Wnt5a and Wnt11 regulate mammalian anterior-posterior axis elongation

Development (Cambridge)

Volumn 142, Issue 8, 2015, Pages 1516-1527

  Andre, Philipp ^a   Song, Hai ^a,d   Kim, Wantae ^a   Kispert, Andreas ^b   Yang, Yingzi ^a,c  

^a NATIONAL HUMAN GENOME RESEARCH INSTITUTE   (United States)

^b HANNOVER MEDICAL SCHOOL   (Germany)

^c HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^d ZHEJIANG UNIVERSITY   (China)

Author keywords

Convergent extension; EMT; Gastrulation; Notochord; Planar cell polarity; Wnt

Indexed keywords

WNT11 PROTEIN; WNT5A PROTEIN; WNT PROTEIN; WNT11 PROTEIN, MOUSE; WNT5A PROTEIN, MOUSE;

ANIMAL CELL; ANTERIOR POSTERIOR AXIS; ARTICLE; CELL ADHESION; CELL POLARITY; CONTROLLED STUDY; EMBRYO; GASTRULATION; GENE CONTROL; GENE FUNCTION; MOUSE; NONHUMAN; NOTOCHORD; PRIORITY JOURNAL; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; REGULATORY MECHANISM; ANIMAL; CELL CULTURE; EMBRYOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; GASTRULA; GENETICS; HUMAN; IN SITU HYBRIDIZATION; METABOLISM; MUTANT MOUSE STRAIN; PHYSIOLOGY;

MAMMALIA; VERTEBRATA;

ANIMALS; CELL POLARITY; CELLS, CULTURED; EPITHELIAL-MESENCHYMAL TRANSITION; GASTRULA; HUMANS; IN SITU HYBRIDIZATION; MICE; MICE, MUTANT STRAINS; NOTOCHORD; WNT PROTEINS;

EID: 84926379944     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.119065     Document Type: Article

References (116)

