF inhibition. Mol. Cell 45, 642-655.
53. Miyakoshi, A., Ueno, N. and Kinoshita, N. (2004). Rho guanine nucleotide exchange factor xNET1 implicated in gastrulation movements during Xenopus development. Differentiation 72, 48-55.
54. 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 125, 579-587.
55. Mohan, S., Rizaldy, R., Das, D., Bauer, R. J., Heroux, A., Trakselis, M. A., Hildebrand, J. D. and VanDemark, A. P. (2012). Structure of Shroom domain 2 reveals a three-segmented coiled-coil required for dimerization, Rock binding, and apical constriction. Mol. Biol. Cell 23, 2131-2142.
56. Morgan, R., Hooiveld, M. H. and Durston, A. J. (1999). A novel guanine exchange factor increases the competence of early ectoderm to respond to neural induction. Mech. Dev. 88, 67-72.
57. Nakajima, H. and Tanoue, T. (2012). The circumferential actomyosin belt in epithelial cells is regulated by the Lulu2-p114RhoGEF system. Small GTPases 3, 91-96.
58. Nalbant, P., Chang, Y. C., Birkenfeld, J., Chang, Z. F. and Bokoch, G. M. (2009). Guanine nucleotide exchange factor-H1 regulates cell migration via localized activation of RhoA at the leading edge. Mol. Biol. Cell 20, 4070-4082.
59. Nandadasa, S., Tao, Q., Menon, N. R., Heasman, J. and Wylie, C. (2009). Nand E-cadherins in Xenopus are specifically required in the neural and nonneural ectoderm, respectively, for F-actin assembly and morphogenetic movements. Development 136, 1327-1338.
60. Newport, J. and Kirschner, M. (1982). A major developmental transition in early Xenopus embryos: I. characterization and timing of cellular changes at the midblastula stage. Cell 30, 675-686.
61. Nieuwkoop, P. D. and Faber, J. (1967). Normal Table of Xenopus Laevis (Daudin). Amsterdam: North Holland.
62. Nishimura, T. and Takeichi, M. (2008). Shroom3-mediated recruitment of Rho kinases to the apical cell junctions regulates epithelial and neuroepithelial planar remodeling. Development 135, 1493-1502.
63. Nishimura, T., Honda, H. and Takeichi, M. (2012). Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149, 1084-1097.
64. Ossipova, O., Tabler, J., Green, J. B. and Sokol, S. Y. (2007). PAR1 specifies ciliated cells in vertebrate ectoderm downstream of aPKC. Development 134, 4297-4306.
65. Ossipova, O., Kim, K., Lake, B. B., Itoh, K., Ioannou, A. and Sokol, S. Y. (2014). Role of Rab11 in planar cell polarity and apical constriction during vertebrate neural tube closure. Nat. Commun. 5:3734, doi: 10.1038/ncomms4734.
66. Panizzi, J. R., Jessen, J. R., Drummond, I. A. and Solnica-Krezel, L. (2007). New functions for a vertebrate Rho guanine nucleotide exchange factor in ciliated epithelia. Development 134, 921-931.
67. Pathak, R., Delorme-Walker, V. D., Howell, M. C., Anselmo, A. N., White, M. A., Bokoch, G. M. and Dermardirossian, C. (2012). The microtubule-associated Rho activating factor GEF-H1 interacts with exocyst complex to regulate vesicle traffic. Dev. Cell 23, 397-411.
68. Plageman, T. F., Jr, Chauhan, B. K., Yang, C., Jaudon, F., Shang, X., Zheng, Y., Lou, M., Debant, A., Hildebrand, J. D. and Lang, R. A. (2011). A Trio-RhoAShroom3 pathway is required for apical constriction and epithelial invagination. Development 138, 5177-5188.
69. Posern, G. and Treisman, R. (2006). Actin' together: serum response factor, its cofactors and the link to signal transduction. Trends Cell Biol. 16, 588-596.
70. Posern, G., Sotiropoulos, A. and Treisman, R. (2002). Mutant actins demonstrate a role for unpolymerized actin in control of transcription by serum response factor. Mol. Biol. Cell 13, 4167-4178.
71. Poznanski, A., Minsuk, S., Stathopoulos, D. and Keller, R. (1997). Epithelial cell wedging and neural trough formation are induced planarly in Xenopus, without persistent vertical interactions with mesoderm. Dev. Biol. 189, 256-269.
72. Rauzi, M., Lenne, P. F. and Lecuit, T. (2010). Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 468, 1110-1114.
73. Ren, Y., Li, R., Zheng, Y. and Busch, H. (1998). Cloning and characterization of GEF-H1, a microtubule-associated guanine nucleotide exchange factor for Rac and Rho GTPases. J. Biol. Chem. 273, 34954-34960.
