An Expanding Role of Vangl Proteins in Embryonic Development

Current Topics in Developmental Biology

Volumn 101, Issue , 2012, Pages 237-261

  Torban, Elena ^a   Iliescu, Alexandra ^a   Gros, Philippe ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cilium; Loop tail; Neural tube defects; Organogenesis; Planar cell polarity; Vangl

Indexed keywords

EID: 84868643887     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394592-1.00005-3     Document Type: Chapter

References (109)

1. Antic D., Stubbs J.L., Suyama K., Kintner C., Scott M.P., Axelrod J.D. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PloS One 2010, 5:e8999.
2. Babayeva S., Zilber Y., Torban E. Planar cell polarity pathway regulates actin rearrangement, cell shape, motility, and nephrin distribution in podocytes. American Journal of Physiology. Renal Physiology 2011, 300:F549-F560.
3. Badano J.L., Mitsuma N., Beales P.L., Katsanis N. The ciliopathies: An emerging class of human genetic disorders. Annual Review of Genomics and Human Genetics 2006, 7:125-148.
4. Bingham S., Higashijima S., Okamoto H., Chandrasekhar A. The Zebrafish trilobite gene is essential for tangential migration of branchiomotor neurons. Developments in Biologicals 2002, 242:149-160.
5. Bingham S.M., Sittaramane V., Mapp O., Patil S., Prince V.E., Chandrasekhar A. Multiple mechanisms mediate motor neuron migration in the zebrafish hindbrain. Developmental Neurobiology 2010, 70:87-99.
6. Borovina A., Superina S., Voskas D., Ciruna B. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nature Cell Biology 2010, 12:407-412.
7. Bramall A.N., Wright A.F., Jacobson S.G., McInnes R.R. The genomic, biochemical, and cellular responses of the retina in inherited photoreceptor degenerations and prospects for the treatment of these disorders. Annual Review of Neuroscience 2010, 33:441-472.
8. Casal J., Lawrence P.A., Struhl G. Two separate molecular systems, Dachsous/Fat and Starry night/Frizzled, act independently to confer planar cell polarity. Development 2006, 133:4561-4572.
9. Collier S., Gubb D. Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. Development 1997, 124:4029-4037.
10. Copp A.J., Greene N.D. Genetics and development of neural tube defects. The Journal of Pathology 2010, 220:217-230.
11. Curtin J.A., Quint E., Tsipouri V., Arkell R.M., Cattanach B., Copp A.J., et al. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Current Biology 2003, 13:1129-1133.
12. Darken R.S., Scola A.M., Rakeman A.S., Das G., Mlodzik M., Wilson P.A. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. The EMBO Journal 2002, 21:976-985.
13. Davenport J.R., Watts A.J., Roper V.C., Croyle M.J., van Groen T., Wyss J.M., et al. Disruption of intraflagellar transport in adult mice leads to obesity and slow-onset cystic kidney disease. Current Biology 2007, 17:1586-1594.
14. Devenport D., Fuchs E. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nature Cell Biology 2008, 10:1257-1268.
15. Etheridge S.L., Ray S., Li S., Hamblet N.S., Lijam N., Tsang M., et al. Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genetics 2008, 4:e1000259.
16. Fenstermaker A.G., Prasad A.A., Bechara A., Adolfs Y., Tissir F., Goffinet A., et al. Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. The Journal of Neuroscience 2010, 30:16053-16064.
17. Fischer E., Legue E., Doyen A., Nato F., Nicolas J.F., Torres V., et al. Defective planar cell polarity in polycystic kidney disease. Nature Genetics 2006, 38:21-23.
18. Fischer E., Pontoglio M. Planar cell polarity and cilia. Seminars in Cell & Developmental Biology 2009, 20:998-1005.
19. Gao B., Song H., Bishop K., Elliot G., Garrett L., English M.A., et al. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Developmental Cell 2011, 20:163-176.
20. Gerdes J.M., Davis E.E., Katsanis N. The vertebrate primary cilium in development, homeostasis, and disease. Cell 2009, 137:32-45.
