Planar cell polarity: One or two pathways?

Nature Reviews Genetics

Volumn 8, Issue 7, 2007, Pages 555-563

  Lawrence, Peter A ^a,b   Struhl, Gary ^c   Casal, José ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^c College of Physicians and Surgeons ^*  (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MORPHOGEN;

CELL POLARITY; FLY; GENE; GENETICS; GENOTYPE; NONHUMAN; PRIORITY JOURNAL; REVIEW;

ANIMALS; CELL POLARITY; CILIA; CLONE CELLS; DROSOPHILA MELANOGASTER; MICE; MODELS, BIOLOGICAL; MORPHOGENESIS; SIGNAL TRANSDUCTION;

DROSOPHILA MELANOGASTER; VERTEBRATA;

EID: 34250781731     PISSN: 14710056     EISSN: 14710064     Source Type: Journal    
DOI: 10.1038/nrg2125     Document Type: Review

References (76)

1. Brenner, S. My Life in Science (BioMed Central, London, 2001).
2. Drubin, D. Cell Polarity (eds Hames, B. & Glover, D.) (Oxford Univ. Press, Oxford, 2000).
3. Gho, M. & Schweisguth, F. Frizzled signalling controls orientation of asymmetric sense organ precursor cell divisions in Drosophila. Nature 393, 178-181 (1998).
4. Lawrence, P. A. Development and determination of hairs and bristles in the milkweed bug, Oncopeltus fasciatus (Lygaeidae, Hemiptera). J. Cell Sci. 1, 475-498 (1966).
5. Wang, Y., Thekdi, N., Smallwood, P. M., Macke, J. P. & Nathans, J. Frizzled-3 is required for the development of major fiber tracts in the rostral CNS. J. Neurosci. 22, 8563-8573 (2002).
6. Morgan, T. H. Regeneration in Allolobophora foetida. Arch. Entwicklungsmech. Organism. 5, 570-586 (1897).
7. Lecuit, T., Samanta, R. & Wieschaus, E. slam encodes a developmental regulator of polarized membrane growth during cleavage of the Drosophila embryo. Dev. Cell 2, 425-436 (2002).
8. Adler, P. N. Planar signaling and morphogenesis in Drosophila. Dev. Cell 2, 525-535 (2002).
9. Nübler-Jung, K., Bonitz, R. & Sonnenschein, M. Cell polarity during wound healing in an insect epidermis. Development 100, 163-170 (1987).
10. Seifert, J. R. & Mlodzik, M. Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nature Rev. Genet. 8, 126-138 (2007).
11. Strutt, D. Frizzled signalling and cell polarisation in Drosophila and vertebrates. Development 130, 4501-4513 (2003).
12. Fanto, M. & McNeill, H. Planar polarity from flies to vertebrates. J. Cell Sci. 117, 527-533 (2004).
13. Klein, T. J. & Mlodzik, M. Planar cell polarization: an emerging model points in the right direction. Annu. Rev. Cell Dev. Biol. 23, 23 (2005).
14. Wallingford, J. B. Planar cell polarity, ciliogenesis and neural tube defects. Hum. Mol. Genet. 15, R227-R234 (2006).
15. 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. 26, 2147-2156 (2006).
16. Wang, Y. & Nathans, J. Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134, 647-658 (2007).
17. Lewis, J. & Davies, A. Planar cell polarity in the inner ear: how do hair cells acquire their oriented structure? J. Neurobiol. 53, 190-201 (2002).
18. Zecca, M., Basler, K. & Struhl, G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 121, 2265-2278 (1995).
19. Heisenberg, C. P. et al. Silberblick/Wnt11 mediates convergent extension movements during zebrafish gastrulation. Nature 405, 76-81 (2000).
20. Kilian, B. et al. The role of Ppt/Wnt5 in regulating cell shape and movement during zebrafish gastrulation. Mech. Dev. 120, 467-476 (2003).
21. Nüsslein-Volhard, C. & Wieschaus, E. Mutations affecting segment number and polarity in Drosophila. Nature 287, 795-801 (1980).
22. Lewis, E. B. A gene complex controlling segmentation in Drosophila. Nature 276, 565-570 (1978).
23. Gubb, D. & Garcia-Bellido, A. A genetic analysis of the determination of cuticular polarity during development in Drosophila melanogaster. J. Embryol. Exp. Morphol. 68, 37-57 (1982).
