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Seven-Pass Transmembrane Cadherin CELSRs, and Fat4 and Dchs1 Cadherins: From Planar Cell Polarity to Three-Dimensional Organ Architecture

  • Dongbo Shi
  • Masaki Arata
  • Tadao Usui
  • Toshihiko Fujimori
  • Tadashi UemuraEmail author
Chapter

Abstract

In this chapter, two subfamilies of atypical cadherins are described: the subfamily of seven-pass transmembrane cadherins (7-TM cadherins) and Fat and Dachsous cadherins. Pioneering genetic studies in Drosophila have defined both subfamilies and dissected their roles in animal development. It is now clear that the founding members in Drosophila and their respective vertebrate homologues make critical and essential contributions to a variety of dynamic behaviors of cell populations, and that malfunctions of those atypical cadherins cause anomalies in embryonic development, resulting in postnatal organ malformation or embryonic demise. Here we discuss how the atypical cadherins control cell behaviors with the emphasis on one particular orchestration of cells along the axes of tissues, organs, or bodies, inclusively designated as planar cell polarity (PCP). Nowadays the purview of PCP ranges from the unidirectional orientation of subcellular structures, such as wing hairs of Drosophila and vertebrate motile cilia, to three-dimensional dynamics of multicellular units, such as tilting hair follicles, neural tube closure, epithelial folding in the oviduct, and collective cell migration. The PCP field is at an extraordinarily exciting juncture, bursting with questions about functions of 7-TM cadherins and Fat and Dachsous cadherins at the cellular and molecular level.

Keywords

Seven-pass transmembrane cadherins (7-TM cadherins) CELSR Fat and Dachsous cadherins Planar cell polarity (PCP) Cilia Three-dimensional organogenesis Hair follicle Neural tube closure Epithelial folding Oviduct Collective cell migration 

Notes

Acknowledgments

This work was supported by a CREST grant and MEXT grands (Kakenhi) to T.U. and T.F,, and by a grant of The Mitsubishi Foundation and Takeda Science Foundation to T.U and a grant from NIBB to T.F. D.S. and M. A. were Research Fellows of the JSPS. Figure 10.4e is reprinted from “Flamingo, a Seven-Pass Transmembrane Cadherin, Regulates Planar Cell Polarity under the Control of Frizzled” by Usui et al., Cell, Volume 98, 585–595, 1999, with permission from Elsevier. We thank J. A. Hejna very much for his constructive suggestions and polishing the manuscript.

References

  1. Abley K, De Reuille PB, Strutt D et al (2013) An intracellular partitioning-based framework for tissue cell polarity in plants and animals. Development 140:2061–2074. doi: 10.1242/dev.062984 PubMedCrossRefGoogle Scholar
  2. Adler PN (2012) The frizzled/stan pathway and planar cell polarity in the Drosophila wing. Curr Top Dev Biol 101:1–31. doi: 10.1016/B978-0-12-394592-1.00001-6 PubMedPubMedCentralCrossRefGoogle Scholar
  3. Agduhr E (1927) Studies on the structure and development of the bursa ovarica and the tuba uterina in the mouse. Acta Zool 8:1–133. doi: 10.1111/j.1463-6395.1927.tb00649.x CrossRefGoogle Scholar
  4. Aigouy B, Farhadifar R, Staple DB et al (2010) Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142:773–786. doi: 10.1016/j.cell.2010.07.042 PubMedCrossRefGoogle Scholar
  5. 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. doi: 10.1002/bdra.23002 PubMedCrossRefGoogle Scholar
  6. Assheton R (1896) Notes on the ciliation of the ectoderm of the amphibian embryo.Google Scholar
  7. Ayukawa T, Akiyama M, Mummery-Widmer JL et al (2014) Dachsous-dependent asymmetric localization of spiny-legs determines planar cell polarity orientation in Drosophila. Cell Rep 8:610–621. doi: 10.1016/j.celrep.2014.06.009 PubMedCrossRefGoogle Scholar
