Transcription factor choice in the Hippo signaling pathway: Homothorax and yorkie regulation of the microRNA bantam in the progenitor domain of the Drosophila eye imaginal disc

Genes and Development

Volumn 23, Issue 19, 2009, Pages 2307-2319

  Peng, H Wayne ^a   Slattery, Matthew ^a   Mann, Richard S ^a  

^a NewYork Presbyterian Hospital   (United States)

Author keywords

Apoptosis; Cell proliferation; Drosophila eye development; Hippo signaling pathway; Homothorax; Yorkie

Indexed keywords

DNA BINDING PROTEIN; GENE PRODUCT; MICRORNA; PROTEIN HIPPO; PROTEIN HOMOTHORAX; PROTEIN SCALLOPED; PROTEIN TEASHIRT; PROTEIN YORKIE; TRANSCRIPTION FACTOR; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BANTAM GENE; CELL CLONE; CELL PROLIFERATION; CELL PROTECTION; CELL SURVIVAL; CONTROLLED STUDY; DNA SEQUENCE; DROSOPHILA; EYE DEVELOPMENT; GENE; GENETIC EPISTASIS; HOMOTHORAX GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; STEM CELL; UPREGULATION; YORKIE GENE;

ANIMALS; CELL LINE; CELL PROLIFERATION; CELL SURVIVAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EYE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HOMEODOMAIN PROTEINS; MICRORNAS; NUCLEAR PROTEINS; PROTEIN BINDING; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS;

ANIMALIA;

EID: 70349624119     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1820009     Document Type: Article

References (58)

