Loss of Wnt5a disrupts second heart field cell deployment and may contribute to OFT malformations in DiGeorge syndrome

Human Molecular Genetics

Volumn 24, Issue 6, 2015, Pages 1704-1716

  Sinha, Tanvi ^a   Li, Ding ^a   Théveniau Ruissy, Magali ^b   Hutson, Mary R ^c   Kelly, Robert G ^b   Wang, Jianbo ^a  

^a UNIVERSITY OF ALABAMA AT BIRMINGHAM   (United States)

^b AIX MARSEILLE UNIVERSITÉ   (France)

^c DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CRE RECOMBINASE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR TBX1; UNCLASSIFIED DRUG; WNT5A PROTEIN; WNT PROTEIN; WNT5A PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL FUNCTION; CELL JUNCTION; CELL SURVIVAL; CONGENITAL HEART MALFORMATION; CONTROLLED STUDY; DIGEORGE SYNDROME; EMBRYO; HEART MUSCLE; HEART OUTFLOW TRACT MALFORMATION; MESODERM; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; TRANSGENE; ANIMAL; CHICK EMBRYO; EMBRYOLOGY; EMBRYONIC STEM CELL; GENE DELETION; GENETICS; HEART; KNOCKOUT MOUSE; PATHOLOGY;

MUS;

ANIMALS; CHICK EMBRYO; DIGEORGE SYNDROME; EMBRYONIC STEM CELLS; GENE DELETION; HEART; MICE; MICE, KNOCKOUT; MYOCARDIUM; WNT PROTEINS;

EID: 84936111665     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu584     Document Type: Article

References (95)

