Planar cell polarity and the developmental control of cell behavior in vertebrate embryos

Annual Review of Cell and Developmental Biology

Volumn 28, Issue , 2012, Pages 627-653

  Wallingford, John B ^a  

^a UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

cilia; cochlea; convergent extension; neural tube defect

Indexed keywords

CELL PROTEIN;

CELL DIVISION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; CELL MOTILITY; CELL MOTION; CELL POLARITY; EMBRYO; EUKARYOTIC FLAGELLUM; HAIR CELL; HAIR FOLLICLE; INNER EAR; KINETOSOME; MECHANOTRANSDUCTION; MOTONEURON; NEURAL TUBE; NONHUMAN; PLANAR CELL POLARITY; PRIORITY JOURNAL; PROTEIN SYNTHESIS; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; VERTEBRATE;

ANIMALS; CELL DIVISION; CELL MOVEMENT; CELL POLARITY; CILIA; EMBRYONIC DEVELOPMENT; FACIAL NERVE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HAIR CELLS, AUDITORY, INNER; HAIR FOLLICLE; HUMANS; MEMBRANE PROTEINS; NEURAL TUBE;

ANIMALIA; VERTEBRATA;

EID: 84870182902     PISSN: 10810706     EISSN: 15308995     Source Type: Book Series    
DOI: 10.1146/annurev-cellbio-092910-154208     Document Type: Review

References (212)

1. Adler PN, Charlton J, Liu J. 1998. Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. Development 125:959-68
2. Aigouy B, Farhadifar R, Staple DB, Sagner A, Roper JC, et al. 2010. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142:773-86
3. Almuedo-Castillo M, Salo E, Adell T. 2011. Dishevelled is essential for neural connectivity and planar cell polarity in planarians. Proc. Natl. Acad. Sci. USA 108:2813-18
4. Antic D, Stubbs JL, Suyama K, Kintner C, ScottMP, Axelrod JD. 2010. Planar cell polarity enables posterior localization of nodal cilia and left-right axis determination during mouse and Xenopus embryogenesis. PLoS ONE 5:e8999
5. Bayly R, Axelrod JD. 2011. Pointing in the right direction: new developments in the field of planar cell polarity. Nat. Rev. Genet. 12:385-91
6. Beloussov LV, Louchinskaia NN, Stein AA. 2000. Tension-dependent collective cell movements in the early gastrula ectoderm of Xenopus laevis embryos. Dev. Genes Evol. 210:92-104
7. Bingham S, Higashijima S, Okamoto H, Chandrasekhar A. 2002. The zebrafish trilobite gene is essential for tangential migration of branchiomotor neurons. Dev. Biol. 242:149-60
8. Borovina A, Superina S, Voskas D, Ciruna B. 2010. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol. 12:407-12
9. Bosoi CM, Capra V, Allache R, Trinh VQ, De Marco P, et al. 2011. Identification and characterization of novel rare mutations in the planar cell polarity gene PRICKLE1 in human neural tube defects. Hum. Mutat. 32:1371-75
10. Brooks SP, Coccia M, Tang HR, Kanuga N, Machesky LM, et al. 2010. The Nance-Horan syndrome protein encodes a functional WAVE homology domain (WHD) and is important for co-ordinating actin remodelling and maintaining cell morphology. Hum. Mol. Genet. 19:2421-32
11. Caddy J, Wilanowski T, Darido C, Dworkin S, Ting SB, et al. 2010. Epidermal wound repair is regulated by the planar cell polarity signaling pathway. Dev. Cell 19:138-47
12. Carreira-Barbosa F, Concha ML, Takeuchi M, Ueno N, Wilson SW, Tada M. 2003. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 130:4037-46
13. Chae J, Kim MJ, Goo JH, Collier S, Gubb D, et al. 1999. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126:5421-29
14. Chandrasekhar A. 2004. Turning heads: development of vertebrate branchiomotor neurons. Dev. Dyn. 229:143-61
15. Cheyette BN,Waxman JS,Miller JR, Takemaru K, Sheldahl LC, et al. 2002. Dapper, aDishevelled-associated antagonist of beta-catenin and JNK signaling, is required for notochord formation. Dev. Cell 2:449-61
16. Ciruna B, Jenny A, Lee D, Mlodzik M, Schier AF. 2006. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 439:220-24
17. Classen AK, Anderson KI, Marois E, Eaton S. 2005. Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9:805-17
18. Colas JF, Schoenwolf GC. 2001. Towards a cellular and molecular understanding of neurulation. Dev. Dyn. 221:117-45
19. Collier S, Gubb D. 1997. Drosophila tissue polarity requires the cell-autonomous activity of the fuzzy gene, which encodes a novel transmembrane protein. Development 124:4029-37
20. Collier S, Lee H, Burgess R, Adler P. 2005. TheWD40 repeat protein Fritz links cytoskeletal planar polarity to Frizzled subcellular localization in the Drosophila epidermis. Genetics 169:2035-45
