Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation

Genes and Development

Volumn 17, Issue 2, 2003, Pages 295-309

  Habas, Raymond ^a,b   Dawid, Igor B ^a   He, Xi ^b  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Frizzled; Gastrulation; Rac; Rho; Vertebrates; Wnt

Indexed keywords

COMPLEMENTARY DNA; GUANOSINE TRIPHOSPHATASE; RAC PROTEIN; RHO FACTOR; WNT PROTEIN;

ANIMAL CELL; ARTICLE; CELL POLARITY; EMBRYO; EMBRYO DEVELOPMENT; GASTRULATION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; VERTEBRATE; XENOPUS;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; CELL LINE; CELL MOVEMENT; CELL POLARITY; DROSOPHILA; FRIZZLED RECEPTORS; GASTRULA; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MITOGEN-ACTIVATED PROTEIN KINASES; MODELS, BIOLOGICAL; PHOSPHOPROTEINS; PROTEINS; PROTO-ONCOGENE PROTEINS; RAC GTP-BINDING PROTEINS; RHO GTP-BINDING PROTEINS; RNA; SIGNAL TRANSDUCTION; WNT PROTEINS; XENOPUS; ZEBRAFISH PROTEINS;

ANIMALIA; MAMMALIA; VERTEBRATA;

EID: 0037439138     PISSN: 08909369     EISSN: None     Source Type: Journal    
DOI: 10.1101/gad.1022203     Document Type: Article

References (70)