1. Bruneau, B.G. (2008) The developmental genetics of congenital heart disease. Nature, 451, 943-948.
2. Momma, K. (2010) Cardiovascular anomalies associated with chromosome 22q11.2 deletion syndrome. Am. J. Cardiol., 105, 1617-1624.
3. Cai, C.L., Liang, X., Shi, Y., Chu, P.H., Pfaff, S.L., Chen, J. and Evans, S. (2003) Isl1 identifies a cardiac progenitor population that proliferates prior to differentiation and contributes a majority of cells to the heart. Dev. Cell, 5, 877-889.
4. Dyer, L.A. and Kirby, M.L. (2009) The role of secondary heart field in cardiac development. Dev. Biol., 336, 137-144.
5. Kelly, R.G., Brown, N.A. and Buckingham, M.E. (2001) The arterial pole of the mouse heart forms from Fgf10-expressing cells in pharyngeal mesoderm. Dev. Cell, 1, 435-440.
6. Li, P., Pashmforoush, M. and Sucov, H.M. (2010) Retinoic acid regulates differentiation of the secondary heart field and TGFbeta-mediated outflow tract septation. Dev. Cell, 18, 480-485.
7. Ma, Q., Zhou, B. and Pu, W.T. (2008) Reassessment of Isl1 and Nkx2-5 cardiac fate maps using a Gata4-based reporter of Cre activity. Dev. Biol., 323, 98-104.
8. Mjaatvedt, C.H., Nakaoka, T., Moreno-Rodriguez, R., Norris, R. A., Kern, M.J., Eisenberg, C.A., Turner, D. and Markwald, R.R. (2001) The outflow tract of the heart is recruited from a novel heart-forming field. Dev. Biol., 238, 97-109.
9. Verzi, M.P., McCulley, D.J., De Val, S., Dodou, E. and Black, B.L. (2005) The right ventricle, outflow tract, and ventricular septum comprise a restricted expression domain within the secondary/anterior heart field. Dev. Biol., 287, 134-145.
10. Waldo, K.L., Kumiski, D.H., Wallis, K.T., Stadt, H.A., Hutson, M.R., Platt, D.H. and Kirby, M.L. (2001) Conotruncal myocardium arises from a secondary heart field. Development, 128, 3179-3188.
11. Xu, H., Morishima, M., Wylie, J.N., Schwartz, R.J., Bruneau, B. G., Lindsay, E.A. and Baldini, A. (2004) Tbx1 has a dual role in the morphogenesis of the cardiac outflow tract. Development, 131, 3217-3227.
12. Liao, J., Aggarwal, V.S., Nowotschin, S., Bondarev, A., Lipner, S. and Morrow, B.E. (2008) Identification of downstream genetic pathways of Tbx1 in the second heart field. Dev. Biol., 316, 524-537.
13. Bajolle, F., Zaffran, S., Meilhac, S.M., Dandonneau, M., Chang, T., Kelly, R.G. and Buckingham, M.E. (2008) Myocardium at the base of the aorta and pulmonary trunk is prefigured in the outflow tract of the heart and in subdomains of the second heart field. Dev. Biol., 313, 25-34.
14. Theveniau-Ruissy, M., Dandonneau, M., Mesbah, K., Ghez, O., Mattei, M.G., Miquerol, L. and Kelly, R.G. (2008) The del22q11.2 candidate gene Tbx1 controls regional outflow tract identity and coronary artery patterning. Circ. Res., 103, 142-148.
15. Bertrand, N., Roux, M., Ryckebusch, L., Niederreither, K., Dolle, P., Moon, A., Capecchi, M. and Zaffran, S. (2011) Hox genes define distinct progenitor sub-domains within the second heart field. Dev. Biol., 353, 266-274.
16. Rochais, F., Dandonneau, M., Mesbah, K., Jarry, T., Mattei, M. G. and Kelly, R.G. (2009) Hes1 is expressed in the second heart field and is required for outflow tract development. PLoS ONE, 4, e6267.
17. Black, B.L. (2007) Transcriptional pathways in second heart field development. Semin. Cell Dev. Biol., 18, 67-76.
18. Kirby, M.L. (2008) Pulmonary atresia or persistent truncus arteriosus: is it important to make the distinction and how do we do it?. Circ. Res., 103, 337-339.
19. McCulley, D.J., Kang, J.O., Martin, J.F. and Black, B.L. (2008) BMP4 is required in the anterior heart field and its derivatives for endocardial cushion remodeling, outflow tract septation, and semilunar valve development. Dev. Dyn., 237, 3200-3209.
