Ect2/Pbl Acts via Rho and Polarity Proteins to Direct the Assembly of an Isotropic Actomyosin Cortex upon Mitotic Entry

Developmental Cell

Volumn 32, Issue 5, 2015, Pages 604-616

  Rosa, André ^a,b   Vlassaks, Evi ^a   Pichaud, Franck ^a   Baum, Buzz ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

^b UNIVERSITY OF PORTO   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN RELATED PROTEIN 2-3 COMPLEX; F ACTIN; MYOSIN ADENOSINE TRIPHOSPHATASE; MYOSIN II; PROTEIN CDC42; PROTEIN KINASE C; RHO FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR ECT2; RHO GUANINE NUCLEOTIDE EXCHANGE FACTOR PBL; UNCLASSIFIED DRUG; CDC42 PROTEIN, DROSOPHILA; DROSOPHILA PROTEIN; GUANINE NUCLEOTIDE BINDING PROTEIN; GUANINE NUCLEOTIDE EXCHANGE FACTOR; PEBBLE PROTEIN, DROSOPHILA; PROTEIN BINDING;

ACTIN FILAMENT; ANAPHASE; ANIMAL CELL; ARTICLE; CELL JUNCTION; CELL POLARITY; CELL SURFACE; CHROMOSOME SEGREGATION; CONTROLLED STUDY; CYTOKINESIS; CYTOSKELETON; DROSOPHILA; EPITHELIUM CELL; INTERPHASE; METAPHASE; MITOSIS; NONHUMAN; PRIORITY JOURNAL; REPOLARIZATION; TELOPHASE; ANIMAL; CELL CULTURE; CELL NUCLEUS; CYTOLOGY; DROSOPHILA MELANOGASTER; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOPRECIPITATION; METABOLISM; PHYSIOLOGY; WESTERN BLOTTING;

ACTIN CYTOSKELETON; ACTIN-RELATED PROTEIN 2-3 COMPLEX; ACTOMYOSIN; ANIMALS; BLOTTING, WESTERN; CELL NUCLEUS; CELLS, CULTURED; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EPITHELIAL CELLS; FLUORESCENT ANTIBODY TECHNIQUE; GTP-BINDING PROTEINS; GUANINE NUCLEOTIDE EXCHANGE FACTORS; IMMUNOPRECIPITATION; MITOSIS; PROTEIN BINDING; PROTEIN KINASE C;

EID: 84924445549     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2015.01.012     Document Type: Article

References (74)

