Growth suppressor lingerer regulates bantam microRNA to restrict organ size

Journal of Molecular Cell Biology

Volumn 7, Issue 5, 2015, Pages 415-428

  Dong, Liang ^a   Li, Jinhui ^a   Huang, Hongling ^a   Yin, Meng Xin ^a   Xu, Jinjin ^a   Li, Peixue ^a   Lu, Yi ^a   Wu, Wenqing ^a   Yang, Hang ^b   Zhao, Yun ^a,c   Zhang, Lei ^a,c  

^a INSTITUTE OF BIOCHEMISTRY AND CELL BIOLOGY   (China)

^b UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

^c SHANGHAITECH UNIVERSITY   (China)

Author keywords

bantam; Hippo; lingerer; Mad; organ size control; Salvador; Yorkie

Indexed keywords

LINGERER; MICRORNA; REGULATOR PROTEIN; SALVADOR PROTEIN; SCAFFOLD PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MAD; TRANSCRIPTION FACTOR YKI; UNCLASSIFIED DRUG; BANTAM MICRORNA, DROSOPHILA; CARRIER PROTEIN; DROSOPHILA PROTEIN; HPO PROTEIN, DROSOPHILA; LINGERER PROTEIN, DROSOPHILA; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; SIGNAL PEPTIDE; TRANSACTIVATOR PROTEIN; YORKIE PROTEIN, DROSOPHILA;

ARTICLE; BANTAM GENE; CARBOXY TERMINAL SEQUENCE; CELL GROWTH; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; GENE; GENE CONTROL; GENE EXPRESSION REGULATION; GENE OVEREXPRESSION; GENE TARGETING; GROWTH REGULATION; NONHUMAN; ORGAN SIZE; PROTEIN DEPLETION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; UPREGULATION; ANIMAL; GENETICS; METABOLISM; PHYSIOLOGY;

ANIMALS; CARRIER PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MICRORNAS; NUCLEAR PROTEINS; ORGAN SIZE; PROTEIN-SERINE-THREONINE KINASES; TRANS-ACTIVATORS;

EID: 84943516854     PISSN: 16742788     EISSN: 17594685     Source Type: Journal    
DOI: 10.1093/jmcb/mjv045     Document Type: Article

References (58)

