The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells

Journal of Cell Biology

Volumn 201, Issue 6, 2013, Pages 875-885

  Lucas, Eliana P ^a   Khanal, Ichha ^a   Gaspar, Pedro ^a   Fletcher, Georgina C ^a   Polesello, Cedric ^a   Tapon, Nicolas ^a   Thompson, Barry J ^a  

^a IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; TRANSCRIPTION FACTOR; TRANSCRIPTIONAL COACTIVATOR YORKIE; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ARTICLE; CELL MIGRATION; CELL POLARITY; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; NONHUMAN; POLARIZATION; POLYMERIZATION; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACTIN CAPPING PROTEINS; ACTIN CYTOSKELETON; ACTINS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL MOVEMENT; CELL POLARITY; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEEDBACK, PHYSIOLOGICAL; FEMALE; GREEN FLUORESCENT PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MALE; NUCLEAR PROTEINS; PHOSPHORYLATION; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSGENES;

ENA;

EID: 84880017102     PISSN: 00219525     EISSN: 15408140     Source Type: Journal    
DOI: 10.1083/jcb.201210073     Document Type: Article

References (70)

1. Abdelilah-Seyfried, S., D.N. Cox, and Y.N. Jan. 2003. Bazooka is a permissive factor for the invasive behavior of discs large tumor cells in Drosophila ovarian follicular epithelia. Development. 130:1927-1935. http://dx.doi.org/10.1242/dev.00420
2. Badouel, C., and H. McNeill. 2011. SnapShot: The hippo signaling pathway. Cell. 145:484-484: e1. http://dx.doi.org/10.1016/j.cell.2011.04.009
3. Bai, J., Y. Uehara, and D.J. Montell. 2000. Regulation of invasive cell behavior by taiman, a Drosophila protein related to AIB1, a steroid receptor co-activator amplifed in breast cancer. Cell. 103:1047-1058. http://dx.doi.org/10.1016/S0092-8674(00)00208-7
4. Baumgartner, R., I. Poernbacher, N. Buser, E. Hafen, and H. Stocker. 2010. The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev. Cell. 18:309-316. http://dx.doi.org/10.1016/j.devcel.2009.12.013
5. Bear, J.E., and F.B. Gertler. 2009. Ena/VASP: towards resolving a pointed controversy at the barbed end. J. Cell Sci. 122:1947-1953. http://dx.doi.org/10.1242/jcs.038125
6. Beccari, S., L. Teixeira, and P. Rørth. 2002. The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech. Dev. 111:115-123. http://dx.doi.org/10.1016/S0925-4773(01)00615-3
7. Bianco, A., M. Poukkula, A. Cliffe, J. Mathieu, C.M. Luque, T.A. Fulga, and P. Rørth. 2007. Two distinct modes of guidance signalling during collective migration of border cells. Nature. 448:362-365. http://dx.doi.org/10.1038/nature05965
8. Boggiano, J.C., and R.G. Fehon. 2012. Growth control by committee: intercellular junctions, cell polarity, and the cytoskeleton regulate Hippo signaling. Dev. Cell. 22:695-702. http://dx.doi.org/10.1016/j.devcel.2012.03.013
9. Borghese, L., G. Fletcher, J. Mathieu, A. Atzberger, W.C. Eades, R.L. Cagan, and P. Rørth. 2006. Systematic analysis of the transcriptional switch inducing migration of border cells. Dev. Cell. 10:497-508. http://dx.doi.org/10.1016/j.devcel.2006.02.004
10. Carmona-Fontaine, C., H.K. Matthews, S. Kuriyama, M. Moreno, G.A. Dunn, M. Parsons, C.D. Stern, and R. Mayor. 2008. Contact inhibition of locomotion in vivo controls neural crest directional migration. Nature. 456:957-961. http://dx.doi.org/10.1038/nature07441
11. Chen, C.L., K.M. Gajewski, F. Hamaratoglu, W. Bossuyt, L. Sansores-Garcia, C. Tao, and G. Halder. 2010. The apical-basal cell polarity determinant Crumbs regulates Hippo signaling in Drosophila. Proc. Natl. Acad. Sci. USA. 107:15810-15815. http://dx.doi.org/10.1073/pnas.1004060107
12. Cobreros-Reguera, L., A. Fernández-Miñán, C.H. Fernández-Espartero, H. López-Schier, A. González-Reyes, and M.D. Martín-Bermudo. 2010. The Ste20 kinase misshapen is essential for the invasive behaviour of ovarian epithelial cells in Drosophila. EMBO Rep. 11:943-949. http://dx.doi.org/10.1038/embor.2010.156
