Asymmetric Protein Localization in Planar Cell Polarity: Mechanisms, Puzzles, and Challenges

Current Topics in Developmental Biology

Volumn 101, Issue , 2012, Pages 33-53

  Peng, Ying ^a   Axelrod, Jeffrey D ^b  

^a MAYO GRADUATE SCHOOL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Core module; Flamingo; Frizzled; Global directional cue; Planar cell polarity; Subcellular asymmetry; Van Gogh

Indexed keywords

CADHERIN; DROSOPHILA PROTEIN; MEMBRANE PROTEIN; STAN PROTEIN, DROSOPHILA; VANG PROTEIN, DROSOPHILA;

ANIMAL; CELL COMMUNICATION; CELL POLARITY; CYTOLOGY; DROSOPHILA; EPITHELIUM; EPITHELIUM CELL; FORELIMB; GENE; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN TRANSPORT; REVIEW;

ANIMALS; CADHERINS; CELL COMMUNICATION; CELL POLARITY; DROSOPHILA; DROSOPHILA PROTEINS; EPITHELIAL CELLS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, INSECT; MEMBRANE PROTEINS; PROTEIN INTERACTION MAPPING; PROTEIN STABILITY; PROTEIN TRANSPORT; WING;

EID: 84876344445     PISSN: 00702153     EISSN: None     Source Type: Book Series    
DOI: 10.1016/B978-0-12-394592-1.00002-8     Document Type: Chapter

References (70)