21. Glasco D.M., Sittaramane V., Bryant W., Fritzsch B., Sawant A., Paudyal A., et al. The mouse Wnt/PCP protein Vangl2 is necessary for migration of facial branchiomotor neurons, and functions independently of Dishevelled. Developments in Biologicals 2012, 369(2):211-222.
22. Goetz S.C., Anderson K.V. The primary cilium: A signalling centre during vertebrate development. Nature Reviews Genetics 2010, 11:331-344.
23. Goodrich L.V., Strutt D. Principles of planar polarity in animal development. Development 2011, 138:1877-1892.
24. Gravel M., Iliescu A., Horth C., Apuzzo S., Gros P. Molecular and cellular mechanisms underlying neural tube defects in the loop-tail mutant mouse. Biochemistry 2010, 49:3445-3455.
25. Gray R.S., Abitua P.B., Wlodarczyk B.J., Szabo-Rogers H.L., Blanchard O., Lee I., et al. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nature Cell Biology 2009, 11:1225-1232.
26. Greene N.D., Gerrelli D., Van Straaten H.W., Copp A.J. Abnormalities of floor plate, notochord and somite differentiation in the loop-tail (Lp) mouse: A model of severe neural tube defects. Mechanisms of Development 1998, 73:59-72.
27. Greene N.D., Stanier P., Copp A.J. Genetics of human neural tube defects. Human Molecular Genetics 2009, 18:R113-R129.
28. Gubb D., Garcia-Bellido A. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. Journal of Embryology and Experimental Morphology 1982, 68:37-57.
29. Guirao B., Meunier A., Mortaud S., Aguilar A., Corsi J.M., Strehl L., et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nature Cell Biology 2010, 12:341-350.
30. Guyot M.C., Bosoi C.M., Kharfallah F., Reynolds A., Drapeau P., Justice M., et al. A novel hypomorphic Looptail allele at the planar cell polarity Vangl2 gene. Developmental Dynamics 2011, 240:839-849.
31. Harris M.J., Juriloff D.M. 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 Research. Part A, Clinical and Molecular Teratology 2010, 88:653-669.
32. Henderson D.J., Conway S.J., Greene N.D., Gerrelli D., Murdoch J.N., Anderson R.H., et al. Cardiovascular defects associated with abnormalities in midline development in the Loop-tail mouse mutant. Circulation Research 2001, 89:6-12.
33. Heydeck W., Zeng H., Liu A. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Developmental Dynamics 2009, 238:3035-3042.
34. Hildebrandt F., Benzing T., Katsanis N. Ciliopathies. The New England Journal of Medicine 2011, 364:1533-1543.
35. Iliescu A., Gravel M., Horth C., Apuzzo S., Gros P. Transmembrane topology of mammalian planar cell polarity protein Vangl1. Biochemistry 2011, 50:2274-2282.
36. Iliescu A., Gravel M., Horth C., Kibar Z., Gros P. Loss of membrane targeting of Vangl proteins causes neural tube defects. Biochemistry 2011, 50:795-804.
37. Jessen J.R., Topczewski J., Bingham S., Sepich D.S., Marlow F., Chandrasekhar A., et al. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nature Cell Biology 2002, 4:610-615.
38. Jin H., Nachury M.V. The BBSome. Current Biology 2009, 19:R472-R473.
39. Jin H., White S.R., Shida T., Schulz S., Aguiar M., Gygi S.P., et al. The conserved Bardet-Biedl syndrome proteins assemble a coat that traffics membrane proteins to cilia. Cell 2010, 141:1208-1219.
40. Jones C., Chen P. Primary cilia in planar cell polarity regulation of the inner ear. Current Topics in Developmental Biology 2008, 85:197-224.
41. Jones C., Roper V.C., Foucher I., Qian D., Banizs B., Petit C., et al. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nature Genetics 2008, 40:69-77.
42. Kalabis J., Rosenberg I., Podolsky D.K. Vangl1 protein acts as a downstream effector of intestinal trefoil factor (ITF)/TFF3 signaling and regulates wound healing of intestinal epithelium. The Journal of Biological Chemistry 2006, 281:6434-6441.
43. Kallay L.M., McNickle A., Brennwald P.J., Hubbard A.L., Braiterman L.T. Scribble associates with two polarity proteins, Lgl2 and Vangl2, via distinct molecular domains. Journal of Cellular Biochemistry 2006, 99:647-664.
