Planar Cell Polarity: Coordinating Morphogenetic Cell Behaviors with Embryonic Polarity

Developmental Cell

Volumn 21, Issue 1, 2011, Pages 120-133

  Gray, Ryan S ^a   Roszko, Isabelle ^a   Solnica Krezel, Lilianna ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BETA CATENIN; CYTOPLASM PROTEIN; MEMBRANE PROTEIN; WNT PROTEIN;

CELL DIFFERENTIATION; CELL FUNCTION; CELL INTERACTION; CELL MEMBRANE; CELL ORGANELLE; CELL POLARITY; CELL POPULATION; CELLULAR DISTRIBUTION; CYTOPLASM; DROSOPHILA; EMBRYO POLARITY; ENDOCYTOSIS; EUKARYOTIC FLAGELLUM; FEEDBACK SYSTEM; KINETOSOME; MORPHOGENESIS; MUTATION; NONHUMAN; PHENOTYPE; POLARIZATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; REVIEW; SIGNAL TRANSDUCTION; TISSUE; VERTEBRATE;

ANIMALS; BODY PATTERNING; CELL POLARITY; CILIA; EMBRYO, MAMMALIAN; FRIZZLED RECEPTORS; HUMANS; MICROTUBULE-ORGANIZING CENTER; SIGNAL TRANSDUCTION;

VERTEBRATA;

EID: 79960240783     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2011.06.011     Document Type: Review

References (156)

1. Adler P.N. Planar signaling and morphogenesis in Drosophila. Dev. Cell 2002, 2:525-535.
2. Adler P.N., Krasnow R.E., Liu J. Tissue polarity points from cells that have higher Frizzled levels towards cells that have lower Frizzled levels. Curr. Biol. 1997, 7:940-949.
3. Adler P.N., Charlton J., Liu J. Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. Development 1998, 125:959-968.
4. Aigouy B., Farhadifar R., Staple D.B., Sagner A., Röper J.C., Jülicher F., Eaton S. Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 2010, 142:773-786.
5. Almuedo-Castillo M., Saló E., Adell T. Dishevelled is essential for neural connectivity and planar cell polarity in planarians. Proc. Natl. Acad. Sci. USA 2011, 108:2813-2818.
6. Amonlirdviman K., Khare N.A., Tree D.R., Chen W.S., Axelrod J.D., Tomlin C.J. Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 2005, 307:423-426.
7. 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.
8. Axelrod J.D. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 2001, 15:1182-1187.
9. Baldari C.T., Rosenbaum J. Intraflagellar transport: it's not just for cilia anymore. Curr. Opin. Cell Biol. 2010, 22:75-80.
10. Bastock R., Strutt H., Strutt D. Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 2003, 130:3007-3014.
11. Borovina A., Superina S., Voskas D., Ciruna B. Vangl2 directs the posterior tilting and asymmetric localization of motile primary cilia. Nat. Cell Biol. 2010, 12:407-412.
12. Brittle A.L., Repiso A., Casal J., Lawrence P.A., Strutt D. Four-jointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Curr. Biol. 2010, 20:803-810.
13. Brodsky M.H., Steller H. Positional information along the dorsal-ventral axis of the Drosophila eye: graded expression of the four-jointed gene. Dev. Biol. 1996, 173:428-446.
14. Cao Y., Park A., Sun Z. Intraflagellar transport proteins are essential for cilia formation and for planar cell polarity. J. Am. Soc. Nephrol. 2010, 21:1326-1333.
15. Carreira-Barbosa F., Concha M.L., Takeuchi M., Ueno N., Wilson S.W., Tada M. Prickle 1 regulates cell movements during gastrulation and neuronal migration in zebrafish. Development 2003, 130:4037-4046.
16. Carreira-Barbosa F., Kajita M., Morel V., Wada H., Okamoto H., Martinez Arias A., Fujita Y., Wilson S.W., Tada M. Flamingo regulates epiboly and convergence/extension movements through cell cohesive and signalling functions during zebrafish gastrulation. Development 2009, 136:383-392.