13. Condeelis, J., R.H. Singer, and J.E. Segall. 2005. The great escape: when cancer cells hijack the genes for chemotaxis and motility. Annu. Rev. Cell Dev. Biol. 21:695-718. http://dx.doi.org/10.1146/annurev.cellbio.21.122303.120306
14. Deng, Y., Y. Matsui, Y. Zhang, and Z.C. Lai. 2013. Hippo activation through homodimerization and membrane association for growth inhibition and organ size control. Dev. Biol. 375:152-159. http://dx.doi.org/10.1016/j.ydbio.2012.12.017
15. Dong, J., G. Feldmann, J. Huang, S. Wu, N. Zhang, S.A. Comerford, M.F. Gayyed, R.A. Anders, A. Maitra, and D. Pan. 2007. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell. 130:1120-1133. http://dx.doi.org/10.1016/j.cell.2007.07.019
16. Duchek, P., and P. Rørth. 2001. Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science. 291:131-133. http://dx.doi.org/10.1126/science.291.5501.131
17. Duchek, P., K. Somogyi, G. Jékely, S. Beccari, and P. Rørth. 2001. Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell. 107: 17-26. http://dx.doi.org/10.1016/S0092-8674(01)00502-5
18. Fernández, B.G., P. Gaspar, C. Brás-Pereira, B. Jezowska, S.R. Rebelo, and F. Janody. 2011. Actin-capping protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development. 138:2337-2346. http://dx.doi.org/10.1242/dev.063545
19. Fletcher, G., E. Lucas, R. Brain, A. Tournier, and B.J. Thompson. 2012. Positive feedback and mutual antagonism combine to polarise Crumbs in epithelial cells. Curr. Biol. 22:1116-1122. http://dx.doi.org/10.1016/j.cub.2012.04.020
20. Friedl, P., and D. Gilmour. 2009. Collective cell migration in morphogenesis, regeneration and cancer. Nat. Rev. Mol. Cell Biol. 10:445-457. http://dx.doi.org/10.1038/nrm2720
21. Fulga, T.A., and P. Rørth. 2002. Invasive cell migration is initiated by guided growth of long cellular extensions. Nat. Cell Biol. 4:715-719. http://dx.doi.org/10.1038/ncb848
22. Gates, J., S.H. Nowotarski, H. Yin, J.P. Mahaffey, T. Bridges, C. Herrera, C.C. Homem, F. Janody, D.J. Montell, and M. Peifer. 2009. Enabled and Capping protein play important roles in shaping cell behavior during Drosophila oogenesis. Dev. Biol. 333:90-107. http://dx.doi.org/10.1016/j.ydbio.2009.06.030
23. Genevet, A., M.C. Wehr, R. Brain, B.J. Thompson, and N. Tapon. 2010. Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev. Cell. 18:300-308. http://dx.doi.org/10.1016/j.devcel.2009.12.011
24. Grusche, F.A., H.E. Richardson, and K.F. Harvey. 2010. Upstream regulation of the hippo size control pathway. Curr. Biol. 20:R574-R582. http://dx.doi.org/10.1016/j.cub.2010.05.023
25. Grzeschik, N.A., L.M. Parsons, M.L. Allott, K.F. Harvey, and H.E. Richardson. 2010. Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 20:573-581. http://dx.doi.org/10.1016/j.cub.2010.01.055
26. Halder, G., and R.L. Johnson. 2011. Hippo signaling: growth control and beyond. Development. 138:9-22. http://dx.doi.org/10.1242/dev.045500
27. Hamaratoglu, F., M. Willecke, M. Kango-Singh, R. Nolo, E. Hyun, C. Tao, H. Jafar-Nejad, and G. Halder. 2006. The tumour-suppressor genes NF2/Merlin and Expanded act through Hippo signalling to regulate cell proliferation and apoptosis. Nat. Cell Biol. 8:27-36. http://dx.doi.org/10.1038/ncb1339
28. Hidalgo-Carcedo, C., S. Hooper, S.I. Chaudhry, P. Williamson, K. Harrington, B. Leitinger, and E. Sahai. 2011. Collective cell migration requires suppression of actomyosin at cell-cell contacts mediated by DDR1 and the cell polarity regulators Par3 and Par6. Nat. Cell Biol. 13:49-58. http://dx.doi.org/10.1038/ncb2133
29. Huang, J., S. Wu, J. Barrera, K. Matthews, and D. Pan. 2005. The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell. 122:421-434. http://dx.doi.org/10.1016/j.cell.2005.06.007