1. Abdelkhalek, H. B., Beckers, A., Schuster-Gossler, K., Pavlova, M. N., Burkhardt, H., Lickert, H., Rossant, J., Reinhardt, R., Schalkwyk, L. C., Müller, I. et al. (2004). The mouse homeobox gene Not is required for caudal notochord development and affected by the truncate mutation. Genes Dev. 18, 1725-1736.
2. Arnold, S. J. and Robertson, E. J. (2009). Making a commitment: cell lineage allocation and axis patterning in the early mouse embryo. Nat. Rev. Mol. Cell Biol. 10, 91-103.
3. Arnold, S. J., Hofmann, U. K., Bikoff, E. K. and Robertson, E. J. (2008). Pivotal roles for eomesodermin during axis formation, epithelium-to-mesenchyme transition and endoderm specification in the mouse. Development 135, 501-511.
4. Barrallo-Gimeno, A. and Nieto, M. A. (2005). The Snail genes as inducers of cell movement and survival: implications in development and cancer. Development 132, 3151-3161.
5. Beddington, R. S. P. and Robertson, E. J. (1999). Axis development and early asymmetry in mammals. Cell 96, 195-209.
6. Bellomo, D., Lander, A., Harragan, I. and Brown, N. A. (1996). Cell proliferation in mammalian gastrulation: the ventral node and notochord are relatively quiescent. Dev. Dyn. 205, 471-485.
7. Bessho, Y., Miyoshi, G., Sakata, R. and Kageyama, R. (2001). Hes7: a bHLH-type repressor gene regulated by Notch and expressed in the presomitic mesoderm. Genes Cells 6, 175-185.
8. Bettenhausen, B., Hrabe de Angelis, M., Simon, D., Guenet, J. L. and Gossler, A. (1995). Transient and restricted expression during mouse embryogenesis of Dll1, a murine gene closely related to Drosophila Delta. Development 121, 2407-2418.
9. Blum, M., Andre, P., Muders, K., Schweickert, A., Fischer, A., Bitzer, E., Bogusch, S., Beyer, T., van Straaten, H.W. M. and Viebahn, C. (2007). Ciliation and gene expression distinguish between node and posterior notochord in the mammalian embryo. Differentiation 75, 133-146.
10. Borovina, A., Superina, S., Voskas, D. and Ciruna, B. (2010). Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol. 12, 407-412.
11. Cambray, N. and Wilson, V. (2002). Axial progenitors with extensive potency are localised to the mouse chordoneural hinge. Development 129, 4855-4866.
12. Cambray, N. and Wilson, V. (2007). Two distinct sources for a population of maturing axial progenitors. Development 134, 2829-2840.
13. Chapman, D. L. and Papaioannou, V. E. (1998). Three neural tubes in mouse embryos with mutations in the T-box gene Tbx6. Nature 391, 695-697.
14. Chen, H.-H., Zhou, X.-L., Shi, Y.-l. and Yang, J. (2013). Roles of p38 MAPK and JNK in TGF-beta1-induced human alveolar epithelial to mesenchymal transition. Arch. Med. Res. 44, 93-98.
15. Chiang, C., Litingtung, Y., Lee, E., Young, K. E., Corden, J. L., Westphal, H. and Beachy, P. A. (1996). Cyclopia and defective axial patterning in mice lacking Sonic hedgehog gene function. Nature 383, 407-413.
16. Ciruna, B. and Rossant, J. (2001). FGF signaling regulates mesoderm cell fate specification and morphogenetic movement at the primitive streak. Dev. Cell 1, 37-49.
17. Cleaver, O. and Krieg, P. A. (2001). Notochord patterning of the endoderm. Dev. Biol. 234, 1-12.
18. Cohen, E. D., Miller, M. F., Wang, Z., Moon, R. T. and Morrisey, E. E. (2012). Wnt5a and Wnt11 are essential for second heart field progenitor development. Development 139, 1931-1940.
19. Collignon, J., Sockanathan, S., Hacker, A., Cohen-Tannoudji, M., Norris, D., Rastan, S., Stevanovic, M., Goodfellow, P. N. and Lovell-Badge, R. (1996). A comparison of the properties of Sox-3 with Sry and two related genes, Sox-1 and Sox-2. Development 122, 509-520.
20. Conlon, R. A., Reaume, A. G. and Rossant, J. (1995). Notch1 is required for the coordinate segmentation of somites. Development 121, 1533-1545.