  8. Badouel C, Zander M, Liscio N et al (2015) Fat1 interacts with Fat4 to regulate neural tube closure, neural progenitor proliferation and apical constriction during mouse brain development. Development 142:2781–2791. doi: 10.1242/dev.123539 PubMedPubMedCentralCrossRefGoogle Scholar
  9. Bagherie-Lachidan M, Reginensi A, Zaveri HP et al (2015) Stromal Fat4 acts non-autonomously with Dachsous1/2 to restrict the nephron progenitor pool. Development 142:2564–2573. doi: 10.1242/dev.122648 PubMedCrossRefGoogle Scholar
  10. Bastock R, Strutt H, Strutt D (2003) Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130:3007–3014PubMedCrossRefGoogle Scholar
  11. Bischoff M (2012) Lamellipodia-based migrations of larval epithelial cells are required for normal closure of the adult epidermis of Drosophila. Dev Biol 363:179–190. doi: 10.1016/j.ydbio.2011.12.033 PubMedCrossRefGoogle Scholar
  12. Boisvieuxulrich E, Laine MC, Sandoz D (1985) The orientation of ciliary basal bodies in quail oviduct is related to the ciliary beating cycle commencement. Biol Cell 55:147–150CrossRefGoogle Scholar
  13. Bosveld F, Bonnet I, Guirao B et al (2012) Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 336:724–727. doi: 10.1126/science.1221071 PubMedCrossRefGoogle Scholar
  14. Boutin C, Labedan P, Dimidschstein J et al (2014) A dual role for planar cell polarity genes in ciliated cells. Proc Natl Acad Sci U S A 111:E3129–E3138. doi: 10.1073/pnas.1404988111 PubMedPubMedCentralCrossRefGoogle Scholar
  15. Brittle AL, Repiso A, Casal J et al (2010) Four-jointed modulates growth and planar polarity by reducing the affinity of dachsous for fat. Curr Biol 20:803–810. doi: 10.1016/j.cub.2010.03.056 PubMedPubMedCentralCrossRefGoogle Scholar
  16. Brooks ER, Wallingford JB (2014) Multiciliated cells. Curr Biol 24:R973–R982. doi: 10.1016/j.cub.2014.08.047 PubMedPubMedCentralCrossRefGoogle Scholar
  17. Butler MT, Wallingford JB (2015) Control of vertebrate core PCP protein localization and dynamics by Prickle2. Development. doi: 10.1242/dev.121384 Google Scholar
  18. Carvajal-Gonzalez JM, Mlodzik M (2014) Mechanisms of planar cell polarity establishment in Drosophila. F1000Prime Rep 6:98. doi: 10.12703/P6-98Google Scholar
  19. Chae J, Kim MJ, Goo JH et al (1999) The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126:5421–5429PubMedGoogle Scholar
  20. Chen W-S, Antic D, Matis M et al (2008) Asymmetric Homotypic Interactions of the Atypical Cadherin Flamingo Mediate Intercellular Polarity Signaling. Cell 133:1093–1105. doi: 10.1016/j.cell.2008.04.048 PubMedPubMedCentralCrossRefGoogle Scholar
  21. Cho E, Irvine KD (2004) Action of fat, four-jointed, dachsous and dachs in distal-to-proximal wing signaling. Development 131:4489–4500. doi: 10.1242/dev.01315 PubMedCrossRefGoogle Scholar
  22. Clark HF, Brentrup D, Schneitz K et al (1995) Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev 9:1530–1542. doi: 10.1101/gad.9.12.1530 PubMedCrossRefGoogle Scholar
  23. Classen AK, Anderson KI, Marois E, Eaton S (2005) Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev Cell 9:805–817. doi: 10.1016/j.devcel.2005.10.016 PubMedCrossRefGoogle Scholar
  24. Cortijo C, Gouzi M, Tissir F, Grapin-Botton A (2012) Planar cell polarity controls pancreatic beta cell differentiation and glucose homeostasis. Cell Rep 2:1593–1606. doi: 10.1016/j.celrep.2012.10.016 PubMedPubMedCentralCrossRefGoogle Scholar
  25. 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. doi: 10.1016/s0960-9822(03)00374-9 PubMedCrossRefGoogle Scholar