17. Casal J., Struhl G., Lawrence P.A. Developmental compartments and planar polarity in Drosophila. Curr. Biol. 2002, 12:1189-1198.
18. 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.
19. Chae J., Kim M.J., Goo J.H., Collier S., Gubb D., Charlton J., Adler P.N., Park W.J. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 1999, 126:5421-5429.
20. Chen W.S., Antic D., Matis M., Logan C.Y., Povelones M., Anderson G.A., Nusse R., Axelrod J.D. Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 2008, 133:1093-1105.
21. Ciani L., Patel A., Allen N.D., ffrench-Constant C. Mice lacking the giant protocadherin mFAT1 exhibit renal slit junction abnormalities and a partially penetrant cyclopia and anophthalmia phenotype. Mol. Cell. Biol. 2003, 23:3575-3582.
22. Ciruna B., Jenny A., Lee D., Mlodzik M., Schier A.F. Planar cell polarity signalling couples cell division and morphogenesis during neurulation. Nature 2006, 439:220-224.
23. Clark H.F., Brentrup D., Schneitz K., Bieber A., Goodman C., Noll M. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev. 1995, 9:1530-1542.
24. Classen A.K., Anderson K.I., Marois E., Eaton S. Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 2005, 9:805-817.
25. 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.
26. Collier S., Lee H., Burgess R., Adler P. The WD40 repeat protein fritz links cytoskeletal planar polarity to frizzled subcellular localization in the Drosophila epidermis. Genetics 2005, 169:2035-2045.
27. Curtin J.A., Quint E., Tsipouri V., Arkell R.M., Cattanach B., Copp A.J., Henderson D.J., Spurr N., Stanier P., Fisher E.M., et al. Mutation of Celsr1 disrupts planar polarity of inner ear hair cells and causes severe neural tube defects in the mouse. Curr. Biol. 2003, 13:1129-1133.
28. Dai D., Zhu H., Wlodarczyk B., Zhang L., Li L., Li A.G., Finnell R.H., Roop D.R., Chen J. Fuz controls the morphogenesis and differentiation of hair follicles through the formation of primary cilia. J. Invest. Dermatol. 2011, 131:302-310.
29. Dann C.E., Hsieh J.C., Rattner A., Sharma D., Nathans J., Leahy D.J. Insights into Wnt binding and signalling from the structures of two Frizzled cysteine-rich domains. Nature 2001, 412:86-90.
30. De Robertis E.M., Larraín J., Oelgeschläger M., Wessely O. The establishment of Spemann's organizer and patterning of the vertebrate embryo. Nat. Rev. Genet. 2000, 1:171-181.
31. Deans M.R., Antic D., Suyama K., Scott M.P., Axelrod J.D., Goodrich L.V. Asymmetric distribution of prickle-like 2 reveals an early underlying polarization of vestibular sensory epithelia in the inner ear. J. Neurosci. 2007, 27:3139-3147.
32. Devenport D., Fuchs E. Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat. Cell Biol. 2008, 10:1257-1268.
33. Ehebauer M.T., Arias A.M. The structural and functional determinants of the Axin and Dishevelled DIX domains. BMC Struct. Biol. 2009, 9:70.
34. Etheridge S.L., Ray S., Li S., Hamblet N.S., Lijam N., Tsang M., Greer J., Kardos N., Wang J., Sussman D.J., 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 Genet. 2008, 4:e1000259.
35. Fanto M., Clayton L., Meredith J., Hardiman K., Charroux B., Kerridge S., McNeill H. The tumor-suppressor and cell adhesion molecule Fat controls planar polarity via physical interactions with Atrophin, a transcriptional co-repressor. Development 2003, 130:763-774.
36. Feiguin F., Hannus M., Mlodzik M., Eaton S. The ankyrin repeat protein Diego mediates Frizzled-dependent planar polarization. Dev. Cell 2001, 1:93-101.