1. Adler, P.N., Taylor, J., Charlton, J., The domineering non-autonomy of frizzled and van Gogh clones in the Drosophila wing is a consequence of a disruption in local signaling. Mechanisms of Development 96 (2000), 197–207.
2. Adler, P.N., Zhu, C., Stone, D., Inturned localizes to the proximal side of wing cells under the instruction of upstream planar polarity proteins. Current Biology 14 (2004), 2046–2051.
3. 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 307 (2005), 423–426.
4. 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, 5, 2010, e8999.
5. Axelrod, J.D., Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes & Development 15 (2001), 1182–1187.
6. Axelrod, J.D., Progress and challenges in understanding planar cell polarity signaling. Seminars in Cell & Developmental Biology 20 (2009), 964–971.
7. Bastock, R., Strutt, H., Strutt, D., Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130 (2003), 3007–3014.
8. Bellaiche, Y., Beaudoin-Massiani, O., Stuttem, I., Schweisguth, F., The planar cell polarity protein Strabismus promotes Pins anterior localization during asymmetric division of sensory organ precursor cells in Drosophila. Development 131 (2004), 469–478.
9. Bellaiche, Y., Gho, M., Kaltschmidt, J.A., Brand, A.H., Schweisguth, F., Frizzled regulates localization of cell-fate determinants and mitotic spindle rotation during asymmetric cell division. Nature Cell Biology 3 (2001), 50–57.
10. 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. Current Biology 20 (2010), 803–810.
11. Brittle, A., Thomas, C., Strutt, D., Planar polarity specification through asymmetric subcellular localization of Fat and Dachsous. Current Biology 22 (2012), 907–914.
12. Burak, Y., Shraiman, B.I., Order and stochastic dynamics in Drosophila planar cell polarity. PLoS Computational Biology, 5, 2009, e1000628.
13. 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 133 (2006), 4561–4572.
14. Casal, J., Struhl, G., Lawrence, P.A., Developmental compartments and planar polarity in Drosophila. Current Biology 12 (2002), 1189–1198.
15. Chen, W.S., Antic, D., Matis, M., Logan, C.Y., Povelones, M., Anderson, G.A., et al. Asymmetric homotypic interactions of the atypical cadherin flamingo mediate intercellular polarity signaling. Cell 133 (2008), 1093–1105.
16. Das, G., Jenny, A., Klein, T.J., Eaton, S., Mlodzik, M., Diego interacts with Prickle and Strabismus/Van Gogh to localize planar cell polarity complexes. Development 131 (2004), 4467–4476.
17. Das, G., Reynolds-Kenneally, J., Mlodzik, M., The atypical cadherin Flamingo links Frizzled and Notch signaling in planar polarity establishment in the Drosophila eye. Developmental Cell 2 (2002), 655–666.
18. Davies, A., Formstone, C., Mason, I., Lewis, J., Planar polarity of hair cells in the chick inner ear is correlated with polarized distribution of c-flamingo-1 protein. Developmental Dynamics 233 (2005), 998–1005.
19. 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. The Journal of Neuroscience 27 (2007), 3139–3147.
20. Devenport, D., Fuchs, E., Planar polarization in embryonic epidermis orchestrates global asymmetric morphogenesis of hair follicles. Nature Cell Biology 10 (2008), 1257–1268.
21. Donoughe, S., DiNardo, S., Dachsous and frizzled contribute separately to planar polarity in the Drosophila ventral epidermis. Development 138 (2011), 2751–2759.
22. Eaton, S., Wepf, R., Simons, K., Roles for Rac1 and Cdc42 in planar polarization and hair outgrowth in the wing of Drosophila. The Journal of Cell Biology 135 (1996), 1277–1289.
23. Goodrich, L.V., Strutt, D., Principles of planar polarity in animal development. Development 138 (2011), 1877–1892.
24. Guirao, B., Meunier, A., Mortaud, S., Aguilar, A., Corsi, J.M., Strehl, L., et al. Coupling between hydrodynamic forces and planar cell polarity orients mammalian motile cilia. Nature Cell Biology 12 (2010), 341–350.
25. Harumoto, T., Ito, M., Shimada, Y., Kobayashi, T.J., Ueda, H.R., Lu, B., et al. Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Developmental Cell 19 (2010), 389–401.
26. Hashimoto, M., Shinohara, K., Wang, J., Ikeuchi, S., Yoshiba, S., Meno, C., et al. Planar polarization of node cells determines the rotational axis of node cilia. Nature Cell Biology 12 (2010), 170–176.
27. 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. Nature Cell Biology 7 (2005), 691–697.
28. Keller, R., Shaping the vertebrate body plan by polarized embryonic cell movements. Science 298 (2002), 1950–1954.
29. Kelly, M., Chen, P., Shaping the mammalian auditory sensory organ by the planar cell polarity pathway. The International Journal of Developmental Biology 51 (2007), 535–547.
30. Lawrence, P.A., The structure and properties of a compartment border: The intersegmental boundary in Oncopeltus. Ciba Foundation Symposium 29 (1975), 3–23.
31. Lawrence, P.A., Casal, J., Struhl, G., Towards a model of the organisation of planar polarity and pattern in the Drosophila abdomen. Development 129 (2002), 2749–2760.
32. Lawrence, P.A., Casal, J., Struhl, G., Cell interactions and planar polarity in the abdominal epidermis of Drosophila. Development 131 (2004), 4651–4664.
33. Le Garrec, J.F., Lopez, P., Kerszberg, M., Establishment and maintenance of planar epithelial cell polarity by asymmetric cadherin bridges: A computer model. Developmental Dynamics 235 (2006), 235–246.
34. Lee, H., Adler, P.N., The function of the frizzled pathway in the Drosophila wing is dependent on inturned and fuzzy. Genetics 160 (2002), 1535–1547.
35. Ma, D., Yang, C.H., McNeill, H., Simon, M.A., Axelrod, J.D., Fidelity in planar cell polarity signalling. Nature 421 (2003), 543–547.