21. Concha ML, Adams RJ. 1998. Oriented cell divisions and cellular morphogenesis in the zebrafish gastrula and neurula: a time-lapse analysis. Development 125:983-94
22. Cotanche DA, Corwin JT. 1991. Stereociliary bundles reorient during hair cell development and regeneration in the chick cochlea. Hear. Res. 52:379-402
23. Courbard JR, Djiane A, Wu J, Mlodzik M. 2009. The apical/basal-polarity determinant Scribble cooperates with the PCP core factor Stbm/Vang and functions as one of its effectors. Dev. Biol. 333:67-77
24. Curtin JA, Quint E, Tsipouri V, Arkell RM, Cattanach B, 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. 13:1129-33
25. Dabdoub A, Donohue MJ, Brennan A,Wolf V, Montcouquiol M, et al. 2003. Wnt signaling mediates reorientation of outer hair cell stereociliary bundles in the mammalian cochlea. Development 130:2375-84
26. Dai D, Zhu H, Wlodarczyk B, Zhang L, Li L, et al. 2011. Fuz controls the morphogenesis and differentiation of hair follicles through the formation of primary cilia. J. Investig. Dermatol. 131:302-10
27. Darken RS, Scola AM, Rakeman AS,Das G, Mlodzik M, Wilson PA. 2002. The planar polarity gene strabismus regulates convergent extension movements in Xenopus. EMBO J. 21:976-85
28. da Silva SM, Vincent JP. 2007. Oriented cell divisions in the extending germband of Drosophila. Development 134:3049-54
29. Deans MR, Antic D, Suyama K, Scott MP, Axelrod JD, Goodrich LV. 2007. Asymmetric distribution of Prickle-like 2 reveals an early underlying polarization of vestibular sensory epithelia in the inner ear. J. Neurosci. 27:3139-47
30. Deardorff MA, Tan C, Conrad LJ, Klein PS. 1998. Frizzled-8 is expressed in the Spemann organizer and plays a role in early morphogenesis. Development 125:2687-700
31. Devenport D, Fuchs E. 2008. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat. Cell Biol. 10:1257-68
32. Devenport D, Oristian D, Heller E, Fuchs E. 2011. Mitotic internalization of planar cell polarity proteins preserves tissue polarity. Nat. Cell Biol. 13:893-902
33. Djiane A, Riou J, Umbhauer M, Boucaut J, Shi D. 2000. Role of frizzled 7 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 127:3091-100
34. Dodds GS. 1930. Row formation and other types of arrangement of cartilage cells in endochondral ossification. Anat. Rec. 46:385-99
35. Eaton S. 1997. Planar polarization of Drosophila and vertebrate epithelia. Curr. Opin. Cell Biol. 9:860-66
36. Eaton S, Wepf R, Simons K. 1996. Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. J. Cell Biol. 135:1277-89
37. Elsdale T, Bard J. 1972. Cellular interactions in mass cultures of human diploid fibroblasts. Nature 236:152-55
38. Elul T, Koehl MA, Keller R. 1997. Cellular mechanism underlying neural convergent extension in Xenopus laevis embryos. Dev. Biol. 191:243-58
39. Essner JJ, Vogan KJ, Wagner MK,Tabin CJ, YostHJ, BruecknerM. 2002. Conserved function for embryonic nodal cilia. Nature 418:37-38
40. Etheridge SL, Ray S, Li S, Hamblet NS, Lijam N, 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
41. Fanto M, Mlodzik M. 1999. Asymmetric Notch activation specifies photoreceptors R3 and R4 and planar polarity in the Drosophila eye. Nature 397:523-26
42. Fanto M,Weber U, Strutt DI, Mlodzik M. 2000. Nuclear signaling by Rac and Rho GTPases is required in the establishment of epithelial planar polarity in the Drosophila eye. Curr. Biol. 10:979-88
43. Feiguin F, Hannus M, Mlodzik M, Eaton S. 2001. The ankyrin repeat protein Diego mediates Frizzleddependent planar polarization. Dev. Cell 1:93-101
44. Fischer E, Legue E, Doyen A, Nato F, Nicolas JF, et al. 2006. Defective planar cell polarity in polycystic kidney disease. Nat. Genet. 38:21-23
45. Frisch D, Farbman AI. 1968. Development of order during ciliogenesis. Anat. Rec. 162:221-32
46. Gao B, Song H, Bishop K, Elliot G, Garrett L, et al. 2011. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 20:163-76
47. Goetz SC, Anderson KV. 2010. The primary cilium: a signalling centre during vertebrate development. Nat. Rev. Genet. 11:331-44
48. Gong Y, Mo C, Fraser SE. 2004. Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430:689-93
49. Goto T, Keller R. 2002. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev. Biol. 247:165-81