20. Ai, D., Fu, X., Wang, J., Lu, M.F., Chen, L., Baldini, A., Klein, W. H. and Martin, J.F. (2007) Canonical Wnt signaling functions in second heart field to promote right ventricular growth. Proc. Natl Acad. Sci. USA, 104, 9319-9324.
21. Cohen, E.D., Wang, Z., Lepore, J.J., Lu, M.M., Taketo, M.M., Epstein, D.J. and Morrisey, E.E. (2007) Wnt/beta-catenin signaling promotes expansion of Isl-1-positive cardiac progenitor cells through regulation of FGF signaling. J. Clin. Invest., 117, 1794-1804.
22. Lin, L., Cui, L., Zhou, W., Dufort, D., Zhang, X., Cai, C.L., Bu, L., Yang, L., Martin, J., Kemler, R. et al. (2007) Beta-catenin directly regulates Islet1 expression in cardiovascular progenitors and is required for multiple aspects of cardiogenesis. Proc. Natl Acad. Sci. USA, 104, 9313-9318.
23. Manisastry, S.M., Han, M. and Linask, K.K. (2006) Early temporal-specific responses and differential sensitivity to lithium and Wnt-3A exposure during heart development. Dev. Dyn., 235, 2160-2174.
24. Park, E.J., Watanabe, Y., Smyth, G., Miyagawa-Tomita, S., Meyers, E., Klingensmith, J., Camenisch, T., Buckingham, M. and Moon, A.M. (2008) An FGF autocrine loop initiated in second heart field mesoderm regulates morphogenesis at the arterial pole of the heart. Development, 135, 3599-3610.
25. Ilagan, R., Abu-Issa, R., Brown, D., Yang, Y.P., Jiao, K., Schwartz, R.J., Klingensmith, J. and Meyers, E.N. (2006) Fgf8 is required for anterior heart field development. Development, 133, 2435-2445.
26. Zhang, J., Lin, Y., Zhang, Y., Lan, Y., Lin, C., Moon, A.M., Schwartz, R.J., Martin, J.F. andWang, F. (2008) Frs2alpha-deficiency in cardiac progenitors disrupts a subset of FGF signals required for outflow tract morphogenesis. Development, 135, 3611-3622.
27. Dyer, L.A. and Kirby, M.L. (2009) Sonic hedgehog maintains proliferation in secondary heart field progenitors and is required for normal arterial pole formation. Dev. Biol., 330, 305-317.
28. Goddeeris, M.M., Schwartz, R., Klingensmith, J. and Meyers, E. N. (2007) Independent requirements for Hedgehog signaling by both the anterior heart field and neural crest cells for outflow tract development. Development, 134, 1593-1604.
29. High, F.A., Jain, R., Stoller, J.Z., Antonucci, N.B., Lu, M.M., Loomes, K.M., Kaestner, K.H., Pear, W.S. and Epstein, J.A. (2009) Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J. Clin. Invest., 119, 1986-1996.
30. Kwon, C., Qian, L., Cheng, P., Nigam, V., Arnold, J. and Srivastava, D. (2009) A regulatory pathway involving Notch1/betacatenin/Isl1 determines cardiac progenitor cell fate. Nat. Cell Biol., 11, 951-957.
31. 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.
32. 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.
33. 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.
34. Keller, R. (2002) Shaping the vertebrate body plan by polarized embryonic cell movements. Science, 298, 1950-1954.
35. Yin, C., Kiskowski, M., Pouille, P.A., Farge, E. and Solnica-Krezel, L. (2008) Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol., 180, 221-232.
36. Wang, J., Mark, S., Zhang, X., Qian, D., Yoo, S.J., Radde-Gallwitz, K., Zhang, Y., Lin, X., Collazo, A., Wynshaw-Boris, A. et al. (2005) Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat. Genet., 37, 980-985.
37. 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.
38. Wang, Y., Guo, N. and Nathans, J. (2006) The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. J. Neurosci., 26, 2147-2156.
39. Devenport, D. and Fuchs, E. (2008) Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat. Cell Biol., 10, 1257-1268.
