The hippo pathway controls border cell migration through distinct mechanisms in outer border cells and polar cells of the drosophila ovary

Genetics

Volumn 198, Issue 3, 2014, Pages 1087-1099

  Lin, Tzu Huai ^a   Yeh, Tsung Han ^a   Wang, Tsu Wei ^a,b   Yu, Jenn Yah ^a  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b NATIONAL TAIWAN NORMAL UNIVERSITY   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

F ACTIN; HIPPO KINASE; JANUS KINASE; PHOSPHOTRANSFERASE; STAT PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; WARTS KINASE; YES ASSOCIATED PROTEIN; YORKIE PROTEIN; DROSOPHILA PROTEIN; GREEN FLUORESCENT PROTEIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CANCER INHIBITION; CELL FATE; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; EPITHELIAL MESENCHYMAL TRANSITION; FEMALE; GENE SILENCING; IN VITRO STUDY; MITOSIS; NONHUMAN; OOCYTE; OOCYTE DEVELOPMENT; OVARY; OVARY CELL; OVARY FOLLICLE CELL; POLAR BODY; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CELL AGGREGATION; CELL COUNT; CELL MOTION; CELL POLARITY; CYTOLOGY; DROSOPHILA MELANOGASTER; METABOLISM;

ANIMALS; CELL AGGREGATION; CELL COUNT; CELL MOVEMENT; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GREEN FLUORESCENT PROTEINS; JANUS KINASES; MODELS, BIOLOGICAL; OVARY; SIGNAL TRANSDUCTION; STAT TRANSCRIPTION FACTORS;

EID: 84908644994     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.167346     Document Type: Article

References (88)