1. Alarcon, C., Zaromytidou, A.I., Xi, Q., et al. (2009). Nuclear CDKsdrive Smad tran-scriptional activation and turnover in BMP and TGF-beta pathways. Cell 139, 757-769.
2. Baumgartner, R., Poernbacher, I., Buser, N., et al. (2010). The WW domain protein Kibra acts upstream of Hippo in Drosophila. Dev. Cell 18, 309-316.
3. Baumgartner, R., Stocker, H., and Hafen, E. (2013). The RNA-binding proteins FMR1, rasputin and caprin act together with the UBA protein lingerer to restrict tissue growth in Drosophila melanogaster. PLoS Genet. 9, e1003598.
4. 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.
5. Bischof, J., Maeda, R.K., Hediger, M., et al. (2007). An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl Acad. Sci. USA 104, 3312-3317.
6. Boggiano, J.C., Vanderzalm, P.J., and Fehon, R.G. (2011). Tao-1 phosphorylates Hippo/MST kinases to regulate the Hippo-Salvador-Warts tumor suppressor pathway. Dev. Cell 21, 888-895.
7. Brennecke, J., Hipfner, D.R., Stark, A., et al. (2003). bantam encodes a develop-mentally regulated microRNA that controls cell proliferation and regulatesthe proapoptotic gene hid in Drosophila. Cell 113, 25-36.
8. Codelia, V.A., and Irvine, K.D. (2012). Hippo signaling goes long range. Cell 150, 669-670.
9. Cziko, A.M., McCann, C.T., Howlett, I.C., et al. (2009). Genetic modifiers of dFMR1 encode RNA granule components in Drosophila. Genetics 182, 1051-1060.
10. Epstein, A.M., Bauer, C.R., Ho, A., et al. (2009). Drosophila Fragile X protein controls cellular proliferation by regulating cbl levels in the ovary. Dev. Biol. 330, 83-92.
11. Genevet, A., Wehr, M.C., Brain, R., et al. (2010). Kibra is a regulator of the Salvador/Warts/Hippo signaling network. Dev. Cell 18, 300-308.
12. Goulev, Y., Fauny, J.D., Gonzalez-Marti, B., et al. (2008). SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr. Biol. 18, 435-441.
13. Grzeschik, N.A., Parsons, L.M., Allott, M.L., et al. (2010). Lgl, aPKC, and Crumbs regulate the Salvador/Warts/Hippo pathway through two distinct mechanisms. Curr. Biol. 20, 573-581.
14. Halder, G., and Johnson, R.L. (2011). Hippo signaling: growth control and beyond. Development 138, 9-22.
15. Hamaratoglu, F., Willecke, M., Kango-Singh, M., et al. (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.
16. Harvey, K.F., Pfleger, C.M., and Hariharan, I.K. (2003). The Drosophila Mst ortho-log, hippo, restricts growthandcellproliferation andpromotesapoptosis. Cell 114, 457-467.
17. Harvey, K.F., Zhang, X., and Thomas, D.M.(2013). The Hippo pathway and human cancer. Nat. Rev. Cancer 13, 246-257.
18. Herranz, H., Hong, X., and Cohen, S.M. (2012). Mutual repression by bantam miRNA and Capicua links the EGFR/MAPK and Hippo pathways in growth control. Curr. Biol. 22, 651-657.
19. Hipfner, D.R., Weigmann, K., andCohen, S.M. (2002).Thebantamgeneregulates Drosophila growth. Genetics 161, 1527-1537.
20. Huang, J., Wu, S., Barrera, J., et al. (2005). The Hippo signaling pathway coordi-nately regulates cell proliferation and apoptosis by inactivating Yorkie, the Drosophila Homolog of YAP. Cell 122, 421-434.
21. Huang, H.L., Wang, S., Yin, M.X., et al. (2013). Par-1 regulates tissue growth by influencing hippo phosphorylation status and hippo-salvador association. PLoS Biol. 11, e1001620.
22. Huang, H., Li, J., Hu, L., et al. (2014). Bantam is essential for Drosophila intestinal stem cell proliferation in response to Hippo signaling. Dev. Biol. 385, 211-219.
23. Justice, R.W., Zilian, O., Woods, D.F., et al. (1995). The Drosophilatumor 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.
24. Kimura, S., Sakakibara, Y., Sato, K., et al. (2015). The Drosophila lingerer protein cooperates with Orb2 in long-term memory formation. J. Neurogenet. 29, 8-17.
25. Kuniyoshi, H., Baba, K., Ueda, R., et al. (2002). lingerer, a Drosophila gene involved in initiation and termination of copulation, encodes a set of novel cytoplasmic proteins. Genetics 162, 1775-1789.
26. Kuniyoshi, H., Usui-Aoki, K., Juni, N., et al. (2003). Expression analysis of the lingerer gene in the larval central nervous system of Drosophila melanogaster. J. Neurogenet. 17, 117-137.
27. Lai, Z.C., Wei, X., Shimizu, T., et al. (2005). Control of cell proliferation and apop-tosis by mob as tumor suppressor, mats. Cell 120, 675-685.
28. Lee, T., and Luo, L. (2001). Mosaic analysis with a repressible cell marker (MARCM) for Drosophila neural development. Trends Neurosci. 24, 251-254.
29. Naz, R.K., and Dhandapani, L. (2010). Identification of human sperm proteins that interact with human zona pellucida3 (ZP3) using yeast two-hybrid system. J. Reprod. Immunol. 84, 24-31.