37. Fenstermaker A.G., Prasad A.A., Bechara A., Adolfs Y., Tissir F., Goffinet A., Zou Y., Pasterkamp R.J. Wnt/planar cell polarity signaling controls the anterior-posterior organization of monoaminergic axons in the brainstem. J. Neurosci. 2010, 30:16053-16064.
38. Gao B., Song H., Bishop K., Elliot G., Garrett L., English M.A., Andre P., Robinson J., Sood R., Minami Y., et al. Wnt signaling gradients establish planar cell polarity by inducing Vangl2 phosphorylation through Ror2. Dev. Cell 2011, 20:163-176.
39. Gong Y., Mo C., Fraser S.E. Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 2004, 430:689-693.
40. Goodrich L.V. The plane facts of PCP in the CNS. Neuron 2008, 60:9-16.
41. Goto T., Keller R. The planar cell polarity gene strabismus regulates convergence and extension and neural fold closure in Xenopus. Dev. Biol. 2002, 247:165-181.
42. Graff J.M., Thies R.S., Song J.J., Celeste A.J., Melton D.A. Studies with a Xenopus BMP receptor suggest that ventral mesoderm-inducing signals override dorsal signals in vivo. Cell 1994, 79:169-179.
43. Gray R.S., Abitua P.B., Wlodarczyk B.J., Szabo-Rogers H.L., Blanchard O., Lee I., Weiss G.S., Liu K.J., Marcotte E.M., Wallingford J.B., Finnell R.H. The planar cell polarity effector Fuz is essential for targeted membrane trafficking, ciliogenesis and mouse embryonic development. Nat. Cell Biol. 2009, 11:1225-1232.
44. Gubb D., García-Bellido A. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morphol. 1982, 68:37-57.
45. Gubb D., Green C., Huen D., Coulson D., Johnson G., Tree D., Collier S., Roote J. The balance between isoforms of the prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. Genes Dev. 1999, 13:2315-2327.
46. Guirao B., Meunier A., Mortaud S., Aguilar A., Corsi J.M., Strehl L., Hirota Y., Desoeuvre A., Boutin C., Han Y.G., et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat. Cell Biol. 2010, 12:341-350.
47. Guo N., Hawkins C., Nathans J. Frizzled6 controls hair patterning in mice. Proc. Natl. Acad. Sci. USA 2004, 101:9277-9281.
48. Hamblet N.S., Lijam N., Ruiz-Lozano P., Wang J., Yang Y., Luo Z., Mei L., Chien K.R., Sussman D.J., Wynshaw-Boris A. Dishevelled 2 is essential for cardiac outflow tract development, somite segmentation and neural tube closure. Development 2002, 129:5827-5838.
49. Harumoto T., Ito M., Shimada Y., Kobayashi T.J., Ueda H.R., Lu B., Uemura T. Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev. Cell 2010, 19:389-401.
50. Hashimoto M., Shinohara K., Wang J., Ikeuchi S., Yoshiba S., Meno C., Nonaka S., Takada S., Hatta K., Wynshaw-Boris A., Hamada H. Planar polarization of node cells determines the rotational axis of node cilia. Nat. Cell Biol. 2010, 12:170-176.
51. Heisenberg C.P., Nüsslein-Volhard C. The function of silberblick in the positioning of the eye anlage in the zebrafish embryo. Dev. Biol. 1997, 184:85-94.
52. Heisenberg C.P., Tada M., Rauch G.J., Saúde L., Concha M.L., Geisler R., Stemple D.L., Smith J.C., Wilson S.W. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 2000, 405:76-81.
53. Heydeck W., Zeng H., Liu A. Planar cell polarity effector gene Fuzzy regulates cilia formation and Hedgehog signal transduction in mouse. Dev. Dyn. 2009, 238:3035-3042.
54. Hirota Y., Meunier A., Huang S., Shimozawa T., Yamada O., Kida Y.S., Inoue M., Ito T., Kato H., Sakaguchi M., et al. Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development 2010, 137:3037-3046.
