PTEN Controls Junction Lengthening and Stability during Cell Rearrangement in Epithelial Tissue

Developmental Cell

Volumn 25, Issue 5, 2013, Pages 534-546

  Bardet, Pierre Luc ^a   Guirao, Boris ^a   Paoletti, Camille ^a   Serman, Fanny ^a   Léopold, Valentine ^a   Bosveld, Floris ^a   Goya, YÛki ^a   Mirouse, Vincent ^b   Graner, François ^a   Bellaïche, Yohanns ^a  

^a INSTITUT CURIE   (France)

^b UNIVERSITÉ CLERMONT AUVERGNE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN II; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; RHO KINASE;

ANIMAL CELL; ANIMAL MODEL; ARTICLE; CELL JUNCTION; CELL STRUCTURE; CONTROLLED STUDY; CYTOPLASM; DEVELOPMENT; DROSOPHILA; EPITHELIUM; GENE; LOSS OF FUNCTION MUTATION; MOLECULAR BIOLOGY; MORPHOGENESIS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PTEN GENE;

ANIMALS; CROSSES, GENETIC; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; EPITHELIUM; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GREEN FLUORESCENT PROTEINS; INTERCELLULAR JUNCTIONS; MORPHOGENESIS; MUTATION; MYOSIN TYPE II; PTEN PHOSPHOHYDROLASE; WING;

EID: 84878963635     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2013.04.020     Document Type: Article

References (57)