  26. Davies A, Formstone C, Mason I, Lewis J (2005) Planar polarity of hair cells in the chick inner ear is correlated with polarized distribution of c-flamingo-1 protein. Dev Dyn 233:998–1005. doi: 10.1002/dvdy.20376 PubMedCrossRefGoogle Scholar
  27. Del Bigio MR (1995) The ependyma: a protective barrier between brain and cerebrospinal fluid. Glia 14:1–13. doi: 10.1002/glia.440140102 PubMedCrossRefGoogle Scholar
  28. Devenport D (2014) Cell biology in development: The cell biology of planar cell polarity. J Cell Biol 207:171–179. doi: 10.1083/jcb.201408039 PubMedPubMedCentralCrossRefGoogle Scholar
  29. Devenport D, Fuchs E (2008) Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nat Cell Biol 10:1257–1268. doi: 10.1038/ncb1784 PubMedPubMedCentralCrossRefGoogle Scholar
  30. 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. doi: 10.1038/ncb2284 PubMedPubMedCentralCrossRefGoogle Scholar
  31. Doudney K, Stanier P (2005) Epithelial cell polarity genes are required for neural tube closure. Am J Med Genet C: Semin Med Genet 135C:42–47. doi: 10.1002/ajmg.c.30052 CrossRefGoogle Scholar
  32. Durst R, Sauls K, Peal DS et al (2015) Mutations in DCHS1 cause mitral valve prolapse. Nature. doi: 10.1038/nature14670 PubMedPubMedCentralGoogle Scholar
  33. Feng Y, Irvine KD (2009) Processing and phosphorylation of the Fat receptor. Proc Natl Acad Sci U S A 106:11989–11994. doi: 10.1073/pnas.0811540106 PubMedPubMedCentralCrossRefGoogle Scholar
  34. Fuchs E (2007) Scratching the surface of skin development. Nature 445:834–842. doi: 10.1038/nature05659 PubMedPubMedCentralCrossRefGoogle Scholar
  35. Gaengel K, Mlodzik M (2003) Egfr signaling regulates ommatidial rotation and cell motility in the Drosophila eye via MAPK/Pnt signaling and the Ras effector Canoe/AF6. Development 130:5413–5423. doi: 10.1242/dev.00759 PubMedCrossRefGoogle Scholar
  36. Gong Y, Mo C, Fraser SE (2004) Planar cell polarity signalling controls cell division orientation during zebrafish gastrulation. Nature 430:689–693. doi: 10.1038/nature02796 PubMedCrossRefGoogle Scholar
  37. Goodrich LV, Strutt D (2011) Principles of planar polarity in animal development. Development 138:1877–1892. doi: 10.1242/dev.054080 PubMedPubMedCentralCrossRefGoogle Scholar
  38. Gray RS, Roszko I, Solnica-Krezel L (2011) Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev Cell 21:120–133. doi: 10.1016/j.devcel.2011.06.011 PubMedPubMedCentralCrossRefGoogle Scholar
  39. Guirao B, Meunier A, Mortaud S et al (2010) Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nat Cell Biol 12:341–350. doi: 10.1038/ncb2040 PubMedCrossRefGoogle Scholar
  40. Hadjantonakis AK, Sheward WJ, Harmar AJ et al (1997) Celsr1, a neural-specific gene encoding an unusual seven-pass transmembrane receptor, maps to mouse chromosome 15 and human chromosome 22qter. Genomics 45:97–104. doi: 10.1006/geno.1997.4892 PubMedCrossRefGoogle Scholar
  41. Hakeda-Suzuki S, Berger-Müller S, Tomasi T et al (2011) Golden Goal collaborates with Flamingo in conferring synaptic-layer specificity in the visual system. Nat Neurosci 14:314–323. doi: 10.1038/nn.2756 PubMedCrossRefGoogle Scholar
  42. Hale R, Brittle AL, Fisher KH et al (2015) Cellular interpretation of the long-range gradient of Four-jointed activity in the Drosophila wing. Elife. doi: 10.7554/eLife.05789 Google Scholar
  43. Harumoto T, Ito M, Shimada Y et al (2010) Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev Cell 19:389–401. doi: 10.1016/j.devcel.2010.08.004 PubMedPubMedCentralCrossRefGoogle Scholar
  44. Heisenberg CP, Bellaïche Y (2013) Forces in Tissue Morphogenesis and Patterning. Cell 153:948–962. doi: 10.1016/j.cell.2013.05.008 PubMedCrossRefGoogle Scholar