1. Bellaïche 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. Nat. Cell Biol. 2001, 3:50-57.
2. Bergstralh D.T., Lovegrove H.E., St Johnston D. Discs large links spindle orientation to apical-basal polarity in Drosophila epithelia. Curr. Biol. 2013, 23:1707-1712.
3. 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.
4. Bovellan M., Romeo Y., Biro M., Boden A., Chugh P., Yonis A., Vaghela M., Fritzsche M., Moulding D., Thorogate R., et al. Cellular control of cortical actin nucleation. Curr. Biol. 2014, 24:1628-1635.
5. Carreno S., Kouranti I., Glusman E.S., Fuller M.T., Echard A., Payre F. Moesin and its activating kinase Slik are required for cortical stability and microtubule organization in mitotic cells. J.Cell Biol. 2008, 180:739-746.
6. Castrillon D.H., Wasserman S.A. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 1994, 120:3367-3377.
7. Cramer L.P., Mitchison T.J. Investigation of the mechanism of retraction of the cell margin and rearward flow of nodules during mitotic cell rounding. Mol. Biol. Cell 1997, 8:109-119.
8. Dao V.T., Dupuy A.G., Gavet O., Caron E., de Gunzburg J. Dynamic changes in Rap1 activity are required for cell retraction and spreading during mitosis. J.Cell Sci. 2009, 122:2996-3004.
9. Dong Y., Pruyne D., Bretscher A. Formin-dependent actin assembly is regulated by distinct modes of Rho signaling in yeast. J.Cell Biol. 2003, 161:1081-1092.
10. Durgan J., Kaji N., Jin D., Hall A. Par6B and atypical PKC regulate mitotic spindle orientation during epithelial morphogenesis. J.Biol. Chem. 2011, 286:12461-12474.
11. Edwards K.A., Demsky M., Montague R.A., Weymouth N., Kiehart D.P. GFP-moesin illuminates actin cytoskeleton dynamics in living tissue and demonstrates cell shape changes during morphogenesis in Drosophila. Dev. Biol. 1997, 191:103-117.
12. Fededa J.P., Gerlich D.W. Molecular control of animal cell cytokinesis. Nat. Cell Biol. 2012, 14:440-447.
13. Fehon R.G., Oren T., LaJeunesse D.R., Melby T.E., McCartney B.M. Isolation of mutations in the Drosophila homologues of the human Neurofibromatosis 2 and yeast CDC42 genes using a simple and efficient reverse-genetic method. Genetics 1997, 146:245-252.
14. Fink J., Carpi N., Betz T., Bétard A., Chebah M., Azioune A., Bornens M., Sykes C., Fetler L., Cuvelier D., Piel M. External forces control mitotic spindle positioning. Nat. Cell Biol. 2011, 13:771-778.
15. Fletcher G.C., Lucas E.P., Brain R., Tournier A., Thompson B.J. Positive feedback and mutual antagonism combine to polarize Crumbs in the Drosophila follicle cell epithelium. Curr. Biol. 2012, 22:1116-1122.
16. Founounou N., Loyer N., Le Borgne R. Septins regulate the contractility of the actomyosin ring to enable adherens junction remodeling during cytokinesis of epithelial cells. Dev. Cell 2013, 24:242-255.
17. Georgiou M., Baum B. Polarity proteins and Rho GTPases cooperate to spatially organise epithelial actin-based protrusions. J.Cell Sci. 2010, 123:1089-1098.
18. Georgiou M., Marinari E., Burden J., Baum B. Cdc42, Par6, and aPKC regulate Arp2/3-mediated endocytosis to control local adherens junction stability. Curr. Biol. 2008, 18:1631-1638.
19. Gotta M., Abraham M.C., Ahringer J. CDC-42 controls early cell polarity and spindle orientation in C.elegans. Curr. Biol. 2001, 11:482-488.
20. Grosshans J., Wenzl C., Herz H.M., Bartoszewski S., Schnorrer F., Vogt N., Schwarz H., Müller H.A. RhoGEF2 and the formin Dia control the formation of the furrow canal by directed actin assembly during Drosophila cellularisation. Development 2005, 132:1009-1020.
21. Guilgur L.G., Prudêncio P., Ferreira T., Pimenta-Marques A.R., Martinho R.G. Drosophila aPKC is required for mitotic spindle orientation during symmetric division of epithelial cells. Development 2012, 139:503-513.
22. Guillot C., Lecuit T. Adhesion disengagement uncouples intrinsic and extrinsic forces to drive cytokinesis in epithelial tissues. Dev. Cell 2013, 24:227-241.
23. Hao Y., Du Q., Chen X., Zheng Z., Balsbaugh J.L., Maitra S., Shabanowitz J., Hunt D.F., Macara I.G. Par3 controls epithelial spindle orientation by aPKC-mediated phosphorylation of apical Pins. Curr. Biol. 2010, 20:1809-1818.
24. Hara T., Abe M., Inoue H., Yu L.R., Veenstra T.D., Kang Y.H., Lee K.S., Miki T. Cytokinesis regulator ECT2 changes its conformation through phosphorylation at Thr-341 in G2/M phase. Oncogene 2006, 25:566-578.
25. Harris K.P., Tepass U. Cdc42 and Par proteins stabilize dynamic adherens junctions in the Drosophila neuroectoderm through regulation of apical endocytosis. J.Cell Biol. 2008, 183:1129-1143.
