A consideration of the evidence that genetic defects in planar cell polarity contribute to the etiology of human neural tube defects

Birth Defects Research Part A - Clinical and Molecular Teratology

Volumn 94, Issue 10, 2012, Pages 824-840

  Juriloff, Diana M ^a   Harris, Muriel J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Craniorachischisis; Exon sequencing; Gene variants; Neural tube; Planar cell polarity

Indexed keywords

ANENCEPHALUS; BIRTH DEFECT; CELL POLARITY; CELSR1 GENE; CRANIORACHISCHISIS; DACT1 GENE; DIASTEMATOMYELIA; DROSOPHILA; FUZ GENE; FZD6 GENE; GASTRULATION; GENE; GENE MUTATION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CODE; GENETIC DISORDER; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HUMAN; LIPOMA; LIPOMYELOMENINGOCELE; MENINGOMYELOCELE; MOUSE MUTANT; NEURAL TUBE DEFECT; NEURULATION; NONHUMAN; PARENT; PATHOGENESIS; PRICKLE1 GENE; PRIORITY JOURNAL; PTK7 GENE; REVIEW; SCRIB GENE; SPINAL DYSRAPHISM; VANGL1 GENE; VANGL2 GENE;

ANIMALS; BODY PATTERNING; CELL POLARITY; GASTRULATION; GENETIC DISEASES, INBORN; HUMANS; MICE; MICE, MUTANT STRAINS; NEURAL TUBE DEFECTS; NEURULATION;

EID: 84867688062     PISSN: 15420752     EISSN: 15420760     Source Type: Journal    
DOI: 10.1002/bdra.23079     Document Type: Review

References (113)