36. Matakatsu, H., Blair, S.S., Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 133 (2006), 2315–2324.
37. 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. Current Biology 19 (2009), 924–929.
38. Montcouquiol, M., Sans, N., Huss, D., Kach, J., Dickman, J.D., Forge, A., et al. Asymmetric localization of Vangl2 and Fz3 indicate novel mechanisms for planar cell polarity in mammals. The Journal of Neuroscience 26 (2006), 5265–5275.
39. 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. Nature Genetics 40 (2008), 871–879.
40. Rawls, A.S., Wolff, T., Strabismus requires Flamingo and Prickle function to regulate tissue polarity in the Drosophila eye. Development 130 (2003), 1877–1887.
41. Repiso, A., Saavedra, P., Casal, J., Lawrence, P.A., Planar cell polarity: The orientation of larval denticles in Drosophila appears to depend on gradients of Dachsous and Fat. Development 137 (2010), 3411–3415.
42. Sagner, A., Merkel, M., Aigouy, B., Gaebel, J., Brankatschk, M., Julicher, F., et al. Establishment of Global Patterns of Planar Polarity during Growth of the Drosophila Wing Epithelium. Current Biology 22 (2012), 1296–1301.
43. Schamberg, S., Houston, P., Monk, N.A., Owen, M.R., Modelling and analysis of planar cell polarity. Bulletin of Mathematical Biology 72 (2010), 645–680.
44. Shimada, Y., Usui, T., Yanagawa, S., Takeichi, M., Uemura, T., Asymmetric colocalization of Flamingo, a seven-pass transmembrane cadherin, and Dishevelled in planar cell polarization. Current Biology 11 (2001), 859–863.
45. Shimada, Y., Yonemura, S., Ohkura, H., Strutt, D., Uemura, T., Polarized transport of Frizzled along the planar microtubule arrays in Drosophila wing epithelium. Developmental Cell 10 (2006), 209–222.
46. Sienknecht, U.J., Anderson, B.K., Parodi, R.M., Fantetti, K.N., Fekete, D.M., Non-cell-autonomous planar cell polarity propagation in the auditory sensory epithelium of vertebrates. Developmental Biology 352 (2011), 27–39.
47. Simon, M.A., Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131 (2004), 6175–6184.
48. Simon, M.A., Xu, A., Ishikawa, H.O., Irvine, K.D., Modulation of fat: Dachsous binding by the cadherin domain kinase four-jointed. Current Biology 20 (2010), 811–817.
49. Song, H., Hu, J., Chen, W., Elliott, G., Andre, P., Gao, B., et al. Planar cell polarity breaks bilateral symmetry by controlling ciliary positioning. Nature 466 (2010), 378–382.
50. Strutt, D.I., Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Molecular Cell 7 (2001), 367–375.
51. Strutt, D., Gradients and the specification of planar polarity in the insect cuticle. Cold Spring Harbor Perspectives in Biology, 1, 2009, a000489.
52. Strutt, D., Johnson, R., Cooper, K., Bray, S., Asymmetric localization of frizzled and the determination of notch-dependent cell fate in the Drosophila eye. Current Biology 12 (2002), 813–824.
53. Strutt, D., Strutt, H., Differential activities of the core planar polarity proteins during Drosophila wing patterning. Developmental Biology 302 (2007), 181–194.
54. Strutt, H., Strutt, D., Differential stability of flamingo protein complexes underlies the establishment of planar polarity. Current Biology 18 (2008), 1555–1564.
55. Strutt, H., Strutt, D., Asymmetric localisation of planar polarity proteins: Mechanisms and consequences. Seminars in Cell & Developmental Biology 20 (2009), 957–963.
56. Strutt, H., Warrington, S.J., Strutt, D., Dynamics of core planar polarity protein turnover and stable assembly into discrete membrane subdomains. Developmental Cell 20 (2011), 511–525.
57. Taylor, J., Abramova, N., Charlton, J., Adler, P.N., Van Gogh: A new Drosophila tissue polarity gene. Genetics 150 (1998), 199–210.
58. Tissir, F., Qu, Y., Montcouquiol, M., Zhou, L., Komatsu, K., Shi, D., et al. Lack of cadherins Celsr2 and Celsr3 impairs ependymal ciliogenesis, leading to fatal hydrocephalus. Nature Neuroscience 13 (2010), 700–707.
59. Tree, D.R., Ma, D., Axelrod, J.D., A three-tiered mechanism for regulation of planar cell polarity. Seminars in Cell & Developmental Biology 13 (2002), 217–224.
60. 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 109 (2002), 371–381.
61. Usui, T., Shima, Y., Shimada, Y., Hirano, S., Burgess, R.W., Schwarz, T.L., et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98 (1999), 585–595.
62. Vinson, C.R., Adler, P.N., Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329 (1987), 549–551.
63. Vladar, E.K., Antic, D., Axelrod, J.D., Planar cell polarity signaling: The developing cell's compass. Cold Spring Harbor Perspectives in Biology, 1, 2009, a002964.
64. Wada, H., Okamoto, H., Roles of noncanonical Wnt/PCP pathway genes in neuronal migration and neurulation in zebrafish. Zebrafish 6 (2009), 3–8.
65. 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. The Journal of Neuroscience 26 (2006), 2147–2156.
66. Wansleeben, C., Meijlink, F., The planar cell polarity pathway in vertebrate development. Developmental Dynamics 240 (2011), 616–626.
67. Webb, S.D., Owen, M.R., Intra-membrane ligand diffusion and cell shape modulate juxtacrine patterning. Journal of Theoretical Biology 230 (2004), 99–117.
68. Wu, J., Mlodzik, M., The frizzled extracellular domain is a ligand for Van Gogh/Stbm during nonautonomous planar cell polarity signaling. Developmental Cell 15 (2008), 462–469.
69. 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 108 (2002), 675–688.
70. Zhu, H., Is anisotropic propagation of polarized molecular distribution the common mechanism of swirling patterns of planar cell polarization?. Journal of Theoretical Biology 256 (2009), 315–325.