Cohesin controls planar cell polarity by regulating the level of the seven-pass transmembrane cadherin Flamingo

Genes to Cells

Volumn 17, Issue 6, 2012, Pages 509-524

  Mouri, Kousuke ^a   Horiuchi, Shin Ya ^a   Uemura, Tadashi ^a,b  

^a KYOTO UNIVERSITY   (Japan)

^b JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CELL PROTEIN; COHESIN; PROTEIN CUT; TRANSMEMBRANE CADHERIN FLAMINGO; TRANSMEMBRANE CADHERIN STARRY NIGHT; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL MEMBRANE; CELL POLARITY; CELL SIZE; CONTROLLED STUDY; DE LANGE SYNDROME; DOWN REGULATION; DROSOPHILA; FEMALE; FORELIMB; GENE; GENE EXPRESSION; GENE FUNCTION; GENE MUTATION; GENETIC SCREENING; LIMB MALFORMATION; MALE; MENTAL DEFICIENCY; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SISTER CHROMATID; SMC3 GENE; UPREGULATION;

ADENOSINE TRIPHOSPHATASES; ANIMALS; CADHERINS; CELL CYCLE PROTEINS; CELL POLARITY; CHROMOSOMAL PROTEINS, NON-HISTONE; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; HOMEODOMAIN PROTEINS; NUCLEAR PROTEINS; TRANSCRIPTION FACTORS; WING;

INVERTEBRATA; VERTEBRATA;

EID: 84861481027     PISSN: 13569597     EISSN: 13652443     Source Type: Journal    
DOI: 10.1111/j.1365-2443.2012.01604.x     Document Type: Article

References (60)