  45. Hirano S, Takeichi M (2012) Cadherins in brain morphogenesis and wiring. Physiol Rev 92:597–634. doi: 10.1152/physrev.00014.2011 PubMedCrossRefGoogle Scholar
  46. Hirota Y, Meunier A, Huang S et al (2010) Planar polarity of multiciliated ependymal cells involves the anterior migration of basal bodies regulated by non-muscle myosin II. Development 137:3037–3046. doi: 10.1242/dev.050120 PubMedCrossRefGoogle Scholar
  47. Hoeng JC, Höng JC, Ivanov NV et al (2004) Identification of new human cadherin genes using a combination of protein motif search and gene finding methods. J Mol Biol 337:307–317. doi: 10.1016/j.jmb.2004.01.026 PubMedCrossRefGoogle Scholar
  48. Ishikawa HO, Takeuchi H, Haltiwanger RS, Irvine KD (2008) Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 321:401–404. doi: 10.1126/science.1158159 PubMedPubMedCentralCrossRefGoogle Scholar
  49. Ishiuchi T, Misaki K, Yonemura S et al (2009) Mammalian Fat and Dachsous cadherins regulate apical membrane organization in the embryonic cerebral cortex. J Cell Biol 185:959–967. doi: 10.1083/jcb.200811030 PubMedPubMedCentralCrossRefGoogle Scholar
  50. Jolly MK, Rizvi MS, Kumar A, Sinha P (2014) Mathematical modeling of sub-cellular asymmetry of fat-dachsous heterodimer for generation of planar cell polarity. PLoS One 9:e97641. doi: 10.1371/journal.pone.0097641 PubMedPubMedCentralCrossRefGoogle Scholar
  51. Juriloff DM, Harris MJ (2012) A consideration of the evidence that genetic defects in planar cell polarity contribute to the etiology of human neural tube defects. Birth Defects Res A Clin Mol Teratol 94:824–840. doi: 10.1002/bdra.23079 PubMedCrossRefGoogle Scholar
  52. Lawrence PA, Casal J (2013) The mechanisms of planar cell polarity, growth and the Hippo pathway: some known unknowns. Dev Biol 377:1–8. doi: 10.1016/j.ydbio.2013.01.030 PubMedPubMedCentralCrossRefGoogle Scholar
  53. Li-Villarreal N, Forbes MM, Loza AJ et al (2015) Dachsous1b cadherin regulates actin and microtubule cytoskeleton during early zebrafish embryogenesis. Development 142:2704–2718. doi: 10.1242/dev.119800 PubMedCrossRefGoogle Scholar
  54. Lu B, Usui T, Uemura T et al (1999) Flamingo controls the planar polarity of sensory bristles and asymmetric division of sensory organ precursors in Drosophila. Curr Biol 9:1247–1250. doi: 10.1016/S0960-9822(99)80505-3 PubMedCrossRefGoogle Scholar
  55. Lu Q, Schafer DA, Adler PN (2015) The Drosophila planar polarity gene multiple wing hairs directly regulates the actin cytoskeleton. Development 142:2478–2486. doi: 10.1242/dev.122119 PubMedCrossRefGoogle Scholar
  56. Lucas AM, Douglas LC (1934) Principles underlying ciliary activity in the respiratory tract: II. A comparison of nasal clearance in man, monkey and other mammals. Arch Otolaryngol Head Neck Surg 20:518–541. doi: 10.1001/archotol.1934.03600040074006 CrossRefGoogle Scholar
  57. Ma D, Yang C, McNeill H et al (2003) Fidelity in planar cell polarity signalling. Nature 421:543–547. doi: 10.1038/nature01366 PubMedCrossRefGoogle Scholar
  58. Mahoney PA, Weber U, Onofrechuk P et al (1991) The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67:853–868. doi: 10.1016/0092-8674(91)90359-7 PubMedCrossRefGoogle Scholar
  59. Mani M, Goyal S, Irvine KD, Shraiman BI (2013) Collective polarization model for gradient sensing via Dachsous-Fat intercellular signaling. Proc Natl Acad Sci U S A 110:20420–20425. doi: 10.1073/pnas.1307459110 PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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. doi: 10.1242/dev.057166 PubMedPubMedCentralCrossRefGoogle Scholar
