New insights into the pathogenesis of bladder exstrophy-epispadias complex

Journal of Pediatric Urology

Volumn 9, Issue 6 PART B, 2013, Pages 996-1005

  Mahfuz, Istiak ^a   Darling, Tom ^a   Wilkins, Simon ^a   White, Stefan ^a   Cheng, Wei ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

Bladder exstrophy; Desmosomes; Development; Gene expression; P63; PERP

Indexed keywords

BONE MORPHOGENETIC PROTEIN 4; PROTEIN; PROTEIN P63; PROTEIN PERP; SONIC HEDGEHOG PROTEIN; UNCLASSIFIED DRUG; WNT PROTEIN;

ANUS ATRESIA; APOPTOSIS; ARTICLE; BASE PAIRING; BLADDER CAPACITY; BLADDER EPITHELIUM; BLADDER EXSTROPHY; BLADDER EXSTROPHY EPISPADIAS COMPLEX; CELL ADHESION; CELL DIFFERENTIATION; CELL PROLIFERATION; CHROMOSOME ABERRATION; CLEFT PALATE; DESMOSOME; DISEASE SEVERITY; DIZYGOTIC TWINS; DOWN REGULATION; ECTODERMAL DYSPLASIA; EMBRYO DEVELOPMENT; ENVIRONMENTAL FACTOR; EPISPADIAS; FECES INCONTINENCE; FIRST TRIMESTER PREGNANCY; GENE EXPRESSION; GENE FREQUENCY; GENE LOCUS; GENETIC POLYMORPHISM; GENOTYPE; GESTATIONAL AGE; INDEL MUTATION; KNOCKOUT MOUSE; MATERNAL SMOKING; MECHANICAL STRESS; MENTAL STRESS; MISSENSE MUTATION; MONOZYGOTIC TWINS; NEGATIVE FEEDBACK; NONHUMAN; ORGANOGENESIS; PATHOGENESIS; PHENOTYPE; PREVALENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; RADIATION EXPOSURE; SEXUAL DYSFUNCTION; SIGNAL TRANSDUCTION; SPINAL DYSRAPHISM; TETRAPLOIDY; UMBILICAL HERNIA;

BLADDER EXSTROPHY; DESMOSOMES; DEVELOPMENT; GENE EXPRESSION; P63; PERP;

ANIMALS; BLADDER EXSTROPHY; DESMOSOMES; EPISPADIAS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; RISK FACTORS; SIGNAL TRANSDUCTION;

EID: 84888432166     PISSN: 14775131     EISSN: 18734898     Source Type: Journal    
DOI: 10.1016/j.jpurol.2013.05.001     Document Type: Review

References (109)