1. Adler, P.N. (2002) Planar signaling and morphogenesis in Drosophila. Dev. Cell 2, 525-535.
2. Adler, P.N., Charlton, J. & Liu, J. (1998) Mutations in the cadherin superfamily member gene dachsous cause a tissue polarity phenotype by altering frizzled signaling. Development 125, 959-968.
3. Adler, P.N., Zhu, C. & Stone, D. (2004) Inturned localizes to the proximal side of wing cells under the instruction of upstream planar polarity proteins. Curr. Biol. 14, 2046-2051.
4. Aigouy, B., Farhadifar, R., Staple, D.B., Sagner, A., Roper, J.C., Julicher, F. & Eaton, S. (2010) Cell flow reorients the axis of planar polarity in the wing epithelium of Drosophila. Cell 142, 773-786.
5. Axelrod, J.D. (2001) Unipolar membrane association of Dishevelled mediates Frizzled planar cell polarity signaling. Genes Dev. 15, 1182-1187.
6. Bastock, R. & Strutt, D. (2007) The planar polarity pathway promotes coordinated cell migration during Drosophila oogenesis. Development 134, 3055-3064.
7. Bastock, R., Strutt, H. & Strutt, D. (2003) Strabismus is asymmetrically localised and binds to Prickle and Dishevelled during Drosophila planar polarity patterning. Development 130, 3007-3014.
8. Bayly, R. & Axelrod, J.D. (2011) Pointing in the right direction: new developments in the field of planar cell polarity. Nat. Rev. Genet. 12, 385-391.
9. Blochlinger, K., Jan, L.Y. & Jan, Y.N. (1993) Postembryonic patterns of expression of cut, a locus regulating sensory organ identity in Drosophila. Development 117, 441-450.
10. Brand, A. & Perrimon, N. (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118, 401-415.
11. Chae, J., Kim, M.J., Goo, J.H., Collier, S., Gubb, D., Charlton, J., Adler, P.N. & Park, W.J. (1999) The Drosophila tissue polarity gene starry night encodes a member of the protocadherin family. Development 126, 5421-5429.
12. Chen, D., Ahlford, A., Schnorrer, F., Kalchhauser, I., Fellner, M., Viragh, E., Kiss, I., Syvanen, A.C. & Dickson, B.J. (2008) High-resolution, high-throughput SNP mapping in Drosophila melanogaster. Nat. Methods 5, 323-329.
13. Classen, A.K., Anderson, K.I., Marois, E. & Eaton, S. (2005) Hexagonal packing of Drosophila wing epithelial cells by the planar cell polarity pathway. Dev. Cell 9, 805-817.
14. 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, 4029-4037.
15. Collier, S., Lee, H., Burgess, R. & Adler, P. (2005) The WD40 repeat protein fritz links cytoskeletal planar polarity to frizzled subcellular localization in the Drosophila epidermis. Genetics 169, 2035-2045.
16. Couso, J.P., Bishop, S.A. & Martinez Arias, A. (1994) The wingless signalling pathway and the patterning of the wing margin in Drosophila. Development 120, 621-636.
17. Dorsett, D. (2007) Roles of the sister chromatid cohesion apparatus in gene expression, development, and human syndromes. Chromosoma 116, 1-13.
18. Dorsett, D., Eissenberg, J.C., Misulovin, Z., Martens, A., Redding, B. & McKim, K. (2005) Effects of sister chromatid cohesion proteins on cut gene expression during wing development in Drosophila. Development 132, 4743-4753.
19. Dorsett, D. & Krantz, I.D. (2009) On the molecular etiology of Cornelia de Lange syndrome. Ann. N. Y. Acad. Sci. 1151, 22-37.
20. Goodrich, L.V. & Strutt, D. (2011) Principles of planar polarity in animal development. Development 138, 1877-1892.
21. Gray, R.S., Roszko, I. & Solnica-Krezel, L. (2011) Planar cell polarity: coordinating morphogenetic cell behaviors with embryonic polarity. Dev. Cell 21, 120-133.
22. Haering, C.H., Lowe, J., Hochwagen, A. & Nasmyth, K. (2002) Molecular architecture of SMC proteins and the yeast cohesin complex. Mol. Cell 9, 773-788.
23. Harumoto, T., Ito, M., Shimada, Y., Kobayashi, T.J., Ueda, H.R., Lu, B. & Uemura, T. (2010) Atypical cadherins Dachsous and Fat control dynamics of noncentrosomal microtubules in planar cell polarity. Dev. Cell 19, 389-401.
24. Hashimoto, M. & Hamada, H. (2010) Translation of anterior-posterior polarity into left-right polarity in the mouse embryo. Curr. Opin. Genet. Dev. 20, 433-437.
25. Hirano, M. & Hirano, T. (2002) Hinge-mediated dimerization of SMC protein is essential for its dynamic interaction with DNA. EMBO J. 21, 5733-5744.
26. Hirokawa, N., Tanaka, Y. & Okada, Y. (2009) Left-right determination: involvement of molecular motor KIF3, cilia, and nodal flow. Cold Spring Harb. Perspect. Biol. 1, a000802.
27. Hong, C.S. & Ganetzky, B. (1996) Molecular characterization of neurally expressing genes in the para sodium channel gene cluster of drosophila. Genetics 142, 879-892.
28. Ishikawa, H.O., Takeuchi, H., Haltiwanger, R.S. & Irvine, K.D. (2008) Four-jointed is a Golgi kinase that phosphorylates a subset of cadherin domains. Science 321, 401-404.
29. Jessen, J.R., Topczewski, J., Bingham, S., Sepich, D.S., Marlow, F., Chandrasekhar, A. & Solnica-Krezel, L. (2002) Zebrafish trilobite identifies new roles for Strabismus in gastrulation and neuronal movements. Nat. Cell Biol. 4, 610-615.
30. Kawauchi, S., Calof, A.L., Santos, R., Lopez-Burks, M.E., Young, C.M., Hoang, M.P., Chua, A., Lao, T., Lechner, M.S., Daniel, J.A., Nussenzweig, A., Kitzes, L., Yokomori, K., Hallgrimsson, B. & Lander, A.D. (2009) Multiple organ system defects and transcriptional dysregulation in the Nipbl(+/-) mouse, a model of Cornelia de Lange Syndrome. PLoS Genet. 5, e1000650.
