A dual function of Drosophila capping protein on DE-cadherin maintains epithelial integrity and prevents JNK-mediated apoptosis

Developmental Biology

Volumn 360, Issue 1, 2011, Pages 143-159

  Jezowska, Barbara ^a   Fernández, Beatriz García ^a   Amândio, Ana Rita ^a   Duarte, Paulo ^a   Mendes, Cláudia ^a   Brás Pereira, Catarina ^a   Janody, Florence ^a  

^a INSTITUTO GULBENKIAN DE CIÊNCIA   (Portugal)

Author keywords

Capping protein; Cell adhesion; DE cadherin; Drosophila disc epithelium; JNK mediated apoptosis; Wingless signalling

Indexed keywords

ARMADILLO DOMAIN PROTEIN; CADHERIN; CAPPING PROTEIN; CARRIER PROTEIN; DE CADHERIN; HETERODIMER; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; WNT1 PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL TISSUE; APOPTOSIS; ARTICLE; CELL JUNCTION; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; ENZYME ACTIVITY; EPITHELIUM CELL; FORELIMB; NONHUMAN; ONCOGENE; ONCOGENE RAS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; TISSUE GROWTH; TRANSCRIPTION REGULATION; UPREGULATION;

ARMADILLO;

EID: 80755133315     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2011.09.016     Document Type: Article

References (78)