21. Crossley, P. H. and Martin, G. R. (1995). The mouse Fgf8 gene encodes a family of polypeptides and is expressed in regions that direct outgrowth and patterning in the developing embryo. Development 121, 439-451.
22. Curtin, J. A., Quint, E., Tsipouri, V., Arkell, R. M., Cattanach, B., Copp, A. J., Henderson, D. J., Spurr, N., Stanier, P., Fisher, E. M. et al. (2003). Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 13, 1129-1133.
23. Dale, J. K., Maroto, M., Dequeant, M.-L., Malapert, P., McGrew, M. and Pourquie, O. (2003). Periodic notch inhibition by lunatic fringe underlies the chick segmentation clock. Nature 421, 275-278.
24. Das, J., Ghosh, J., Manna, P. and Sil, P. C. (2011). Taurine suppresses doxorubicin-triggered oxidative stress and cardiac apoptosis in rat via up- regulation of PI3-K/Akt and inhibition of p53, p38-JNK. Biochem. Pharmacol. 81, 891-909.
25. DasGupta, R. and Fuchs, E. (1999). Multiple roles for activated LEF/TCF transcription complexes during hair follicle development and differentiation. Development 126, 4557-4568.
26. Dohn, M. R., Mundell, N. A., Sawyer, L. M., Dunlap, J. A. and Jessen, J. R. (2013). Planar cell polarity proteins differentially regulate extracellular matrix organization and assembly during zebrafish gastrulation. Dev. Biol. 383, 39-51.
27. Dunwoodie, S. L., Henrique, D., Harrison, S. M. and Beddington, R. S. (1997). Mouse Dll3: a novel divergent Delta gene which may complement the function of other Delta homologues during early pattern formation in the mouse embryo. Development 124, 3065-3076.
28. Dzamba, B. J., Jakab, K. R., Marsden, M., Schwartz, M. A. and DeSimone, D.W. (2009). Cadherin adhesion, tissue tension, and noncanonical Wnt signaling regulate fibronectin matrix organization. Dev. Cell 16, 421-432.
29. Echelard, Y., Epstein, D. J., St-Jacques, B., Shen, L., Mohler, J., McMahon, J. A. and McMahon, A. P. (1993). Sonic hedgehog, a member of a family of putative signaling molecules, is implicated in the regulation of CNS polarity. Cell 75, 1417-1430.
30. Ericson, J., Rashbass, P., Schedl, A., Brenner-Morton, S., Kawakami, A., van Heyningen, V., Jessell, T. M. and Briscoe, J. (1997). Pax6 controls progenitor cell identity and neuronal fate in response to graded Shh signaling. Cell 90, 169-180.
31. Gao, B., Song, H., Bishop, K., Elliot, G., Garrett, L., English, M. A., Andre, P., Robinson, J., Sood, R., Minami, Y. et al. (2011). Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 20, 163-176.
32. Gardner, R. L. and Beddington, R. S. P. (1988). Multi-lineage ‘stem’ cells in the mammalian embryo. J. Cell. Sci. 1988 Suppl. 10, 11-27.
33. George, E. L., Georges-Labouesse, E. N., Patel-King, R. S., Rayburn, H. and Hynes, R. O. (1993). Defects in mesoderm, neural tube and vascular development in mouse embryos lacking fibronectin. Development 119, 1079-1091.
34. Goto, T., Davidson, L., Asashima, M. and Keller, R. (2005). Planar cell polarity genes regulate polarized extracellular matrix deposition during frog gastrulation. Curr. Biol. 15, 787-793.
35. Greene, N. D. E., Gerrelli, D., Van Straaten, H. W. M. and Copp, A. J. (1998). Abnormalities of floor plate, notochord and somite differentiation in the loop-tail (Lp) mouse: a model of severe neural tube defects. Mech. Dev. 73, 59-72.
36. Gros, J. and Tabin, C. J. (2014). Vertebrate limb bud formation is initiated by localized epithelial-to-mesenchymal transition. Science 343, 1253-1256.
37. Hashimoto, M., Shinohara, K., Wang, J., Ikeuchi, S., Yoshiba, S., Meno, C., Nonaka, S., Takada, S., Hatta, K., Wynshaw-Boris, A. et al. (2010). Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 12, 170-176.