  61. Mao Y, Francis-West P, Irvine KD (2015) A Fat4-Dchs1 signal between stromal and cap mesenchyme cells influences nephrogenesis and ureteric bud branching. Development 142:2574–2585. doi: 10.1242/dev.122630 PubMedPubMedCentralCrossRefGoogle Scholar
  62. Matakatsu H, Blair SS (2004) Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131:3785–3794. doi: 10.1242/dev.01254 PubMedCrossRefGoogle Scholar
  63. Matis M, Axelrod JD (2013) Regulation of PCP by the Fat signaling pathway. Genes Dev 27:2207–2220. doi: 10.1101/gad.228098.113 PubMedPubMedCentralCrossRefGoogle Scholar
  64. Matis M, Russler-Germain DA, Hu Q et al (2014) Microtubules provide directional information for core PCP function. Elife 3:e02893. doi: 10.7554/eLife.02893 PubMedPubMedCentralCrossRefGoogle Scholar
  65. Matsubara D, Horiuchi S-Y, Shimono K et al (2011) The seven-pass transmembrane cadherin Flamingo controls dendritic self-avoidance via its binding to a LIM domain protein, Espinas, in Drosophila sensory neurons. Genes Dev 25:1982–1996. doi: 10.1101/gad.16531611 PubMedPubMedCentralCrossRefGoogle Scholar
  66. May-Simera H, Kelley MW (2012) Planar cell polarity in the inner ear. Curr Top Dev Biol 101:111–140. doi: 10.1016/B978-0-12-394592-1.00006-5 PubMedCrossRefGoogle Scholar
  67. Merkel M, Sagner A, Gruber FS et al (2014) The balance of prickle/spiny-legs isoforms controls the amount of coupling between core and fat PCP systems. Curr Biol 24:2111–2123. doi: 10.1016/j.cub.2014.08.005 PubMedCrossRefGoogle Scholar
  68. Mirzadeh Z, Han Y-G, Soriano-Navarro M et al (2010) Cilia organize ependymal planar polarity. J Neurosci 30:2600–2610. doi: 10.1523/JNEUROSCI.3744-09.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  69. Nakajima D, Nakayama M, Kikuno R et al (2001) Identification of three novel non-classical cadherin genes through comprehensive analysis of large cDNAs. Mol Brain Res 94:85–95. doi: 10.1016/S0169-328X(01)00218-2 PubMedCrossRefGoogle Scholar
  70. Nakayama M, Nakajima D, Nagase T et al (1998) Identification of high-molecular-weight proteins with multiple EGF-like motifs by motif-trap screening. Genomics 51:27–34. doi: 10.1006/geno.1998.5341 PubMedCrossRefGoogle Scholar
  71. Nishimura T (2014) Making the Neural Plate to Fold into a Tube. In: Kondoh H, Kuroiwa A (eds) New Principles in Developmental Processes. Springer Japan, Tokyo, pp 123–136CrossRefGoogle Scholar
  72. Nishimura T, Honda H, Takeichi M (2012) Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 149:1084–1097. doi: 10.1016/j.cell.2012.04.021 PubMedCrossRefGoogle Scholar
  73. Olofsson J, Sharp KA, Matis M et al (2014) Prickle/spiny-legs isoforms control the polarity of the apical microtubule network in planar cell polarity. Development 141:2866–2874. doi: 10.1242/dev.105932 PubMedPubMedCentralCrossRefGoogle Scholar
  74. Qu Y, Glasco DM, Zhou L et al (2010) Atypical cadherins Celsr1-3 differentially regulate migration of facial branchiomotor neurons in mice. J Neurosci 30:9392–9401. doi: 10.1523/JNEUROSCI.0124-10.2010 PubMedPubMedCentralCrossRefGoogle Scholar
  75. Ravni A, Qu Y, Goffinet AM, Tissir F (2009) Planar cell polarity cadherin Celsr1 regulates skin hair patterning in the mouse. J Invest Dermatol 129:2507–2509. doi: 10.1038/jid.2009.84 PubMedCrossRefGoogle Scholar
  76. 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. doi: 10.1002/humu.21662 PubMedPubMedCentralCrossRefGoogle Scholar
  77. Rock R, Schrauth S, Gessler M (2005) Expression of mouse dchs1, fjx1, and fat-j suggests conservation of the planar cell polarity pathway identified in Drosophila. Dev Dyn 234:747–755. doi: 10.1002/dvdy.20515 PubMedCrossRefGoogle Scholar
  78. 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. doi: 10.1038/ng.179 PubMedCrossRefGoogle Scholar