1. Adachi-Yamada T., Fujimura-Kamada K., Nishida Y., Matsumoto K. Distortion of proximodistal information causes JNK-dependent apoptosis in Drosophila wing. Nature 1999, 400:166-169.
2. Aegerter-Wilmsen T., Aegerter C.M., Hafen E., Basler K. Model for the regulation of size in the wing imaginal disc of Drosophila. Mech. Dev. 2007, 124:318-326.
3. Aegerter-Wilmsen T., Smith A.C., Christen A.J., Aegerter C.M., Hafen E., Basler K. Exploring the effects of mechanical feedback on epithelial topology. Development 2010, 137:499-506.
4. Assemat E., Bazellieres E., Pallesi-Pocachard E., Le Bivic A., Massey-Harroche D. Polarity complex proteins. Biochim. Biophys. Acta 2008, 1778:614-630.
5. Baker N.E. Transcription of the segment-polarity gene wingless in the imaginal discs of Drosophila, and the phenotype of a pupal-lethal wg mutation. Development 1988, 102:489-497.
6. Brodsky M.H., Nordstrom W., Tsang G., Kwan E., Rubin G.M., Abrams J.M. Drosophila p53 binds a damage response element at the reaper locus. Cell 2000, 101:103-113.
7. Brumby A.M., Richardson H.E. Scribble mutants cooperate with oncogenic Ras or Notch to cause neoplastic overgrowth in Drosophila. EMBO J. 2003, 22:5769-5779.
8. Casares F., Mann R.S. Control of antennal versus leg development in Drosophila. Nature 1998, 392:723-726.
9. Cavallaro U., Christofori G. Multitasking in tumor progression: signaling functions of cell adhesion molecules. Ann. N. Y. Acad. Sci. 2004, 1014:58-66.
10. Cavey M., Lecuit T. Molecular bases of cell-cell junctions stability and dynamics. Cold Spring Harb. Perspect. Biol. 2009, 1:a002998.
11. Cooper J.A., Sept D. New insights into mechanism and regulation of actin capping protein. Int. Rev. Cell Mol. Biol. 2008, 267:183-206.
12. Delalle I., Pfleger C.M., Buff E., Lueras P., Hariharan I.K. Mutations in the Drosophila orthologs of the F-actin capping protein alpha- and beta-subunits cause actin accumulation and subsequent retinal degeneration. Genetics 2005, 171:1757-1765.
13. Desprat N., Supatto W., Pouille P.A., Beaurepaire E., Farge E. Tissue deformation modulates twist expression to determine anterior midgut differentiation in Drosophila embryos. Dev. Cell 2008, 15:470-477.
14. Dow L.E., Humbert P.O. Polarity regulators and the control of epithelial architecture, cell migration, and tumorigenesis. Int. Rev. Cytol. 2007, 262:253-302.
15. Fan Y., Bergmann A. Apoptosis-induced compensatory proliferation. The Cell is dead. Long live the Cell!. Trends Cell Biol. 2008, 18:467-473.
16. Fernandez B.G., Gaspar P., Bras-Pereira C., Jezowska B., Rebelo S.R., Janody F. Actin-capping protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 2011, 138:2337-2346.
17. Frame M.C. Newest findings on the oldest oncogene; how activated src does it. J. Cell Sci. 2004, 117:989-998.
18. Gates J., Nowotarski S.H., Yin H., Mahaffey J.P., Bridges T., Herrera C., Homem C.C., Janody F., Montell D.J., Peifer M. Enabled and capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev. Biol. 2009, 333:90-107.
19. Genevet A., Polesello C., Blight K., Robertson F., Collinson L.M., Pichaud F., Tapon N. The Hippo pathway regulates apical-domain size independently of its growth-control function. J. Cell Sci. 2009, 122:2360-2370.
20. Giannone G., Sheetz M.P. Substrate rigidity and force define form through tyrosine phosphatase and kinase pathways. Trends Cell Biol. 2006, 16:213-223.
21. Gottardi C.J., Wong E., Gumbiner B.M. E-cadherin suppresses cellular transformation by inhibiting beta-catenin signaling in an adhesion-independent manner. J. Cell Biol. 2001, 153:1049-1060.
22. Goyal L., McCall K., Agapite J., Hartwieg E., Steller H. Induction of apoptosis by Drosophila reaper, hid and grim through inhibition of IAP function. EMBO J. 2000, 19:589-597.
23. Hariharan I.K., Bilder D. Regulation of imaginal disc growth by tumor-suppressor genes in Drosophila. Annu. Rev. Genet. 2006, 40:335-361.
24. Hay B.A., Wolff T., Rubin G.M. Expression of baculovirus P35 prevents cell death in Drosophila. Development 1994, 120:2121-2129.
25. Hermiston M.L., Wong M.H., Gordon J.I. Forced expression of E-cadherin in the mouse intestinal epithelium slows cell migration and provides evidence for nonautonomous regulation of cell fate in a self-renewing system. Genes Dev. 1996, 10:985-996.
26. Igaki T. Correcting developmental errors by apoptosis: lessons from Drosophila JNK signaling. Apoptosis 2009, 14:1021-1028.
27. Igaki T., Pagliarini R.A., Xu T. Loss of cell polarity drives tumor growth and invasion through JNK activation in Drosophila. Curr. Biol. 2006, 16:1139-1146.