30. Jang, A.C., Y.C. Chang, J. Bai, and D. Montell. 2009. Border-cell migration requires integration of spatial and temporal signals by the BTB protein Abrupt. Nat. Cell Biol. 11:569-579. http://dx.doi.org/10.1038/ncb1863
31. Jia, J., W. Zhang, B. Wang, R. Trinko, and J. Jiang. 2003. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes Dev. 17:2514-2519. http://dx.doi.org/10.1101/gad.1134003
32. Kim, N.G., E. Koh, X. Chen, and B.M. Gumbiner. 2011. E-cadherin mediates contact inhibition of proliferation through Hippo signaling-pathway components. Proc. Natl. Acad. Sci. USA. 108:11930-11935. http://dx.doi.org/10.1073/pnas.1103345108
33. Lee, T., and L. Luo. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron. 22:451- 461. http://dx.doi.org/10.1016/S0896-6273(00)80701-1
34. Ling, C., Y. Zheng, F. Yin, J. Yu, J. Huang, Y. Hong, S. Wu, and D. Pan. 2010. The apical transmembrane protein Crumbs functions as a tumor suppressor that regulates Hippo signaling by binding to Expanded. Proc. Natl. Acad. Sci. USA. 107:10532-10537. http://dx.doi.org/10.1073/pnas.1004279107
35. McDonald, J.A., E.M. Pinheiro, and D.J. Montell. 2003. PVF1, a PDGF/VEGF homolog, is suffcient to guide border cells and interacts genetically with Taiman. Development. 130:3469-3478. http://dx.doi.org/10.1242/dev.00574
36. McDonald, J.A., A. Khodyakova, G. Aranjuez, C. Dudley, and D.J. Montell. 2008. PAR-1 kinase regulates epithelial detachment and directional protrusion of migrating border cells. Curr. Biol. 18:1659-1667. http://dx.doi.org/10.1016/j.cub.2008.09.041
37. Montell, D.J. 2008. Morphogenetic cell movements: diversity from modular mechanical properties. Science. 322:1502-1505. http://dx.doi.org/10.1126/science.1164073
38. Montell, D.J., P. Rorth, and A.C. Spradling. 1992. slow border cells, a locus required for a developmentally regulated cell migration during oogen-esis, encodes Drosophila C/EBP. Cell. 71:51-62. http://dx.doi.org/10.1016/0092-8674(92)90265-E
39. Niewiadomska, P., D. Godt, and U. Tepass. 1999. DE-Cadherin is required for intercellular motility during Drosophila oogenesis. J. Cell Biol. 144:533- 547. http://dx.doi.org/10.1083/jcb.144.3.533
40. Oh, H., and K.D. Irvine. 2008. In vivo regulation of Yorkie phosphoryla-tion and localization. Development. 135:1081-1088. http://dx.doi.org/10.1242/dev.015255
41. Oh, H., and K.D. Irvine. 2009. In vivo analysis of Yorkie phosphorylation sites. Oncogene. 28:1916-1927. http://dx.doi.org/10.1038/onc.2009.43
42. Oh, H., and K.D. Irvine. 2010. Yorkie: the fnal destination of Hippo signaling. Trends Cell Biol. 20:410-417. http://dx.doi.org/10.1016/j.tcb.2010.04.005
43. Pacquelet, A., and P. Rørth. 2005. Regulatory mechanisms required for DE-cadherin function in cell migration and other types of adhesion. J. Cell Biol. 170:803-812. http://dx.doi.org/10.1083/jcb.200506131
44. Pan, D. 2010. The hippo signaling pathway in development and cancer. Dev. Cell. 19:491-505. http://dx.doi.org/10.1016/j.devcel.2010.09.011
45. Pignoni, F., and S.L. Zipursky. 1997. Induction of Drosophila eye development by decapentaplegic. Development. 124:271-278.
46. Pinheiro, E.M., and D.J. Montell. 2004. Requirement for Par-6 and Bazooka in Drosophila border cell migration. Development. 131:5243-5251. http://dx.doi.org/10.1242/dev.01412
47. Poukkula, M., A. Cliffe, R. Changede, and P. Rørth. 2011. Cell behaviors regulated by guidance cues in collective migration of border cells. J. Cell Biol. 192:513-524. http://dx.doi.org/10.1083/jcb.201010003
48. Rauskolb, C., G. Pan, B.V. Reddy, H. Oh, and K.D. Irvine. 2011. Zyxin links fat signaling to the hippo pathway. PLoS Biol. 9:e1000624. http://dx.doi.org/10.1371/journal.pbio.1000624
49. Ridley, A.J. 2011. Life at the leading edge. Cell. 145:1012-1022. http://dx.doi.org/10.1016/j.cell.2011.06.010