1. Alarcon, C., A. I. Zaromytidou, Q. Xi, S. Gao, J. Yu et al., 2009 Nuclear CDKs drive Smad transcriptional activation and turnover in BMP and TGF-beta pathways. Cell 139: 757–769.
2. Badouel, C., A. Garg, and H. McNeill, 2009 Herding Hippos: regulating growth in flies and man. Curr. Opin. Cell Biol. 21: 837–843.
3. Bai, J., and D. Montell, 2002 Eyes absent, a key repressor of polar cell fate during Drosophila oogenesis. Development 129: 5377–5388.
4. 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 coactivator amplified in breast cancer. Cell 103: 1047–1058.
5. Beccari, S., L. Teixeira, and P. Rorth, 2002 The JAK/STAT pathway is required for border cell migration during Drosophila oogenesis. Mech. Dev. 111: 115–123.
6. Boggiano, J. C., P. J. Vanderzalm, and R. G. Fehon, 2011 Tao-1 phosphorylates Hippo/MST kinases to regulate the Hippo-Salvador-Warts tumor suppressor pathway. Dev. Cell 21: 888–895.
7. Borghese, L., G. Fletcher, J. Mathieu, A. Atzberger, W. C. Eades et al., 2006 Systematic analysis of the transcriptional switch inducing migration of border cells. Dev. Cell 10: 497–508.
8. Chen, H. J., C. M. Wang, T. W. Wang, G. J. Liaw, T. H. Hsu et al., 2011 The Hippo pathway controls polar cell fate through Notch signaling during Drosophila oogenesis. Dev. Biol. 357: 370–379.
9. Chen, J., and E. M. Verheyen, 2012 Homeodomain-interacting protein kinase regulates Yorkie activity to promote tissue growth. Curr. Biol. 22: 1582–1586.
10. Das Thakur, M., Y. Feng, R. Jagannathan, M. J. Seppa, J. B. Skeath et al., 2010 Ajuba LIM proteins are negative regulators of the Hippo signaling pathway. Curr. Biol. 20: 657–662.
11. Dong, J., G. Feldmann, J. Huang, S. Wu, N. Zhang et al., 2007 Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130: 1120–1133.
12. Duchek, P., and P. Rorth, 2001 Guidance of cell migration by EGF receptor signaling during Drosophila oogenesis. Science 291: 131–133.
13. Duchek, P., K. Somogyi, G. Jekely, S. Beccari, and P. Rorth, 2001 Guidance of cell migration by the Drosophila PDGF/VEGF receptor. Cell 107: 17–26.
14. Fernandez, B. G., P. Gaspar, C. Bras-Pereira, B. Jezowska, S. R. Rebelo et al., 2011 Actin-Capping Protein and the Hippo pathway regulate F-actin and tissue growth in Drosophila. Development 138: 2337–2346.
15. 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.
16. Ghiglione, C., O. Devergne, E. Georgenthum, F. Carballes, C. Medioni et al., 2002 The Drosophila cytokine receptor Domeless controls border cell migration and epithelial polarization during oogenesis. Development 129: 5437–5447.
17. Goulev, Y., J. D. Fauny, B. Gonzalez-Marti, D. Flagiello, J. Silber et al., 2008 SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr. Biol. 18: 435–441.
18. Halder, G., and R. L. Johnson, 2011 Hippo signaling: growth control and beyond. Development 138: 9–22.
19. Hall, C. A., R. Wang, J. Miao, E. Oliva, X. Shen et al., 2010 Hippo pathway effector Yap is an ovarian cancer oncogene. Cancer Res. 70: 8517–8525.
20. Harvey, K., and N. Tapon, 2007 The Salvador-Warts-Hippo pathway: an emerging tumour-suppressor network. Nat. Rev. Cancer 7: 182–191.
21. Harvey, K. F., C. M. Pfleger, and I. K. Hariharan, 2003 The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114: 457–467.
22. Harvey, K. F., X. Zhang, and D. M. Thomas, 2013 The Hippo pathway and human cancer. Nat. Rev. Cancer 13: 246–257.
23. Horne-Badovinac, S., and D. Bilder, 2005 Mass transit: epithelial morphogenesis in the Drosophila egg chamber. Dev. Dyn. 232: 559–574.
24. Hou, S. X., Z. Zheng, X. Chen, and N. Perrimon, 2002 The Jak/STAT pathway in model organisms: emerging roles in cell movement. Dev. Cell 3: 765–778.
25. Huang, J., and D. Kalderon, 2014 Coupling of Hedgehog and Hippo pathways promotes stem cell maintenance by stimulating proliferation. J. Cell Biol. 205: 325–338.
26. 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.
27. Inaki, M., S. Vishnu, A. Cliffe, and P. Rorth, 2012 Effective guidance of collective migration based on differences in cell states. Proc. Natl. Acad. Sci. USA 109: 2027–2032.
28. Jang, A. C., M. Starz-Gaiano, and D. J. Montell, 2007 Modeling migration and metastasis in Drosophila. J. Mammary Gland Biol. Neoplasia 12: 103–114.
29. 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.
30. Jukam, D., B. Xie, J. Rister, D. Terrell, M. Charlton-Perkins et al., 2013 Opposite feedbacks in the Hippo pathway for growth control and neural fate. Science 342: 1238016.
31. Justice, R. W., O. Zilian, D. F. Woods, M. Noll, and P. J. Bryant, 1995 The Drosophila tumor suppressor gene warts encodes a homolog of human myotonic dystrophy kinase and is required for the control of cell shape and proliferation. Genes Dev. 9: 534–546.