55. Hu Q., Milenkovic L., Jin H., Scott M.P., Nachury M.V., Spiliotis E.T., Nelson W.J. A septin diffusion barrier at the base of the primary cilium maintains ciliary membrane protein distribution. Science 2010, 329:436-439.
56. Huang P., Schier A.F. Dampened Hedgehog signaling but normal Wnt signaling in zebrafish without cilia. Development 2009, 136:3089-3098.
57. Huangfu D., Liu A., Rakeman A.S., Murcia N.S., Niswander L., Anderson K.V. Hedgehog signalling in the mouse requires intraflagellar transport proteins. Nature 2003, 426:83-87.
58. Iliescu A., Gravel M., Horth C., Apuzzo S., Gros P. Transmembrane topology of mammalian planar cell polarity protein Vangl1. Biochemistry 2011, 50:2274-2282.
59. Ishikawa H.O., Takeuchi H., Haltiwanger R.S., Irvine K.D. Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 2008, 321:401-404.
60. Jenny A., Reynolds-Kenneally J., Das G., Burnett M., Mlodzik M. Diego and Prickle regulate Frizzled planar cell polarity signalling by competing for Dishevelled binding. Nat. Cell Biol. 2005, 7:691-697.
61. Jessen J.R., Solnica-Krezel L. Identification and developmental expression pattern of van gogh-like 1, a second zebrafish strabismus homologue. Gene Expr. Patterns 2004, 4:339-344.
62. Jessen J.R., Topczewski J., Bingham S., Sepich D.S., Marlow F., Chandrasekhar A., Solnica-Krezel L. Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 2002, 4:610-615.
63. Jiang D., Munro E.M., Smith W.C. Ascidian prickle regulates both mediolateral and anterior-posterior cell polarity of notochord cells. Curr. Biol. 2005, 15:79-85.
64. Jones C., Chen P. Primary cilia in planar cell polarity regulation of the inner ear. Curr. Top. Dev. Biol. 2008, 85:197-224.
65. Karner C.M., Chirumamilla R., Aoki S., Igarashi P., Wallingford J.B., Carroll T.J. Wnt9b signaling regulates planar cell polarity and kidney tubule morphogenesis. Nat. Genet. 2009, 41:793-799.
66. Keller R. Shaping the vertebrate body plan by polarized embryonic cell movements. Science 2002, 298:1950-1954.
67. Keller R., Davidson L., Edlund A., Elul T., Ezin M., Shook D., Skoglund P. Mechanisms of convergence and extension by cell intercalation. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2000, 355:897-922.
68. 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. Nat. Genet. 2001, 28:251-255.
69. Kibar Z., Torban E., McDearmid J.R., Reynolds A., Berghout J., Mathieu M., Kirillova I., De Marco P., Merello E., Hayes J.M., et al. Mutations in VANGL1 associated with neural-tube defects. N. Engl. J. Med. 2007, 356:1432-1437.
70. Kilian B., Mansukoski H., Barbosa F.C., Ulrich F., Tada M., Heisenberg C.P. The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev. 2003, 120:467-476.
71. Kim S.K., Shindo A., Park T.J., Oh E.C., Ghosh S., Gray R.S., Lewis R.A., Johnson C.A., Attie-Bittach T., Katsanis N., Wallingford J.B. Planar cell polarity acts through septins to control collective cell movement and ciliogenesis. Science 2010, 329:1337-1340.
72. Kinoshita N., Iioka H., Miyakoshi A., Ueno N. PKC delta is essential for Dishevelled function in a noncanonical Wnt pathway that regulates Xenopus convergent extension movements. Genes Dev. 2003, 17:1663-1676.
73. Lawrence P.A., Casal J., Struhl G. Cell interactions and planar polarity in the abdominal epidermis of Drosophila. Development 2004, 131:4651-4664.