50. Gray RS, Abitua PB, Wlodarczyk BJ, Szabo-Rogers HL, Blanchard O, et al. 2009. The planar cell polarity effector Fuz is essential for targetedmembrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 11:1225-32
51. Gray RS, Roszko I, Solnica-Krezel L. 2011. Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell 21:120-33
52. Grimsley-Myers CM, Sipe CW, Geleoc GS, Lu X. 2009. The small GTPase Rac1 regulates auditory hair cell morphogenesis. J. Neurosci. 29:15859-69
53. Gubb D, Garcia-Bellido A. 1982. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morphol. 68:37-57
54. Gubb D, Green C, Huen D, Coulson D, Johnson G, et al. 1999. The balance between isoforms of the Prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. Genes Dev. 13:2315-27
55. Guirao B, Meunier A, Mortaud S, Aguilar A, Corsi JM, et al. 2010. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat. Cell Biol. 12:341-50
56. Guo N, Hawkins C, Nathans J. 2004. Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. USA 101:9277-81
57. Habas R, Dawid IB, He X. 2003. Coactivation of Rac and Rho by Wnt/Frizzled signaling is required for vertebrate gastrulation. Genes Dev. 17:295-309
58. Habas R, Kato Y, He X. 2001. Wnt/Frizzled activation of Rho regulates vertebrate gastrulation and requires a novel Formin homology protein Daam1. Cell 107:843-54
59. Hamblet NS, Lijam N, Ruiz-Lozano P, Wang J, Yang Y, et al. 2002. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 129:5827-38
60. Hannus M, Feiguin F, Heisenberg CP, Eaton S. 2002. Planar cell polarization requires Widerborst, a B- regulatory subunit of protein phosphatase 2A. Development 129:3493-503
61. Hartmann C, Tabin CJ. 2000. Dual roles of Wnt signaling during chondrogenesis in the chicken limb. Development 127:3141-59
62. Hashimoto M, Shinohara K, Wang J, Ikeuchi S, Yoshiba S, et al. 2010. Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 12:170-76
63. Heisenberg C-P, Tada M, Rauch G-J, Saude L, Concha ML, et al. 2000. Silberblick/Wnt11 activity mediates convergent extension movements during zebrafish gastrulation. Nature 405:76-81
64. HeydeckW, 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. 240:1938-48
65. Heydeck W, Zeng H, Liu A. 2009. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev. Dyn. 238:3035-42
66. Hikasa H, Shibata M, Hiratani I, Taira M. 2002. The Xenopus receptor tyrosine kinase Xror2 modulates morphogenetic movements of the axial mesoderm and neuroectoderm via Wnt signaling. Development 129:5227-39
67. Hirota Y, Meunier A,Huang S, Shimozawa T, Yamada O, et al. 2010. Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development 137:3037-46
68. Ho YH, Lien MT, Lin CM, Wei SY, Chang LH, Hsu JC. 2010. Echinoid regulates Flamingo endocytosis to control ommatidial rotation in the Drosophila eye. Development 137:745-54
69. Holtfreter J. 1943. A study of the mechanics of gastrulation, part I. J. Exp. Zool. 94:261-318
70. Jacobson AG, Gordon R. 1976. Changes in the shape of the developing vertebrate nervous system analyzed experimentally, mathematically and by computer simulation. J. Exp. Zool. 197:191-246
71. Jenny A. 2010. Planar cell polarity signaling in the Drosophila eye. Curr. Top. Dev. Biol. 93:189-227
72. Jessen JR, Topczewski J, Bingham S, Sepich DS,Marlow F, et al. 2002. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4:610-15
73. Jiang D, Munro EM, Smith WC. 2005. Ascidian prickle regulates both mediolateral and anterior-posterior cell polarity of notochord cells. Curr. Biol. 15:79-85
74. Jones C, Roper VC, Foucher I, Qian D, Banizs B, et al. 2008. Ciliary proteins link basal body polarization to planar cell polarity regulation. Nat. Genet. 40:69-77
75. Karner CM, Chirumamilla R, Aoki S, Igarashi P, Wallingford JB, Carroll TJ. 2009. Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet. 41:793-99
76. Keller R, Shih J,Domingo C. 1992a.The patterning and functioning of protrusive activity during convergence and extension of the Xenopus organiser. Development 116(Suppl.):81-91
77. Keller R, Shih J, Sater A. 1992b. The cellular basis of the convergence and extension of the Xenopus neural plate. Dev. Dyn. 193:199-217
78. Kelly MC,Chen P. 2009. Development of form and function in themammalian cochlea. Curr. Opin. Neurobiol. 19:395-401
