Drosophila PI4KIIIalpha is required in follicle cells for oocyte polarization and Hippo signaling

Development

Volumn 138, Issue 9, 2011, Pages 1697-1703

  Yan, Yan ^a   Denef, Natalie ^a   Tang, Charm ^a   Schüpbach, Trudi ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Drosophila; Hippo signaling; Merlin; Oocyte polarity; PI4 kinase

Indexed keywords

MERLIN; PHOSPHATIDYLINOSITOL 4 KINASE III ALPHA; PHOSPHATIDYLINOSITOL KINASE; UNCLASSIFIED DRUG;

ANIMAL CELL; APICAL MEMBRANE; ARTICLE; CELL POLARITY; COMPLEX FORMATION; CONTROLLED STUDY; DROSOPHILA; FEMALE; GENE MUTATION; INTRACELLULAR SIGNALING; MUTATIONAL ANALYSIS; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; CELL POLARITY; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MUTATION; NEUROFIBROMIN 2; OOCYTES; OOGENESIS; OVARIAN FOLLICLE; PHENOTYPE; PHOSPHOTRANSFERASES (ALCOHOL GROUP ACCEPTOR); PROTEIN-SERINE-THREONINE KINASES; SIGNAL TRANSDUCTION;

EID: 79955427372     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.059279     Document Type: Article

References (69)