1. J.P. Gearhart, and R.D. Jeffs State-of-the-art reconstructive surgery for bladder exstrophy at the Johns Hopkins Hospital Am J Dis Child 143 1989 1475 1478
2. N. Smeulders, and C.R. Woodhouse Neoplasia in adult exstrophy patients BJU Int 87 2001 623 628
3. R.R. Ricketts, J.R. Woodard, G.T. Zwiren, H.G. Andrews, and B.H. Broecker Modern treatment of cloacal exstrophy J Pediatr Surg 26 1991 444 448 discussion 48-50
4. W.G. Reiner, and J.P. Gearhart Discordant sexual identity in some genetic males with cloacal exstrophy assigned to female sex at birth N Engl J Med 350 2004 333 341
5. E.C. Muecke The role of the cloacal membrane in exstrophy: the first successful experimental study J Urol 92 1964 659 667
6. V. Marshall, and E.C. Muecke Congenital abnormalities of the bladder Handbuch de Urologic 1968 Springer New York 165
7. S.S. Ambrose, and D.P. O'Brien 3rd Surgical embryology of the exstrophy-epispadias complex Surg Clin North Am 54 1974 1379 1390
8. S.W. Bruch, N.S. Adzick, R.B. Goldstein, and M.R. Harrison Challenging the embryogenesis of cloacal exstrophy J Pediatr Surg 31 1996 768 770
9. H. Mildenberger, D. Kluth, and M. Dziuba Embryology of bladder exstrophy J Pediatr Surg 23 1988 166 170
10. B.M. Patten, and A. Barry The genesis of exstrophy of the bladder and epispadias Am J Anat 90 1952 35 57
11. B.L. Slaughenhoupt, C.J. Chen, and J.P. Gearhart Creation of a model of bladder exstrophy in the fetal lamb J Urol 156 1996 816 818
12. J. Manner, and D. Kluth A chicken model to study the embryology of cloacal exstrophy J Pediatr Surg 38 2003 678 681
13. S. Beaudoin, P. Barbet, and F. Bargy Pelvic development in the rabbit embryo: implications in the organogenesis of bladder exstrophy Anat Embryol (Berl) 208 2004 425 430
14. W. Cheng, W.B. Jacobs, J.J. Zhang, A. Moro, J.H. Park, and M. Kushida DeltaNp63 plays an anti-apoptotic role in ventral bladder development Development 133 2006 4783 4792
15. J. Quiroz-Guerrero, M. Badillo, N. Munoz, J. Anaya, G. Rico, and R. Maldonado-Valadez Bladder augmentation in a young adult female exstrophy patient with associated omphalocele: an extremely unusual case J Pediatr Urol 5 2009 330 332
16. J.K. Singh, J.K. Mahajan, M. Bawa, and K.L.N. Rao Covered exstrophy with anorectal malformation and vaginal duplication J Indian Assoc Pediatr Surg 16 2011 26 28
17. T.M.L. Boemers, T.P.V.M. de Jong, M.H. Rövekamp, N.M.A. Bax, and J.D. van Gool Covered exstrophy associated with an anorectal malformation: a rare variant of classical bladder exstrophy Pediatr Surg Int 9 1994 438 440
18. T.A. Ince, A.P. Cviko, B.J. Quade, A. Yang, F.D. McKeon, and G.L. Mutter p63 Coordinates anogenital modeling and epithelial cell differentiation in the developing female urogenital tract Am J Pathol 161 2002 1111 1117
19. J.A. Cadeddu, J.E. Benson, R.I. Silver, Y. Lakshmanan, R.D. Jeffs, and J.P. Gearhart Spinal abnormalities in classic bladder exstrophy Br J Urol 79 1997 975 978
20. A.A. Mills, B. Zheng, X.J. Wang, H. Vogel, D.R. Roop, and A. Bradley p63 is a p53 homologue required for limb and epidermal morphogenesis Nature 398 1999 708 713
21. J. Celli, P. Duijf, B.C. Hamel, M. Bamshad, B. Kramer, and A.P. Smits Heterozygous germline mutations in the p53 homolog p63 are the cause of EEC syndrome Cell 99 1999 143 153
22. T. Rinne, B. Hamel, H. van Bokhoven, and H.G. Brunner Pattern of p63 mutations and their phenotypes - update Am J Med Genet A 140 2006 1396 1406
23. A. Yang, R. Schweitzer, D. Sun, M. Kaghad, N. Walker, and R.T. Bronson p63 is essential for regenerative proliferation in limb, craniofacial and epithelial development Nature 398 1999 714 718
24. G. Moretti, E. Mazzaglia, A. D'Anieri, V. Merlino, L. Magaudda, and M.R. Mondello Epidermolysis bullosa junctionalis associated with urinary bladder exstrophy: a case report Pediatr Dermatol 12 1995 239 241