74. Lawrence P.A., Struhl G., Casal J. Planar cell polarity: one or two pathways?. Nat. Rev. Genet. 2007, 8:555-563.
75. Lei Y.P., Zhang T., Li H., Wu B.L., Jin L., Wang H.Y. VANGL2 mutations in human cranial neural-tube defects. N. Engl. J. Med. 2010, 362:2232-2235.
76. Lin F., Sepich D.S., Chen S., Topczewski J., Yin C., Solnica-Krezel L., Hamm H. Essential roles of Galpha12/13 signaling in distinct cell behaviors driving zebrafish convergence and extension gastrulation movements. J. Cell Biol. 2005, 169:777-787.
77. 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.
78. Ma D., Yang C.H., McNeill H., Simon M.A., Axelrod J.D. Fidelity in planar cell polarity signalling. Nature 2003, 421:543-547.
79. Mahoney P.A., Weber U., Onofrechuk P., Biessmann H., Bryant P.J., Goodman C.S. The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 1991, 67:853-868.
80. Mao Y., Mulvaney J., Zakaria S., Yu T., Morgan K.M., Allen S., Basson M.A., Francis-West P., Irvine K.D. Characterization of a Dchs1 mutant mouse reveals requirements for Dchs1-Fat4 signaling during mammalian development. Development 2011, 138:947-957.
81. Marlow F., Zwartkruis F., Malicki J., Neuhauss S.C., Abbas L., Weaver M., Driever W., Solnica-Krezel L. Functional interactions of genes mediating convergent extension, knypek and trilobite, during the partitioning of the eye primordium in zebrafish. Dev. Biol. 1998, 203:382-399.
82. Marlow F., Topczewski J., Sepich D., Solnica-Krezel L. Zebrafish Rho kinase 2 acts downstream of Wnt11 to mediate cell polarity and effective convergence and extension movements. Curr. Biol. 2002, 12:876-884.
83. Masiakowski P., Carroll R.D. A novel family of cell surface receptors with tyrosine kinase-like domain. J. Biol. Chem. 1992, 267:26181-26190.
84. Matakatsu H., Blair S.S. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 2004, 131:3785-3794.
85. 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. Curr. Biol. 2009, 19:924-929.
86. Montcouquiol M., Sans N., Huss D., Kach J., Dickman J.D., Forge A., Rachel R.A., Copeland N.G., Jenkins N.A., Bogani D., et al. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. J. Neurosci. 2006, 26:5265-5275.
87. Murcia N.S., Richards W.G., Yoder B.K., Mucenski M.L., Dunlap J.R., Woychik R.P. The Oak Ridge Polycystic Kidney (orpk) disease gene is required for left-right axis determination. Development 2000, 127:2347-2355.
88. Myers D.C., Sepich D.S., Solnica-Krezel L. Bmp activity gradient regulates convergent extension during zebrafish gastrulation. Dev. Biol. 2002, 243:81-98.
89. Nachury M.V., Loktev A.V., Zhang Q., Westlake C.J., Peränen J., Merdes A., Slusarski D.C., Scheller R.H., Bazan J.F., Sheffield V.C., Jackson P.K. A core complex of BBS proteins cooperates with the GTPase Rab8 to promote ciliary membrane biogenesis. Cell 2007, 129:1201-1213.
90. Nachury M.V., Seeley E.S., Jin H. Trafficking to the ciliary membrane: how to get across the periciliary diffusion barrier?. Annu. Rev. Cell Dev. Biol. 2010, 26:59-87.
91. Nakayama M., Nakajima D., Nagase T., Nomura N., Seki N., Ohara O. Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics 1998, 51:27-34.
92. Nejsum L.N., Nelson W.J. Epithelial cell surface polarity: the early steps. Front. Biosci. 2009, 14:1088-1098.
93. Ninomiya H., Elinson R.P., Winklbauer R. Antero-posterior tissue polarity links mesoderm convergent extension to axial patterning. Nature 2004, 430:364-367.
94. Nonaka S., Yoshiba S., Watanabe D., Ikeuchi S., Goto T., Marshall W.F., Hamada H. De novo formation of left-right asymmetry by posterior tilt of nodal cilia. PLoS Biol. 2005, 3:e268.