40. 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.
41. 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.
42. Murdoch, J.N., Doudney, K., Paternotte, C., Copp, A.J. and Stanier, P. (2001) Severe neural tube defects in the loop-tail mouse result from mutation of Lpp1, a novel gene involved in floor plate specification. Hum. Mol. Genet., 10, 2593-2601.
43. 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 neuraltube defects. N. Engl J. Med., 356, 1432-1437.
44. De Marco, P., Merello, E., Consales, A., Piatelli, G., Cama, A., Kibar, Z. and Capra, V. (2013) Genetic analysis of disheveled 2 and disheveled 3 in human neural tube defects. J. Mol. Neurosci., 49, 582-588.
45. De Marco, P., Merello, E., Rossi, A., Piatelli, G., Cama, A., Kibar, Z. and Capra, V. (2012) FZD6 is a novel gene for human neural tube defects. Hum. Mutat., 33, 384-390.
46. Wang, B., Sinha, T., Jiao, K., Serra, R. and Wang, J. (2011) Disruption of PCP signaling causes limb morphogenesis and skeletal defects and may underlie Robinow syndrome and brachydactyly type B. Hum. Mol. Genet., 20, 271-285.
47. 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.
48. Gros, J., Hu, J.K., Vinegoni, C., Feruglio, P.F., Weissleder, R. and Tabin, C.J. (2010) WNT5A/JNK and FGF/MAPK pathways regulate the cellular events shaping the vertebrate limb bud. Curr. Biol., 20, 1993-2002.
49. Person, A.D., Beiraghi, S., Sieben, C.M., Hermanson, S., Neumann, A.N., Robu, M.E., Schleiffarth, J.R., Billington, C.J. Jr, van Bokhoven, H., Hoogeboom, J.M. et al. (2010) WNT5Amutations in patients with autosomal dominant Robinow syndrome. Dev. Dyn., 239, 327-337.
50. Afzal, A.R., Rajab, A., Fenske, C.D., Oldridge, M., Elanko, N., Ternes-Pereira, E., Tuysuz, B., Murday, V.A., Patton, M.A., Wilkie, A.O. et al. (2000) Recessive Robinow syndrome, allelic to dominant brachydactyly type B, is caused by mutation of ROR2. Nat. Genet., 25, 419-422.
51. DeChiara, T.M., Kimble, R.B., Poueymirou, W.T., Rojas, J., Masiakowski, P., Valenzuela, D.M. andYancopoulos, G.D. (2000) Ror2, encoding a receptor-like tyrosine kinase, is required for cartilage and growth plate development. Nat. Genet., 24, 271-274.
52. Oldridge, M., Fortuna, A.M., Maringa, M., Propping, P., Mansour, S., Pollitt, C., DeChiara, T.M., Kimble, R.B., Valenzuela, D.M., Yancopoulos, G.D. et al. (2000) Dominant mutations in ROR2, encoding an orphan receptor tyrosine kinase, cause brachydactyly type B. Nat. Genet., 24, 275-278.
53. Hamblet, N.S., Lijam, N., Ruiz-Lozano, P., Wang, J., Yang, Y., Luo, Z., Mei, L., Chien, K.R., Sussman, D.J. and Wynshaw-Boris, A. (2002) Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development, 129, 5827-5838.
54. Nassar, H., Paul, M., Ahmad, I., Berkovits, D., Bettan, M., Collon, P., Dababneh, S., Ghelberg, S., Greene, J.P., Heger, A. et al. (2005) Stellar (n, gamma) cross section of 62Ni. Phys. Rev. Lett., 94, 092504.
55. Phillips, H.M., Murdoch, J.N., Chaudhry, B., Copp, A.J. and Henderson, D.J. (2005) Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circ. Res., 96, 292-299.
56. Schleiffarth, J.R., Person, A.D., Martinsen, B.J., Sukovich, D.J., Neumann, A., Baker, C.V., Lohr, J.L., Cornfield, D.N., Ekker, S. C. and Petryk, A. (2007) Wnt5a is required for cardiac outflow tract septation in mice. Pediatr. Res., 61, 386-391.
57. Sinha, T., Wang, B., Evans, S., Wynshaw-Boris, A. andWang, J. (2012) Disheveled mediated planar cell polarity signaling is required in the second heart field lineage for outflow tract morphogenesis. Dev. Biol., 370, 135-144.