25. A.R. Caton, A. Bloom, C.M. Druschel, and R.S. Kirby Epidemiology of bladder and cloacal exstrophies in New York State, 1983-1999 Birth Defects Res A Clin Mol Teratol 79 2007 781 787
26. Y. Tang, C.X. Ma, W. Cui, V. Chang, M. Ariet, and S.B. Morse The risk of birth defects in multiple births: a population-based study Matern Child Health J 10 2006 75 81
27. Anonymous Epidemiology of bladder exstrophy and epispadias: a communication from the International Clearinghouse for Birth Defects Monitoring Systems Teratology 36 1987 221 227
28. H. Reutter, S.A. Boyadjiev, L. Gambhir, A.K. Ebert, W.H. Rösch, and R. Stein Phenotype severity in the bladder exstrophy-epispadias complex: analysis of genetic and nongenetic contributing factors in 441 families from North America and Europe J Pediatr 2011
29. S.A. Boyadjiev, J.L. Dodson, C.L. Radford, G.H. Ashrafi, T.H. Beaty, and R.I. Mathews Clinical and molecular characterization of the bladder exstrophy-epispadias complex: analysis of 232 families BJU Int 94 2004 1337 1343
30. A.K. Ebert, H. Reutter, M. Ludwig, and W.H. Rösch The exstrophy-epispadias complex Orphanet J Rare Dis 4 2009 23
31. H. Reutter, L. Qi, J.P. Gearhart, T. Boemers, A.K. Ebert, and W. Rösch Concordance analyses of twins with bladder exstrophy-epispadias complex suggest genetic etiology Am J Med Genet A 143A 2007 2751 2756
32. J.P. Gearhart, and R.D. Jeffs Exstrophy-epispadias complex and bladder anomalies P.C. Walsh, A.B. Retik, E.D. Vaughan, A.J. Wein, Campbell's urology 7th ed. 1998 WB Saunders Co Philadelphia 1939 1990
33. A. Wiesel, A. Queisser-Luft, M. Clementi, S. Bianca, and C. Stoll Prenatal detection of congenital renal malformations by fetal ultrasonographic examination: an analysis of 709,030 births in 12 European countries Eur J Med Genet 48 2005 131 144
34. R.S. Hurwitz, G.A. Manzoni, P.G. Ransley, and F.D. Stephens Cloacal exstrophy: a report of 34 cases J Urol 138 1987 1060 1064
35. E. Shapiro, H. Lepor, and R.D. Jeffs The inheritance of the exstrophy-epispadias complex J Urol 132 1984 308 310
36. C.P. Nelson, R.L. Dunn, and J.T. Wei Contemporary epidemiology of bladder exstrophy in the United States J Urol 173 2005 1728 1731
37. J. Raboch Incidence of hypospadia and epispadia in chromatin-positive men Andrologia 7 1975 237 239
38. A. Chipail, V. Constantinescu, M. Covic, and T. Angheloni Phenotypic and cytogenetic analysis of an unusual malformative syndrome (trisomy 9 p+) Rev Pediatr Obstet Ginecol Pediatr 25 1976 201 210
39. H.J. Lin, F. Ndiforchu, and S. Patell Exstrophy of the cloaca in a 47, XXX child: review of genitourinary malformations in triple-X patients Am J Med Genet 45 1993 761 763
40. G. Nicholls, and P.G. Duffy Anatomical correction of the exstrophy-epispadias complex: analysis of 34 patients Br J Urol 82 1998 865 869
41. D.A. Husmann, and D.R. Vandersteen Anatomy of the cloacal exstrophy J.P. Gearhard, R. Matthews, The epispadias-exstrophy complex 1999 Kluwer Academic/Plenum New York 199 206
42. N.J. Leonard, and D.J. Tomkins Diploid/tetraploid/t(1;6) mosaicism in a 17-year-old female with hypomelanosis of Ito, multiple congenital anomalies, and body asymmetry Am J Med Genet 112 2002 86 90
43. C. Thauvin-Robinet, L. Faivre, V. Cusin, P. Khau Van Kien, P. Callier, and K.L. Parker Cloacal exstrophy in an infant with 9q34.1-qter deletion resulting from a de novo unbalanced translocation between chromosome 9q and Yq Am J Med Genet A 126A 2004 303 307
44. R. Kosaki, Y. Fukuhara, M. Kosuga, T. Okuyama, N. Kawashima, and T. Honna OEIS complex with del(3)(q12.2q13.2) Am J Med Genet A 135 2005 224 226
45. S.A. Boyadjiev, S.T. South, C.L. Radford, A. Patel, G. Zhang, and D.J. Hur A reciprocal translocation 46, XY, t(8;9)(p11.2;q13) in a bladder exstrophy patient disrupts CNTNAP3 and presents evidence of a pericentromeric duplication on chromosome 9 Genomics 85 2005 622 629
46. M. Ludwig, B. Utsch, and H. Reutter Genetische und molekularbiologische Aspekte des Blasenekstrophie-Epispadie-Komplexes (BEEK) Der Urologe 44 2005 1037 1044