26. Hatan M., Shinder V., Israeli D., Schnorrer F., Volk T. The Drosophila blood brain barrier is maintained by GPCR-dependent dynamic actin structures. J.Cell Biol. 2011, 192:307-319.
27. Herszterg S., Leibfried A., Bosveld F., Martin C., Bellaiche Y. Interplay between the dividing cell and its neighbors regulates adherens junction formation during cytokinesis in epithelial tissue. Dev. Cell 2013, 24:256-270.
28. Homem C.C., Peifer M. Diaphanous regulates myosin and adherens junctions to control cell contractility and protrusive behavior during morphogenesis. Development 2008, 135:1005-1018.
29. Hutterer A., Betschinger J., Petronczki M., Knoblich J.A. Sequential roles of Cdc42, Par-6, aPKC, and Lgl in the establishment of epithelial polarity during Drosophila embryogenesis. Dev. Cell 2004, 6:845-854.
30. Jaffe A.B., Kaji N., Durgan J., Hall A. Cdc42 controls spindle orientation to position the apical surface during epithelial morphogenesis. J.Cell Biol. 2008, 183:625-633.
31. Johnson D.I. Cdc42: An essential Rho-type GTPase controlling eukaryotic cell polarity. Microbiol. Mol. Biol. Rev. 1999, 63:54-105.
32. Kondo T., Hayashi S. Mitotic cell rounding accelerates epithelial invagination. Nature 2013, 494:125-129.
33. Kunda P., Baum B. The actin cytoskeleton in spindle assembly and positioning. Trends Cell Biol. 2009, 19:174-179.
34. Kunda P., Pelling A.E., Liu T., Baum B. Moesin controls cortical rigidity, cell rounding, and spindle morphogenesis during mitosis. Curr. Biol. 2008, 18:91-101.
35. Kunda P., Rodrigues N.T., Moeendarbary E., Liu T., Ivetic A., Charras G., Baum B. PP1-mediated moesin dephosphorylation couples polar relaxation to mitotic exit. Curr. Biol. 2012, 22:231-236.
36. Lancaster O.M., Le Berre M., Dimitracopoulos A., Bonazzi D., Zlotek-Zlotkiewicz E., Picone R., Duke T., Piel M., Baum B. Mitotic rounding alters cell geometry to ensure efficient bipolar spindle formation. Dev. Cell 2013, 25:270-283.
37. Liu X.F., Ishida H., Raziuddin R., Miki T. Nucleotide exchange factor ECT2 interacts with the polarity protein complex Par6/Par3/protein kinase Czeta (PKCzeta) and regulates PKCzeta activity. Mol. Cell. Biol. 2004, 24:6665-6675.
38. Liu X.F., Ohno S., Miki T. Nucleotide exchange factor ECT2 regulates epithelial cell polarity. Cell. Signal. 2006, 18:1604-1615.
39. Lu B., Roegiers F., Jan L.Y., Jan Y.N. Adherens junctions inhibit asymmetric division in the Drosophila epithelium. Nature 2001, 409:522-525.
40. Luxenburg C., Pasolli H.A., Williams S.E., Fuchs E. Developmental roles for Srf, cortical cytoskeleton and cell shape in epidermal spindle orientation. Nat. Cell Biol. 2011, 13:203-214.
41. Maddox A.S., Burridge K. RhoA is required for cortical retraction and rigidity during mitotic cell rounding. J.Cell Biol. 2003, 160:255-265.
42. Marinari E., Mehonic A., Curran S., Gale J., Duke T., Baum B. Live-cell delamination counterbalances epithelial growth to limit tissue overcrowding. Nature 2012, 484:542-545.
43. Matthews H.K., Delabre U., Rohn J.L., Guck J., Kunda P., Baum B. Changes in Ect2 localization couple actomyosin-dependent cell shape changes to mitotic progression. Dev. Cell 2012, 23:371-383.
44. McGill M.A., McKinley R.F., Harris T.J. Independent cadherin-catenin and Bazooka clusters interact to assemble adherens junctions. J.Cell Biol. 2009, 185:787-796.
45. Mitsushima M., Toyoshima F., Nishida E. Dual role of Cdc42 in spindle orientation control of adherent cells. Mol. Cell. Biol. 2009, 29:2816-2827.
46. Monier B., Pelissier-Monier A., Brand A.H., Sanson B. An actomyosin-based barrier inhibits cell mixing at compartmental boundaries in Drosophila embryos. Nat Cell Biol 2010, 12:60-65. sup pp 61-69.
47. Mummery-Widmer J.L., Yamazaki M., Stoeger T., Novatchkova M., Bhalerao S., Chen D., Dietzl G., Dickson B.J., Knoblich J.A. Genome-wide analysis of Notch signalling in Drosophila by transgenic RNAi. Nature 2009, 458:987-992.
48. Nakajima Y., Meyer E.J., Kroesen A., McKinney S.A., Gibson M.C. Epithelial junctions maintain tissue architecture by directing planar spindle orientation. Nature 2013, 500:359-362.
49. Narumiya S., Yasuda S. Rho GTPases in animal cell mitosis. Curr. Opin. Cell Biol. 2006, 18:199-205.
50. Niiya F., Tatsumoto T., Lee K.S., Miki T. Phosphorylation of the cytokinesis regulator ECT2 at G2/M phase stimulates association of the mitotic kinase Plk1 and accumulation of GTP-bound RhoA. Oncogene 2006, 25:827-837.
51. O'Keefe L., Somers W.G., Harley A., Saint R. The pebble GTP exchange factor and the control of cytokinesis. Cell Struct. Funct. 2001, 26:619-626.