1. Allache R, De Marco P, Merello E, et al. 2012. Role of the planar cell polarity gene CELSR1 in neural tube defects and caudal agenesis. Birth Defects Res A Clin Mol Teratol 94: 176-181.
2. Antic D, Stubbs JL, Suyama K, et al. 2010. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS One 5: e8999.
3. Bayly R, Axelrod JD. 2011. Pointing in the right direction: new developments in the field of planar cell polarity. Nat Rev Genet 12: 385-391.
4. Borovina A, Superina S, Voskas D, Ciruna B. 2010. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat Cell Biol 12: 407-412.
5. Bosoi CM, Capra V, Allache R, et al. 2011. Identification and characterization of novel rare mutations in the planar cell polarity gene PRICKLE1 in human neural tube defects. Hum Mutat 32: 1371-1375.
6. Caddy J, Wilanowski T, Darido C, et al. 2010. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev Cell 19: 138-147.
7. Carter CO. 1969. Polygenic inheritance and common diseases. Lancet 1: 1252-1256.
8. Carter CO. 1974. Clues to the aetiology of neural tube malformations. Dev Med Child Neurol 16 (6 Suppl 32): 3-15.
9. Copp AJ, Checiu I, Henson JN. 1994. Developmental basis of severe neural tube defects in the loop-tail (Lp) mutant mouse: use of microsatellite DNA markers to identify embryonic genotype. Dev Biol 165: 20-29.
10. Copp AJ, Greene ND, Murdoch JN. 2003a. Dishevelled: linking convergent extension with neural tube closure. Trends Neurosci 26: 453-455.
11. Copp AJ, Greene ND, Murdoch JN. 2003b. The genetic basis of mammalian neurulation. Nat Rev Genet 4: 784-793.
12. Curtin JA, Quint E, Tsipouri V, 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.
13. Czeizel AE, Dudás I. 1992. Prevention of the first occurrence of neural-tube defects by periconceptional vitamin supplementation. N Eng J Med 327: 1832-1835.
14. Czeizel A, Métneki J. 1984. Recurrence risk after neural tube defects in a genetic counselling clinic. J Med Genet 21: 413-416.
15. Dabdoub A, Donohue MJ, Brennan A, et al. 2003. Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130: 2375-2384.
16. De Marco P, Merello E, Rossi A, et al. 2012. FZD6 is a novel gene for human neural tube defects. Hum Mutat 33: 384-390.
17. Doudney K, Ybot-Gonzalez P, Paternotte C, et al. 2005. Analysis of the planar cell polarity gene Vangl2 and its co-expressed paralogue Vangl1 in neural tube defect patients. Am J Med Genet A 136: 90-92.
18. Etheridge SL, Ray S, Li S, et al. 2008. Murine dishevelled 3 functions in redundant pathways with dishevelled 1 and 2 in normal cardiac outflow tract, cochlea, and neural tube development. PLoS Genet 4: e1000259.
19. Falconer DS, Mackay TFC. 1996. Introduction to Quantitative Genetics. Fourth Edition. Essex, England: Longman Group Limited. pp. 299-308.
20. Gao B, Song H, Bishop K, et al. 2011. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev Cell 20: 163-176.
21. Goodrich LV, Strutt D. 2011. Principles of planar polarity in animal development. Development 138: 1877-1892.
22. Gray RS, Abitua PB, Wlodarczyk BJ, et al. 2009. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat Cell Biol 11: 1225-1232.
23. Gray RS, Roszko I, Solnica-Krezel L. 2011. Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev Cell 21: 120-133.
24. Greene ND, Copp AJ. 2009. Development of the vertebrate central nervous system: formation of the neural tube. Prenat Diagn 29: 303-311.
25. Greene ND, Gerrelli D, Van Straaten HW, Copp AJ. 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.
26. Gunn TM, Juriloff DM, Harris MJ. 1996. Exencephaly and cleft cerebellum in SELH/Bc mouse embryos are alternative developmental consequences of the same underlying genetic defect. Teratology 54: 230-236.
27. Guo N, Hawkins C, Nathans J. 2004. Frizzled6 controls hair patterning in mice. Proc Natl Acad Sci U S A 101: 9277-9281.
28. Hamblet NS, Lijam N, Ruiz-Lozano P, et al. 2002. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129: 5827-5838.
29. Harris MJ, Juriloff DM. 2007. Mouse mutants with neural tube closure defects and their role in understanding human neural tube defects. Birth Defects Res A Clin Mol Teratol 79: 187-210.
30. Harris MJ, Juriloff DM. 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.