47. M. Draaken, H. Reutter, C. Schramm, E. Bartels, T.M. Boemers, and A.K. Ebert Microduplications at 22q11.21 are associated with non-syndromic classic bladder exstrophy Eur J Med Genet 53 2010 55 60
48. M.S. Zaki, G. Gillessen-Kaesbach, I. Vater, A. Caliebe, R. Siebert, and A.K. Kamel Bladder exstrophy and extreme genital anomaly in a patient with pure terminal 1q deletion: expansion of phenotypic spectrum Eur J Med Genet 55 2012 43 48
49. M. Draaken, S.S. Mughal, T. Pennimpede, S. Wolter, L. Wittler, and A.K. Ebert Isolated bladder exstrophy associated with a de novo 0.9 Mb microduplication on chromosome 19p13.12 Birth Defects Res A Clin Mol Teratol 2013
50. H. Reutter, F. Ruschendorf, M. Mattheisen, M. Draaken, E. Bartels, and N. Hubner Evidence for linkage of the bladder exstrophy-epispadias complex on chromosome 4q31.21-22 and 19q13.31-41 from a consanguineous Iranian family Birth Defects Res A Clin Mol Teratol 88 2010 757 761
51. M. Ludwig, F. Rüschendorf, K. Saar, N. Hübner, L. Siekmann, and S.A. Boyadjiev Genome-wide linkage scan for bladder exstrophy-epispadias complex Birth Defects Res A Clin Mol Teratol 85 2009 174 178
52. L.S. Baskin, S.W. Hayward, P. Young, and G.R. Cunha Role of mesenchymal-epithelial interactions in normal bladder development J Urol 156 1996 1820 1827
53. L.S. Baskin, S.W. Hayward, R.A. Sutherland, M.J. DiSandro, A.A. Thomson, and J. Goodman Mesenchymal-epithelial interactions in the bladder World J Urol 14 1996 301 309
54. R. Haraguchi, J. Motoyama, H. Sasaki, Y. Satoh, S. Miyagawa, and N. Nakagata Molecular analysis of coordinated bladder and urogenital organ formation by Hedgehog signaling Development (England) 2007 525 533
55. Y. Shiroyanagi, B. Liu, M. Cao, K. Agras, J. Li, and M.H. Hsieh Urothelial sonic hedgehog signaling plays an important role in bladder smooth muscle formation Differentiation 75 2007 968 977
56. W. Cheng, C.K. Yeung, Y.K. Ng, J.R. Zhang, C.C. Hui, and P.C. Kim Sonic Hedgehog mediator Gli2 regulates bladder mesenchymal patterning J Urol 180 2008 1543 1550
57. G. Tasian, G. Cunha, and L. Baskin Smooth muscle differentiation and patterning in the urinary bladder Differentiation 2010 106 117 England: 2010 International Society of Differentiation. Published by Elsevier B.V.
58. A. Yang, M. Kaghad, Y. Wang, E. Gillett, M.D. Fleming, and V. Dötsch p63, a p53 homolog at 3q27-29, encodes multiple products with transactivating, death-inducing, and dominant-negative activities Mol Cell 2 1998 305 316
59. M.I. Koster, S. Kim, A.A. Mills, F.J. DeMayo, and D.R. Roop p63 is the molecular switch for initiation of an epithelial stratification program Genes Dev 18 2004 126 131
60. M.I. Koster, and D.R. Roop Transgenic mouse models provide new insights into the role of p63 in epidermal development Cell Cycle 3 2004 411 413
61. O. Karni-Schmidt, M. Castillo-Martin, T. HuaiShen, N. Gladoun, J. Domingo-Domenech, and M. Sanchez-Carbayo Distinct expression profiles of p63 variants during urothelial development and bladder cancer progression Am J Pathol 178 2011 1350 1360
62. M. Castillo-Martin, J. Domingo-Domenech, O. Karni-Schmidt, T. Matos, and C. Cordon-Cardo Molecular pathways of urothelial development and bladder tumorigenesis Urologic Oncol Semin Original Invest 28 2010 401 408
63. R.A. Ihrie, M.R. Marques, B.T. Nguyen, J.S. Horner, C. Papazoglu, and R.T. Bronson Perp is a p63-regulated gene essential for epithelial integrity Cell 120 2005 843 856
64. J. Laurikkala, M.L. Mikkola, M. James, M. Tummers, A.A. Mills, and I. Thesleff p63 regulates multiple signalling pathways required for ectodermal organogenesis and differentiation Development 133 2006 1553 1563
65. M. Senoo, F. Pinto, C.P. Crum, and F. McKeon p63 is essential for the proliferative potential of stem cells in stratified epithelia Cell 129 2007 523 536
66. C.E. Barbieri, and J.A. Pietenpol p63 and epithelial biology Exp Cell Res United States 2006 695 706