1. Audhya, A. and Emr, S. D. (2002). Stt4 PI 4-kinase localizes to the plasma membrane and functions in the Pkc1-mediated MAP kinase cascade. Dev. Cell 2, 593-605.
2. Audhya, A. M., Foti, M. and Emr, S. D. (2000). Distinct roles for the yeast phosphatidylinositol 4-kinases, Stt4p and Pik1p, in secretion, cell growth, and organelle membrane dynamics. Mol. Biol. Cell 11, 2673-2689.
3. Bach, E. A., Ekas, L. A., Ayala-Camargo, A., Flaherty, M. S., Lee, H., Perrimon, N. and Baeg, G. H. (2007). GFP reporters detect the activation of the Drosophila JAK/STAT pathway in vivo. Gene Expr. Patterns 7, 323-331.
4. Badouel, C., Gardano, L., Amin, N., Garg, A., Rosenfeld, R., Le Bihan, T. and McNeill, H. (2009). The FERM-domain protein expanded regulates Hippo pathway activity via direct interactions with the transcriptional activator Yorkie. Dev. Cell 16, 411-420.
5. Balla, A. and Balla, T. (2006). Phosphatidylinositol 4-kinases: old enzymes with emerging functions. Trends Cell Biol. 16, 351-361.
6. Barret, C., Roy, C., Montcourrier, P. and Niggli, V. (2000). Mutagenesis of the phosphatidylinositol 4,5-bisphosphate (PIP(2) binding site in the NH(2)-terminal domain of ezrin correlates with its altered cellular distribution. J. Cell Biol. 151, 1067-1080.
7. Baumgartner, R., Poernbacher, I., Buser, N., Hafen, E. and Stocker, H. (2010). The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev. Cell 18, 309-316.
8. Bennett, F. C. and Harvey, K. F. (2006). Fat cadherin modulates organ size in Drosophila via the Salvador/Warts/Hippo signaling pathway. Curr. Biol. 16, 2101-2110.
9. Boedigheimer, M. and Laughon, A. (1993). Expanded: a gene involved in the control of cell proliferation in imaginal discs. Development 118, 1291-1301.
10. Cho, E., Feng, Y., Rauskolb, C., Maitra, S., Fehon, R. and Irvine, K. D. (2006). Delineation of a fat tumor suppressor pathway. Nat. Genet. 38, 1142-1150.
11. Clark, I., Giniger, E., Ruohola-Baker, H., Jan, L. Y. and Jan Y. N. (1994). Transient posterior localization of a kinesin fusion protein reflects anteroposterior polarity of the Drosophila oocyte. Curr. Biol. 4, 289-300.
12. D'Alterio, C., Tran, D. D., Yeung, M. W., Hwang, M. S., Li, M. A., Arana, C. J., Mulligan, V. K., Kubesh, M., Sharma, P., Chase, M. et al. (2005). Drosophila melanogaster Cad99C, the orthologue of human Usher cadherin PCDH15, regulates the length of microvilli. J. Cell Biol. 171, 549-558.
13. Denef, N., Chen, Y., Weeks, S. D., Barcelo, G. and Schüpbach, T. (2008). Crag regulates epithelial architecture and polarized deposition of basement membrane proteins in Drosophila. Dev. Cell 14, 354-364.
14. Deng, W. M., Althauser, C. and Ruohola-Baker, H. (2001). Notch-Delta signaling induces a transition from mitotic cell cycle to endocycle in Drosophila follicle cells. Development 128, 4737-4746.
15. Dong, J., Feldmann, G., Huang, J., Wu, S., Zhang, N., Comerford, S. A., Gayyed, M. F., Anders, R. A., Maitra, A. and Pan, D. (2007). Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130, 1120-1133.
16. Duffy, J. B., Harrison, D. A. and Perrimon, N. (1998). Identifying loci required for follicular patterning using directed mosaics. Development 125, 2263-2271.
17. Edgar, B. A. (2006). From cell structure to transcription: Hippo forges a new path. Cell 124, 267-273.
18. Emoto, K., Parrish, J. Z., Jan, L. Y and Jan, Y. N. (2006). The tumour suppressor Hippo acts with the NDR kinases in dendritic tiling and maintenance. Nature 443, 210-213.
19. Fehon, R. G., McClatchey, A. I. and Bretscher, A. (2010). Organizing the cell cortex: the role of ERM proteins. Nat. Rev. Mol. Cell Biol. 11, 276-287.
20. Fievet, B. T., Gautreau, A., Roy, C., Del Maestro, L., Mangeat, P., Louvard, D. and Arpin, M. (2004). Phosphoinositide binding and phosphorylation act sequentially in the activation mechanism of ezrin. J. Cell Biol. 164, 653-659.
21. Genevet, A., Polesello, C., Blight, K., Robertson, F., Collinson, L. M., Pichaud, F. and Tapon, N. (2009). The Hippo pathway regulates apical-domain size independently of its growth-control function. J. Cell Sci. 122, 2360-2370.
22. Genevet, A., Wehr, M. C., Brain, R., Thompson, B. J. and Tapon, N. (2010). Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev. Cell 18, 300-308.