31. Harris MJ, Juriloff DM, Gunn TM, Miller JE. 1994. Development of the cerebellar defect in ataxic SELH/Bc mice. Teratology 50: 63-73.
32. He F, Xiong W, Yu X, et al. 2008. Wnt5a regulates directional cell migration and cell proliferation via Ror2-mediated noncanonical pathway in mammalian palate development. Development 135: 3871-3879.
33. Heisenberg CP, Tada M, Rauch GJ, et al. 2000. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405: 76-81.
34. Henderson DJ, Chaudhry B. 2011. Getting to the heart of planar cell polarity signaling. Birth Defects Res A Clin Mol Teratol 91: 460-467.
35. Henderson DJ, Conway SJ, Greene ND, et al. 2001. Cardiovascular defects associated with abnormalities in midline development in the Loop-tail mouse mutant. Circ Res 89: 6-12.
36. Heydeck W, Liu A. 2011. PCP effector proteins inturned and fuzzy play nonredundant roles in the patterning but not convergent extension of mammalian neural tube. Dev Dyn 240: 1938-1948.
37. Heydeck W, Zeng H, Liu A. 2009. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev Dyn 238: 3035-3042.
38. Johnson KM, Suarez L, Felkner MM, Hendricks K. 2004. Prevalence of craniorachischisis in a Texas-Mexico border population. Birth Defects Res A Clin Mol Teratol 70: 92-94.
39. Juriloff DM, Harris MJ. 2000. Mouse models for neural tube closure defects. Hum Mol Genet 9: 993-1000.
40. Kibar Z, Bosoi CM, Kooistra M, et al. 2009. Novel mutations in VANGL1 in neural tube defects. Hum Mutat 30: E706-E715.
41. Kibar Z, Salem S, Bosoi CM, et al. 2011. Contribution of VANGL2 mutations to isolated neural tube defects. Clin Genet 80: 76-82.
42. Kibar Z, Torban E, McDearmid JR, et al. 2007. Mutations in VANGL1 associated with neural-tube defects. N Engl J Med 356: 1432-1437.
43. Kibar Z, Vogan KJ, Groulx N, et al. 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. Lei YP, Zhang T, Li H, et al. 2010. VANGL2 mutations in human cranial neural-tube defects. N Engl J Med 362: 2232-2235.
45. Lijam N, Paylor R, McDonald MP, et al. 1997. Social interaction and sensorimotor gating abnormalities in mice lacking Dvl1. Cell 90: 895-905.
46. Liu C, Nathans J. 2008. An essential role for frizzled 5 in mammalian ocular development. Development 135: 3567-3576.
47. Lu X, Borchers AG, Jolicoeur C, et al. 2004. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430: 93-98.
48. Majumdar A, Vainio S, Kispert A, et al. 2003. Wnt11 and Ret/Gdnf pathways cooperate in regulating ureteric branching during metanephric kidney development. Development 130: 3175-3185.
49. Manolio TA, Collins FS, Cox NJ, et al. 2009. Finding the missing heritability of complex diseases. Nature 461: 747-753.
50. Mao Y, Mulvaney J, Zakaria S, et al. 2011. Characterization of a Dchs1 mutant mouse reveals requirements for Dchs1-Fat4 signaling during mammalian development. Development 138: 947-957.
51. Merte J, Jensen D, Wright K, et al. 2010. Sec24b selectively sorts Vangl2 to regulate planar cell polarity during neural tube closure. Nat Cell Biol 12:41-46; sup pp 1-8.
52. Mouse Genome Informatics. 2012. The Jackson Laboratory, Bar Harbor, Maine. Available at:http://www.informatics.jax.org. Accessed May 1, 2012.
53. Mitchell LE. 1997. Genetic epidemiology of birth defects: nonsyndromic cleft lip and neural tube defects. Epidemiol Rev 19: 61-68.
54. Moore CA, Li S, Li Z, et al. 1997. Elevated rates of severe neural tube defects in a high-prevalence area in northern China. Am J Med Genet 73: 113-118.
55. Morishima M, Yasui H, Nakazawa M, et al. 1998. Situs variation and cardiovascular anomalies in the transgenic mouse insertional mutation, inv. Teratology 57: 302-309.
56. MRC Vitamin Study Research Group. 1991. Prevention of neural tube defects: results of the Medical Research Council Vitamin Study. Lancet 338: 131-137.
57. Murdoch JN, Doudney K, Paternotte C, et al. 2001a. 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.
58. Murdoch JN, Henderson DJ, Doudney K, et al. 2003. Disruption of scribble (Scrb1) causes severe neural tube defects in the circletail mouse. Hum Mol Genet 12: 87-98.
59. Murdoch JN, Rachel RA, Shah S, et al. 2001b. Circletail, a new mouse mutant with severe neural tube defects: chromosomal localization and interaction with the loop-tail mutation. Genomics 78: 55-63.