32. Karpowicz, P., J. Perez, and N. Perrimon, 2010 The Hippo tumor suppressor pathway regulates intestinal stem cell regeneration. Development 137: 4135–4145.
33. Lai, Z. C., X. Wei, T. Shimizu, E. Ramos, M. Rohrbaugh et al., 2005 Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 120: 675–685.
34. Lian, I., J. Kim, H. Okazawa, J. Zhao, B. Zhao et al., 2010 The role of YAP transcription coactivator in regulating stem cell self-renewal and differentiation. Genes Dev. 24: 1106–1118.
35. Lu, L., Y. Li, S. M. Kim, W. Bossuyt, P. Liu et al., 2010 Hippo signaling is a potent in vivo growth and tumor suppressor pathway in the mammalian liver. Proc. Natl. Acad. Sci. USA 107: 1437–1442.
36. Lucas, E. P., I. Khanal, P. Gaspar, G. C. Fletcher, C. Polesello et al., 2013 The Hippo pathway polarizes the actin cytoskeleton during collective migration of Drosophila border cells. J. Cell Biol. 201: 875–885.
37. Ma, H., H. Xu, and P. H. O’Farrell, 2014 Transmission of mitochondrial mutations and action of purifying selection in Drosophila melanogaster. Nat. Genet. 46: 393–397.
38. McDonald, J. A., E. M. Pinheiro, and D. J. Montell, 2003 PVF1, a PDGF/VEGF homolog, is sufficient to guide border cells and interacts genetically with Taiman. Development 130: 3469–3478.
39. McDonald, J. A., E. M. Pinheiro, L. Kadlec, T. Schupbach, and D. J. Montell, 2006 Multiple EGFR ligands participate in guiding migrating border cells. Dev. Biol. 296: 94–103.
40. McGuire, S. E., P. T. Le, A. J. Osborn, K. Matsumoto, and R. L. Davis, 2003 Spatiotemporal rescue of memory dysfunction in Drosophila. Science 302: 1765–1768.
41. Meignin, C., I. Alvarez-Garcia, I. Davis, and I. M. Palacios, 2007 The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr. Biol. 17: 1871–1878.
42. Montell, D. J., 2003 Border-cell migration: the race is on. Nat. Rev. Mol. Cell Biol. 4: 13–24.
43. Montell, D. J., P. Rorth, and A. C. Spradling, 1992 slow border cells, a locus required for a developmentally regulated cell migration during oogenesis, encodes Drosophila C/EBP. Cell 71: 51–62.
44. Nagaraj, R., S. Gururaja-Rao, K. T. Jones, M. Slattery, N. Negre et al., 2012 Control of mitochondrial structure and function by the Yorkie/YAP oncogenic pathway. Genes Dev. 26: 2027–2037.
45. Naora, H., and D. J. Montell, 2005 Ovarian cancer metastasis: integrating insights from disparate model organisms. Nat. Rev. Cancer 5: 355–366.
46. Oh, H., and K. D. Irvine, 2008 In vivo regulation of Yorkie phosphorylation and localization. Development 135: 1081–1088.
47. Oh, H., and K. D. Irvine, 2009 In vivo analysis of Yorkie phosphorylation sites. Oncogene 28: 1916–1927.
48. Oh, H., and K. D. Irvine, 2010 Yorkie: the final destination of Hippo signaling. Trends Cell Biol. 20: 410–417.
49. Ota, M., and H. Sasaki, 2008 Mammalian Tead proteins regulate cell proliferation and contact inhibition as transcriptional mediators of Hippo signaling. Development 135: 4059–4069.
50. Overholtzer, M., J. Zhang, G. A. Smolen, B. Muir, W. Li et al., 2006 Transforming properties of YAP, a candidate oncogene on the chromosome 11q22 amplicon. Proc. Natl. Acad. Sci. USA 103: 12405–12410.
51. Pan, D., 2010 The hippo signaling pathway in development and cancer. Dev. Cell 19: 491–505.
52. Pantalacci, S., N. Tapon, and P. Leopold, 2003 The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5: 921–927.
53. Peifer, M., S. Orsulic, D. Sweeton, and E. Wieschaus, 1993 A role for the Drosophila segment polarity gene armadillo in cell adhesion and cytoskeletal integrity during oogenesis. Development 118: 1191–1207.
54. Pinheiro, E. M., and D. J. Montell, 2004 Requirement for Par-6 and Bazooka in Drosophila border cell migration. Development 131: 5243–5251.
55. Poernbacher, I., R. Baumgartner, S. K. Marada, K. Edwards, and H. Stocker, 2012 Drosophila Pez acts in Hippo signaling to restrict intestinal stem cell proliferation. Curr. Biol. 22: 389–396.
56. Polesello, C., and N. Tapon, 2007 Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr. Biol. 17: 1864–1870.
57. Reddy, B. V., and K. D. Irvine, 2011 Regulation of Drosophila glial cell proliferation by Merlin-Hippo signaling. Development 138: 5201–5212.
58. Ren, F., B. Wang, T. Yue, E. Y. Yun, Y. T. Ip et al., 2010a Hippo signaling regulates Drosophila intestine stem cell proliferation through multiple pathways. Proc. Natl. Acad. Sci. USA 107: 21064–21069.
59. Ren, F., L. Zhang, and J. Jiang, 2010b Hippo signaling regulates Yorkie nuclear localization and activity through 14–3-3 dependent and independent mechanisms. Dev. Biol. 337: 303–312.