1. 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.
2. Amano M., Nakayama M., Kaibuchi K. Rho-kinase/ROCK: a key regulator of the cytoskeleton and cell polarity. Cytoskeleton 2010, 67:545-554.
3. Bellaïche 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 2004, 131:469-478.
4. Bertet C., Sulak L., Lecuit T. Myosin-dependent junction remodelling controls planar cell intercalation and axis elongation. Nature 2004, 429:667-671.
5. Bosveld F., Bonnet I., Guirao B., Tlili S., Wang Z., Petitalot A., Marchand R., Bardet P.-L., Marcq P., Graner F., Bellaïche Y. Mechanical control of morphogenesis by Fat/Dachsous/Four-jointed planar cell polarity pathway. Science 2012, 336:724-727.
6. Britton J.S., Lockwood W.K., Li L., Cohen S.M., Edgar B.A. Drosophila's insulin/PI3-kinase pathway coordinates cellular metabolism with nutritional conditions. Dev. Cell 2002, 2:239-249.
7. Chalhoub N., Baker S.J. PTEN and the PI3-kinase pathway in cancer. Annu. Rev. Pathol. 2009, 4:127-150.
8. Clark K., Langeslag M., Figdor C.G., van Leeuwen F.N. Myosin II and mechanotransduction: a balancing act. Trends Cell Biol. 2007, 17:178-186.
9. 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.
10. Classen A.K., Aigouy B., Giangrande A., Eaton S. Imaging Drosophila pupal wing morphogenesis. Methods Mol. Biol. 2008, 420:265-275.
11. de Matos Simões S., Blankenship J.T., Weitz O., Farrell D.L., Tamada M., Fernandez-Gonzalez R., Zallen J.A. Rho-kinase directs Bazooka/Par-3 planar polarity during Drosophila axis elongation. Dev. Cell 2010, 19:377-388.
12. Doyle K., Hogan J., Lester M., Collier S. The Frizzled planar cell polarity signaling pathway controls Drosophila wing topography. Dev. Biol. 2008, 317:354-367.
13. Farhadifar R., Röper J.C., Aigouy B., Eaton S., Jülicher F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 2007, 17:2095-2104.
14. Fernandez-Gonzalez R., de Matos Simões S., Röper J.C., Eaton S., Zallen J.A. Myosin II dynamics are regulated by tension in intercalating cells. Dev. Cell 2009, 17:736-743.
15. Gho M., Bellaïche Y., Schweisguth F. Revisiting the Drosophila microchaete lineage: a novel intrinsically asymmetric cell division generates a glial cell. Development 1999, 126:3573-3584.
16. Gibson M.C., Patel A.B., Nagpal R., Perrimon N. The emergence of geometric order in proliferating metazoan epithelia. Nature 2006, 442:1038-1041.
17. Glazier J.A., Graner F. Simulation of the differential adhesion driven rearrangement of biological cells. Phys. Rev. E 1993, 47:2128-2154.
18. Graner F., Glazier J.A. Simulation of biological cell sorting using a two-dimensional extended Potts model. Phys. Rev. Lett. 1992, 69:2013-2016.
19. Graner F., Sawada Y. Can surface adhesion drive cell rearrangement? Part II: a geometrical model. J.Theor. Biol. 1993, 164:477-506.
20. Hales T.C. The honeycomb conjecture. Disc. Comp. Geom. 2001, 25:1-22.
21. 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.
22. Hilgenfeldt S., Erisken S., Carthew R.W. Physical modeling of cell geometric order in an epithelial tissue. Proc. Natl. Acad. Sci. USA 2008, 105:907-911.
23. Hutson M.S., Ma X. Plasma and cavitation dynamics during pulsed laser microsurgery invivo. Phys. Rev. Lett. 2007, 99:158104.
24. Hutson M.S., Veldhuis J., Ma X., Lynch H.E., Cranston P.G., Brodland G.W. Combining laser microsurgery and finite element modeling to assess cell-level epithelial mechanics. Biophys. J. 2009, 97:3075-3085.
25. Käfer J., Hayashi T., Marée A.F., Carthew R.W., Graner F. Cell adhesion and cortex contractility determine cell patterning in the Drosophila retina. Proc. Natl. Acad. Sci. USA 2007, 104:18549-18554.
26. Keller R. Mechanisms of elongation in embryogenesis. Development 2006, 133:2291-2302.
27. Knox A.L., Brown N.H. Rap1 GTPase regulation of adherens junction positioning and cell adhesion. Science 2002, 295:1285-1288.
28. Krieg M., Arboleda-Estudillo Y., Puech P.H., Käfer J., Graner F., Müller D.J., Heisenberg C.P. Tensile forces govern germ-layer organization in zebrafish. Nat. Cell Biol. 2008, 10:429-436.
29. Lecuit T., Lenne P.F. Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8:633-644.
30. Lecuit T., Lenne P.F., Munro E. Force generation, transmission, and integration during cell and tissue morphogenesis. Annu. Rev. Cell Dev. Biol. 2011, 27:157-184.
31. Li Z., Dong X., Wang Z., Liu W., Deng N., Ding Y., Tang L., Hla T., Zeng R., Li L., Wu D. Regulation of PTEN by Rho small GTPases. Nat. Cell Biol. 2005, 7:399-404.
32. Ma D., Amonlirdviman K., Raffard R.L., Abate A., Tomlin C.J., Axelrod J.D. Cell packing influences planar cell polarity signaling. Proc. Natl. Acad. Sci. USA 2008, 105:18800-18805.