60. Murdoch JN, Copp AJ. 2010. The relationship between sonic Hedgehog signaling, cilia, and neural tube defects. Birth Defects Res A Clin Mol Teratol 88: 633-652.
61. Nagy II, Railo A, Rapila R, et al. 2010. Wnt-11 signalling controls ventricular myocardium development by patterning N-cadherin and beta-catenin expression. Cardiovasc Res 85: 100-109.
62. Narimatsu M, Bose R, Pye M, et al. 2009. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137: 295-307.
63. Parr BA, McMahon AP. 1995. Dorsalizing signal Wnt-7a required for normal polarity of D-V and A-P axes of mouse limb. Nature 374: 350-353.
64. Paudyal A, Damrau C, Patterson VL, et al. 2010. The novel mouse mutant, chuzhoi, has disruption of Ptk7 protein and exhibits defects in neural tube, heart and lung development and abnormal planar cell polarity in the ear. BMC Dev Biol 10: 87.
65. Phillips HM, Rhee HJ, Murdoch JN, et al. 2007. Disruption of planar cell polarity signaling results in congenital heart defects and cardiomyopathy attributable to early cardiomyocyte disorganization. Circ Res 101: 137-145.
66. Probst B, Rock R, Gessler M, et al. 2007. The rodent Four-jointed ortholog Fjx1 regulates dendrite extension. Dev Biol 312: 461-470.
67. Qian D, Jones C, Rzadzinska A, et al. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev Biol 306: 121-133.
68. Reynolds A, McDearmid JR, Lachance S, et al. 2010. VANGL1 rare variants associated with neural tube defects affect convergent extension in zebrafish. Mech Dev 127: 385-392.
69. Rieger R, Michaelis A, Green MM. 1976. Glossary of genetics and cytogenetics. New York: Springer-Verlag. p. 476.
70. Robinson A, Escuin S, Doudney K, et al. 2012. Mutations in the planar cell polarity genes CELSR1 and SCRIB are associated with the severe neural tube defect craniorachischisis. Hum Mutat 33: 440-447.
71. Rocha PP, Bleis W, Schrewe H. 2010a. Mosaic expression of Med12 in female mice leads to exencephaly, spina bifida, and craniorachischisis. Birth Defects Res A Clin Mol Teratol 88: 626-632.
72. Rocha PP, Scholze M, Bleiss W, Schrewe H. 2010b. Med12 is essential for early mouse development and for canonical Wnt and Wnt/PCP signaling. Development 137: 2723-2731.
73. Saburi S, Hester I, Fischer E, et al. 2008. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat Genet 40: 1010-1015.
74. Satoh W, Matsuyama M, Takemura H, et al. 2008. Sfrp1, Sfrp2, and Sfrp5 regulate the Wnt/beta-catenin and the planar cell polarity pathways during early trunk formation in mouse. Genesis 46: 92-103.
75. Savory JG, Mansfield M, Rijli FM, Lohnes D. 2011. Cdx mediates neural tube closure through transcriptional regulation of the planar cell polarity gene Ptk7. Development 138: 1361-1370.
76. Schleiffarth JR, Person AD, Martinsen BJ, et al. 2007. Wnt5a is required for cardiac outflow tract septation in mice. Pediatr Res 61: 386-391.
77. Sebold CD, Melvin EC, Siegel D, et al. 2005. Recurrence risks for neural tube defects in siblings of patients with lipomyelomeningocele. Genet Med 7: 64-67.
78. Seo JH, Zilber Y, Babayeva S, et al. 2011. Mutations in the planar cell polarity gene, Fuzzy, are associated with neural tube defects in humans. Hum Mol Genet 20: 4324-4333.
79. Shi Y, Ding Y, Lei YP et al. 2012. Identification of novel rare mutations of DACT1 in human neural tube defects. Hum Mutat [Epub ahead of print].
80. Simons M, Gloy J, Ganner A, et al. 2005. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat Genet 37: 537-543.
81. Simons M, Mlodzik M. 2008. Planar cell polarity signaling: from fly development to human disease. Annu Rev Genet 42: 517-540.
82. Song H, Hu J, Chen W, et al. 2010. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466: 378-382.
83. Suriben R, Kivimäe S, Fisher DA, et al. 2009. Posterior malformations in Dact1 mutant mice arise through misregulated Vangl2 at the primitive streak. Nat Genet 41: 977-985.
84. Tada N, Smith JC. 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.
85. Tao H, Inoue KI, Kiyonari H, et al. 2012. Nuclear localization of Prickle2 is required to establish cell polarity during early mouse embryogenesis. Dev Biol 15: 138-148.