28. Jafar-Nejad H., Tien A.C., Acar M., Bellen H.J. Senseless and Daughterless confer neuronal identity to epithelial cells in the Drosophila wing margin. Development 2006, 133:1683-1692.
29. Jaiswal M., Agrawal N., Sinha P. Fat and Wingless signaling oppositely regulate epithelial cell-cell adhesion and distal wing development in Drosophila. Development 2006, 133:925-935.
30. Jamora C., Fuchs E. Intercellular adhesion, signalling and the cytoskeleton. Nat. Cell Biol. 2002, 4:E101-E108.
31. Janody F., Treisman J.E. Actin capping protein alpha maintains vestigial-expressing cells within the Drosophila wing disc epithelium. Development 2006, 133:3349-3357.
32. Jeanes A., Gottardi C.J., Yap A.S. Cadherins and cancer: how does cadherin dysfunction promote tumor progression?. Oncogene 2008, 27:6920-6929.
33. Karim F.D., Rubin G.M. Ectopic expression of activated Ras1 induces hyperplastic growth and increased cell death in Drosophila imaginal tissues. Development 1998, 125:1-9.
34. Kim J.Y., Lee Y.G., Kim M.Y., Byeon S.E., Rhee M.H., Park J., Katz D.R., Chain B.M., Cho J.Y. Src-mediated regulation of inflammatory responses by actin polymerization. Biochem. Pharmacol. 2009, 79:431-443.
35. Klein T., Arias A.M. Different spatial and temporal interactions between Notch, wingless, and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev. Biol. 1998, 194:196-212.
36. Kuranaga E., Kanuka H., Igaki T., Sawamoto K., Ichijo H., Okano H., Miura M. Reaper-mediated inhibition of DIAP1-induced DTRAF1 degradation results in activation of JNK in Drosophila. Nat. Cell Biol. 2002, 4:705-710.
37. Kurant E., Pai C.Y., Sharf R., Halachmi N., Sun Y.H., Salzberg A. Dorsotonals/homothorax, the Drosophila homologue of meis1, interacts with extradenticle in patterning of the embryonic PNS. Development 1998, 125:1037-1048.
38. Lee J.D., Treisman J.E. Sightless has homology to transmembrane acyltransferases and is required to generate active Hedgehog protein. Curr. Biol. 2001, 11:1147-1152.
39. Leong G.R., Goulding K.R., Amin N., Richardson H.E., Brumby A.M. Scribble mutants promote aPKC and JNK-dependent epithelial neoplasia independently of Crumbs. BMC Biol. 2009, 7:62.
40. Maitra S., Kulikauskas R.M., Gavilan H., Fehon R.G. The tumor suppressors Merlin and Expanded function cooperatively to modulate receptor endocytosis and signaling. Curr. Biol. 2006, 16:702-709.
41. Martin-Blanco E., Gampel A., Ring J., Virdee K., Kirov N., Tolkovsky A.M., Martinez-Arias A. Puckered encodes a phosphatase that mediates a feedback loop regulating JNK activity during dorsal closure in Drosophila. Genes Dev. 1998, 12:557-570.
42. McEwen D.G., Peifer M. Puckered, a Drosophila MAPK phosphatase, ensures cell viability by antagonizing JNK-induced apoptosis. Development 2005, 132:3935-3946.
43. Minn A.J., Gupta G.P., Siegel P.M., Bos P.D., Shu W., Giri D.D., Viale A., Olshen A.B., Gerald W.L., Massague J. Genes that mediate breast cancer metastasis to lung. Nature 2005, 436:518-524.
44. Neumann C.J., Cohen S.M. Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 1997, 124:871-880.
45. Nicolai M., Lasbleiz C., Dura J.M. Gain-of-function screen identifies a role of the Src64 oncogene in Drosophila mushroom body development. J. Neurobiol. 2003, 57:291-302.
46. Nienhaus U., Aegerter-Wilmsen T., Aegerter C.M. Determination of mechanical stress distribution in Drosophila wing discs using photoelasticity. Mech. Dev. 2009, 126:942-949.
47. Nolo R., Abbott L.A., Bellen H.J. Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 2000, 102:349-362.
48. Ollmann M., Young L.M., Di Como C.J., Karim F., Belvin M., Robertson S., Whittaker K., Demsky M., Fisher W.W., Buchman A., Duyk G., Friedman L., Prives C., Kopczynski C. Drosophila p53 is a structural and functional homolog of the tumor suppressor p53. Cell 2000, 101:91-101.
49. Orsulic S., Huber O., Aberle H., Arnold S., Kemler R. E-cadherin binding prevents beta-catenin nuclear localization and beta-catenin/LEF-1-mediated transactivation. J. Cell Sci. 1999, 112(Pt 8):1237-1245.
50. Pagliarini R.A., Xu T. A genetic screen in Drosophila for metastatic behavior. Science 2003, 302:1227-1231.
51. Panganiban G., Sebring A., Nagy L., Carroll S. The development of crustacean limbs and the evolution of arthropods. Science 1995, 270:1363-1366.
52. Peifer M., Pai L.M., Casey M. Phosphorylation of the Drosophila adherens junction protein Armadillo: roles for wingless signal and zeste-white 3 kinase. Dev. Biol. 1994, 166:543-556.