1. Adler, P.N. 2002. Planar signaling and morphogenesis in Drosophila. Dev. Cell. 2: 525-535.
2. Akasaki, T., Koga, H., and Sumimoto, H. 1999. Phosphoinositide 3-kinase-dependent and -independent activation of the small GTPase Rac2 in human neutrophils. J. Biol. Chem. 274: 18055-18059.
3. Axelrod, J.D. 2001. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes & Dev. 15: 1182-1187.
4. 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.
5. Benard, V., Bohl, B.P., and Bokoch, G.M. 1999. Characterization of Rac and Cdc42 activation in chemoattractant-stimulated human neutrophils using a novel assay for active GTPases. J. Biol. Chem. 274: 13198-13204.
6. Boutros, M. and Mlodzik, M. 1999. Dishevelled: At the crossroads of divergent intracellular signaling pathways. Mech. Dev. 83: 27-37.
7. Boutros, M., Paricio, N., Strutt, D.I., and Mlodzik, M. 1998. Dishevelled activates JNK and discriminates between JNK pathways in planar polarity and wingless signaling. Cell 94: 109-118.
8. Brown, A.M., Wildin, R.S., Prendergast, T.J., and Varmus, H.E. 1986. A retrovirus vector expressing the putative mammary oncogene int-1 causes partial transformation of a mammary epithelial cell line. Cell 46: 1001-1009.
9. 2+ signaling pathway. Dev. Bio. 244: 342-357.
10. Coso, O.A., Chiariello, M., Yu, J.C., Teramoto, H., Crespo, P., Xu, N., Miki, T., and Gutkind, J.S. 1995. The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81: 1137-1146.
11. Darken, R.S., Scola, A.M., Rakeman, A.S., Das, G., Mlodzik, M., and Wilson, P.A. 2002. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J. 21: 976-985.
12. Das, G., Reynolds-Kenneally, J., and Mlodzik, M. 2002. The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye. Dev. Cell. 2: 655-666.
13. Deardorff, M.A., Tan, C., Conrad, L.J., and Klein, P.S. 1998. Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. Development 125: 2687-2700.
14. Djiane, A., Riou, J.F., Umbhauer, M., Boucaut, J.C., and Shi, D.L. 2000. Role of Frizzled7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127: 3091-3400.
15. Eaton, S., Wepf, R., and Simons, K. 1996. Roles of Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135: 1277-1289.
16. Fanto, M., Weber, U., Strutt, D.I., and Mlodzik, M. 2000. Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr. Biol. 10: 979-988.
17. Goto, T. and Keller, R. 2002. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev Biol. 247: 165-181.
18. 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.
19. Hakeda-Suzuki, S., Ng, J., Tzu, J., Dietzl, G., Sun, Y., Harms, M., Nardine, T., Luo, L., and Dickson, B.J. 2002. Rac function and regulation during Drosophila development. Nature 416: 438-442.
20. Hall, A. 1998. Rho GTPases and the actin cytoskeleton. Science 279: 509-514.
21. Hart, M, Eva, A., Zangrilli, D., Aaronson, S., Evens, T., Cerione, R., and Zheng, Y. 1994. Cellular transformation and guanine nucleotide exchange activity are catalyzed by a common domain on the dbl oncogene product. J. Biol. Chem. 269: 6265.
22. He, X., Saint-Jeannet, J.P., Wang, Y., Nathans, J., Dawid, I., and Varmus, H. 1997. A member of the Frizzled protein family mediating axis induction by Wnt-5A. Science 275: 1652-1654.
23. Heisenberg, C.P., Tada, M., Rauch, G.J., Saude, L., Concha, M.L., Geisler, R., Stemple, D.L., Smith, J.C., and Wilson, S.W. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
24. Jessen, J.R., Topczewski, J., Bingham, S., Sepich, D.S., Marlow, F., Chandrasekhar, A., and Solnica-Krezel, L. 2002. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat Cell Biol. 4: 610-615.
25. Kaibuchi, K., Kuroda, S., and Amano, M. 1999. Regulation of the cytoskeleton and cell adhesion by the Rho family GTPases in mammalian cells. Annu. Rev. Biochem. 68: 459-486.
26. Kato, Y., Shi, Y., and He, X. 1999. Neuralization of the Xenopus embryo by inhibition of p300/CREB-binding protein function. J. Neuroscience. 19: 9364-9373.
27. Li, L., Yuan, H., Xie, W., Mao, J., Caruso, A.M., McMahon, A.P., Sussman, D.J., and Wu, D. 1999. Dishevelled proteins lead to two signaling pathways. Regulation of LEF-1 and c-Jun Nterminal kinase in mammalian cells. J. Biol. Chem. 274: 129-134.
28. Lisovsky, M., Itoh, K., and Sokol, S.Y. 2002. Frizzled receptors activate a novel JNK-dependent pathway that may lead to apoptosis. Curr Biol. 12: 53-58.
29. Lucas, J, M., Nikolic, I., and Hens, M.D. 2002. cDNA cloning, sequence comparison, and developmental expression of Xenopus racl. Mech Dev. 115: 113-116.
30. Marlow, F., Topczewski, J., Sepich, D., 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.
31. McEwen, D.G., Cox, R.T., and Peifer, M. 2000. The canonical Wg and JNK signaling cascades collaborate to promote both dorsal closure and ventral patterning. Development 127: 3607-3617.
32. Medina, A., Reintsch, W., and Steinbeisser, H. 2000. Xenopus Frizzled 7 can act in canonical and non-canonical Wnt signaling pathways; implications on early patterning and morphogenesis. Mech. Dev. 92: 227-237.
33. Miller, J.R., Hocking, A.M., Brown, J.D., and Moon, R.T. 1999. Mechanism and function of signal transduction by the Wnt/ beta-catenin and Wnt/Ca2+ pathways. Oncogene 18: 7860-7872.
34. Minden, A., Lin, A., Claret, F.X., Abo, A., and Karin, M. 1995. Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81: 1147-1157.
35. Mlodzik, M. 1999. Planar polarity in the Drosophila eye: a multifaceted view of signaling specificity and cross talk. EMBO J. 18: 6873-6879.
36. Moriguchi, T., Kawachi, K., Kamakura, S., Masuyama, N., Yamanaka, H., Matsumoto, K., Kikuchi, A., and Nishida, E. 1999. Distinct domains of mouse dishevelled are responsible for the c-Jun N-terminal kinase/stress-activated protein kinase activation and the axis formation in vertebrates. J. Biol. Chem. 274: 30957-30962.