  79. Saburi S, Hester I, Goodrich L, McNeill H (2012) Functional interactions between Fat family cadherins in tissue morphogenesis and planar polarity. Development 139:1806–1820. doi: 10.1242/dev.077461 PubMedPubMedCentralCrossRefGoogle Scholar
  80. Sadeqzadeh E, de Bock CE, Thorne RF (2014) Sleeping giants: emerging roles for the fat cadherins in health and disease. Med Res Rev 34:190–221. doi: 10.1002/med.21286 PubMedCrossRefGoogle Scholar
  81. Sagner A, Merkel M, Aigouy B et al (2012) Establishment of global patterns of planar polarity during growth of the Drosophila wing epithelium. Curr Biol 22:1296–1301. doi: 10.1016/j.cub.2012.04.066 PubMedCrossRefGoogle Scholar
  82. Sai X, Yonemura S, Ladher RK (2014) Junctionally restricted RhoA activity is necessary for apical constriction during phase 2 inner ear placode invagination. Dev Biol 394:206–216. doi: 10.1016/j.ydbio.2014.08.022 PubMedCrossRefGoogle Scholar
  83. Schwabe T, Neuert H, Clandinin TR (2013) A network of cadherin-mediated interactions polarizes growth cones to determine targeting specificity. Cell 154:351–364. doi: 10.1016/j.cell.2013.06.011 PubMedPubMedCentralCrossRefGoogle Scholar
  84. Sharma P, McNeill H (2013) Regulation of long-range planar cell polarity by Fat-Dachsous signaling. Development 140:3869–3881. doi: 10.1242/dev.094730 PubMedCrossRefGoogle Scholar
  85. Shi D, Fujimori T, Uemura T (2013) Atypical cadherin negotiates a turn. Dev Cell 26:1–2PubMedCrossRefGoogle Scholar
  86. Shi D, Komatsu K, Hirao M et al (2014) Celsr1 is required for the generation of polarity at multiple levels of the mouse oviduct. Development 141:4558–4568. doi: 10.1242/dev.115659 PubMedCrossRefGoogle Scholar
  87. Shima Y, Kawaguchi S, Kosaka K et al (2007) Opposing roles in neurite growth control by two seven-pass transmembrane cadherins. Nat Neurosci 10:963–969. doi: 10.1038/nn1933 PubMedCrossRefGoogle Scholar
  88. Shimada Y, Yonemura S, Ohkura H et al (2006) Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Dev Cell 10:209–222. doi: 10.1016/j.devcel.2005.11.016 PubMedCrossRefGoogle Scholar
  89. Shrestha R, Little KA, Tamayo JV et al (2015) Mitotic Control of Planar Cell Polarity by Polo-like Kinase 1. Dev Cell 33:522–534. doi: 10.1016/j.devcel.2015.03.024 PubMedCrossRefGoogle Scholar
  90. Simon MA, Xu A, Ishikawa HO, Irvine KD (2010) Modulation of fat:dachsous binding by the cadherin domain kinase four-jointed. Curr Biol 20:811–817. doi: 10.1016/j.cub.2010.04.016 PubMedPubMedCentralCrossRefGoogle Scholar
  91. Sopko R, Silva E, Clayton L et al (2009) Phosphorylation of the tumor suppressor fat is regulated by its ligand Dachsous and the kinase discs overgrown. Curr Biol 19:1112–1117. doi: 10.1016/j.cub.2009.05.049 PubMedPubMedCentralCrossRefGoogle Scholar
  92. St Johnston D, Sanson B (2011) Epithelial polarity and morphogenesis. Curr Opin Cell Biol 23:540–546. doi: 10.1016/j.ceb.2011.07.005 PubMedCrossRefGoogle Scholar
  93. Striedter GF, Srinivasan S, Monuki ES (2015) Cortical folding: when, where, how, and why? Annu Rev Neurosci 38:291–307. doi: 10.1146/annurev-neuro-071714-034128 PubMedCrossRefGoogle Scholar
  94. Strutt DI (2001) Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol Cell 7:367–375PubMedCrossRefGoogle Scholar
  95. Strutt H, Strutt D (2002) Nonautonomous planar polarity patterning in Drosophila: dishevelled-independent functions of frizzled. Dev Cell 3:851–863PubMedCrossRefGoogle Scholar
  96. Strutt H, Strutt D (2008) Differential stability of flamingo protein complexes underlies the establishment of planar polarity. Curr Biol 18:1555–1564. doi: 10.1016/j.cub.2008.08.063 PubMedPubMedCentralCrossRefGoogle Scholar