52. Oceguera-Yanez F., Kimura K., Yasuda S., Higashida C., Kitamura T., Hiraoka Y., Haraguchi T., Narumiya S. Ect2 and MgcRacGAP regulate the activation and function of Cdc42 in mitosis. J.Cell Biol. 2005, 168:221-232.
53. Petronczki M., Glotzer M., Kraut N., Peters J.M. Polo-like kinase 1 triggers the initiation of cytokinesis in human cells by promoting recruitment of the RhoGEF Ect2 to the central spindle. Dev. Cell 2007, 12:713-725.
54. Prokopenko S.N., Brumby A., O'Keefe L., Prior L., He Y., Saint R., Bellen H.J. A putative exchange factor for Rho1 GTPase is required for initiation of cytokinesis in Drosophila. Genes Dev. 1999, 13:2301-2314.
55. Prokopenko S.N., Saint R., Bellen H.J. Tissue distribution of PEBBLE RNA and pebble protein during Drosophila embryonic development. Mech. Dev. 2000, 90:269-273.
56. Reinsch S., Karsenti E. Orientation of spindle axis and distribution of plasma membrane proteins during cell division in polarized MDCKII cells. J.Cell Biol. 1994, 126:1509-1526.
57. Ren G., Vajjhala P., Lee J.S., Winsor B., Munn A.L. The BAR domain proteins: molding membranes in fission, fusion, and phagy. Microbiol. Mol. Biol. Rev. 2006, 70:37-120.
58. Riedl J., Crevenna A.H., Kessenbrock K., Yu J.H., Neukirchen D., Bista M., Bradke F., Jenne D., Holak T.A., Werb Z., et al. Lifeact: a versatile marker to visualize F-actin. Nat. Methods 2008, 5:605-607.
59. Rosenblatt J., Cramer L.P., Baum B., McGee K.M. Myosin II-dependent cortical movement is required for centrosome separation and positioning during mitotic spindle assembly. Cell 2004, 117:361-372.
60. Schindelin J., Arganda-Carreras I., Frise E., Kaynig V., Longair M., Pietzsch T., Preibisch S., Rueden C., Saalfeld S., Schmid B., et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 2012, 9:676-682.
61. Sedzinski J., Biro M., Oswald A., Tinevez J.Y., Salbreux G., Paluch E. Polar actomyosin contractility destabilizes the position of the cytokinetic furrow. Nature 2011, 476:462-466.
62. Somers W.G., Saint R. A RhoGEF and Rho family GTPase-activating protein complex links the contractile ring to cortical microtubules at the onset of cytokinesis. Dev. Cell 2003, 4:29-39.
63. St Johnston D., Ahringer J. Cell polarity in eggs and epithelia: parallels and diversity. Cell 2010, 141:757-774.
64. Stewart M.P., Helenius J., Toyoda Y., Ramanathan S.P., Muller D.J., Hyman A.A. Hydrostatic pressure and the actomyosin cortex drive mitotic cell rounding. Nature 2011, 469:226-230.
65. Su K.C., Takaki T., Petronczki M. Targeting of the RhoGEF Ect2 to the equatorial membrane controls cleavage furrow formation during cytokinesis. Dev. Cell 2011, 21:1104-1115.
66. Tatsumoto T., Xie X., Blumenthal R., Okamoto I., Miki T. Human ECT2 is an exchange factor for Rho GTPases, phosphorylated in G2/M phases, and involved in cytokinesis. J.Cell Biol. 1999, 147:921-928.
67. Théry M., Racine V., Pépin A., Piel M., Chen Y., Sibarita J.B., Bornens M. The extracellular matrix guides the orientation of the cell division axis. Nat. Cell Biol. 2005, 7:947-953.
68. Touré A., Dorseuil O., Morin L., Timmons P., Jégou B., Reibel L., Gacon G. MgcRacGAP, a new human GTPase-activating protein for Rac and Cdc42 similar to Drosophila rotundRacGAP gene product, is expressed in male germ cells. J.Biol. Chem. 1998, 273:6019-6023.
69. van Impel A., Schumacher S., Draga M., Herz H.M., Grosshans J., Müller H.A. Regulation of the Rac GTPase pathway by the multifunctional Rho GEF Pebble is essential for mesoderm migration in the Drosophila gastrula. Development 2009, 136:813-822.
70. Warner S.J., Longmore G.D. Cdc42 antagonizes Rho1 activity at adherens junctions to limit epithelial cell apical tension. J.Cell Biol. 2009, 187:119-133.
71. Wirtz-Peitz F., Nishimura T., Knoblich J.A. Linking cell cycle to asymmetric division: Aurora-A phosphorylates the Par complex to regulate Numb localization. Cell 2008, 135:161-173.
72. Zang J.H., Cavet G., Sabry J.H., Wagner P., Moores S.L., Spudich J.A. On the role of myosin-II in cytokinesis: division of Dictyostelium cells under adhesive and nonadhesive conditions. Mol. Biol. Cell 1997, 8:2617-2629.
73. Zavortink M., Contreras N., Addy T., Bejsovec A., Saint R. Tum/RacGAP50C provides a critical link between anaphase microtubules and the assembly of the contractile ring in Drosophila melanogaster. J.Cell Sci. 2005, 118:5381-5392.
74. Zhu X., Wang J., Moriguchi K., Liow L.T., Ahmed S., Kaverina I., Murata-Hori M. Proper regulation of Cdc42 activity is required for tight actin concentration at the equator during cytokinesis in adherent mammalian cells. Exp. Cell Res. 2011, 317:2384-2389.