24. Vinson, C. R. & Adler, P. N. Directional non-cell autonomy and the transmission of polarity information by the frizzled gene of Drosophila. Nature 329, 549-551 (1987).
25. Lawrence, P. A., Casal, J. & Struhl, G. Cell interactions and planar polarity in the abdominal epidermis of Drosophila. Development 131, 4651-4664 (2004).
26. 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. 7, 940-949 (1997).
27. Karner, C., Wharton, K. A. Jr & Carroll, T. J. Planar cell polarity and vertebrate organogenesis. Semin. Cell Dev. Biol. 17, 194-203 (2006).
28. Ma, D., Yang, C. H., McNeill, H., Simon, M. A. & Axelrod, J. D. Fidelity in planar cell polarity signalling. Nature 421, 543-547 (2003).
29. Yang, C., Axelrod, J. D. & Simon, M. A. Regulation of Frizzled by Fat-like cadherins during planar polarity signaling in the Drosophila compound eye. Cell 108, 675-688 (2002).
30. Wong, L. L. & Adler, P. N. Tissue polarity genes of Drosophila regulate the subcellular location for prehair initiation in pupal wing cells. J. Cell Biol. 123, 209-221 (1993).
31. Deans, M. R. et al. Asymmetric distribution of Prickle-like 2 reveals an early underlying polarization of vestibular sensory epithelia in the inner ear. J. Neurosci. 27, 3139-3147 (2007).
32. 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, 4561-4572 (2006).
33. 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 125, 959-968 (1998).
34. Casal, J., Struhl, G. & Lawrence, P. A. Developmental compartments and planar polarity in Drosophila. Curr. Biol. 12, 1189-1198 (2002).
35. Clark, H. F. et al. Dachsous encodes a member of the cadherin superfamily that controls imaginal disc morphogenesis in Drosophila. Genes Dev. 9, 1530-1542 (1995).
36. Zeidler, M. P., Perrimon, N. & Strutt, D. I. The four-jointed gene is required in the Drosophila eye for ommatidial polarity specification. Curr. Biol. 9, 1363-1372 (1999).
37. Zeidler, M. P., Perrimon, N. & Strutt, D. I. Multiple roles for four-jointed in planar polarity and limb patterning. Dev. Biol. 228, 181-196 (2000).
38. Simon, M. A. Planar cell polarity in the Drosophila eye is directed by graded Four-jointed and Dachsous expression. Development 131, 6175-6184 (2004).
39. Mao, Y. et al. Dachs: an unconventional myosin that functions downstream of Fat to regulate growth, affinity and gene expression in Drosophila. Development 133, 2539-2551 (2006).
40. Strutt, H. & Strutt, D. Nonautonomous planar polarity patterning in Drosophila: Dishevelled-independent functions of frizzled. Dev. Cell 3, 851-863 (2002).
41. Matakatsu, H. & Blair, S. S. Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131, 3785-3794 (2004).
42. Matakatsu, H. & Blair, S. S. Separating the adhesive and signaling functions of the Fat and Dachsous protocadherins. Development 133, 2315-2324 (2006).
43. Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595. (1999).
44. Strutt, D. & Strutt, H. Differential activities of the core planar polarity proteins during Drosophila wing patterning. Dev. Biol. 302, 181-194 (2007).
45. Amonlirdviman, K. et al. Mathematical modeling of planar cell polarity to understand domineering nonautonomy. Science 307, 423-426 (2005).
46. Tree, D. R. et al. Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381 (2002).
47. Axelrod, J. D. Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 15, 1182-1187 (2001).
48. Strutt, D. I. Asymmetric localization of Frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367-375 (2001).
49. Strutt, D. I. The asymmetric subcellular localisation of components of the planar polarity pathway. Semin. Cell Dev. Biol. 13, 225-231 (2002).
50. Bastock, R., Strutt, H. & Strutt, D. Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130, 3007-3014 (2003).
51. 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. Mech. Dev. 96, 197-207 (2000).