44. Keller R.E. Vital dye mapping of the gastrula and neurula of Xenopus laevis. I. Prospective areas and morphogenetic movements of the superficial layer. Developments in Biologicals 1975, 42:222-241.
45. Keller R.E. Vital dye mapping of the gastrula and neurula of Xenopus laevis. II. Prospective areas and morphogenetic movements of the deep layer. Developments in Biologicals 1976, 51:118-137.
46. Kibar Z., Bosoi C.M., Kooistra M., Salem S., Finnell R.H., De Marco P., et al. Novel mutations in VANGL1 in neural tube defects. Human Mutation 2009, 30:E706-E715.
47. Kibar Z., Capra V., Gros P. Toward understanding the genetic basis of neural tube defects. Clinical Genetics 2007, 71:295-310.
48. Kibar Z., Gauthier S., Lee S.H., Vidal S., Gros P. Rescue of the neural tube defect of loop-tail mice by a BAC clone containing the Ltap gene. Genomics 2003, 82:397-400.
49. Kibar Z., Salem S., Bosoi C.M., Pauwels E., De Marco P., Merello E., et al. Contribution of VANGL2 mutations to isolated neural tube defects. Clinical Genetics 2011, 80:76-82.
50. Kibar Z., Underhill D.A., Canonne-Hergaux F., Gauthier S., Justice M.J., Gros P. Identification of a new chemically induced allele (Lp(m1Jus)) at the loop-tail locus: Morphology, histology, and genetic mapping. Genomics 2001, 72:331-337.
51. Kibar Z., Vogan K.J., Groulx N., Justice M.J., Underhill D.A., Gros P. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in the mouse neural tube mutant Loop-tail. Nature Genetics 2001, 28:251-255.
52. Lake B.B., Sokol S.Y. Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. The Journal of Cell Biology 2009, 185:59-66.
53. Lei Y.P., Zhang T., Li H., Wu B.L., Jin L., Wang H.Y. VANGL2 mutations in human cranial neural-tube defects. The New England Journal of Medicine 2010, 362:2232-2235.
54. Lu X., Borchers A.G., Jolicoeur C., Rayburn H., Baker J.C., Tessier-Lavigne M. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 2004, 430:93-98.
55. Matsuyama M., Aizawa S., Shimono A. Sfrp controls apicobasal polarity and oriented cell division in developing gut epithelium. PLoS Genetics 2009, 5:e1000427.
56. May-Simera H.L., Kai M., Hernandez V., Osborn D.P., Tada M., Beales P.L. Bbs8, together with the planar cell polarity protein Vangl2, is required to establish left-right asymmetry in zebrafish. Developments in Biologicals 2010, 345:215-225.
57. McNeill H. Planar cell polarity: Keeping hairs straight is not so simple. Cold Spring Harbor Perspectives in Biology 2010, 2:a003376.
58. Merte J., Jensen D., Wright K., Sarsfield S., Wang Y., Schekman R., et al. Sec24b selectively sorts Vangl2 to regulate planar cell polarity during neural tube closure. Nature Cell Biology 2010, 12:41-46. Suppl. pp. 1-8.
59. Mitchell B., Stubbs J.L., Huisman F., Taborek P., Yu C., Kintner C. The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Current Biology 2009, 19:924-929.
60. Montcouquiol M., Rachel R.A., Lanford P.J., Copeland N.G., Jenkins N.A., Kelley M.W. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 2003, 423:173-177.
61. Montcouquiol M., Sans N., Huss D., Kach J., Dickman J.D., Forge A., et al. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. The Journal of Neuroscience 2006, 26:5265-5275.
62. Murdoch J.N., Henderson D.J., Doudney K., Gaston-Massuet C., Phillips H.M., Paternotte C., et al. Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Human Molecular Genetics 2003, 12:87-98.
63. Nachury M.V., Loktev A.V., Zhang Q., Westlake C.J., Peranen J., Merdes A., et al. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007, 129:1201-1213.
64. Park T.J., Haigo S.L., Wallingford J.B. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nature Genetics 2006, 38:303-311.
65. Park T.J., Mitchell B.J., Abitua P.B., Kintner C., Wallingford J.B. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nature Genetics 2008, 40:871-879.