33. Maître J.L., Berthoumieux H., Krens S.F., Salbreux G., Jülicher F., Paluch E., Heisenberg C.P. Adhesion functions in cell sorting by mechanically coupling the cortices of adhering cells. Science 2012, 338:253-256.
34. Martin-Belmonte F., Gassama A., Datta A., Yu W., Rescher U., Gerke V., Mostov K. PTEN-mediated apical segregation of phosphoinositides controls epithelial morphogenesis through Cdc42. Cell 2007, 128:383-397.
35. McGuire S.E., Le P.T., Osborn A.J., Matsumoto K., Davis R.L. Spatiotemporal rescue of memory dysfunction in Drosophila. Science 2003, 302:1765-1768.
36. McKenzie E., Krupin A., Kelley M.W. Cellular growth and rearrangement during the development of the mammalian organ of Corti. Dev. Dyn. 2004, 229:802-812.
37. Narimatsu M., Bose R., Pye M., Zhang L., Miller B., Ching P., Sakuma R., Luga V., Roncari L., Attisano L., Wrana J.L. Regulation of planar cell polarity by Smurf ubiquitin ligases. Cell 2009, 137:295-307.
38. Nishimura T., Honda H., Takeichi M. Planar cell polarity links axes of spatial dynamics in neural-tube closure. Cell 2012, 149:1084-1097.
39. Nowak R.B., Fischer R.S., Zoltoski R.K., Kuszak J.R., Fowler V.M. Tropomodulin1 is required for membrane skeleton organization and hexagonal geometry of fiber cells in the mouse lens. J. Cell Biol. 2009, 186:915-928.
40. Oda H., Tsukita S. Real-time imaging of cell-cell adherens junctions reveals that Drosophila mesoderm invagination begins with two phases of apical constriction of cells. J. Cell Sci. 2001, 114:493-501.
41. Papusheva E., Heisenberg C.P. Spatial organization of adhesion: force-dependent regulation and function in tissue morphogenesis. EMBO J. 2010, 29:2753-2768.
42. Perez T.D., Tamada M., Sheetz M.P., Nelson W.J. Immediate-early signaling induced by E-cadherin engagement and adhesion. J.Biol. Chem. 2008, 283:5014-5022.
43. Pickering K., Alves-Silva J., Goberdhan D., Millard T.H. Par3/Bazooka and phosphoinositides regulate actin protrusion formation during Drosophila dorsal closure and wound healing. Development 2013, 140:800-809.
44. Pinal N., Goberdhan D.C., Collinson L., Fujita Y., Cox I.M., Wilson C., Pichaud F. Regulated and polarized PtdIns(3,4,5)P3 accumulation is essential for apical membrane morphogenesis in photoreceptor epithelial cells. Curr. Biol. 2006, 16:140-149.
45. Rauzi M., Verant P., Lecuit T., Lenne P.F. Nature and anisotropy of cortical forces orienting Drosophila tissue morphogenesis. Nat. Cell Biol. 2008, 10:1401-1410.
46. Rauzi M., Lenne P.F., Lecuit T. Planar polarized actomyosin contractile flows control epithelial junction remodelling. Nature 2010, 468:1110-1114.
47. Rivard N. Phosphatidylinositol 3-kinase: a key regulator in adherens junction formation and function. Front. Biosci. 2009, 14:510-522.
48. Royou A., Field C., Sisson J.C., Sullivan W., Karess R. Reassessing the role and dynamics of nonmuscle myosin II during furrow formation in early Drosophila embryos. Mol. Biol. Cell 2004, 15:838-850.
49. Staple D.B., Farhadifar R., Röper J.-C., Aigouy B., Eaton S., Jülicher F. Mechanics and remodelling of cell packings in epithelia. Eur. Phys. J. E. Soft Matter. 2010, 33:117-127.
50. Stocker H., Andjelkovic M., Oldham S., Laffargue M., Wymann M.P., Hemmings B.A., Hafen E. Living with lethal PIP3 levels: viability of flies lacking PTEN restored by a PH domain mutation in Akt/PKB. Science 2002, 295:2088-2091.
51. Tardieu A. Eye lens proteins and transparency: from light transmission theory to solution X-ray structural analysis. Annu. Rev. Biophys. Biophys. Chem. 1988, 17:47-70.
52. Togashi H., Kominami K., Waseda M., Komura H., Miyoshi J., Takeichi M., Takai Y. Nectins establish a checkerboard-like cellular pattern in the auditory epithelium. Science 2011, 333:1144-1147.
53. Warrington S.J., Strutt H., Strutt D. The Frizzled-dependent planar polarity pathway locally promotes E-cadherin turnover via recruitment of RhoGEF2. Development 2013, 140:1045-1054.
54. Winter C.G., Wang B., Ballew A., Royou A., Karess R., Axelrod J.D., Luo L. Drosophila Rho-associated kinase (Drok) links Frizzled-mediated planar cell polarity signaling to the actin cytoskeleton. Cell 2001, 105:81-91.
55. Xu T., Rubin G.M. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 1993, 117:1223-1237.
56. Yamada S., Nelson W.J. Localized zones of Rho and Rac activities drive initiation and expansion of epithelial cell-cell adhesion. J. Cell Biol. 2007, 178:517-527.
57. Zallen J.A., Wieschaus E. Patterned gene expression directs bipolar planar polarity in Drosophila. Dev. Cell 2004, 6:343-355.