50. Rørth, P. 2009. Collective cell migration. Annu. Rev. Cell Dev. Biol. 25:407-429. http://dx.doi.org/10.1146/annurev.cellbio.042308.113231
51. Rørth, P., K. Szabo, A. Bailey, T. Laverty, J. Rehm, G.M. Rubin, K. Weigmann, M. Milán, V. Benes, W. Ansorge, and S.M. Cohen. 1998. Systematic gain-of-function genetics in Drosophila. Development. 125:1049-1057.
52. Sahai, E. 2005. Mechanisms of cancer cell invasion. Curr. Opin. Genet. Dev. 15:87-96. http://dx.doi.org/10.1016/j.gde.2004.12.002
53. Sansores-Garcia, L., W. Bossuyt, K. Wada, S. Yonemura, C. Tao, H. Sasaki, and G. Halder. 2011. Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 30:2325-2335. http://dx.doi.org/10.1038/emboj.2011.157
54. Shaw, R.L., A. Kohlmaier, C. Polesello, C. Veelken, B.A. Edgar, and N. Tapon. 2010. The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development. 137:4147-4158. http://dx.doi.org/10.1242/dev.052506
55. Silver, D.L., and D.J. Montell. 2001. Paracrine signaling through the JAK/STAT pathway activates invasive behavior of ovarian epithelial cells in Drosophila. Cell. 107:831-841. http://dx.doi.org/10.1016/S0092-8674(01)00607-9
56. Somogyi, K., and P. Rørth. 2004. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev. Cell. 7:85-93. http://dx.doi.org/10.1016/j.devcel.2004.05.020
57. Staley, B.K., and K.D. Irvine. 2010. Warts and Yorkie mediate intestinal regeneration by infuencing stem cell proliferation. Curr. Biol. 20:1580-1587. http://dx.doi.org/10.1016/j.cub.2010.07.041
58. Starz-Gaiano, M., and D.J. Montell, 2004. Genes that drive invasion and migration in Drosophila. Curr. Opin. Genet. Dev. 14:86-91. http://dx.doi.org/10.1016/j.gde.2003.12.001
59. Sudol, M., and K.F. Harvey. 2010. Modularity in the Hippo signaling pathway. Trends Biochem. Sci. 35:627-633. http://dx.doi.org/10.1016/j.tibs.2010.05.010
60. Tepass, U. 2012. The apical polarity protein network in Drosophila epithelial cells: regulation of polarity, junctions, morphogenesis, cell growth, and survival. Annu. Rev. Cell Dev. Biol. 28:655-685. http://dx.doi.org/10.1146/annurev-cellbio-092910-154033
61. Udan, R.S., M. Kango-Singh, R. Nolo, C. Tao, and G. Halder. 2003. Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5:914-920. http://dx.doi.org/10.1038/ncb1050
62. Van Haastert, P.J., and P.N. Devreotes. 2004. Chemotaxis: signalling the way forward. Nat. Rev. Mol. Cell Biol. 5:626-634. http://dx.doi.org/10.1038/nrm1435
63. Wada, K., K. Itoga, T. Okano, S. Yonemura, and H. Sasaki. 2011. Hippo pathway regulation by cell morphology and stress fbers. Development. 138: 3907-3914. http://dx.doi.org/10.1242/dev.070987
64. Weijer, C.J. 2009. Collective cell migration in development. J. Cell Sci. 122:3215-3223. http://dx.doi.org/10.1242/jcs.036517
65. Wu, S., J. Huang, J. Dong, and D. Pan. 2003. hippo encodes a Ste-20 family protein kinase that restricts cell proliferation and promotes apoptosis in conjunction with salvador and warts. Cell. 114:445-456. http://dx.doi.org/10.1016/S0092-8674(03)00549-X
66. Xi, R., J.R. McGregor, and D.A. Harrison. 2003. A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium. Dev. Cell. 4:167-177. http://dx.doi.org/10.1016/S1534-5807(02)00412-4
67. Xu, T., and G.M. Rubin. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development. 117:1223-1237.
68. Xu, T., W. Wang, S. Zhang, R.A. Stewart, and W. Yu. 1995. Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development. 121:1053-1063.
69. Yu, J., Y. Zheng, J. Dong, S. Klusza, W.M. Deng, and D. Pan. 2010. Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell. 18:288-299. http://dx.doi.org/10.1016/j.devcel.2009.12.012
70. Zhao, B., X. Wei, W. Li, R.S. Udan, Q. Yang, J. Kim, J. Xie, T. Ikenoue, J. Yu, L. Li, et al. 2007. Inactivation of YAP oncoprotein by the Hippo pathway is involved in cell contact inhibition and tissue growth control. Genes Dev. 21:2747-2761. http://dx.doi.org/10.1101/gad.1602907