58. Chen, L., Fulcoli, F.G., Ferrentino, R., Martucciello, S., Illingworth, E.A. and Baldini, A. (2012) Transcriptional control in cardiac progenitors: Tbx1 interacts with the BAF chromatin remodeling complex and regulates Wnt5a. PLoS Genet., 8, e1002571.
59. Scambler, P.J. (2000) The 22q11 deletion syndromes. Hum. Mol. Genet., 9, 2421-2426.
60. Scambler, P.J., Kelly, D., Lindsay, E., Williamson, R., Goldberg, R., Shprintzen, R., Wilson, D.I., Goodship, J.A., Cross, I.E. and Burn, J. (1992) Velo-cardio-facial syndrome associated with chromosome 22 deletions encompassing the DiGeorge locus. Lancet, 339, 1138-1139.
61. Jerome, L.A. and Papaioannou, V.E. (2001) DiGeorge syndrome phenotype in mice mutant for the T-box gene, Tbx1. Nat. Genet., 27, 286-291.
62. Liao, J., Kochilas, L., Nowotschin, S., Arnold, J.S., Aggarwal, V. S., Epstein, J.A., Brown, M.C., Adams, J. and Morrow, B.E. (2004) Full spectrum of malformations in velo-cardio-facial syndrome/DiGeorge syndrome mouse models by altering Tbx1 dosage. Hum. Mol. Genet., 13, 1577-1585.
63. Merscher, S., Funke, B., Epstein, J.A., Heyer, J., Puech, A., Lu, M. M., Xavier, R.J., Demay, M.B., Russell, R.G., Factor, S. et al. (2001) TBX1 is responsible for cardiovascular defects in velo-cardio-facial/DiGeorge syndrome. Cell, 104, 619-629.
64. Aggarwal, V.S. and Morrow, B.E. (2008) Genetic modifiers of the physical malformations in velo-cardio-facial syndrome/DiGeorge syndrome. Dev. Disabil. Res. Rev., 14, 19-25.
65. Chen, L., Fulcoli, F.G., Tang, S. and Baldini, A. (2009) Tbx1 regulates proliferation and differentiation of multipotent heart progenitors. Circ. Res., 105, 842-851.
66. Frank, D.U., Fotheringham, L.K., Brewer, J.A., Muglia, L.J., Tristani-Firouzi, M., Capecchi, M.R. and Moon, A.M. (2002) An Fgf8 mouse mutant phenocopies human 22q11 deletion syndrome. Development, 129, 4591-4603.
67. Aggarwal, V.S., Liao, J., Bondarev, A., Schimmang, T., Lewandoski, M., Locker, J., Shanske, A., Campione, M. and Morrow, B.E. (2006) Dissection of Tbx1 and Fgf interactions in mouse models of 22q11DS suggests functional redundancy. Hum. Mol. Genet., 15, 3219-3228.
68. Umeda, K., Matsui, T., Nakayama, M., Furuse, K., Sasaki, H., Furuse, M. and Tsukita, S. (2004) Establishment and characterization of cultured epithelial cells lacking expression of ZO-1. J. Biol. Chem., 279, 44785-44794.
69. Stevenson, B.R., Siliciano, J.D., Mooseker, M.S. and Goodenough, D.A. (1986) Identification of ZO-1: a high molecular weight polypeptide associated with the tight junction (zonula occludens) in a variety of epithelia. J. Cell Biol., 103, 755-766.
70. Waldo, K.L., Hutson, M.R., Ward, C.C., Zdanowicz, M., Stadt, H. A., Kumiski, D., Abu-Issa, R. and Kirby, M.L. (2005) Secondary heart field contributes myocardium and smooth muscle to the arterial pole of the developing heart. Dev. Biol., 281, 78-90.
71. Kelly, R.G. and Papaioannou, V.E. (2007) Visualization of outflowtract development in the absence of Tbx1 using an FgF10 enhancer trap transgene. Dev. Dyn., 236, 821-828.
72. Madisen, L., Zwingman, T.A., Sunkin, S.M., Oh, S.W., Zariwala, H.A., Gu, H., Ng, L.L., Palmiter, R.D., Hawrylycz, M.J., Jones, A.R. et al. (2010) A robust and high-throughput Cre reporting and characterization system for the whole mouse brain. Nat. Neurosci., 13, 133-140.
73. Ezin, M. and Fraser, S. (2008) Time-lapse imaging of the early avian embryo. Methods Cell Biol., 87, 211-236.
74. Bodmer, D., Levine-Wilkinson, S., Richmond, A., Hirsh, S. and Kuruvilla, R. (2009) Wnt5a mediates nerve growth factor-dependent axonal branching and growth in developing sympathetic neurons. J. Neurosci., 29, 7569-7581.