23. Gervais, L., Claret, S., Januschke, J., Roth, S. and Guichet, A. (2008). PIP5Kdependent production of PIP2 sustains microtubule organization to establish polarized transport in the Drosophila oocyte. Development 135, 3829-3838.
24. Gonzalez-Agosti, C., Wiederhold, T., Herndon, M. E., Gusella, J. and Ramesh, V. (1999). Interdomain interaction of merlin isoforms and its influence on intermolecular binding to NHE-RF. J. Biol. Chem. 274, 34438-34442.
25. Gonzalez-Reyes, A., Elliott, H. and St Johnston, D. (1995). Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375, 654-658.
26. Grusche, F. A., Richardson, H. E. and Harvey, K. F. (2010). Upstream regulation of the Hippo size control pathway. Curr. Biol. 20, R574-R582.
27. Grzeschik, N. A., Parsons, L. M., Allott, M. L., Harvey, K. F. and Richardson, H. E. (2010). Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 20, 573-581.
28. Hamaratoglu, F., Willecke, M., Kango-Singh, M., Nolo, R., Hyun, E., Tao, C., Jafar-Nejad, H. and Halder, G. (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.
29. Harvey, K. F., Pfleger, C. M. and Hariharan, I. K. (2003). The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114, 457-467.
30. Hay, B. A., Wassarman, D. A. and Rubin, G. M. (1995). Drosophila homologs of baculovirus inhibitor of apoptosis proteins function to block cell death. Cell 83, 1253-1262.
31. Huang, J., Wu, S., Barrera, J., Matthews, K. and Pan, D. (2005). The Hippo signaling pathway coordinately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila homolog of YAP. Cell 122, 421-434.
32. Justice, R. W., Zilian, O., Woods, D. F., Noll, M. and Bryant, P. J. (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.
33. Lai, Z. C., Wei, X., Shimizu, T., Ramos, E., Rohrbaugh, M., Nikolaidis, N., Ho, L. L. and Li, Y. (2005). Control of cell proliferation and apoptosis by mob as tumor suppressor, mats. Cell 120, 675-685.
34. Lopez-Schier, H. and St Johnston, D. (2001). Delta signaling from the germ line controls the proliferation and differentiation of the somatic follicle cells during Drosophila oogenesis. Genes Dev. 15, 1393-1405.
35. Maitra, S., Kulikauskas, R. M., Gavilan, H. and Fehon, R. G. (2006). The tumor suppressors Merlin and Expanded function cooperatively to modulate receptor endocytosis and signaling. Curr. Biol. 16, 702-709.
36. Marchler-Bauer, A., Anderson, J. B., Chitsaz, F., Derbyshire, M. K., DeWeese-Scott, C., Fong, J. H., Geer, R. C., Gonzales, N. R., Gwadz, M. and He, S. (2009). CDD: specific functional annotation with the conserved domain database. Nucleic Acids Res. 37, D205-D210.
37. McCartney, B. M. and Fehon, R. G. (1996). Distinct cellular and subcellular patterns of expression imply distinct functions for the Drosophila homologues of moesin and the neurofibromatosis 2 tumor suppressor, merlin. J. Cell Biol. 133, 843-852.
38. McCartney, B. M., Kulikauskas, R. M., LaJeunesse, D. R. and Fehon, R. G. (2000). The neurofibromatosis-2 homologue, Merlin, and the tumor suppressor expanded function together in Drosophila to regulate cell proliferation and differentiation. Development 127, 1315-1324.
39. McClatchey, A. I. and Fehon, R. G. (2009). Merlin and the ERM proteinsregulators of receptor distribution and signaling at the cell cortex. Trends Cell Biol. 19, 198-206.
40. Meignin, C., Alvarez-Garcia, I., Davis, I. and Palacios, I. M. (2007). The salvador-warts-hippo pathway is required for epithelial proliferation and axis specification in Drosophila. Curr. Biol. 17, 1871-1878.
41. Mikeladze-Dvali, T., Wernet, M. F., Pistillo, D., Mazzoni, E. O., Teleman, A. A., Chen, Y. W., Cohen, S., Desplan, C. et al. (2005). The growth regulators warts/lats and melted interact in a bistable loop to specify opposite fates in Drosophila R8 photoreceptors. Cell 122, 775-787.
42. Nakamura, F., Huang, L., Pestonjamasp, K., Luna, E. J. and Furthmayr, H. (1999). Regulation of F-actin binding to platelet moesin in vitro by both phosphorylation of threonine 558 and polyphosphatidylinositides. Mol. Biol. Cell 10, 2669-2685.
43. Okada, T., You, L. and Giancotti, F. G. (2007). Shedding light on Merlin's wizardry. Trends Cell Biol. 17, 222-229.
44. Pai, L. M., Barcelo, G. and Schüpbach, T. (2000). D-cbl, a negative regulator of the Egfr pathway, is required for dorsoventral patterning in Drosophila oogenesis. Cell 103, 51-61.
45. Pan, D. (2007). Hippo signaling in organ size control. Genes Dev. 21, 886-897.