79. Keys DN, Levine M, Harland RM, Wallingford JB. 2002. Control of intercalation is cell-autonomous in the notochord of Ciona intestinalis. Dev. Biol. 246:329-40
80. Kibar Z, Salem S, Bosoi CM, Pauwels E, De Marco P, et al. 2011. Contribution of VANGL2 mutations to isolated neural tube defects. Clin. Genet. 80:76-82
81. Kibar Z, Torban E, McDearmid JR, Reynolds A, Berghout J, et al. 2007. Mutations in VANGL1 associated with neural-tube defects. N. Engl. J. Med. 356:1432-37
82. Kibar Z, Vogan KJ, Groulx N, Justice MJ, Underhill DA, Gros P. 2001. Ltap, a mammalian homolog of Drosophila Strabismus/Van Gogh, is altered in themouse neural tube mutant Loop-tail. Nat. Genet. 28:251-55
83. Kieserman EK, Wallingford JB. 2009. In vivo imaging reveals a role for Cdc42 in spindle positioning and planar orientation of cell divisions during vertebrate neural tube closure. J. Cell Sci. 122:2481-90
84. KimHY, Davidson LA. 2011. Punctuated actin contractions during convergent extension and their permissive regulation by the non-canonical Wnt-signaling pathway. J. Cell Sci. 124:635-46
85. Kim SK, Shindo A, Park TJ, Oh EC, Ghosh S, et al. 2010. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 329:1337-40
86. Kim SW, Park JI, Spring CM, Sater AK, Ji H, et al. 2004. Non-canonical Wnt signals are modulated by the Kaiso transcriptional repressor and p120-catenin. Nat. Cell Biol. 6:1212-20
87. KinoshitaN, Iioka H, Miyakoshi A, UenoN. 2003. PKC?is essential forDishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev. 17:1663-76
88. Kirillova I, Novikova I, Auge J, Audollent S, Esnault D, et al. 2000. Expression of the sonic hedgehog gene in human embryos with neural tube defects. Teratology 61:347-54
89. Koonce MP, Kohler J, Neujahr R, Schwartz JM, Tikhonenko I, Gerisch G. 1999. Dynein motor regulation stabilizes interphase microtubule arrays and determines centrosome position. EMBO J. 18:6786-92
90. Kumburegama S,Wijesena N, Xu R,Wikramanayake AH. 2011. Strabismus-mediated primary archenteron invagination is uncoupled from Wnt/β-catenin-dependent endoderm cell fate specification in Nematostella vectensis (Anthozoa, Cnidaria): implications for the evolution of gastrulation. EvoDevo 2:2
91. Lake BB, Sokol SY. 2009. Strabismus regulates asymmetric cell divisions and cell fate determination in the mouse brain. J. Cell Biol. 185:59-66
92. Lawrence PA. 1966. Gradients in the insect segment: the orientation of hairs in the milkweed bug, Oncopeltus fasciatus. J. Exp. Zool. 44:607-20
93. LeeH, Adler PN. 2004. The grainy head transcription factor is essential for the function of the frizzled pathway in the Drosophila wing. Mech. Dev. 121:37-49
94. Lei YP, Zhang T, Li H, Wu BL, Jin L, Wang HY. 2010. VANGL2 mutations in human cranial neural-tube defects. N. Engl. J. Med. 362:2232-35
95. Li S, Esterberg R, Lachance V, RenD, Radde-Gallwitz K, et al. 2011. Rack1 is required for Vangl2membrane localization and planar cell polarity signaling while attenuating canonical Wnt activity. Proc. Natl. Acad. Sci. USA 108:2264-69
96. Li Y, Dudley AT. 2009. Noncanonical frizzled signaling regulates cell polarity of growth plate chondrocytes. Development 136:1083-92
97. Lowenstein O, Wersall J. 1959. A functional interpretation of the electron-microscopic structure of the sensory hairs in the cristae of the elasmobranch Raja clavata in terms of directional sensitivity. Nature 184:1807-8
98. Lu X, Borchers AG, Jolicoeur C, Rayburn H, Baker JC, Tessier-Lavigne M. 2004. PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates. Nature 430:93-98
99. Mao Y, Mulvaney J, Zakaria S, Yu T, Morgan KM, et al. 2011. Characterization of a Dchs1 mutant mouse reveals requirements for Dchs1-Fat4 signaling duringmammalian development. Development 138:947-57
100. Mapp OM, Walsh GS, Moens CB, Tada M, Prince VE. 2011. Zebrafish Prickle1b mediates facial branchiomotor neuron migration via a farnesylation-dependent nuclear activity. Development 138:2121-32
101. Mapp OM,Wanner SJ, Rohrschneider MR, Prince VE. 2010. Prickle1b mediates interpretation of migratory cues during zebrafish facial branchiomotor neuron migration. Dev. Dyn. 239:1596-608
102. Marean A, Graf A, Zhang Y, Niswander L. 2011. Folic acid supplementation can adversely affect murine neural tube closure and embryonic survival. Hum. Mol. Genet. 20:3678-83