74. Rolo, A., Skoglund, P. and Keller, R. (2009). Morphogenetic movements driving neural tube closure in Xenopus require myosin IIB. Dev. Biol. 327, 327-338.
75. Rossman, K. L., Der, C. J. and Sondek, J. (2005). GEF means go: turning on RHO GTPases with guanine nucleotide-exchange factors. Nat. Rev. Mol. Cell Biol. 6, 167-180.
76. Saka, Y. and Smith, J. C. (2001). Spatial and temporal patterns of cell division during early Xenopus embryogenesis. Dev. Biol. 229, 307-318.
77. Sawyer, J. M., Harrell, J. R., Shemer, G., Sullivan-Brown, J., Roh-Johnson, M. and Goldstein, B. (2010). Apical constriction: a cell shape change that can drive morphogenesis. Dev. Biol. 341, 5-19.
78. Schroeder, T. E. (1970). Neurulation in Xenopus laevis. An analysis and model based upon light and electron microscopy. J. Embryol. Exp. Morphol. 23, 427-462.
79. Sokol, S. Y. (1996). Analysis of Dishevelled signalling pathways during Xenopus development. Curr. Biol. 6, 1456-1467.
80. Suzuki, M., Morita, H. and Ueno, N. (2012). Molecular mechanisms of cell shape changes that contribute to vertebrate neural tube closure. Dev. Growth Differ. 54, 266-276.
81. Tanegashima, K., Zhao, H. and Dawid, I. B. (2008). WGEF activates Rho in the Wnt-PCP pathway and controls convergent extension in Xenopus gastrulation. EMBO J. 27, 606-617.
82. Tsapara, A., Luthert, P., Greenwood, J., Hill, C. S., Matter, K. and Balda, M. S. (2010). The RhoA activator GEF-H1/Lfc is a transforming growth factor-beta target gene and effector that regulates alpha-smooth muscle actin expression and cell migration. Mol. Biol. Cell 21, 860-870.
83. Tsuji, T., Ohta, Y., Kanno, Y., Hirose, K., Ohashi, K. and Mizuno, K. (2010). Involvement of p114-RhoGEF and Lfc in Wnt-3a-and dishevelled-induced RhoA activation and neurite retraction in N1E-115 mouse neuroblastoma cells. Mol. Biol. Cell 21, 3590-3600.
84. Tullio, A. N., Bridgman, P. C., Tresser, N. J., Chan, C. C., Conti, M. A., Adelstein, R. S. and Hara, Y. (2001). Structural abnormalities develop in the brain after ablation of the gene encoding nonmuscle myosin II-B heavy chain. J. Comp. Neurol. 433, 62-74.
85. Turner, D. L. and Weintraub, H. (1994). Expression of achaete-scute homolog 3 in Xenopus embryos converts ectodermal cells to a neural fate. Genes Dev. 8, 1434-1447.
86. Vicente-Manzanares, M., Ma, X., Adelstein, R. S. and Horwitz, A. R. (2009). Non-muscle myosin II takes centre stage in cell adhesion and migration. Nat. Rev. Mol. Cell Biol. 10, 778-790.
87. Wallingford, J. B., Niswander, L. A., Shaw, G. M. and Finnell, R. H. (2013). The continuing challenge of understanding, preventing, and treating neural tube defects. Science 339, 1222002.
88. Ward, Y., Yap, S. F., Ravichandran, V., Matsumura, F., Ito, M., Spinelli, B. and Kelly, K. (2002). The GTP binding proteins Gem and Rad are negative regulators of the Rho-Rho kinase pathway. J. Cell Biol. 157, 291-302.
89. Yamahashi, Y., Saito, Y., Murata-Kamiya, N. and Hatakeyama, M. (2011). Polarity-regulating kinase partitioning-defective 1b (PAR1b) phosphorylates guanine nucleotide exchange factor H1 (GEF-H1) to regulate RhoA-dependent actin cytoskeletal reorganization. J. Biol. Chem. 286, 44576-44584.
90. Yoshimura, Y. and Miki, H. (2011). Dynamic regulation of GEF-H1 localization at microtubules by Par1b/MARK2. Biochem. Biophys. Res. Commun. 408, 322-328.
91. Zhou, J., Kim, H. Y., Wang, J. H. and Davidson, L. A. (2010). Macroscopic stiffening of embryonic tissues via microtubules, RhoGEF and the assembly of contractile bundles of actomyosin. Development 137, 2785-2794.