38. Hay, E. D. and Zuk, A. (1995). Transformations between epithelium and mesenchyme: normal, pathological, and experimentally induced. Am. J. Kidney Dis. 26, 678-690.
39. Heisenberg, C.-P., Tada, M., Rauch, G.-J., Saúde, 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.
40. Kageyama, R., Masamizu, Y. and Niwa, Y. (2007). Oscillator mechanism of Notch pathway in the segmentation clock. Dev. Dyn. 236, 1403-1409.
41. Kanai-Azuma, M., Kanai, Y., Gad, J. M., Tajima, Y., Taya, C., Kurohmaru, M., Sanai, Y., Yonekawa, H., Yazaki, K., Tam, P. P. et al. (2002). Depletion of definitive gut endoderm in Sox17-null mutant mice. Development 129, 2367-2379.
42. Keller, R. (2002). Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298, 1950-1954.
43. Kibar, Z., Vogan, K. J., Groulx, N., Justice, M. J., Underhill, D. A. and Gros, P. (2001). Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nat. Genet. 28, 251-255.
44. Kibar, Z., Torban, E., McDearmid, J. R., Reynolds, A., Berghout, J., Mathieu, M., Kirillova, I., De Marco, P., Merello, E., Hayes, J. M. et al. (2007). Mutations in VANGL1 associated with neural-tube defects. N. Engl. J. Med. 356, 1432-1437.
45. Kikuchi, A., Yamamoto, H., Sato, A. and Matsumoto, S. (2012). Wnt5a: its signalling, functions and implication in diseases. Acta Physiol. 204, 17-33.
46. Kispert, A., Vainio, S., Shen, L., Rowitch, D. H. and McMahon, A. P. (1996). Proteoglycans are required for maintenance of Wnt-11 expression in the ureter tips. Development 122, 3627-3637.
47. Klein, T. J. and Mlodzik, M. (2005). Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell Dev. Biol. 21, 155-176.
48. Lawson, K. A., Meneses, J. J. and Pedersen, R. A. (1991). Clonal analysis of epiblast fate during germ layer formation in the mouse embryo. Development 113, 891-911.
49. Lei, Y.-P., Zhang, T., Li, H., Wu, B.-L., Jin, L. and Wang, H.-Y. (2010). VANGL2 mutations in human cranial neural-tube defects. N. Engl. J. Med. 362, 2232-2235.
50. Loebel, D. A. F., Watson, C. M., De Young, R. A. and Tam, P. P. L. (2003). Lineage choice and differentiation in mouse embryos and embryonic stem cells. Dev. Biol. 264, 1-14.
51. Logan, C. Y. and Nusse, R. (2004). The Wnt signaling pathway in development and disease. Annu. Rev. Cell Dev. Biol. 20, 781-810.
52. Logan, M., Pagán-Westphal, S. M., Smith, D. M., Paganessi, L. and Tabin, C. J. (1998). The transcription factor Pitx2 mediates situs-specific morphogenesis in response to left-right asymmetric signals. Cell 94, 307-317.
53. Lowe, L. A., Supp, D. M., Sampath, K., Yokoyama, T., Wright, C. V. E., Potter, S. S., Overbeek, P. and Kuehn, M. R. (1996). Conserved left-right asymmetry of nodal expression and alterations in murine situs inversus. Nature 381, 158-161.
54. Lyons, I., Parsons, L. M., Hartley, L., Li, R., Andrews, J. E., Robb, L. and Harvey, R. P. (1995). Myogenic and morphogenetic defects in the heart tubes of murine embryos lacking the homeo box gene Nkx2-5. Genes Dev. 9, 1654-1666.
55. Ma, L. and Wang, H.-Y. (2007). Mitogen-activated protein kinase p38 regulates the Wnt/cyclic GMP/Ca2+ non-canonical pathway. J. Biol. Chem. 282, 28980-28990.
56. Mahaffey, J. P., Grego-Bessa, J., Liem, K. F., Jr and Anderson, K. V. (2013). Cofilin and Vangl2 cooperate in the initiation of planar cell polarity in the mouse embryo. Development 140, 1262-1271.
57. Majumdar, A., Vainio, S., Kispert, A., McMahon, J. and McMahon, A. P. (2003). Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130, 3175-3185.
58. Mansouri, A., Yokota, Y., Wehr, R., Copeland, N. G., Jenkins, N. A. and Gruss, P. (1997). Paired-related murine homeobox gene expressed in the developing sclerotome, kidney, and nervous system. Dev. Dyn. 210, 53-65.