53. Perez-Garijo A., Shlevkov E., Morata G. The role of Dpp and Wg in compensatory proliferation and in the formation of hyperplastic overgrowths caused by apoptotic cells in the Drosophila wing disc. Development 2009, 136:1169-1177.
54. Prober D.A., Edgar B.A. Ras1 promotes cellular growth in the Drosophila wing. Cell 2000, 100:435-446.
55. Prober D.A., Edgar B.A. Interactions between Ras1, dMyc, and dPI3K signaling in the developing Drosophila wing. Genes Dev. 2002, 16:2286-2299.
56. Ryoo H.D., Bergmann A., Gonen H., Ciechanover A., Steller H. Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat. Cell Biol. 2002, 4:432-438.
57. Ryoo H.D., Gorenc T., Steller H. Apoptotic cells can induce compensatory cell proliferation through the JNK and the Wingless signaling pathways. Dev. Cell 2004, 7:491-501.
58. Sanson B., White P., Vincent J.P. Uncoupling cadherin-based adhesion from wingless signalling in Drosophila. Nature 1996, 383:627-630.
59. Sansores-Garcia L., Bossuyt W., Wada K.I., Yonemura S., Tao C., Sasaki H., Halder G. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 2011, 30:2325-2335.
60. Shindo M., Wada H., Kaido M., Tateno M., Aigaki T., Tsuda L., Hayashi S. Dual function of Src in the maintenance of adherens junctions during tracheal epithelial morphogenesis. Development 2008, 135:1355-1364.
61. Spradling A.C., Stern D., Beaton A., Rhem E.J., Laverty T., Mozden N., Misra S., Rubin G.M. The Berkeley Drosophila Genome Project gene disruption project: single P-element insertions mutating 25% of vital Drosophila genes. Genetics 1999, 153:135-177.
62. Stockinger A., Eger A., Wolf J., Beug H., Foisner R. E-cadherin regulates cell growth by modulating proliferation-dependent beta-catenin transcriptional activity. J. Cell Biol. 2001, 154:1185-1196.
63. Sun G., Irvine K.D. Regulation of Hippo signaling by Jun kinase signaling during compensatory cell proliferation and regeneration, and in neoplastic tumors. Dev. Biol. 2011, 350:139-151.
64. Tang C.Y., Sun Y.H. Use of mini-white as a reporter gene to screen for GAL4 insertions with spatially restricted expression pattern in the developing eye in Drosophila. Genesis 2002, 34:39-45.
65. Tepass U., Gruszynski-DeFeo E., Haag T.A., Omatyar L., Torok T., Hartenstein V. Shotgun encodes Drosophila E-cadherin and is preferentially required during cell rearrangement in the neurectoderm and other morphogenetically active epithelia. Genes Dev. 1996, 10:672-685.
66. Uemura T., Oda H., Kraut R., Hayashi S., Kotaoka Y., Takeichi M. Zygotic Drosophila E-cadherin expression is required for processes of dynamic epithelial cell rearrangement in the Drosophila embryo. Genes Dev. 1996, 10:659-671.
67. Uhlirova M., Bohmann D. JNK- and Fos-regulated Mmp1 expression cooperates with Ras to induce invasive tumors in Drosophila. EMBO J. 2006, 25:5294-5304.
68. Uhlirova M., Jasper H., Bohmann D. Non-cell-autonomous induction of tissue overgrowth by JNK/Ras cooperation in a Drosophila tumor model. Proc. Natl. Acad. Sci. U. S. A. 2005, 102:13123-13128.
69. van Roy F., Berx G. The cell-cell adhesion molecule E-cadherin. Cell. Mol. Life Sci. 2008, 65:3756-3788.
70. Vidal M., Larson D.E., Cagan R.L. Csk-deficient boundary cells are eliminated from normal Drosophila epithelia by exclusion, migration, and apoptosis. Dev. Cell 2006, 10:33-44.
71. Vidal M., Warner S., Read R., Cagan R.L. Differing Src signaling levels have distinct outcomes in Drosophila. Cancer Res. 2007, 67:10278-10285.
72. Wang S.L., Hawkins C.J., Yoo S.J., Muller H.A., Hay B.A. The Drosophila caspase inhibitor DIAP1 is essential for cell survival and is negatively regulated by HID. Cell 1999, 98:453-463.
73. Widmann T.J., Dahmann C. Wingless signaling and the control of cell shape in Drosophila wing imaginal discs. Dev. Biol. 2009, 334:161-173.
74. Winder S.J., Ayscough K.R. Actin-binding proteins. J. Cell Sci. 2005, 118:651-654.
75. Wodarz A., Hinz U., Engelbert M., Knust E. Expression of crumbs confers apical character on plasma membrane domains of ectodermal epithelia of Drosophila. Cell 1995, 82:67-76.
76. Wu M., Pastor-Pareja J.C., Xu T. Interaction between Ras(V12) and scribbled clones induces tumour growth and invasion. Nature 2010, 463:545-548.
77. Yoo S.J., Huh J.R., Muro I., Yu H., Wang L., Wang S.L., Feldman R.M., Clem R.J., Muller H.A., Hay B.A. Hid, Rpr and Grim negatively regulate DIAP1 levels through distinct mechanisms. Nat. Cell Biol. 2002, 4:416-424.
78. Zecca M., Basler K., Struhl G. Direct and long-range action of a wingless morphogen gradient. Cell 1996, 87:833-844.