103. Marin-Padilla M. 1966. Study of the vertebral column in human craniorhachischisis: the significance of the notochordal alterations. Acta Anat. 63:32-48
104. Marlow F, Topczewski J, Sepich D, Solnica-Krezel L. 2002. Zebrafish Rho kinase 2 acts downstream ofWnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 12:876-84
105. May-Simera HL, Kai M, Hernandez V, Osborn DP, Tada M, Beales PL. 2010. Bbs8, together with the planar cell polarity protein Vangl2, is required to establish left-right asymmetry in zebrafish. Dev. Biol. 345:215-25
106. Merte J, Jensen D, Wright K, Sarsfield S, Wang Y, et al. 2010. Sec24b selectively sorts Vangl2 to regulate planar cell polarity during neural tube closure. Nat. Cell Biol. 12:41-46
107. Mitchell B, Stubbs JL, Huisman F, Taborek P, Yu C, Kintner C. 2009. The PCP pathway instructs the planar orientation of ciliated cells in the Xenopus larval skin. Curr. Biol. 19:924-29
108. Montcouquiol M, Rachel RA, Lanford PJ, Copeland NG, Jenkins NA, Kelley MW. 2003. Identification of Vangl2 and Scrb1 as planar polarity genes in mammals. Nature 423:173-77
109. Montcouquiol M, Sans N, Huss D, Kach J, Dickman JD, et al. 2006. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J. Neurosci. 26:5265-75
110. Moon RT, Campbell RM, Christian JL, McGrew LL, Shih J, Fraser S. 1993. Xwnt-5A: a maternal Wnt that affects morphogenetic movements after overexpression in embryos of Xenopus laevis. Development 119:97-111
111. Morin X, Bellaiche Y. 2011. Mitotic spindle orientation in asymmetric and symmetric cell divisions during animal development. Dev. Cell 21:102-19
112. Munro EM, Odell GM. 2002. Polarized basolateral cell motility underlies invagination and convergent extension of the ascidian notochord. Development 129:13-24
113. Murdoch JN, Copp AJ. 2010. The relationship between sonic Hedgehog signaling, cilia, and neural tube defects. Birth Defects Res. A 88:633-52
114. Murdoch JN, Doudney K, Paternotte C, Copp AJ, 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. 10:2593-601
115. Narimatsu M, Bose R, Pye M, Zhang L, Miller B, et al. 2009. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 137:295-307
116. Nishio S, Tian X, Gallagher AR, Yu Z, Patel V, et al. 2010. Loss of oriented cell division does not initiate cyst formation. J. Am. Soc. Nephrol. 21:295-302
117. Oishi I, Kawakami Y, Raya A, Callol-Massot C, Izpisua Belmonte JC. 2006. Regulation of primary cilia formation and left-right patterning in zebrafish by a noncanonical Wnt signaling mediator, duboraya. Nat. Genet. 38:1316-22
118. Okada Y, Takeda S, Tanaka Y, Belmonte JC, Hirokawa N. 2005. Mechanism of nodal flow: a conserved symmetry breaking event in left-right axis determination. Cell 121:633-44
119. Olguin P, Glavic A, Mlodzik M. 2011. Intertissue mechanical stress affects Frizzled-mediated planar cell polarity in the Drosophila notum epidermis. Curr. Biol. 21:236-42
120. Oteiza P, Koppen M, Krieg M, Pulgar E, Farias C, et al. 2010. Planar cell polarity signalling regulates cell adhesion properties in progenitors of the zebrafish laterality organ. Development 137:3459-68
121. Park M, Moon RT. 2002. The planar cell-polarity gene stbm regulates cell behaviour and cell fate in vertebrate embryos. Nat. Cell Biol. 4:20-25
122. Park TJ, Haigo SL, Wallingford JB. 2006. Ciliogenesis defects in embryos lacking inturned or fuzzy function are associated with failure of planar cell polarity and Hedgehog signaling. Nat. Genet. 38:303-11
123. Park TJ, Mitchell BJ, Abitua PB, Kintner C, Wallingford JB. 2008. Dishevelled controls apical docking and planar polarization of basal bodies in ciliated epithelial cells. Nat. Genet. 40:871-79
124. Park WJ, Liu J, Sharp EJ, Adler PN. 1996. The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 122:961-69
125. Philipp I, Aufschnaiter R, Ozbek S, Pontasch S, Jenewein M, et al. 2009. Wnt/β-Catenin and noncanonical Wnt signaling interact in tissue evagination in the simple eumetazoan Hydra. Proc. Natl. Acad. Sci. USA 106:4290-95
126. Pitaval A, Tseng Q, Bornens M, Thery M. 2010. Cell shape and contractility regulate ciliogenesis in cell cycle-arrested cells. J. Cell Biol. 191:303-12
127. Qian D, JonesC,Rzadzinska A,Mark S,Zhang X, et al. 2007. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 306:121-33
128. Qu Y, Glasco DM, Zhou L, Sawant A, Ravni A, et al. 2010. Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. J. Neurosci. 30:9392-401