95. Nübler-Jung K., Bonitz R., Sonnenschein M. Cell polarity during wound healing in an insect epidermis. Development 1987, 100:163-170.
96. Ohkawara B., Yamamoto T.S., Tada M., Ueno N. Role of glypican 4 in the regulation of convergent extension movements during gastrulation in Xenopus laevis. Development 2003, 130:2129-2138.
97. Olguín P., Glavic A., Mlodzik M. Intertissue mechanical stress affects Frizzled-mediated planar cell polarity in the Drosophila notum epidermis. Curr. Biol. 2011, 21:236-242.
98. Park W.J., Liu J., Sharp E.J., Adler P.N. The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 1996, 122:961-969.
99. 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. Nat. Genet. 2006, 38:303-311.
100. 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. Nat. Genet. 2008, 40:871-879.
101. Paudyal A., Damrau C., Patterson V.L., Ermakov A., Formstone C., Lalanne Z., Wells S., Lu X., Norris D.P., Dean C.H., et al. 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. 2010, 10:87.
102. Probst B., Rock R., Gessler M., Vortkamp A., Püschel A.W. The rodent Four-jointed ortholog Fjx1 regulates dendrite extension. Dev. Biol. 2007, 312:461-470.
103. Qian D., Jones C., Rzadzinska A., Mark S., Zhang X., Steel K.P., Dai X., Chen P. Wnt5a functions in planar cell polarity regulation in mice. Dev. Biol. 2007, 306:121-133.
104. Quesada-Hernández E., Caneparo L., Schneider S., Winkler S., Liebling M., Fraser S.E., Heisenberg C.P. Stereotypical cell division orientation controls neural rod midline formation in zebrafish. Curr. Biol. 2010, 20:1966-1972.
105. Rauch G.J., Hammerschmidt M., Blader P., Schauerte H.E., Strähle U., Ingham P.W., McMahon A.P., Haffter P. Wnt5 is required for tail formation in the zebrafish embryo. Cold Spring Harb. Symp. Quant. Biol. 1997, 62:227-234.
106. Ren Q., Zhou J., Zhao X.F., Wang J.X. Molecular cloning and characterization of a receptor for activated protein kinase C1 (RACK1) from Chinese white shrimp; Fenneropenaeus chinensis. Dev. Comp. Immunol. 2011, 35:629-634.
107. Rock R., Schrauth S., Gessler M. Expression of mouse dchs1, fjx1, and fat-j suggests conservation of the planar cell polarity pathway identified in Drosophila. Dev. Dyn. 2005, 234:747-755.
108. Ross A.J., May-Simera H., Eichers E.R., Kai M., Hill J., Jagger D.J., Leitch C.C., Chapple J.P., Munro P.M., Fisher S., et al. Disruption of Bardet-Biedl syndrome ciliary proteins perturbs planar cell polarity in vertebrates. Nat. Genet. 2005, 37:1135-1140.
109. Saburi S., Hester I., Fischer E., Pontoglio M., Eremina V., Gessler M., Quaggin S.E., Harrison R., Mount R., McNeill H. Loss of Fat4 disrupts PCP signaling and oriented cell division and leads to cystic kidney disease. Nat. Genet. 2008, 40:1010-1015.
110. Sepich D.S., Usmani M., Pawlicki S., Solnica-Krezel L. Wnt/PCP signaling controls intracellular position of MTOCs during gastrulation convergence and extension movements. Development 2011, 138:543-552.
111. Shih J., Keller R. Cell motility driving mediolateral intercalation in explants of Xenopus laevis. Development 1992, 116:901-914.
112. Shimada Y., Yonemura S., Ohkura H., Strutt D., Uemura T. Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev. Cell 2006, 10:209-222.
113. Simon M.A., Xu A., Ishikawa H.O., Irvine K.D. Modulation of fat:dachsous binding by the cadherin domain kinase four-jointed. Curr. Biol. 2010, 20:811-817.