67. C. Blanpain, and E. Fuchs p63: revving up epithelial stem-cell potential Nat Cell Biol 9 2007 731 733
68. C.J. Di Como, M.J. Urist, I. Babayan, M. Drobnjak, C.V. Hedvat, and J. Teruya-Feldstein p63 expression profiles in human normal and tumor tissues Clin Cancer Res 8 2002 494 501
69. L. Guerrini, A. Costanzo, and G.R. Merlo A symphony of regulations centered on p63 to control development of ectoderm-derived structures J Biomed Biotechnol 2011 2011 864904
70. R.A. Ihrie, and L.D. Attardi A new Perp in the lineup: linking p63 and desmosomal adhesion Cell Cycle 4 2005 873 876
71. M.I. Koster, and D.R. Roop The role of p63 in development and differentiation of the epidermis J Dermatol Sci 34 2004 3 9
72. D.K. Carroll, J.S. Carroll, C.O. Leong, F. Cheng, M. Brown, and A.A. Mills p63 regulates an adhesion programme and cell survival in epithelial cells Nat Cell Biol 8 2006 551 561
73. J. Bakkers, M. Hild, C. Kramer, M. Furutani-Seiki, and M. Hammerschmidt Zebrafish DeltaNp63 is a direct target of Bmp signaling and encodes a transcriptional repressor blocking neural specification in the ventral ectoderm Dev Cell 2 2002 617 627
74. B.J. Ching, L. Wittler, J. Proske, G. Yagnik, L. Qi, and M. Draaken p63 (TP73L) a key player in embryonic urogenital development with significant dysregulation in human bladder exstrophy tissue Int J Mol Med 26 2010 861 867
75. S. Wilkins, K.W. Zhang, I. Mahfuz, R. Quantin, N. D'Cruz, and J. Hutson Insertion/deletion polymorphisms in the ΔNp63 promoter are a risk factor for bladder exstrophy epispadias complex PLOS Genet 8 2012 e1003070
76. T. Darling, S. Wilkins, I. Mahfuz, S. White, and W. Cheng No TAp63 promoter mutation is detected in bladder exstrophy-epispadias complex patients 46th Conference of the Pacific Association of Pediatric Surgery. Hunter Valley, Australia 7-11 April 2013
77. L. Qi, K. Chen, D.J. Hur, G. Yagnik, Y. Lakshmanan, and L.E. Kotch Genome-wide expression profiling of urinary bladder implicates desmosomal and cytoskeletal dysregulation in the bladder exstrophy-epispadias complex Int J Mol Med 27 2011 755 765
78. E.R. Flores, K.Y. Tsai, D. Crowley, S. Sengupta, A. Yang, and F. McKeon p63 and p73 are required for p53-dependent apoptosis in response to DNA damage Nature 416 2002 560 564
79. R.A. Ihrie, E. Reczek, J.S. Horner, L. Khachatrian, J. Sage, and T. Jacks Perp is a mediator of p53-dependent apoptosis in diverse cell types Curr Biol 13 2003 1985 1990
80. M.R. Marques, J.S. Horner, R.A. Ihrie, R.T. Bronson, and L.D. Attardi Mice lacking the p53/p63 target gene Perp are resistant to papilloma development Cancer Res 65 2005 6551 6556
81. R.A. Ihrie, R.T. Bronson, and L.D. Attardi Adult mice lacking the p53/p63 target gene Perp are not predisposed to spontaneous tumorigenesis but display features of ectodermal dysplasia syndromes Cell Death Differ 13 2006 1614 1618
82. M.R. Marques, R.A. Ihrie, J.S. Horner, and L.D. Attardi The requirement for perp in postnatal viability and epithelial integrity reflects an intrinsic role in stratified epithelia J Invest Dermatol 126 2006 69 73
83. V.G. Beaudry, R.A. Ihrie, S.B. Jacobs, B. Nguyen, N. Pathak, and E. Park Loss of the desmosomal component perp impairs wound healing in vivo Dermatol Res Pract 2010 2010 759731
84. B. Holthofer, R. Windoffer, S. Troyanovsky, and R.E. Leube Structure and function of desmosomes Int Rev Cytol 264 2007 65 163
85. S. Getsios, A.C. Huen, and K.J. Green Working out the strength and flexibility of desmosomes Nat Rev Mol Cell Biol 5 2004 271 281
86. E. Delva, D.K. Tucker, and A.P. Kowalczyk The desmosome Cold Spring Harb Perspect Biol 1 2009 a002543
87. H. Mueller, and W.W. Franke Biochemical and immunological characterization of desmoplakins I and II, the major polypeptides of the desmosomal plaque J Mol Biol 163 1983 647 671
88. C.M. Borrmann, C. Mertens, A. Schmidt, L. Langbein, C. Kuhn, and W.W. Franke Molecular diversity of plaques of epithelial-adhering junctions Ann N Y Acad Sci 915 2000 144 150