86. Tao H, Suzuki M, Kiyonari H, et al. 2009. Mouse prickle1, the homolog of a PCP gene, is essential for epiblast apical-basal polarity. Proc Natl Acad Sci U S A 106: 14426-14431.
87. Ting SB, Wilanowski T, Auden A, et al. 2003. Inositol- and folate-resistant neural tube defects in mice lacking the epithelial-specific factor Grhl-3. Nat Med 9: 1513-1519.
88. Tissir F, Bar I, Jossin Y, et al. 2005. Protocadherin Celsr3 is crucial in axonal tract development. Nat Neurosci 8: 451-457.
89. Tissir F, Qu Y, Montcouquiol M, et al. 2010. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat Neurosci 13: 700-707.
90. Torban E, Patenaude AM, Leclerc S, et al. 2008. Genetic interaction between members of the Vangl family causes neural tube defects in mice. Proc Natl Acad Sci U S A 105: 3449-3454.
91. Tortori-Donati P, Rossi A, Cama A. 2000. Spinal dysraphism: a review of neuroradiological features with embryological correlations and proposal for a new classification. Neuroradiology 42: 471-491.
92. Wallingford JB, Rowning BA, Vogeli KM, et al. 2000. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405: 81-85.
93. Wallingford JB, Harland RM. 2002. Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 129: 5815-5825.
94. Wang J, Hamblet NS, Mark S, et al. 2006a. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133: 1767-1778.
95. Wang J, Mark S, Zhang X, et al. 2005. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat Genet 37: 980-985.
96. Wang Y, Guo N, Nathans J. 2006b. 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.
97. Wang Y, Huso D, Cahill H, et al. 2001. Progressive cerebellar, auditory, and esophageal dysfunction caused by targeted disruption of the frizzled-4 gene. J Neurosci 21: 4761-4771.
98. Wang Y, Thekdi N, Smallwood PM, et al. 2002. Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J Neurosci 22: 8563-8573.
99. Wang L, Wang F, Guan J, et al. 2010. Relation between hypomethylation of long interspersed nucleotide elements and risk of neural tube defects. Am J Clin Nutr 91: 1359-1367.
100. Wansleeben C, Feitsma H, Montcouquiol M, et al. 2010. Planar cell polarity defects and defective Vangl2 trafficking in mutants for the COPII gene Sec24b. Development 137: 1067-1073.
101. Wansleeben C, van Gurp L, Feitsma H, et al. 2011. An ENU-mutagenesis screen in the mouse: identification of novel developmental gene functions. PLoS One 6: e19357.
102. Watanabe D, Saijoh Y, Nonaka S, et al. 2003. The left-right determinant Inversin is a component of node monocilia and other 9+0 cilia. Development 130: 1725-1734.
103. Wen J, Chiang YJ, Gao C, et al. 2010a. Loss of Dact1 disrupts planar cell polarity signaling by altering dishevelled activity and leads to posterior malformation in mice. J Biol Chem 285: 11023-11030.
104. Wen S, Zhu H, Lu W, et al. 2010b. Planar cell polarity pathway genes and risk for spina bifida. Am J Med Genet A 152A: 299-304.
105. Yamaguchi TP, Bradley A, McMahon AP, Jones S. 1999. A Wnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126: 1211-1223.
106. Yamamoto S, Nishimura O, Misaki K, et al. 2008. Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev Cell 15: 23-36.
107. Yates LL, Papakrivopoulou J, Long DA, et al. 2010a. The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. Hum Mol Genet 19: 4663-4676.
108. Yates LL, Schnatwinkel C, Murdoch JN, et al. 2010b. The PCP genes Celsr1 and Vangl2 are required for normal lung branching morphogenesis. Hum Mol Genet 19: 2251-2267.
109. Ybot-Gonzalez P, Cogram P, Gerrelli D, Copp AJ. 2002. Sonic hedgehog and the molecular regulation of mouse neural tube closure. Development 129: 2507-2517.
110. Ybot-Gonzalez P, Savery D, Gerrelli D, et al. 2007. Convergent extension, planar-cell-polarity signalling and initiation of mouse neural tube closure. Development 134: 789-799.
111. Yokoyama T, Copeland NG, Jenkins NA, et al. 1993. Reversal of left-right asymmetry: a situs inversus mutation. Science 260: 679-682.
112. Yu H, Smallwood PM, Wang Y, et al. 2010. Frizzled 1 and frizzled 2 genes function in palate, ventricular septum and neural tube closure: general implications for tissue fusion processes. Development 137: 3707-3717.
113. Zeng H, Hoover AN, Liu A. 2010. PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals. Dev Biol 339: 418-428.