  97. Sugimura K, Ishihara S (2013) The mechanical anisotropy in a tissue promotes ordering in hexagonal cell packing. Development 140:4091–4101. doi: 10.1242/dev.094060 PubMedCrossRefGoogle Scholar
  98. Sugimura R, He XC, Venkatraman A et al (2012) Noncanonical Wnt signaling maintains hematopoietic stem cells in the niche. Cell 150:351–365. doi: 10.1016/j.cell.2012.05.041 PubMedPubMedCentralCrossRefGoogle Scholar
  99. Sulik K, Dehart DB, Iangaki T et al (1994) Morphogenesis of the murine node and notochordal plate. Dev Dyn 201:260–278. doi: 10.1002/aja.1002010309 PubMedCrossRefGoogle Scholar
  100. Tada M, Heisenberg C-P (2012) Convergent extension: using collective cell migration and cell intercalation to shape embryos. Development 139:3897–3904. doi: 10.1242/dev.073007 PubMedCrossRefGoogle Scholar
  101. Tada M, Kai M (2012) Planar cell polarity in coordinated and directed movements. Curr Top Dev Biol 101:77–110. doi: 10.1016/B978-0-12-394592-1.00004-1 PubMedCrossRefGoogle Scholar
  102. Takeichi M (2007) The cadherin superfamily in neuronal connections and interactions. Nat Rev Neurosci 8:11–20. doi: 10.1038/nrn2043 PubMedCrossRefGoogle Scholar
  103. Tanoue T, Takeichi M (2004) Mammalian Fat1 cadherin regulates actin dynamics and cell-cell contact. J Cell Biol 165:517–528. doi: 10.1083/jcb.200403006 PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tatin F, Taddei A, Weston A et al (2013) Planar cell polarity protein celsr1 regulates endothelial adherens junctions and directed cell rearrangements during valve morphogenesis. Dev Cell 26:31–44. doi: 10.1016/j.devcel.2013.05.015 PubMedPubMedCentralCrossRefGoogle Scholar
  105. Taylor J, Abramova N, Charlton J, Adler PN (1998) Van Gogh: a new Drosophila tissue polarity gene. Genetics 150:199–210PubMedPubMedCentralGoogle Scholar
  106. Thomas C, Strutt D (2012) The roles of the cadherins Fat and Dachsous in planar polarity specification in Drosophila. Dev Dyn 241:27–39. doi: 10.1002/dvdy.22736 PubMedCrossRefGoogle Scholar
  107. Tissir F, Goffinet AM (2013) Shaping the nervous system: role of the core planar cell polarity genes. Nat Rev Neurosci 14:525–535. doi: 10.1038/nrn3525 PubMedCrossRefGoogle Scholar
  108. 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. doi: 10.1038/nn.2555 PubMedCrossRefGoogle Scholar
  109. Tsukasaki Y, Miyazaki N, Matsumoto A et al (2014) Giant cadherins Fat and Dachsous self-bend to organize properly spaced intercellular junctions. Proc Natl Acad Sci U S A 111:16011–16016. doi: 10.1073/pnas.1418990111 PubMedPubMedCentralCrossRefGoogle Scholar
  110. Usui T, Shima Y, Shimada Y et al (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of frizzled. Cell 98:585–595. doi: 10.1016/S0092-8674(00)80046-X PubMedCrossRefGoogle Scholar
  111. Vichas A, Zallen JA (2011) Translating cell polarity into tissue elongation. Semin Cell Dev Biol 22:858–864. doi: 10.1016/j.semcdb.2011.09.013 PubMedPubMedCentralCrossRefGoogle Scholar
  112. Villano J, Katz F (1995) four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 121:2767–2777PubMedGoogle Scholar
  113. Vladar EK, Antic D, Axelrod JD (2009) Planar cell polarity signaling: the developing cell’s compass. Cold Spring Harb Perspect Biol 1:a002964. doi: 10.1101/cshperspect.a002964 PubMedPubMedCentralCrossRefGoogle Scholar
  114. Vladar EK, Bayly RD, Sangoram AM et al (2012) Microtubules enable the planar cell polarity of airway cilia. Curr Biol 22:2203–2212. doi: 10.1016/j.cub.2012.09.046 PubMedPubMedCentralCrossRefGoogle Scholar
  115. Vladar EK, Lee YL, Stearns T, Axelrod JD (2015) Observing planar cell polarity in multiciliated mouse airway epithelial cells. Methods Cell Biol 127:37–54. doi: 10.1016/bs.mcb.2015.01.016 PubMedPubMedCentralCrossRefGoogle Scholar