46. Pantalacci, S., Tapon, N. and Léopold, P. (2003). The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5, 921-927.
47. Polesello, C. and Tapon, N. (2007). Salvador-warts-hippo signaling promotes Drosophila posterior follicle cell maturation downstream of notch. Curr. Biol. 17, 1864-1870.
48. Polevoy, G., Wei, H. C., Wong, R., Szentpetery, Z., Kim, Y. J., Goldbach, P., Steinbach, S. K., Balla, T. and Brill, J. A. (2009). Dual roles for the Drosophila PI 4-kinase four wheel drive in localizing Rab11 during cytokinesis. J. Cell Biol. 187, 847-858.
49. Raghu, P., Coessens, E., Manifava, M., Georgiev, P., Pettitt, T., Wood, E., Garcia-Murillas, I., Okkenhaug, H., Trivedi, D., Zhang, Q. et al. (2009). Rhabdomere biogenesis in Drosophila photoreceptors is acutely sensitive to phosphatidic acid levels. J. Cell Biol. 185, 129-145.
50. Robinson, B. S., Huang, J., Hong, Y. and Moberg, K. H. (2010). Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein expanded. Curr. Biol. 20, 582-590.
51. Rogulja, D., Rauskolb, C. and Irvine, K. D. (2008). Morphogen control of wing growth through the Fat signaling pathway. Dev. Cell 15, 309-321.
52. Roth, S. and Lynch, J. A. (2009). Symmetry breaking during Drosophila oogenesis. Cold Spring Harb. Perspect. Biol. 1, a001891.
53. Roth, S., Neuman-Silberberg, F. S., Barcelo, G. and Schüpbach, T. (1995). Cornichon and the EGF receptor signaling process are necessary for both anteriorposterior and dorsal-ventral pattern formation in Drosophila. Cell 81, 967-978.
54. Silva, E., Tsatskis, Y., Gardano, L., Tapon, N. and McNeill, H. (2006). The tumor-suppressor gene fat controls tissue growth upstream of expanded in the hippo signaling pathway. Curr. Biol. 16, 2081-2089.
55. Skwarek, L. C. and Boulianne, G. L. (2009). Great expectations for PIP: phosphoinositides as regulators of signaling during development and disease. Dev. Cell 16, 12-20.
56. St Johnston, D., Beuchle, D. and Nüsslein-Volhard, C. (1991). Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63.
57. Sun, J. and Deng, W. M. (2005). Notch-dependent downregulation of the homeodomain gene cut is required for the mitotic cycle/endocycle switch and cell differentiation in Drosophila follicle cells. Development 132, 4299-4308.
58. Sun, J. and Deng, W. M. (2007). Hindsight mediates the role of notch in suppressing hedgehog signaling and cell proliferation. Dev. Cell 12, 431-442.
59. Takeuchi, K., Sato, N., Kasahara, H., Funayama, N., Nagafuchi, A., Yonemura, S., Tsukita, S. and Tsukita, S. (1994). Perturbation of cell adhesion and microvilli formation by antisense oligonucleotides to ERM family members. J. Cell Biol. 125, 1371-1384.
60. Tapon, N., Harvey, K. F., Bell, D. W., Wahrer, D. C., Schiripo, T. A., Haber, D. A. and Hariharan, I. K. (2002). Salvador Promotes both cell cycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110, 467-478.
61. Udan, R. S., Kango-Singh, M., Nolo, R., Tao, C. and Halder, G. (2003). Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5, 914-920.
62. van Eeden, F. and St Johnston, D. (1999). The polarisation of the anteriorposterior and dorsal-ventral axes during Drosophila oogenesis. Curr. Opin. Genet. Dev. 9, 396-404.
63. Wei, X., Shimizu, T. and Lai, Z. C. (2007). Mob as tumor suppressor is activated by Hippo kinase for growth inhibition in Drosophila. EMBO J. 26, 1772-1781.
64. Willecke, M., Hamaratoglu, F., Kango-Singh, M., Udan, R., Chen, C. L., Tao, C., Zhang, X. and Halder, G. (2006). The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr. Biol. 16, 2090-2100.
65. Wu, S., Huang, J., Dong, J. and Pan, D. (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.
66. Xi, R., McGregor, J. R. and Harrison, D. A. (2003). A gradient of JAK pathway activity patterns the anterior-posterior axis of the follicular epithelium. Dev. Cell 4, 167-177.
67. Xu, T., Wang, W., Zhang, S., Stewart, R. A. and Yu, W. (1995). Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121, 1053-1063.
68. Yu, J., Poulton, J., Huang, Y. C. and Deng, W. M. (2008). The hippo pathway promotes Notch signaling in regulation of cell differentiation, proliferation, and oocyte polarity. PLoS One 3, e1761.
69. Yu, J., Zheng, Y., Dong, J., Klusza, S., Dang, W. M. and Pan, D. (2010). Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell 18, 288-299.