129. Quesada-Hernandez E, Caneparo L, Schneider S, Winkler S, Liebling M, et al. 2010. Stereotypical cell division orientation controls neural rod midline formation in zebrafish. Curr. Biol. 20:1966-72
130. Radulescu AE, Cleveland DW. 2010. NuMA after 30 years: the matrix revisited. Trends Cell Biol. 20:214-22
131. Ravni A,Qu Y,Goffinet AM, Tissir F. 2009. Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J. Investig. Dermatol. 129:2507-9
132. Robinson A, Escuin S, Doudney K, Vekemans M, Stevenson RE, et al. 2012. Mutations in the planar cell polarity genes CELSR1 and SCRIB are associated with the severe neural tube defect craniorachischisis. Hum. Mutat. 33:440-47
133. Rocha PP, Scholze M, Bleiss W, Schrewe H. 2010. Med12 is essential for early mouse development and for canonical Wnt and Wnt/PCP signaling. Development 137:2723-31
134. Rohrschneider MR, Elsen GE, Prince VE. 2007. Zebrafish Hoxb1a regulates multiple downstream genes including prickle1b. Dev. Biol. 309:358-72
135. Ross AJ, May-Simera H, Eichers ER, Kai M, Hill J, et al. 2005. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 37:1135-40
136. Saburi S, Hester I, Fischer E, Pontoglio M, Eremina V, et al. 2008. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 40:1010-15
137. 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 138:1361-70
138. Schlessinger K, McManus EJ, Hall A. 2007. Cdc42 and noncanonical Wnt signal transduction pathways cooperate to promote cell polarity. J. Cell Biol. 178:355-61
139. SegalenM, Johnston CA, Martin CA,Dumortier JG, Prehoda KE, et al. 2010. The Fz-Dsh planar cell polarity pathway induces oriented cell division via Mud/NuMA in Drosophila and zebrafish. Dev. Cell 19:740-52
140. Seo JH, Zilber Y, Babayeva S, Liu J, Kyriakopoulos P, et al. 2011. Mutations in the planar cell polarity gene, Fuzzy, are associated with neural tube defects in humans. Hum. Mol. Genet. 20:4324-33
141. Sepich DS, Usmani M, Pawlicki S, Solnica-Krezel L. 2011. Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. Development 138:543-52
142. Shih J,Keller R. 1992. Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 116:901-14
143. Shimada Y, Yonemura S, Ohkura H, Strutt D, Uemura T. 2006. Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev. Cell 10:209-22
144. Shindo A, Yamamoto TS, Ueno N. 2008. Coordination of cell polarity during Xenopus gastrulation. PLoS ONE 3:e1600
145. Simons M, Gloy J, Ganner A, Bullerkotte A, BashkurovM, et al. 2005. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 37:537-43
146. Sipe CW, Lu X. 2011. Kif3a regulates planar polarization of auditory hair cells through both ciliary and non-ciliary mechanisms. Development 138:3441-49
147. Sittaramane V, Sawant A, Wolman MA, Maves L, Halloran MC, Chandrasekhar A. 2009. The cell adhesion molecule Tag1, transmembrane protein Stbm/Vangl2, and Lamininα1 exhibit genetic interactions during migration of facial branchiomotor neurons in zebrafish. Dev. Biol. 325:363-73
148. Smith JS, Stein KF. 1962. Axial elongation in the mouse and its retardation in homozygous looptail mice. J. Embryol. Exp. Morph. 10:73-87
149. Sokol SY. 1996. Analysis ofDishevelled signalling pathways during Xenopus development. Curr. Biol. 6:1456-67
150. Song H, Hu J, Chen W, Elliott G, Andre P, et al. 2010. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466:378-82
151. Song MR, Shirasaki R, Cai CL, Ruiz EC, Evans SM, et al. 2006. T-Box transcription factor Tbx20 regulates a genetic program for cranial motor neuron cell body migration. Development 133:4945-55
152. Stein KF, Rudin IA. 1953. Development of mice homozygous for the gene for looptail. J. Hered. 44:59-69
153. Strong LC, HollanderWF. 1949. Hereditary loop-tail in the house mouse. J. Hered. 40:329-34
154. Sugiyama Y, Stump RJ, Nguyen A, Wen L, Chen Y, et al. 2010. Secreted frizzled-related protein disrupts PCP in eye lens fiber cells that have polarised primary cilia. Dev. Biol. 338:193-201
155. Suriben R, Kivimae S, Fisher DA, Moon RT, Cheyette BN. 2009. Posterior malformations in Dact1 mutant mice arise through misregulated Vangl2 at the primitive streak. Nat Genet. 41:977-85
156. Tada M, Smith JC. 2000. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 127:2227-38
157. Tahinci E, Symes K. 2003. Distinct functions of Rho and Rac are required for convergent extension during Xenopus gastrulation. Dev. Biol. 259:318-35