59. McNeill, H. (2010). Planar cell polarity: keeping hairs straight is not so simple. Cold Spring Harb. Perspect. Biol. 2, a003376.
60. Mendez, M. G., Kojima, S. and Goldman, R. D. (2010). Vimentin induces changes in cell shape, motility, and adhesion during the epithelial to mesenchymal transition. FASEB J. 24, 1838-1851.
61. Minowada, G., Jarvis, L. A., Chi, C. L., Neubuser, A., Sun, X., Hacohen, N., Krasnow, M. A. and Martin, G. R. (1999). Vertebrate Sprouty genes are induced by FGF signaling and can cause chondrodysplasia when overexpressed. Development 126, 4465-4475.
62. Montcouquiol, M., Rachel, R. A., Lanford, P. J., Copeland, N. G., Jenkins, N. A. and Kelley, M. W. (2003). Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423, 173-177.
63. Nonaka, S., Shiratori, H., Saijoh, Y. and Hamada, H. (2002). Determination of leftright patterning of the mouse embryo by artificial nodal flow. Nature 418, 96-99.
64. Nonaka, S., Yoshiba, S., Watanabe, D., Ikeuchi, S., Goto, T., Marshall, W. F. and Hamada, H. (2005). De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol. 3, e268.
65. Nowotschin, S., Ferrer-Vaquer, A., Concepcion, D., Papaioannou, V. E. and Hadjantonakis, A.-K. (2012). Interaction of Wnt3a, Msgn1 and Tbx6 in neural versus paraxial mesoderm lineage commitment and paraxial mesoderm differentiation in the mouse embryo. Dev. Biol. 367, 1-14.
66. Pallet, N., Thervet, E. and Anglicheau, D. (2012). C-Jun-N-terminal kinase signaling is involved in cyclosporine-induced epithelial phenotypic changes. J. Transplant. 2012, 348-604.
67. Pandur, P., Läsche, M., Eisenberg, L.M. and Kühl, M. (2002). Wnt-11 activation of a non-canonical Wnt signalling pathway is required for cardiogenesis. Nature 418, 636-641.
68. Pankov, R. and Yamada, K. M. (2002). Fibronectin at a glance. J. Cell Sci. 115, 3861-3863.
69. Placzek, M., Jessell, T. M. and Dodd, J. (1993). Induction of floor plate differentiation by contact-dependent, homeogenetic signals. Development 117, 205-218.
70. Plouhinec, J.-L., Granier, C., Le Mentec, C., Lawson, K. A., Sabéran-Djoneidi, D., Aghion, J., Shi, D. L., Collignon, J. and Mazan, S. (2004). Identification of the mammalian Not gene via a phylogenomic approach. Gene Expr. Patterns 5, 11-22.
71. Qian, D., Jones, C., Rzadzinska, A., Mark, S., Zhang, X., Steel, K. P., Dai, X. and Chen, P. (2007). Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306, 121-133.
72. Rauch, G. J., Hammerschmidt, M., Blader, P., Schauerte, H. E., Strahle, U., Ingham, P. W., McMahon, A. P. and Haffter, P. (1997). Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb. Symp. Quant. Biol. 62, 227-234.
73. Rivera-Pérez, J. A., Jones, V. and Tam, P. P. L. (2010). Culture of whole mouse embryos at early postimplantation to organogenesis stages: developmental staging and methods. Methods Enzymol. 476, 185-203.
74. Roszko, I., Sawada, A. and Solnica-Krezel, L. (2009). Regulation of convergence and extension movements during vertebrate gastrulation by the Wnt/PCP pathway. Semin. Cell Dev. Biol. 20, 986-997.
75. Saga, Y., Hata, N., Koseki, H. and Taketo, M. M. (1997). Mesp2: a novel mouse gene expressed in the presegmented mesoderm and essential for segmentation initiation. Genes Dev. 11, 1827-1839.
76. Sausedo, R. A. and Schoenwolf, G. C. (1994). Quantitative analyses of cell behaviors underlying notochord formation and extension in mouse embryos. Anat. Rec. 239, 103-112.
77. Seifert, J. R. K. and Mlodzik, M. (2007). Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8, 126-138.