75. Blakely, B.D., Bye, C.R., Fernando, C.V., Horne, M.K., Macheda, M.L., Stacker, S.A., Arenas, E. and Parish, C.L. (2011) Wnt5a regulates midbrain dopaminergic axon growth and guidance. PLoS ONE, 6, e18373.
76. Yelbuz, T.M., Waldo, K.L., Kumiski, D.H., Stadt, H.A., Wolfe, R. R., Leatherbury, L. and Kirby, M.L. (2002) Shortened outflow tract leads to altered cardiac looping after neural crest ablation. Circulation, 106, 504-510.
77. 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, 405, 81-85.
78. Vincent, S.D. and Buckingham, M.E. (2010) How to make a heart: the origin and regulation of cardiac progenitor cells. Curr. Top. Dev. Biol., 90, 1-41.
79. Evans, S.M., Yelon, D., Conlon, F.L. and Kirby, M.L. (2010) Myocardial lineage development. Circ. Res., 107, 1428-1444.
80. Kilian, B., Mansukoski, H., Barbosa, F.C., Ulrich, F., Tada, M. and Heisenberg, C.P. (2003) The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev., 120, 467-476.
81. Wallingford, J.B., Vogeli, K.M. and Harland, R.M. (2001) Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. Int. J. Dev. Biol., 45, 225-227.
82. Gong, Y., Mo, C. and Fraser, S.E. (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature, 430, 689-693.
83. Saburi, S., Hester, I., Fischer, E., Pontoglio, M., Eremina, V., Gessler, M., Quaggin, S.E., Harrison, R., Mount, R. and McNeill, H. (2008) Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet., 40, 1010-1015.
84. 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.
85. Lienkamp, S.S., Liu, K., Karner, C.M., Carroll, T.J., Ronneberger, O., Wallingford, J.B. andWalz, G. (2012) Vertebrate kidney tubules elongate using a planar cell polarity-dependent, rosette-based mechanism of convergent extension. Nat. Genet., 44, 1382-1387.
86. Nishimura, T., Honda, H. and Takeichi, M. (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell, 149, 1084-1097.
87. Yamaguchi, T.P., Bradley, A., McMahon, A.P. and Jones, S. (1999) A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development, 126, 1211-1223.
88. Pryor, S.E., Massa, V., Savery, D., Andre, P., Yang, Y., Greene, N. D. and Copp, A.J. (2014) Vangl-dependent planar cell polarity signalling is not required for neural crest migration in mammals. Development, 141, 3153-3158.
89. Brown, C.B., Feiner, L., Lu, M.M., Li, J., Ma, X., Webber, A.L., Jia, L., Raper, J.A. and Epstein, J.A. (2001) PlexinA2 and semaphorin signaling during cardiac neural crest development. Development, 128, 3071-3080.
90. Feiner, L., Webber, A.L., Brown, C.B., Lu, M.M., Jia, L., Feinstein, P., Mombaerts, P., Epstein, J.A. and Raper, J.A. (2001) Targeted disruption of semaphorin 3C leads to persistent truncus arteriosus and aortic arch interruption. Development, 128, 3061-3070.
91. Vitelli, F., Lania, G., Huynh, T. and Baldini, A. (2010) Partial rescue of the Tbx1 mutant heart phenotype by Fgf8: genetic evidence of impaired tissue response to Fgf8. J. Mol. Cell Cardiol., 49, 836-840.
92. Benazeraf, B., Francois, P., Baker, R.E., Denans, N., Little, C.D. and Pourquie, O. (2010) A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature, 466, 248-252.
93. Soriano, P. (1999) Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet., 21, 70-71.
94. Bajolle, F., Zaffran, S., Kelly, R.G., Hadchouel, J., Bonnet, D., Brown, N.A. and Buckingham, M.E. (2006) Rotation of the myocardial wall of the outflow tract is implicated in the normal positioning of the great arteries. Circ. Res., 98, 421-428.
95. Kelly, R., Alonso, S., Tajbakhsh, S., Cossu, G. and Buckingham, M. (1995) Myosin light chain 3F regulatory sequences confer regionalized cardiac and skeletal muscle expression in transgenic mice. J. Cell Biol., 129, 383-396.