  116. Wada H, Okamoto H (2009) Roles of planar cell polarity pathway genes for neural migration and differentiation. Dev Growth Differ 51:233–240. doi: 10.1111/j.1440-169X.2009.01092.x PubMedCrossRefGoogle Scholar
  117. Wada H, Tanaka H, Nakayama S et al (2006) Frizzled3a and Celsr2 function in the neuroepithelium to regulate migration of facial motor neurons in the developing zebrafish hindbrain. Development 133:4749–4759. doi: 10.1242/dev.02665 PubMedCrossRefGoogle Scholar
  118. Wallingford JB (2012) Planar cell polarity and the developmental control of cell behavior in vertebrate embryos. Annu Rev Cell Dev Biol 28:627–653. doi: 10.1146/annurev-cellbio-092910-154208 PubMedCrossRefGoogle Scholar
  119. Wallingford JB, Niswander LA, Shaw GM, Finnell RH (2013) The continuing challenge of understanding, preventing, and treating neural tube defects. Science 339:1222002. doi: 10.1126/science.1222002 PubMedPubMedCentralCrossRefGoogle Scholar
  120. Wang X-J, Zhang D-L, Xu Z-G et al (2014a) Understanding cadherin EGF LAG seven-pass G-type receptors. J Neurochem 131:699–711. doi: 10.1111/jnc.12955 PubMedPubMedCentralCrossRefGoogle Scholar
  121. Wang Y, Yan J, Lee H et al (2014b) The proteins encoded by the Drosophila Planar Polarity Effector genes inturned, fuzzy and fritz interact physically and can re-pattern the accumulation of “upstream” Planar Cell Polarity proteins. Dev Biol 394:156–169. doi: 10.1016/j.ydbio.2014.07.013 PubMedPubMedCentralCrossRefGoogle Scholar
  122. Wolff T, Rubin GM (1998) Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125:1149–1159PubMedGoogle Scholar
  123. Wong LL, Adler PN (1993) Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J Cell Biol 123:209–221PubMedCrossRefGoogle Scholar
  124. Wu J, Roman A-C, Carvajal-Gonzalez JM, Mlodzik M (2013) Wg and Wnt4 provide long-range directional input to planar cell polarity orientation in Drosophila. Nat Cell Biol 15:1045–1055. doi: 10.1038/ncb2806 PubMedPubMedCentralCrossRefGoogle Scholar
  125. Yamaguchi Y, Miura M (2013) How to form and close the brain: insight into the mechanism of cranial neural tube closure in mammals. Cell Mol Life Sci 70:3171–3186. doi: 10.1007/s00018-012-1227-7 PubMedPubMedCentralCrossRefGoogle Scholar
  126. Yang Y (ed) (2012) Planar cell polarity during development, 1st edn. Academic, USAGoogle Scholar
  127. Yang C, Axelrod JD, Simon MA (2002) Regulation of Frizzled by Fat-like Cadherins during Planar Polarity Signaling in the Drosophila Compound Eye. Cell 108:675–688. doi: 10.1016/S0092-8674(02)00658-X PubMedCrossRefGoogle Scholar
  128. Zakaria S, Mao Y, Kuta A et al (2014) Regulation of neuronal migration by Dchs1-Fat4 planar cell polarity. Curr Biol 24:1620–1627. doi: 10.1016/j.cub.2014.05.067 PubMedPubMedCentralCrossRefGoogle Scholar
  129. Zecca M, Struhl G (2010) A feed-forward circuit linking wingless, fat-dachsous signaling, and the warts-hippo pathway to Drosophila wing growth. PLoS Biol 8:e1000386. doi: 10.1371/journal.pbio.1000386 PubMedPubMedCentralCrossRefGoogle Scholar
  130. Zeidler MP, Perrimon N, Strutt DI (2000) Multiple roles for four-jointed in planar polarity and limb patterning. Dev Biol 228:181–196. doi: 10.1006/dbio.2000.9940 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Japan 2016

Authors and Affiliations

  • Dongbo Shi
    • 1
    • 2
  • Masaki Arata
    • 1
  • Tadao Usui
    • 1
  • Toshihiko Fujimori
    • 2
  • Tadashi Uemura
    • 1
    Email author
  1. 1.Laboratory of Cell Recognition and Pattern Formation, Graduate School of BiostudiesKyoto UniversityKyotoJapan
  2. 2.Division of EmbryologyNational Institute for Basic BiologyOkazakiJapan

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