66. Pazour G.J., Dickert B.L., Vucica Y., Seeley E.S., Rosenbaum J.L., Witman G.B., et al. Chlamydomonas IFT88 and its mouse homologue, polycystic kidney disease gene tg737, are required for assembly of cilia and flagella. The Journal of Cell Biology 2000, 151:709-718.
67. Phillips H.M., Murdoch J.N., Chaudhry B., Copp A.J., Henderson D.J. Vangl2 acts via RhoA signaling to regulate polarized cell movements during development of the proximal outflow tract. Circulation Research 2005, 96:292-299.
68. Rachel R.A., Murdoch J.N., Beermann F., Copp A.J., Mason C.A. Retinal axon misrouting at the optic chiasm in mice with neural tube closure defects. Genesis 2000, 27:32-47.
69. Ramamurthy V., Cayouette M. Development and disease of the photoreceptor cilium. Clinical Genetics 2009, 76:137-145.
70. Rawls A.S., Guinto J.B., Wolff T. The cadherins fat and dachsous regulate dorsal/ventral signaling in the Drosophila eye. Current Biology 2002, 12:1021-1026.
71. Reynolds A., McDearmid J.R., Lachance S., De Marco P., Merello E., Capra V., et al. VANGL1 rare variants associated with neural tube defects affect convergent extension in zebrafish. Mechanisms of Development 2010, 127:385-392.
72. Ross A.J., May-Simera H., Eichers E.R., Kai M., Hill J., Jagger D.J., et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nature Genetics 2005, 37:1135-1140.
73. Saburi S., Hester I., Fischer E., Pontoglio M., Eremina V., Gessler M., et al. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nature Genetics 2008, 40:1010-1015.
74. Scholey J.M. Intraflagellar transport motors in cilia: Moving along the cell's antenna. The Journal of Cell Biology 2008, 180:23-29.
75. Shafer B., Onishi K., Lo C., Colakoglu G., Zou Y. Vangl2 promotes Wnt/planar cell polarity-like signaling by antagonizing Dvl1-mediated feedback inhibition in growth cone guidance. Developmental Cell 2011, 20:177-191.
76. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Kronig C., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nature Genetics 2005, 37:537-543.
77. Simons M., Mlodzik M. Planar cell polarity signaling: From fly development to human disease. Annual Review of Genetics 2008, 42:517-540.
78. Smith L.J., Stein K.F. Planar cell polarity signaling: From fly development to human disease. Journal of Embryology and Experimental Morphology 1962, 10:73-87.
79. Song H., Hu J., Chen W., Elliott G., Andre P., Gao B., et al. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 2010, 466:378-382.
80. Stein K.F., Mackensen J.A. Abnormal development of the thoracic skeleton in mice homozygous for the gene for looped-tail. The American Journal of Anatomy 1957, 100:205-223.
81. Strong L.C., Hollander F. Hereditary Loop-tail in the house mouse: Accompanied by imperforate vagina and with lethal craniorachischisis when homozygous. The Journal of Heredity 1949, 40:329-334.
82. Taylor J., Abramova N., Charlton J., Adler P.N. Van Gogh: A new Drosophila tissue polarity gene. Genetics 1998, 150:199-210.
83. Tissir F., Goffinet A.M. Planar cell polarity signaling in neural development. Current Opinion in Neurobiology 2010, 20:572-577.
84. Torban E., Kor C., Gros P. Van Gogh-like2 (Strabismus) and its role in planar cell polarity and convergent extension in vertebrates. Trends in Genetics 2004, 20:570-577.
85. Torban E., Patenaude A.M., Leclerc S., Rakowiecki S., Gauthier S., Andelfinger G., et al. Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proceedings of the National Academy of Sciences of the United States of America 2008, 105:3449-3454.
86. Torban E., Wang H.J., Groulx N., Gros P. Independent mutations in mouse Vangl2 that cause neural tube defects in looptail mice impair interaction with members of the Dishevelled family. The Journal of Biological Chemistry 2004, 279:52703-52713.