30. Nolo, R., Morrison, C.M., Tao, C., et al. (2006).The bantammicroRNAisatargetof the hippo tumor-suppressor pathway. Curr. Biol. 16, 1895-1904.
31. Oh, H., and Irvine, K.D. (2011). Cooperative regulation of growth by Yorkie and Mad through bantam. Dev. Cell 20, 109-122.
32. Pan, D. (2010). The hippo signaling pathway in development and cancer. Dev. Cell 19, 491-505.
33. Pantalacci, S., Tapon, N., and Leopold, P. (2003). The Salvador partner Hippo promotes apoptosis and cell-cycle exit in Drosophila. Nat. Cell Biol. 5, 921-927.
34. Peng, H.W., Slattery, M., and Mann, R.S. (2009). Transcription factorchoiceinthe Hippo signaling pathway: homothorax and yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc. Genes Dev. 23, 2307-2319.
35. Poon, C.L., Lin, J.I., Zhang, X., et al. (2011). The sterile 20-like kinase Tao-1 con-trolstissue growthbyregulatingtheSalvador-Warts-Hippo pathway.Dev. Cell 21, 896-906.
36. Ramos, A., and Camargo, F.D. (2012). The Hippo signaling pathway and stem cell biology. Trends Cell Biol. 22, 339-346.
37. Robinson, B.S., Huang, J., Hong, Y., et al. (2010). Crumbs regulates Salvador/Warts/Hippo signaling in Drosophila via the FERM-domain protein Expanded. Curr. Biol. 20, 582-590.
38. Silva, E., Tsatskis, Y., Gardano, L., et al. (2006). The tumor-suppressor gene fat controls tissue growth upstream of expandedinthe hippo signaling pathway. Curr. Biol. 16, 2081-2089.
39. Tapon, N., Harvey, K.F., Bell, D.W., et al.(2002).salvador Promotesbothcellcycle exit and apoptosis in Drosophila and is mutated in human cancer cell lines. Cell 110, 467-478.
40. Thompson, B.J., and Cohen, S.M. (2006). The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126, 767-774.
41. Tsuneizumi, K., Nakayama, T., Kamoshida, Y., et al. (1997). Daughters against dpp modulates dpp organizing activity in Drosophila wing development. Nature 389, 627-631.
42. Udan, R.S., Kango-Singh, M., Nolo, R., et al.(2003).Hippo promotes proliferation arrest and apoptosis in the Salvador/Warts pathway. Nat. Cell Biol. 5, 914-920.
43. Varelas, X., Samavarchi-Tehrani, P., Narimatsu, M., et al. (2010). The Crumbs complex couples cell density sensing to Hippo-dependent control of the TGF-beta-SMAD pathway. Dev. Cell 19, 831-844.
44. Wilde, I.B., Brack, M., Winget, J.M., et al. (2011). Proteomic characterization of aggregating proteins after the inhibition of the ubiquitin proteasome system. J. Proteome Res. 10, 1062-1072.
45. Willecke, M., Hamaratoglu, F., Kango-Singh, M., et al. (2006). The fat cadherin acts through the hippo tumor-suppressor pathway to regulate tissue size. Curr. Biol. 16, 2090-2100.
46. Willecke, M., Hamaratoglu, F., Sansores-Garcia, L., et al. (2008). Boundaries of Dachsous Cadherin activity modulate the Hippo signaling pathway to induce cell proliferation. Proc. Natl Acad. Sci. USA 105, 14897-14902.
47. Wu, S., Huang, J., Dong, J., et al. (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.
48. Wu, S., Liu, Y., Zheng, Y., et al. (2008). The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev. Cell 14, 388-398.
49. Xu, T., Wang, W., Zhang, S., et al. (1995). Identifying tumor suppressors in genetic mosaics: the Drosophila lats gene encodes a putative protein kinase. Development 121, 1053-1063.
50. Yang, Y., Xu, S., Xia, L., et al. (2009). The bantam microRNA is associated with drosophila fragileXmental retardation protein and regulates the fateofgerm-line stem cells. PLoS Genet. 5, e1000444.
51. Yin, M., and Zhang, L. (2011). Hippo signaling: a hub of growth control, tumor suppression and pluripotency maintenance.J.Genet. Genomics 38, 471-481.
52. Yu, J., Zheng, Y., Dong, J., et al. (2010). Kibra functions as a tumor suppressor protein that regulates Hippo signaling in conjunction with Merlin and Expanded. Dev. Cell 18, 288-299.
53. Yu, F.X., Zhao, B., Panupinthu, N., et al. (2012). Regulation of the Hippo-YAP pathway by G-protein-coupled receptor signaling. Cell 150, 780-791.
54. Yue, T., Tian, A., and Jiang, J. (2012). The cell adhesion molecule echinoid functions as a tumor suppressor and upstream regulator of the Hippo signaling pathway. Dev. Cell 22, 255-267.
55. Zhang, L., Ren, F., Zhang, Q., et al. (2008). The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev. Cell 14, 377-387.
56. Zhao, Y., Tong, C., and Jiang, J. (2007). Hedgehogregulates smoothened activity by inducing a conformational switch. Nature 450, 252-258.
57. Zhao, B., Li, L., Lei, Q., et al. (2010). The Hippo-YAP pathwayinorgan size control and tumorigenesis: an updated version. Genes Dev. 24, 862-874.
58. Zhao, B., Tumaneng, K., and Guan, K.L. (2011). The Hippo pathwayin organ size control, tissue regeneration and stem cell self-renewal. Nat. Cell Biol. 13, 877-883.