89. G.I. Gallicano, P. Kouklis, C. Bauer, M. Yin, V. Vasioukhin, and L. Degenstein Desmoplakin is required early in development for assembly of desmosomes and cytoskeletal linkage J Cell Biol 143 1998 2009 2022
90. E.A. Bornslaeger, C.M. Corcoran, T.S. Stappenbeck, and K.J. Green Breaking the connection: displacement of the desmosomal plaque protein desmoplakin from cell-cell interfaces disrupts anchorage of intermediate filament bundles and alters intercellular junction assembly J Cell Biol 134 1996 985 1001
91. D. Garrod, and M. Chidgey Desmosome structure, composition and function Biochim Biophys Acta Neth 2008 572 587
92. A.P. Kowalczyk, T.S. Stappenbeck, D.A. Parry, H.L. Palka, M.L. Virata, and E.A. Bornslaeger Structure and function of desmosomal transmembrane core and plaque molecules Biophys Chem 50 1994 97 112
93. A.C. Huen, J.K. Park, L.M. Godsel, X. Chen, L.J. Bannon, and E.V. Amargo Intermediate filament-membrane attachments function synergistically with actin-dependent contacts to regulate intercellular adhesive strength J Cell Biol 159 2002 1005 1017
94. V. Vasioukhin, E. Bowers, C. Bauer, L. Degenstein, and E. Fuchs Desmoplakin is essential in epidermal sheet formation Nat Cell Biol 3 2001 1076 1085
95. M.F. Jonkman, A.M. Pasmooij, S.G. Pasmans, M.P. van den Berg, H.J. Ter Horst, and A. Timmer Loss of desmoplakin tail causes lethal acantholytic epidermolysis bullosa Am J Hum Genet 77 2005 653 660
96. M. Bektas, and D.S. Rubenstein Perp and pemphigus: a disease of desmosome destabilization J Invest Dermatol 129 2009 1606 1608
97. P.J. Koch, M.G. Mahoney, H. Ishikawa, L. Pulkkinen, J. Uitto, and L. Shultz Targeted disruption of the pemphigus vulgaris antigen (desmoglein 3) gene in mice causes loss of keratinocyte cell adhesion with a phenotype similar to pemphigus vulgaris J Cell Biol 137 1997 1091 1102
98. K.J. Green, and C.A. Gaudry Are desmosomes more than tethers for intermediate filaments? Nat Rev Mol Cell Biol 1 2000 208 216
99. V.G. Beaudry, N. Pathak, M.I. Koster, and L.D. Attardi Differential PERP regulation by TP63 mutants provides insight into AEC pathogenesis Am J Med Genet A 149A 2009 1952 1957
100. M.M. Lowik, P.J. Groenen, E.N. Levtchenko, L.A. Monnens, and L.P. van den Heuvel Molecular genetic analysis of podocyte genes in focal segmental glomerulosclerosis - a review Eur J Pediatr 168 2009 1291 1304
101. P. Mundel, H.W. Heid, T.M. Mundel, M. Kruger, J. Reiser, and W. Kriz Synaptopodin: an actin-associated protein in telencephalic dendrites and renal podocytes J Cell Biol 139 1997 193 204
102. S. Angers, and R.T. Moon Proximal events in Wnt signal transduction Nat Rev Mol Cell Biol 10 2009 468 477
103. C.Y. Logan, and R. Nusse The Wnt signaling pathway in development and disease Annu Rev Cell Dev Biol 20 2004 781 810
104. P. Andre, Q. Wang, N. Wang, B. Gao, A. Schilit, and M.M. Halford The Wnt coreceptor Ryk regulates Wnt/planar cell polarity by modulating the degradation of the core planar cell polarity component Vangl2 J Biol Chem 2012 287
105. B. Gao, H. Song, K. Bishop, G. Elliot, L. Garrett, and M.A. English Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2 Dev Cell 20 2011 163 176
106. C.P. Heisenberg, M. Tada, G.J. Rauch, L. Saude, M.L. Concha, and R. Geisler Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation Nature 405 2000 76 81
107. D. Qian, C. Jones, A. Rzadzinska, S. Mark, X. Zhang, and K.P. Steel Wnt5a functions in planar cell polarity regulation in mice Dev Biol 306 2007 121 133
108. G.J. Rauch, M. Hammerschmidt, P. Blader, H.E. Schauerte, U. Strahle, and P.W. Ingham Wnt5 is required for tail formation in the zebrafish embryo Cold Spring Harb Symp Quant Biol 62 1997 227 234
109. G. Liu, A. Moro, J.J. Zhang, W. Cheng, W. Qiu, and P.C. Kim The role of Shh transcription activator Gli2 in chick cloacal development Dev Biol 303 2007 448 460