31. Lawrence, P.A. (1966) Gradients in the insect segment: the orientation of hairs in the milkweed bug oncopeltus fasciatus. J. Exp. Biol. 44, 607-620.
32. Losada, A. & Hirano, T. (2005) Dynamic molecular linkers of the genome: the first decade of SMC proteins. Genes Dev. 19, 1269-1287.
33. Lu, Q., Yan, J. & Adler, P.N. (2010) The Drosophila planar polarity proteins inturned and multiple wing hairs interact physically and function together. Genetics 185, 549-558.
34. Ma, D., Yang, C., McNeill, H., Simon, M. & Axelrod, J. (2003) Fidelity in planar cell polarity signalling. Nature 421, 543-547.
35. Matakatsu, H. & Blair, S. (2004) Interactions between Fat and Dachsous and the regulation of planar cell polarity in the Drosophila wing. Development 131, 3785-3794.
36. Matsubara, D., Horiuchi, S.Y., Shimono, K., Usui, T. & Uemura, T. (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.
37. McQuilton, P., St Pierre, SE., Tharmond, J. & FlyBase consortium (2012) FlyBase 101 - the basics of navigating FlyBase. Nucleic Acids Res. 40, D706-D714.
38. Melby, T.E., Ciampaglio, C.N., Briscoe, G. & Erickson, H.P. (1998) The symmetrical structure of structural maintenance of chromosomes (SMC) and MukB proteins: long, antiparallel coiled coils, folded at a flexible hinge. J. Cell Biol. 142, 1595-1604.
39. Misulovin, Z., Schwartz, Y.B., Li, X.Y., Kahn, T.G., Gause, M., MacArthur, S., Fay, J.C., Eisen, M.B., Pirrotta, V., Biggin, M.D. & Dorsett, D. (2008) Association of cohesin and Nipped-B with transcriptionally active regions of the Drosophila melanogaster genome. Chromosoma 117, 89-102.
40. Muto, A., Calof, A.L., Lander, A.D. & Schilling, T.F. (2011) Multifactorial origins of heart and gut defects in nipbl-deficient zebrafish, a model of Cornelia de Lange Syndrome. PLoS Biol. 9, e1001181.
41. Nagaso, H., Murata, T., Day, N. & Yokoyama, K.K. (2001) Simultaneous detection of RNA and protein by in situ hybridization and immunological staining. J. Histochem. Cytochem. 49, 1177-1182.
42. Park, W.J., Liu, J., Sharp, E.J. & Adler, P.N. (1996) The Drosophila tissue polarity gene inturned acts cell autonomously and encodes a novel protein. Development 122, 961-969.
43. Pauli, A., Althoff, F., Oliveira, R.A., Heidmann, S., Schuldiner, O., Lehner, C.F., Dickson, B.J. & Nasmyth, K. (2008) Cell-type-specific TEV protease cleavage reveals cohesin functions in Drosophila neurons. Dev. Cell 14, 239-251.
44. Rollins, R.A., Korom, M., Aulner, N., Martens, A. & Dorsett, D. (2004) Drosophila nipped-B protein supports sister chromatid cohesion and opposes the stromalin/Scc3 cohesion factor to facilitate long-range activation of the cut gene. Mol. Cell. Biol. 24, 3100-3111.
45. Schuldiner, O., Berdnik, D., Levy, J.M., Wu, J.S., Luginbuhl, D., Gontang, A.C. & Luo, L. (2008) piggyBac-based mosaic screen identifies a postmitotic function for cohesin in regulating developmental axon pruning. Dev. Cell 14, 227-238.
46. Seifert, J.R. & Mlodzik, M. (2007) Frizzled/PCP signalling: a conserved mechanism regulating cell polarity and directed motility. Nat. Rev. Genet. 8, 126-138.
47. 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, 209-222.
48. Strutt, D. (2001) Asymmetric localization of frizzled and the establishment of cell polarity in the Drosophila wing. Mol. Cell 7, 367-375.
49. Strutt, D. (2008) The planar polarity pathway. Curr. Biol. 18, R898-902.
50. Strutt, H. & Strutt, D. (2002) Nonautonomous planar polarity patterning in Drosophila: dishevelled-independent functions of frizzled. Dev. Cell 3, 851-863.
51. Thomas, C. & Strutt, D. (2012) The roles of the cadherins Fat and Dachsous in planar polarity specification in Drosophila. Dev. Dyn. 241, 27-39.
52. Tissir, F., Bar, I., Jossin, Y., De Backer, O. & Goffinet, A.M. (2005) Protocadherin Celsr3 is crucial in axonal tract development. Nat. Neurosci. 8, 451-457.
53. Tree, D.R., Shulman, J.M., Rousset, R., Scott, M.P., Gubb, D. & Axelrod, J.D. (2002) Prickle mediates feedback amplification to generate asymmetric planar cell polarity signaling. Cell 109, 371-381.
54. Usui, T., Shima, Y., Shimada, Y., Hirano, S., Burgess, R., Schwarz, T., Takeichi, M. & Uemura, T. (1999) Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585-595.
55. Vass, S., Cotterill, S., Valdeolmillos, A.M., Barbero, J.L., Lin, E., Warren, W.D. & Heck, M.M. (2003) Depletion of Drad21/Scc1 in Drosophila cells leads to instability of the cohesin complex and disruption of mitotic progression. Curr. Biol. 13, 208-218.
56. Wang, Y. & Nathans, J. (2007) Tissue/planar cell polarity in vertebrates: new insights and new questions. Development 134, 647-658.
57. Wei, S.Y., Escudero, L.M., Yu, F., Chang, L.H., Chen, L.Y., Ho, Y.H., Lin, C.M., Chou, C.S., Chia, W., Modolell, J. & Hsu, J.C. (2005) Echinoid is a component of adherens junctions that cooperates with DE-Cadherin to mediate cell adhesion. Dev. Cell 8, 493-504.
58. Woods, D.F. & Bryant, P.J. (1991) The discs-large tumor suppressor gene of Drosophila encodes a guanylate kinase homolog localized at septate junctions. Cell 66, 451-464.
59. Zallen, J.A. (2007) Planar polarity and tissue morphogenesis. Cell 129, 1051-1063.
60. Zhou, L.B., Bar, I., Achouri, Y., Campbell, K., De Backer, O., Hebert, J.M., Jones, K., Kessaris, N., de Rouvroit, C.L., O'Leary, D., Richardson, W.D., Goffinet, A.M. & Tissir, F. (2008) Early forebrain wiring: genetic dissection using conditional Celsr3 mutant mice. Science 320, 946-949.