78. Shang, X., Marchioni, F., Sipes, N., Evelyn, C. R., Jerabek-Willemsen, M., Duhr, S., Seibel, W., Wortman, M. and Zheng, Y. (2012). Rational design of small molecule inhibitors targeting RhoA subfamily Rho GTPases. Chem. Biol. 19, 699-710.
79. Shook, D. and Keller, R. (2003). Mechanisms, mechanics and function of epithelialmesenchymal transitions in early development. Mech. Dev. 120, 1351-1383.
80. Sirbu, I. O. and Duester, G. (2006). Retinoic-acid signalling in node ectoderm and posterior neural plate directs left-right patterning of somitic mesoderm. Nat. Cell Biol. 8, 271-277.
81. Smyth, N., Vatansever, H. S., Murray, P., Meyer, M., Frie, C., Paulsson, M. and Edgar, D. (1999). Absence of basement membranes after targeting the LAMC1 gene results in embryonic lethality due to failure of endoderm differentiation. J. Cell Biol. 144, 151-160.
82. Song, H., Hu, J., Chen, W., Elliott, G., Andre, P., Gao, B. and Yang, Y. (2010). Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466, 378-382.
83. Sulik, K., Dehart, D. B., Iangaki, T., Carson, J. L., Vrablic, T., Gesteland, K. and Schoenwolf, G. C. (1994). Morphogenesis of the murine node and notochord plate. Dev. Dyn. 201, 260-278.
84. Sun, X., Meyers, E. N., Lewandoski, M. and Martin, G. R. (1999). Targeted disruption of Fgf8 causes failure of cell migration in the gastrulating mouse embryo. Genes Dev. 13, 1834-1846.
85. 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.
86. Takada, S., Stark, K. L., Shea, M. J., Vassileva, G., McMahon, J. A. and McMahon, A. P. (1994). Wnt-3a regulates somite and tailbud formation in the mouse embryo. Genes Dev. 8, 174-189.
87. Takemoto, T., Uchikawa, M., Yoshida, M., Bell, D. M., Lovell-Badge, R., Papaioannou, V. E. and Kondoh, H. (2011). Tbx6-dependent Sox2 regulation determines neural or mesodermal fate in axial stem cells. Nature 470, 394-398.
88. Tam, P. P. and Beddington, R. S. (1987). The formation of mesodermal tissues in the mouse embryo during gastrulation and early organogenesis. Development 99, 109-126.
89. Tam, P. P. L. and Behringer, R. R. (1997). Mouse gastrulation: the formation of a mammalian body plan. Mech. Dev. 68, 3-25.
90. Tam, P. P. L. and Loebel, D. A. F. (2007). Gene function in mouse embryogenesis: get set for gastrulation. Nat. Rev. Genet. 8, 368-381.
91. Tam, P. P., Goldman, D., Camus, A. and Schoenwolf, G. C. (2000). Early events of somitogenesis in higher vertebrates: allocation of precursor cells during gastrulation and the organization of a meristic pattern in the paraxial mesoderm. Curr. Top. Dev. Biol. 47, 1-32.
92. Tanaka, H., Iwasaki, Y., Yamato, H., Mori, Y., Komaba, H., Watanabe, H., Maruyama, T. and Fukagawa, M. (2013). P-Cresyl sulfate induces osteoblast dysfunction through activating JNK and p38 MAPK pathways. Bone 56, 347-354.
93. Thiery, J. P., Acloque, H., Huang, R. Y. J. and Nieto, M. A. (2009). Epithelialmesenchymal transitions in development and disease. Cell 139, 871-890.
94. Topol, L., Jiang, X., Choi, H., Garrett-Beal, L., Carolan, P. J. and Yang, Y. (2003). Wnt-5a inhibits the canonical Wnt pathway by promoting GSK-3-independent beta-catenin degradation. J. Cell Biol. 162, 899-908.
95. Tree, D. R. P., Ma, D. and Axelrod, J. D. (2002). A three-tiered mechanism for regulation of planar cell polarity. Semin. Cell Dev. Biol. 13, 217-224.
96. Ukita, K., Hirahara, S., Oshima, N., Imuta, Y., Yoshimoto, A., Jang, C.-W., Oginuma, M., Saga, Y., Behringer, R. R., Kondoh, H. et al. (2009). Wnt signaling maintains the notochord fate for progenitor cells and supports the posterior extension of the notochord. Mech. Dev. 126, 791-803.
97. Vermot, J. and Pourquié, O. (2005). Retinoic acid coordinates somitogenesis and left-right patterning in vertebrate embryos. Nature 435, 215-220.