87. Torban E., Wang H.J., Patenaude A.M., Riccomagno M., Daniels E., Epstein D., et al. Tissue, cellular and sub-cellular localization of the Vangl2 protein during embryonic development: Effect of the Lp mutation. Gene Expression Patterns 2007, 7:346-354.
88. van Abeelen J.H., Raven S.M. Enlarged ventricles in the cerebrum of loop-tail mice. Experientia 1968, 24:191-192.
89. Vandenberg A.L., Sassoon D.A. Non-canonical Wnt signaling regulates cell polarity in female reproductive tract development via van gogh-like 2. Development 2009, 136:1559-1570.
90. Wallingford J.B. Neural tube closure and neural tube defects: Studies in animal models reveal known knowns and known unknowns. American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 2005, 135C:59-68.
91. Wallingford J.B., Fraser S.E., Harland R.M. Convergent extension: The molecular control of polarized cell movement during embryonic development. Developmental Cell 2002, 2:695-706.
92. Wallingford J.B., Mitchell B. Strange as it may seem: The many links between Wnt signaling, planar cell polarity, and cilia. Genes & Development 2011, 25:201-213.
93. Wang Y., Guo N., Nathans J. The role of Frizzled3 and Frizzled6 in neural tube closure and in the planar polarity of inner-ear sensory hair cells. The Journal of Neuroscience 2006, 26:2147-2156.
94. Wang J., Hamblet N.S., Mark S., Dickinson M.E., Brinkman B.C., Segil N., et al. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 2006, 133:1767-1778.
95. Wang J., Mark S., Zhang X., Qian D., Yoo S.J., Radde-Gallwitz K., et al. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nature Genetics 2005, 37:980-985.
96. Wang B., Sinha T., Jiao K., Serra R., Wang J. Disruption of PCP signaling causes limb morphogenesis and skeletal defects and may underlie Robinow syndrome and brachydactyly type B. Human Molecular Genetics 2011, 20:271-285.
97. Wansleeben C., Feitsma H., Montcouquiol M., Kroon C., Cuppen E., Meijlink F. Planar cell polarity defects and defective Vangl2 trafficking in mutants for the COPII gene Sec24b. Development 2010, 137:1067-1073.
98. Wansleeben C., Meijlink F. The planar cell polarity pathway in vertebrate development. Developmental Dynamics 2011, 240:616-626.
99. Williams C.L., Li C., Kida K., Inglis P.N., Mohan S., Semenec L., et al. MKS and NPHP modules cooperate to establish basal body/transition zone membrane associations and ciliary gate function during ciliogenesis. The Journal of Cell Biology 2011, 192:1023-1041.
100. Wilson D.B., Center E.M. Differences in cerebral morphology in 2 stocks of mutant mice heterozygous for the loop-tail (Lp)-gene. Experientia 1977, 33:1502-1503.
101. Wolff T., Rubin G.M. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 1998, 125:1149-1159.
102. Yang C.H., Axelrod J.D., Simon M.A. Regulation of Frizzled by fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 2002, 108:675-688.
103. Yates L.L., Papakrivopoulou J., Long D.A., Goggolidou P., Connolly J.O., Woolf A.S., et al. The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. Human Molecular Genetics 2010, 19:4663-4676.
104. Yates L.L., Schnatwinkel C., Murdoch J.N., Bogani D., Formstone C.J., Townsend S., et al. The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis. Human Molecular Genetics 2010, 19:2251-2267.
105. Yen W.W., Williams M., Periasamy A., Conaway M., Burdsal C., Keller R., et al. PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation. Development 2009, 136:2039-2048.
106. Yin H., Copley C.O., Goodrich L.V., Deans M.R. Comparison of phenotypes between different vangl2 mutants demonstrates dominant effects of the Looptail mutation during hair cell development. PLoS One 2012, 7:e31988.
107. Yu H., Smallwood P.M., Wang Y., Vidaltamayo R., Reed R., Nathans J. Frizzled 1 and frizzled 2 genes function in palate, ventricular septum and neural tube closure: General implications for tissue fusion processes. Development 2010, 137:3707-3717.
108. Zeidler M.P., Perrimon N., Strutt D.I. The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification. Current Biology 1999, 9:1363-1372.
109. Zeng H., Hoover A.N., Liu A. PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals. Developments in Biologicals 2010, 339:418-428.