158. Takeuchi M, Nakabayashi J, Sakaguchi T, Yamamoto TS, Takahashi H, et al. 2003. The prickle-related gene in vertebrates is essential for gastrulation cell movements. Curr. Biol. 13:674-79
159. Tanegashima K, Zhao H, Dawid IB. 2008. WGEF activates Rho in the Wnt-PCP pathway and controls convergent extension in Xenopus gastrulation. EMBO J. 27:606-17
160. Tao H, Suzuki M, Kiyonari H, Abe T, Sasaoka T, Ueno N. 2009. Mouse prickle1, the homolog of a PCP gene, is essential for epiblast apical-basal polarity. Proc. Natl. Acad. Sci. USA 106:14426-31
161. Tawk M, Araya C, Lyons DA, Reugels AM, Girdler GC, et al. 2007. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 446:797-800
162. Taylor J, Abramova N, Charlton J, Adler PN. 1998. Van Gogh: a new Drosophila tissue polarity gene. Genetics 150:199-210
163. Theisen H, Purcell J, Bennett M, Kansagara D, Syed A,Marsh JL. 1994. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 120:347-60
164. Tilney LG, Saunders JC. 1983. Actin filaments, stereocilia, and hair cells of the bird cochlea. I. Length, number, width, and distribution of stereocilia of each hair cell are related to the position of the hair cell on the cochlea. J. Cell Biol. 96:807-21
165. Ting SB, Wilanowski T, Auden A, Hall M, Voss AK, et al. 2003. Inositol-and folate-resistant neural tube defects in mice lacking the epithelial-specific factor Grhl-3. Nat. Med. 9:1513-19
166. Tissir F, Qu Y, Montcouquiol M, Zhou L, Komatsu K, et al. 2010. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 13:700-7
167. Topczewski J, Sepich DS, Myers DC, Walker C, Amores A, et al. 2001. The zebrafish glypican Knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 1:251-64
168. Ulrich F, KriegM, Schotz EM, Link V, Castanon I, et al. 2005. Wnt11 functions in gastrulation by controlling cell cohesion through Rab5c and E-cadherin. Dev. Cell 9:555-64
169. Usui T, Shima Y, Shimada Y, Hirano S, Burgess RW, et al. 1999. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98:585-95
170. Veeman MT, Slusarski DC, Kaykas A, Louie SH, Moon RT. 2003. Zebrafish prickle, a modulator of noncanonical Wnt/Fz signaling, regulates gastrulation movements. Curr. Biol. 13:680-85
171. Vinson CR, Adler PN. 1987. Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329:549-51
172. Vinson CR, Conover S, Adler PN. 1989. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338:263-64
173. Vivancos V, Chen P, Spassky N, Qian D, Dabdoub A, et al. 2009. Wnt activity guides facial branchiomotor neuron migration, and involves the PCP pathway and JNK and ROCK kinases. Neural Dev. 4:7
174. Vogt W. 1922. Die Einrollung und Streckung Der Urmundlippen bei Triton nach Versuchen mit einer neuen Methode embryonaler Transplantation. Verhandl. Dtsch. Zool. Ges. 27:49-51
175. Wada H, IwasakiM, Sato T,Masai I, Nishiwaki Y, et al. 2005. Dual roles of zygotic and maternal Scribble1 in neural migration and convergent extension movements in zebrafish embryos. Development 132:2273-85
176. Wada H, Tanaka H, Nakayama S, Iwasaki M, Okamoto H. 2006. Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 133:4749-59
177. Wallingford JB. 2010. Planar cell polarity signaling, cilia and polarized ciliary beating. Curr. Opin. Cell Biol. 22:597-604
178. Wallingford JB, Harland RM. 2001. Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development 128:2581-92
179. Wallingford JB, HarlandRM.2002. Neural tube closure requiresDishevelled- dependent convergent extension of the midline. Development 129:5815-25
180. Wallingford JB, Mitchell B. 2011. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 25:201-13
181. Wallingford JB, Rowning BA, Vogeli KM, Rothbacher U, Fraser SE,Harland RM. 2000. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 405:81-85
182. Wallingford JB, Vogeli KM, Harland RM. 2001. Regulation of convergent extension in Xenopus by Wnt5a and Frizzled-8 is independent of the canonical Wnt pathway. Int. J. Dev. Biol. 45:225-27
183. WalshGS, Grant PK, Morgan JA, MoensCB. 2011. Planar polarity pathway andNance-Horan syndrome-like 1b have essential cell-autonomous functions in neuronal migration. Development 138:3033-42
184. Wang B, Sinha T, Jiao K, Serra R, 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. 20:271-85