52. 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. 234, 747-755 (2005).
53. Day, S. J. & Lawrence, P. A. Measuring dimensions: the regulation of size and shape. Development 127, 2977-2987 (2000).
54. Lawrence, P. A. Last hideout of the unknown? Nature 429, 247 (2004).
55. Cho, E. et al. Delineation of a Fat tumor suppressor pathway. Nature Genet. 38, 1142-1150 (2006).
56. Bennett, F. C. & Harvey, K. F. Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr. Biol. 16, 2101-2110 (2006).
57. Silva, E., Tsatskis, Y., Gardano, L., Tapon, N. & McNeill, H. The tumor-suppressor gene fat controls tissue growth upstream of expanded in the Hippo signaling pathway. Curr. Biol. 16, 2081-2089 (2006).
58. Willecke, M. et al. The Fat cadherin acts through the Hippo tumor-suppressor pathway to regulate tissue size. Curr. Biol. 16, 2090-2100 (2006).
59. Villano, J. L. & Katz, F. N. four-jointed is required for intermediate growth in the proximal-distal axis in Drosophila. Development 121, 2767-2777 (1995).
60. 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. 173, 428-446 (1996).
61. Strutt, H., Mundy, J., Hofstra, K. & Strutt, D. Cleavage and secretion is not required for Four-jointed function in Drosophila patterning. Development 131, 881-890 (2004).
62. Ashery-Padan, R., Alvarez-Bolado, G., Klamt, B., Gessler, M. & Gruss, P. Fjx1, the murine homologue of the Drosophila four-jointed gene, codes for a putative secreted protein expressed in restricted domains of the developing and adult brain. Mech. Dev. 80, 213-217 (1999).
63. Mahoney, P. A. et al. The fat tumor suppressor gene in Drosophila encodes a novel member of the cadherin gene superfamily. Cell 67, 853-868 (1991).
64. Rawls, A. S., Guinto, J. B. & Wolff, T. The cadherins Fat and Dachsous regulate dorsal/ventral signaling in the Drosophila eye. Curr. Biol. 12, 1021-1026 (2002).
65. Chae, J. et al. The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126, 5421-5429 (1999).
66. Curtin, J. A. et al. 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 (2003).
67. Vinson, C. R., Conover, S. & Adler, P. N. A Drosophila tissue polarity locus encodes a protein containing seven potential transmembrane domains. Nature 338, 263-264 (1989).
68. Wolff, T. & Rubin, G. M. Strabismus, a novel gene that regulates tissue polarity and cell fate decisions in Drosophila. Development 125, 1149-1159 (1998).
69. Taylor, J., Abramova, N., Charlton, J. & Adler, P. N. Van Gogh: a new Drosophila tissue polarity gene. Genetics 150, 199-210 (1998).
70. Montcouquiol, M. et al. Asymmetric localization of VANGL2 and FZ3 indicate novel mechanisms for planar cell polarity in mammals. J. Neurosci. 26, 5265-5275 (2006).
71. Gubb, D. et al. The balance between isoforms of the Prickle LIM domain protein is critical for planar polarity in Drosophila imaginal discs. Genes Dev. 13, 2315-2327 (1999).
72. Katoh, M. & Katoh, M. Identification and characterization of human PRICKLE1 and PRICKLE2 genes as well as mouse Prickle1 and Prickle2 genes homologous to Drosophila tissue polarity gene prickle. Int. J. Mol. Med. 11, 249-256 (2003).
73. Bekman, E. & Henrique, D. Embryonic expression of three mouse genes with homology to the Drosophila melanogaster prickle gene. Mech. Dev. 119, S77-S81 (2002).
74. Theisen, H. et al. dishevelled is required during Wingless signaling to establish both cell polarity and cell identity. Development 120, 347-360 (1994).
75. Klingensmith, J., Nusse, R. & Perrimon, N. The Drosophila segment polarity gene dishevelled encodes a novel protein required for response to the Wingless signal. Genes Dev. 8, 118-130 (1994).
76. Krasnow, R. E., Wong, L. L. & Adler, P. N. Dishevelled is a component of the Frizzled signaling pathway in Drosophila. Development 121, 4095-4102 (1995).