114. Simons M., Gloy J., Ganner A., Bullerkotte A., Bashkurov M., Krönig C., Schermer B., Benzing T., Cabello O.A., Jenny A., et al. Inversin, the gene product mutated in nephronophthisis type II, functions as a molecular switch between Wnt signaling pathways. Nat. Genet. 2005, 37:537-543.
115. Song H., Hu J., Chen W., Elliott G., Andre P., Gao B., Yang Y. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 2010, 466:378-382.
116. Strutt D.I. Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 2001, 7:367-375.
117. Strutt D. Frizzled signalling and cell polarisation in Drosophila and vertebrates. Development 2003, 130:4501-4513.
118. Strutt H., Strutt D. Differential stability of flamingo protein complexes underlies the establishment of planar polarity. Curr. Biol. 2008, 18:1555-1564.
119. Tada M., Smith J.C. Xwnt11 is a target of Xenopus Brachyury: regulation of gastrulation movements via Dishevelled, but not through the canonical Wnt pathway. Development 2000, 127:2227-2238.
120. Tanoue T., Takeichi M. New insights into Fat cadherins. J. Cell Sci. 2005, 118:2347-2353.
121. Tao H., Manak J.R., Sowers L., Mei X., Kiyonari H., Abe T., Dahdaleh N.S., Yang T., Wu S., Chen S., et al. Mutations in prickle orthologs cause seizures in flies, mice, and humans. Am. J. Hum. Genet. 2011, 88:138-149.
122. Tawk M., Araya C., Lyons D.A., Reugels A.M., Girdler G.C., Bayley P.R., Hyde D.R., Tada M., Clarke J.D. A mirror-symmetric cell division that orchestrates neuroepithelial morphogenesis. Nature 2007, 446:797-800.
123. Taylor J., Abramova N., Charlton J., Adler P.N. Van Gogh: a new Drosophila tissue polarity gene. Genetics 1998, 150:199-210.
124. Theisen H., Purcell J., Bennett M., Kansagara D., Syed A., Marsh J.L. dishevelled is required during wingless signaling to establish both cell polarity and cell identity. Development 1994, 120:347-360.
125. Thisse B., Wright C.V., Thisse C. Activin- and Nodal-related factors control antero-posterior patterning of the zebrafish embryo. Nature 2000, 403:425-428.
126. Tissir F., Qu Y., Montcouquiol M., Zhou L., Komatsu K., Shi D., Fujimori T., Labeau J., Tyteca D., Courtoy P., et al. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nat. Neurosci. 2010, 13:700-707.
127. Topczewski J., Sepich D.S., Myers D.C., Walker C., Amores A., Lele Z., Hammerschmidt M., Postlethwait J., Solnica-Krezel L. The zebrafish glypican knypek controls cell polarity during gastrulation movements of convergent extension. Dev. Cell 2001, 1:251-264.
128. Tree D.R., Shulman J.M., Rousset R., Scott M.P., Gubb D., Axelrod J.D. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 2002, 109:371-381.
129. Usui T., Shima Y., Shimada Y., Hirano S., Burgess R.W., Schwarz T.L., Takeichi M., Uemura T. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 1999, 98:585-595.
130. Villano J.L., Katz F.N. four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 1995, 121:2767-2777.
131. Vinson C.R., Adler P.N. Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 1987, 329:549-551.
132. Vinson C.R., Conover S., Adler P.N. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 1989, 338:263-264.
133. Wada H., Tanaka H., Nakayama S., Iwasaki M., Okamoto H. Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 2006, 133:4749-4759.
134. Wallingford J.B., Habas R. The developmental biology of Dishevelled: an enigmatic protein governing cell fate and cell polarity. Development 2005, 132:4421-4436.
135. Wallingford J.B., Harland R.M. Xenopus Dishevelled signaling regulates both neural and mesodermal convergent extension: parallel forces elongating the body axis. Development 2001, 128:2581-2592.