185. Wang J, Hamblet N, Mark S, Dickinson M, Brinkman B, et al. 2006. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 133:1767-78
186. Wang J, Mark S, Zhang X, Qian D, Yoo SJ, et al. 2005. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat. Genet. 37:980-85
187. Wang Y, Badea T, Nathans J. 2006a. Order from disorder: self-organization in mammalian hair patterning. Proc. Natl. Acad. Sci. USA 103:19800-5
188. Wang Y, Chang H, Nathans J. 2010. When whorls collide: the development of hair patterns in frizzled 6 mutant mice. Development 137:4091-99
189. 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. 26:2147-56
190. Wansleeben C, Feitsma H, Montcouquiol M, Kroon C, Cuppen E, Meijlink F. 2010. Planar cell polarity defects and defective Vangl2 trafficking in mutants for the COPII gene Sec24b. Development 137:1067-73
191. Wehner P, Shnitsar I, Urlaub H, Borchers A. 2011. RACK1 is a novel interaction partner of PTK7 that is required for neural tube closure. Development 138:1321-27
192. Wen J, Chiang YJ, Gao C, Xue H, Xu J, et al. 2010. Loss of Dact1 disrupts planar cell polarity signaling by altering Dishevelled activity and leads to posterior malformation in mice. J. Biol. Chem. 285:11023-30
193. Wen S, Zhu H, Lu W, Mitchell LE, Shaw GM, et al. 2010. Planar cell polarity pathway genes and risk for spina bifida. Am. J. Med. Genet. A 152A:299-304
194. Werner ME, Hwang P, Huisman F, Taborek P, Yu CC, Mitchell BJ. 2011. Actin and microtubules drive differential aspects of planar cell polarity in multiciliated cells. J. Cell Biol. 195:19-26
195. Wigglesworth VB. 1940. Local and general factors in the development of pattern in Rhodnius prolixus (Hemiptera). J. Exp. Biol. 17:180-200
196. Wilson P, Keller R. 1991. Cell rearrangement during gastrulation of Xenopus: direct observation of cultured explants. Development 112:289-300
197. Winter CG,Wang B, Ballew A, Royou A, Karess R, et al. 2001. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 105:81-91
198. Wolff T, Rubin GM. 1998. strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125:1149-59
199. WyngaardenLA, VogeliKM,CirunaBG, Wells M, HadjantonakisAK, Hopyan S. 2010. Oriented cell motility and division underlie early limb bud morphogenesis. Development 137:2551-58
200. Yamaguchi TP, Bradley A, McMahon AP, Jones S. 1999. AWnt5a pathway underlies outgrowth of multiple structures in the vertebrate embryo. Development 126:1211-23
201. Yamanaka Y, Tamplin OJ, Beckers A, Gossler A, Rossant J. 2007. Live imaging and genetic analysis of mouse notochord formation reveals regional morphogenetic mechanisms. Dev. Cell 13:884-96
202. Yang CH, Axelrod JD, Simon MA. 2002. Regulation of Frizzled by Fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108:675-88
203. Yates LL, Papakrivopoulou J, Long DA, Goggolidou P, Connolly JO, et al. 2010. The planar cell polarity gene Vangl2 is required for mammalian kidney-branching morphogenesis and glomerular maturation. Hum. Mol. Genet. 19:4663-76
204. Ybot-Gonzalez P, Savery D, Gerrelli D, Signore M, Mitchell CE, et al. 2007. Convergent extension, planarcell-polarity signalling and initiation of mouse neural tube closure. Development 134:789-99
205. Yen WW, WilliamsM, Periasamy A, Conaway M, Burdsal C, et al. 2009. PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation. Development 136:2039-48
206. Yin C, Kiskowski M, Pouille PA, Farge E, Solnica-Krezel L. 2008. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol. 180:221-32
207. Yu A, Rual JF, Tamai K, Harada Y, Vidal M, et al. 2007. Association of Dishevelled with the clathrin AP-2 adaptor is required for Frizzled endocytosis and planar cell polarity signaling. Dev. Cell 12:129-41
208. Zallen JA, Wieschaus E. 2004. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 6:343-55
209. ZeidlerMP, PerrimonN, Strutt DI. 1999. The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification. Curr. Biol. 9:1363-72
210. 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. 339:418-28
211. Zhou J, KimHY, Wang JH,DavidsonLA. 2010. Macroscopic stiffening of embryonic tissues viamicrotubules, RhoGEF and the assembly of contractile bundles of actomyosin. Development 137:2785-94
212. Zigman M, Trinh LA, Fraser SE, Moens CB. 2011. Zebrafish neural tube morphogenesis requires Scribbledependent oriented cell divisions. Curr. Biol. 21:79-86