98. Vermot, J., Gallego Llamas, J., Fraulob, V., Niederreither, K., Chambon, P. and Dollé, P. (2005). Retinoic acid controls the bilateral symmetry of somite formation in the mouse embryo. Science 308, 563-566.
99. Walentek, P., Schneider, I., Schweickert, A. and Blum, M. (2013). Wnt11b is involved in cilia-mediated symmetry breakage during Xenopus left-right development. PLoS ONE 8, e73646.
100. 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 2, 695-706.
101. 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 133, 1767-1778.
102. Westfall, T. A., Brimeyer, R., Twedt, J., Gladon, J., Olberding, A., Furutani-Seiki, M. and Slusarski, D.C. (2003).Wnt-5/pipetail functions in vertebrate axis formation as a negative regulator of Wnt/beta-catenin activity. J. Cell Biol. 162, 889-898.
103. White, J. A., Ramshaw, H., Taimi, M., Stangle, W., Zhang, A., Everingham, S., Creighton, S., Tam, S.-P., Jones, G. and Petkovich, M. (2000). Identification of the human cytochrome P450, P450RAI-2, which is predominantly expressed in the adult cerebellum and is responsible for all-trans-retinoic acid metabolism. Proc. Natl. Acad. Sci. USA 97, 6403-6408.
104. Widenmaier, S. B., Ao, Z., Kim, S.-J., Warnock, G. and McIntosh, C. H. (2009). Suppression of p38 MAPK and JNK via Akt-mediated inhibition of apoptosis signal-regulating kinase 1 constitutes a core component of the beta-cell prosurvival effects of glucose-dependent insulinotropic polypeptide. J. Biol. Chem. 284, 30372-30382.
105. Wilson, V., Manson, L., Skarnes, W. C. and Beddington, R. S. (1995). The T gene is necessary for normal mesodermal morphogenetic cell movements during gastrulation. Development 121, 877-886.
106. Wilson, V., Olivera-Martinez, I. and Storey, K. G. (2009). Stem cells, signals and vertebrate body axis extension. Development 136, 1591-1604.
107. Yamaguchi, T. P. (2008). Genetics of Wnt signaling during early mammalian development. Methods Mol. Biol. 468, 287-305.
108. Yamaguchi, T. P., Bradley, A., McMahon, A. P. and Jones, S. (1999a). A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126, 1211-1223.
109. Yamaguchi, T. P., Takada, S., Yoshikawa, Y., Wu, N. and McMahon, A. P. (1999b). T (Brachyury) is a direct target of Wnt3a during paraxial mesoderm specification. Genes Dev. 13, 3185-3190.
110. Yamanaka, H., Moriguchi, T., Masuyama, N., Kusakabe, M., Hanafusa, H., Takada, R., Takada, S. and Nishida, E. (2002). JNK functions in the noncanonical Wnt pathway to regulate convergent extension movements in vertebrates. EMBO Rep. 3, 69-75.
111. Yamanaka, Y., Tamplin, O. J., Beckers, A., Gossler, A. and Rossant, J. (2007). Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms. Dev. Cell 13, 884-896.
112. Yang, Y. (2012). Wnt signaling in development and disease. Cell. Biosci. 2, 14.
113. Ybot-Gonzalez, P., Savery, D., Gerrelli, D., Signore, M., Mitchell, C. E., Faux, C. H., Greene, N. D. E. and Copp, A. J. (2007). Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134, 789-799.
114. Zhao, D., McCaffery, P., Ivins, K. J., Neve, R. L., Hogan, P., Chin, W. W. and Dräger, U. C. (1996). Molecular identification of a major retinoic-acid-synthesizing enzyme, a retinaldehyde-specific dehydrogenase. Eur. J. Biochem. 240, 15-22.
115. Zhu, S., Liu, L., Korzh, V., Gong, Z. and Low, B. C. (2006). RhoA acts downstream of Wnt5 and Wnt11 to regulate convergence and extension movements by involving effectors Rho kinase and Diaphanous: use of zebrafish as an in vivo model for GTPase signaling. Cell Signal. 18, 359-372.
116. Zohn, I. E., Li, Y., Skolnik, E. Y., Anderson, K. V., Han, J. and Niswander, L. (2006). P38 and a p38-interacting protein are critical for downregulation of E-cadherin during mouse gastrulation. Cell 125, 957-969.