136. Wallingford J.B., Harland R.M. Neural tube closure requires Dishevelled-dependent convergent extension of the midline. Development 2002, 129:5815-5825.
137. Wallingford J.B., Mitchell B. Strange as it may seem: the many links between Wnt signaling, planar cell polarity, and cilia. Genes Dev. 2011, 25:201-213.
138. Wallingford J.B., Rowning B.A., Vogeli K.M., Rothbächer U., Fraser S.E., Harland R.M. Dishevelled controls cell polarity during Xenopus gastrulation. Nature 2000, 405:81-85.
139. Wang J., Mark S., Zhang X., Qian D., Yoo S.J., Radde-Gallwitz K., Zhang Y., Lin X., Collazo A., Wynshaw-Boris A., Chen P. Regulation of polarized extension and planar cell polarity in the cochlea by the vertebrate PCP pathway. Nat. Genet. 2005, 37:980-985.
140. Wang J., Hamblet N.S., Mark S., Dickinson M.E., Brinkman B.C., Segil N., Fraser S.E., Chen P., Wallingford J.B., Wynshaw-Boris A. Dishevelled genes mediate a conserved mammalian PCP pathway to regulate convergent extension during neurulation. Development 2006, 133:1767-1778.
141. 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. J. Neurosci. 2006, 26:2147-2156.
142. Wehner P., Shnitsar I., Urlaub H., Borchers A. RACK1 is a novel interaction partner of PTK7 that is required for neural tube closure. Development 2011, 138:1321-1327.
143. Wolff T., Rubin G.M. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 1998, 125:1149-1159.
144. Wong H.C., Mao J., Nguyen J.T., Srinivas S., Zhang W., Liu B., Li L., Wu D., Zheng J. Structural basis of the recognition of the dishevelled DEP domain in the Wnt signaling pathway. Nat. Struct. Biol. 2000, 7:1178-1184.
145. Wu J., Mlodzik M. The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Dev. Cell 2008, 15:462-469.
146. Yamamoto S., Nishimura O., Misaki K., Nishita M., Minami Y., Yonemura S., Tarui H., Sasaki H. Cthrc1 selectively activates the planar cell polarity pathway of Wnt signaling by stabilizing the Wnt-receptor complex. Dev. Cell 2008, 15:23-36.
147. 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.
148. Yen W.W., Williams M., Periasamy A., Conaway M., Burdsal C., Keller R., Lu X., Sutherland A. PTK7 is essential for polarized cell motility and convergent extension during mouse gastrulation. Development 2009, 136:2039-2048.
149. Yin C., Kiskowski M., Pouille P.A., Farge E., Solnica-Krezel L. Cooperation of polarized cell intercalations drives convergence and extension of presomitic mesoderm during zebrafish gastrulation. J. Cell Biol. 2008, 180:221-232.
150. Yu A., Xing Y., Harrison S.C., Kirchhausen T. Structural analysis of the interaction between Dishevelled2 and clathrin AP-2 adaptor, a critical step in noncanonical Wnt signaling. Structure 2010, 18:1311-1320.
151. Zaghloul N.A., Katsanis N. Mechanistic insights into Bardet-Biedl syndrome, a model ciliopathy. J. Clin. Invest. 2009, 119:428-437.
152. Zallen J.A. Planar polarity and tissue morphogenesis. Cell 2007, 129:1051-1063.
153. Zallen J.A., Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 2004, 6:343-355.
154. Zeidler M.P., Perrimon N., Strutt D.I. Multiple roles for four-jointed in planar polarity and limb patterning. Dev. Biol. 2000, 228:181-196.
155. Zeng H., Hoover A.N., Liu A. PCP effector gene Inturned is an important regulator of cilia formation and embryonic development in mammals. Dev. Biol. 2010, 339:418-428.
156. Zuo X., Guo W., Lipschutz J.H. The exocyst protein Sec10 is necessary for primary ciliogenesis and cystogenesis in vitro. Mol. Biol. Cell 2009, 20:2522-2529.