37. Noselli, S. 1998. JNK signaling and morphogenesis in Drosophila. Trends Genet. 14: 33-38.
38. Park, M. and Moon, R.T. 2002. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol. 4: 20-25.
39. Pinson, K.I., Brennan, J., Monkley, S., Avery, B.J., and Skarnes, W.C. 2000. An LDL-receptor-related protein mediates Wnt signaling in mice. Nature 407: 535-538.
40. Ren, X.D., Kiosses, W.B., and Schwartz, M.A. 1999. Regulation of the small GTP-binding protein Rho by cell adhesion and the cytoskeleton. EMBO J. 18: 578-585.
41. Rijsewijk, F., van Deemter, L., Wagenaar, E., Sonnenberg, A., and Nusse, R. 1987. Transfection of the int-1 mammary oncogene in cuboidal RAC mammary cell line results in morphological transformation and tumorigenicity. EMBO J. 6: 127-131.
42. Schmidt, A. and Hall, A. 2002. Guanine nucleotide exchange factors for Rho GTPases: Turning on the switch. Genes & Dev. 16: 1587-1609.
43. Shamah, S.H., Lin, M.Z., Goldberg, J.L., Estrach, S., Sahin, M., Hu, L., Bazalakova, M., Neve, R.L., Corfas, G., Debant, A., et al. 2001. EphA receptors regulate growth cone dynamics through the novel guanine exchange factor Ephexin. Cell 105: 233-244.
44. Sheldahl, L.C., Park, M., Malbon, C.C., and Moon, R.T. 1999. Protein kinase C is differentially stimulated by Wnt and Frizzled homologs in a G-protein-dependent manner. Curr. Biol. 9: 695-698.
45. Shih, J. and Keller, R. 1992. Patterns of cell motility in the organizer and dorsal mesoderm of Xenopus laevis. Development 116: 915-930.
46. Shulman, J.M., Perrimon, N., and Axelrod, J.D. 1998. Frizzled signaling and the developmental control of cell polarity. Trends Genet. 14: 452-458.
47. Sokol, S.Y. 1996. Analysis of Dishevelled signaling pathways during Xenopus development. Curr. Biol. 6: 1456-1467.
48. Sokol, S.Y., Li, Z., Sacks, D.B. 2001. The effect of IQGAP1 on Xenopus embryonic ectoderm requires Cdc42. J. Biol. Chem. 276: 48425-48430.
49. Strutt, D.I. 2001. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol Cell. 7: 367-375.
50. Strutt, D.I., Weber, U., and Mlodzik, M. 1997. The role of RhoA in tissue polarity and Frizzled signaling. Nature 387: 292-295.
51. Strutt, D., Johnson, R., Cooper, K., and Bray, S. 2002. Asymmetric localization of frizzled and the determination of notchdependent cell fate in the Drosophila eye. Curr. Biol. 12: 813-824.
52. Sugihara, K., Nakatsuji, N., Nakamura, K., Nakao, K., Hashimoto, R., Otani, H., Sakagami, H., Kondo, H., Nozawa, S., Aiba, A., et al. 1998. Rac1 is required for the formation of three germ layers during gastrulation. Oncogene 17: 3427-3433.
53. Sumanas, S., Strege, P., Heasman, J., and Ekker, S.C. 2000. The putative Wnt receptor Xenopus frizzled-7 functions upstream of β-catenin in vertebrate dorsoventral mesoderm patterning. Development 127: 1981-1990.
54. Sun, T.Q., Lu, B., Feng, J.J., Reinhard, C., Jan, Y.N., Fantl, W.J., Williams, L.T. 2001. PAR-1 is a Dishevelled-associated kinase and a positive regulator of Wnt signaling. Nat Cell Biol. 3: 628-636.
55. Symes, K. and Smith, J.C. 1987. Gastrulation movements provide an early marker of mesoderm induction in Xenopus laevis. Development 101: 339-349.
56. 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 127: 2227-2238.
57. Tamai, K., Semenov, M., Kato, Y., Spokony, R., Liu, C., Katsuyama, Y., Hess, F., Saint-Jeannet, J.P., and He, X. 2000. LDL-receptor-related proteins in Wnt signal transduction. Nature. 407: 530-535.
58. Tree, D.R.P., Shulman, J.M., Rousset, R., Scott, M.P., Gubb, D., and Axelrod, J.D. 2002. Prickle mediates feedback amplification to generate asymmetric planar polarity signaling. Cell 109: 371-381.
59. Usui, T., Shima, Y., Shimada, Y., Hirano, S., Burgess, R.W., Schwarz, T.L., Takeichi, M., and Uemura. T. 1999. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98: 585595.
60. Van, Aelst, L. and Symons, M. 2002. Role of Rho family GTPases in epithelial morphogenesis. Genes & Dev. 16: 1032-1054.
61. Wallingford, J.B., Rowning, B.A., Vogeli, K., M., Rothbacher, U., Fraser, S.E., and Harland, R.M. 2000. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 404: 81-85.
62. Wallingford, J.B., Fraser, S.E., and Harland, R.M. 2002. Convergent extension: The molecular control of polarized cell movement during embryonic development. Dev. Cell. 6: 695-706.
63. Wehrli, M., Dougan, S.T., Caldwell, K., O'Keefe, L., Schwartz, S., Vaizel-Ohayon, D., Schejter, E., Tomlinson, A., and DiNardo, S. 2000. arrow encodes an Ldl-receptor-related protein essential for Wingless signaling. Nature 407: 527-530.
64. Winklbauer, R., Medina, A., Swain, R.K., and Steinbeisser, H. 2001. Frizzled-7 signalling controls tissue separation during Xenopus gastrulation. Nature 413: 856-860.
65. 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.
66. Wodarz, A. and Nusse, R. 1998. Mechanisms of Wnt signaling in development. Annu. Rev. Cell Dev. Biol. 14: 59-88.
67. Wolff, T. and Rubin, G.M. 1998. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125: 1149-1159.
68. Wunnenberg-Stapleton, K., Blitz, I.L., Hashimoto, C., and Cho, K.W. 1999. Involvement of the small GTPases XRhoA and XRndl in cell adhesion and head formation in early Xenopus development. Development 126: 5339-5351.
69. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S., and Nishida, E. 2002. JNK functions in the non-canonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3: 69-75.
70. Yang-Snyder, J., Miller, J.R., Brown, J.D., Lai, C-J., and Moon, R.T. 1996. A Frizzled homolog functions in a vertebrate Wnt signaling pathway. Curr. Biol. 6: 1302-1306.