60. Rorth, P., K. Szabo, A. Bailey, T. Laverty, J. Rehm et al., 1998 Systematic gain-of-function genetics in Drosophila. Development 125: 1049–1057.
61. Rorth, P., K. Szabo, and G. Texido, 2000 The level of C/EBP protein is critical for cell migration during Drosophila oogenesis and is tightly controlled by regulated degradation. Mol. Cell 6: 23–30.
62. Ruohola, H., K. A. Bremer, D. Baker, J. R. Swedlow, L. Y. Jan et al., 1991 Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66: 433–449.
63. Sansores-Garcia, L., W. Bossuyt, K. Wada, S. Yonemura, C. Tao et al., 2011 Modulating F-actin organization induces organ growth by affecting the Hippo pathway. EMBO J. 30: 2325–2335.
64. Shaw, R. L., A. Kohlmaier, C. Polesello, C. Veelken, B. A. Edgar et al., 2010 The Hippo pathway regulates intestinal stem cell proliferation during Drosophila adult midgut regeneration. Development 137: 4147–4158.
65. 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.
66. Silver, D. L., E. R. Geisbrecht, and D. J. Montell, 2005 Requirement for JAK/STAT signaling throughout border cell migration in Drosophila. Development 132: 3483–3492.
67. Staley, B. K., and K. D. Irvine, 2010 Warts and Yorkie mediate intestinal regeneration by influencing stem cell proliferation. Curr. Biol. 20: 1580–1587.
68. Thiery, J. P., H. Acloque, R. Y. Huang, and M. A. Nieto, 2009 Epithelial-mesenchymal transitions in development and disease. Cell 139: 871–890.
69. Wang, X., J. Bo, T. Bridges, K. D. Dugan, T. C. Pan et al., 2006 Analysis of cell migration using whole-genome expression profiling of migratory cells in the Drosophila ovary. Dev. Cell 10: 483–495.
70. Wang, X., J. C. Adam, and D. Montell, 2007 Spatially localized Kuzbanian required for specific activation of Notch during border cell migration. Dev. Biol. 301: 532–540.
71. Wang, X., L. He, Y. I. Wu, K. M. Hahn, and D. J. Montell, 2010 Lightmediated activation reveals a key role for Rac in collective guidance of cell movement in vivo. Nat. Cell Biol. 12: 591–597.
72. Wang, Y. H., and M. L. Huang, 2010 Organogenesis and tumorigenesis: insight from the JAK/STAT pathway in the Drosophila eye. Dev. Dyn. 239: 2522–2533.
73. Watson, K. L., 1995 Drosophila warts–tumor suppressor and member of the myotonic dystrophy protein kinase family. Bio-Essays 17: 673–676.
74. Wei, X., T. Shimizu, and Z. C. Lai, 2007 Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. EMBO J. 26: 1772–1781.
75. 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.
76. Wu, S., Y. Liu, Y. Zheng, J. Dong, and D. Pan, 2008 The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev. Cell 14: 388–398.
77. Xu, M. Z., S. W. Chan, A. M. Liu, K. F. Wong, S. T. Fan et al., 2011 AXL receptor kinase is a mediator of YAP-dependent oncogenic functions in hepatocellular carcinoma. Oncogene 30: 1229–1240.
78. Xu, T., and G. M. Rubin, 1993 Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223–1237.
79. Yang, N., M. Inaki, A. Cliffe, and P. Rorth, 2012 Microtubules and Lis-1/NudE/dynein regulate invasive cell-on-cell migration in Drosophila. PLoS ONE 7: e40632.
80. Yu, J., J. Poulton, Y. C. Huang, and W. M. Deng, 2008 The hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation, and oocyte polarity. PLoS ONE 3: e1761.
81. Zeng, Q., and W. Hong, 2008 The emerging role of the hippo pathway in cell contact inhibition, organ size control, and cancer development in mammals. Cancer Cell 13: 188–192.
82. Zhang, J., J. Y. Ji, M. Yu, M. Overholtzer, G. A. Smolen et al., 2009 YAP-dependent induction of amphiregulin identifies a non-cell-autonomous component of the Hippo pathway. Nat. Cell Biol. 11: 1444–1450.
83. Zhang, L., F. Ren, Q. Zhang, Y. Chen, B. Wang et al., 2008 The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev. Cell 14: 377–387.
84. Zhang, T., Q. Zhou, and F. Pignoni, 2011a Yki/YAP, Sd/TEAD and Hth/MEIS control tissue specification in the Drosophila eye disc epithelium. PLoS ONE 6: e22278.
85. Zhang, X., J. George, S. Deb, J. L. Degoutin, E. A. Takano et al., 2011b The Hippo pathway transcriptional co-activator, YAP, is an ovarian cancer oncogene. Oncogene 30: 2810–2822.
86. Zhao, B., X. Ye, J. Yu, L. Li, W. Li et al., 2008a TEAD mediates YAP-dependent gene induction and growth control. Genes Dev. 22: 1962–1971.
87. Zhao, M., P. Szafranski, C. A. Hall, and S. Goode, 2008b Basolateral junctions utilize warts signaling to control epithelial-mesenchymal transition and proliferation crucial for migration and invasion of Drosophila ovarian epithelial cells. Genetics 178: 1947–1971.
88. Ziosi, M., L. A. Baena-Lopez, D. Grifoni, F. Froldi, A. Pession et al., 2010 dMyc functions downstream of Yorkie to promote the supercompetitive behavior of hippo pathway mutant cells. PLoS Genet. 6: e1001140.