1. Azpiazu N, Morata G. 2000. Function and regulation of homothorax in the wing imaginal disc of Drosophila. Development 127: 2685-2693. (Pubitemid 30426815)
2. Bessa J, Casares F. 2005. Restricted teashirt expression confers eye-specific responsiveness to Dpp and Wg signals during eye specification in Drosophila. Development 132: 5011-5020. (Pubitemid 41764012)
3. Bessa J, Gebelein B, Pichaud F, Casares F, Mann RS. 2002. Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes & Dev 16: 2415-2427. (Pubitemid 35034410)
4. Brennecke J, Hipfner DR, Stark A, Russell RB, Cohen SM. 2003. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113: 25-36. (Pubitemid 36411957)
5. Campbell S, Inamdar M, Rodrigues V, Raghavan V, Palazzolo M, Chovnick A. 1992. The scalloped gene encodes a novel, evolutionarily conserved transcription factor required for sensory organ differentiation in Drosophila. Genes & Dev 6: 367-379.
6. Casares F, Mann RS. 2000. A dual role for homothorax in inhibiting wing blade development and specifying proximal wing identities in Drosophila. Development 127: 1499-1508. (Pubitemid 30232600)
7. Culi J, Mann RS. 2003. Boca, an endoplasmic reticulum protein required for wingless signaling and trafficking of LDL receptor family members in Drosophila. Cell 112: 343-354. (Pubitemid 36187420)
8. de la Cova C, Abril M, Bellosta P, Gallant P, Johnston LA. 2004. Drosophila myc regulates organ size by inducing cell competition. Cell 117: 107-116. (Pubitemid 38469902)
9. Desplan C. 1997. Eye development: Governed by a dictator or a junta? Cell 91: 861-864.
10. Dominguez M, Ferres-Marco D, Gutierrez-Avino FJ, Speicher SA, Beneyto M. 2004. Growth and specification of the eye are controlled independently by Eyegone and Eyeless in Drosophila melanogaster. Nat Genet 36: 31-39. (Pubitemid 38056205)
11. Dong J, Feldmann G, Huang J, Wu S, Zhang N, Comerford SA, Gayyed MF, Anders RA, Maitra A, Pan D. 2007. Elucidation of a universal size-control mechanism in Drosophila and mammals. Cell 130: 1120-1133. (Pubitemid 47410268)
12. Ekas LA, Baeg GH, Flaherty MS, Ayala-Camargo A, Bach EA. 2006. JAK/STATsignaling promotes regional specification by negatively regulating wingless expression in Drosophila. Development 133: 4721-4729. (Pubitemid 46063084)
13. Estella C, Mann RS. 2008. Logic of Wg and Dpp induction of distal and medial fates in the Drosophila leg. Development 135: 627-636.
14. Fasano L, Roder L, Core N, Alexandre E, Vola C, Jacq B, Kerridge S. 1991. The gene teashirt is required for the development of Drosophila embryonic trunk segments and encodes a protein with widely spaced zinc finger motifs. Cell 64: 63-79. (Pubitemid 121001139)
15. Firth LC, Baker NE. 2005. Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye. Dev Cell 8: 541-551.
16. Gehring WJ. 1996. The master control gene for morphogenesis and evolution of the eye. Genes Cells 1: 11-15.
17. Goulev Y, Fauny JD, Gonzalez-Marti B, Flagiello D, Silber J, Zider A. 2008. SCALLOPED interacts with YORKIE, the nuclear effector of the hippo tumor-suppressor pathway in Drosophila. Curr Biol 18: 435-441.
18. Harvey KF, Pfleger CM, Hariharan IK. 2003. The Drosophila Mst ortholog, hippo, restricts growth and cell proliferation and promotes apoptosis. Cell 114: 457-467.
19. Hipfner DR, Weigmann K, Cohen SM. 2002. The bantam gene regulates Drosophila growth. Genetics 161: 1527-1537. (Pubitemid 35014754)
20. Hou XS, Melnick MB, Perrimon N. 1996. Marelle acts down-stream of the Drosophila HOP/JAK kinase and encodes a protein similar to the mammalian STATs. Cell 84: 411-419. (Pubitemid 26058566)
21. Huang J, Wu S, Barrera J, Matthews K, 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. (Pubitemid 41127143)
22. Jia J, Zhang W, Wang B, Trinko R, Jiang J. 2003. The Drosophila Ste20 family kinase dMST functions as a tumor suppressor by restricting cell proliferation and promoting apoptosis. Genes & Dev 17: 2514-2519. (Pubitemid 37271421)
23. Kenyon KL, Ranade SS, Curtiss J, Mlodzik M, Pignoni F. 2003. Coordinating proliferation and tissue specification to promote regional identity in the Drosophila head. Dev Cell 5: 403-414. (Pubitemid 37107670)
24. Laugier E, Yang Z, Fasano L, Kerridge S, Vola C. 2005. A critical role of teashirt for patterning the ventral epidermis is masked by ectopic expression of tiptop, a paralog of teashirt in Drosophila. Dev Biol 283: 446-458. (Pubitemid 40977962)
25. Lee T, Luo L. 1999. Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22: 451-461. (Pubitemid 29159845)
26. Lee JD, Treisman JE. 2001. The role of Wingless signaling in establishing the anteroposterior and dorsoventral axes of the eye disc. Development 128: 1519-1529.
27. McKay DJ, Estella C, Mann RS. 2009. The origins of the Drosophila leg revealed by the cis-regulatory architecture of the Distalless gene. Development 136: 61-71.
28. Morante J, Desplan C, Celik A. 2007. Generating patterned arrays of photoreceptors. Curr Opin Genet Dev 17: 314-319.
29. Morata G, Martin FA. 2007. Cell competition: The embrace of death. Dev Cell 13: 1-2.
30. Moreno E, Basler K. 2004. dMyc transforms cells into super-competitors. Cell 117: 117-129.
31. Nolo R, Morrison CM, Tao C, Zhang X, Halder G. 2006. The bantam microRNA is a target of the hippo tumor-suppressor pathway. Curr Biol 16: 1895-1904. (Pubitemid 44486764)
32. Noro B, Culi J, McKay DJ, Zhang W, Mann RS. 2006. Distinct functions of homeodomain-containing and homeodomainless isoforms encoded by homothorax. Genes & Dev 20: 1636-1650. (Pubitemid 43901102)
33. Oh H, Irvine KD. 2008. In vivo regulation of Yorkie phosphorylation and localization. Development 135: 1081-1088.
34. Pan D. 2007. Hippo signaling in organ size control. Genes & Dev 21: 886-897. (Pubitemid 46625638)
35. Pichaud F, Casares F. 2000. homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc. Mech Dev 96: 15-25. (Pubitemid 30625263)
36. Ready DF, Hanson TE, Benzer S. 1976. Development of the Drosophila retina, a neurocrystalline lattice. Dev Biol 53: 217-240.
37. Richardson H, O'Keefe LV, Marty T, Saint R. 1995. Ectopic cyclin E expression induces premature entry into S phase and disrupts pattern formation in the Drosophila eye imaginal disc. Development 121: 3371-3379.
38. Rieckhof GE, Casares F, Ryoo HD, Abu-Shaar M, Mann RS. 1997. Nuclear translocation of extradenticle requires homothorax, which encodes an extradenticle-related homeodomain protein. Cell 91: 171-183. (Pubitemid 27456385)
39. Silver SJ, Rebay I. 2005. Signaling circuitries in development: Insights from the retinal determination gene network. Development 132: 3-13. (Pubitemid 40207962)
40. Simpson P, Morata G. 1981. Differential mitotic rates and patterns of growth in compartments in the Drosophila wing. Dev Biol 85: 299-308. (Pubitemid 13142508)
41. Srivastava A, Simmonds AJ, Garg A, Fossheim L, Campbell SD, Bell JB. 2004. Molecular and functional analysis of scalloped recessive lethal alleles in Drosophila melanogaster. Genetics 166: 1833-1843. (Pubitemid 38621064)
42. Stowers RS, Schwarz TL. 1999. A genetic method for generating Drosophila eyes composed exclusively of mitotic clones of a single genotype. Genetics 152: 1631-1639.
43. Struhl G, Basler K. 1993. Organizing activity of wingless protein in Drosophila. Cell 72: 527-540. (Pubitemid 23077741)
44. Thompson BJ, Cohen SM. 2006. The Hippo pathway regulates the bantam microRNA to control cell proliferation and apoptosis in Drosophila. Cell 126: 767-774.
45. Treisman JE, Heberlein U. 1998. Eye development in Drosophila: Formation of the eye field and control of differentiation. Curr Top Dev Biol 39: 119-158.
46. Tsai YC, Yao JG, Chen PH, Posakony JW, Barolo S, Kim J, Sun YH. 2007. Upd/Jak/STAT signaling represses wg transcription to allow initiation of morphogenetic furrow in Drosophila eye development. Dev Biol 306: 760-771. (Pubitemid 46881068)
47. Udan RS, Kango-Singh M, Nolo R, Tao C, Halder G. 2003. Hippo promotes proliferation arrest and apoptosis in the Salvador/ Warts pathway. Nat Cell Biol 5: 914-920. (Pubitemid 37220698)
48. Wu J, Cohen SM. 2000. Proximal distal axis formation in the Drosophila leg: Distinct functions of teashirt and homothorax in the proximal leg. Mech Dev 94: 47-56. (Pubitemid 30332387)
49. Wu J, Cohen SM. 2002. Repression of Teashirt marks the initiation of wing development. Development 129: 2411-2418. (Pubitemid 34863849)
50. Wu S, Huang J, Dong J, 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. (Pubitemid 37100993)
51. Wu S, Liu Y, Zheng Y, Dong J, Pan D. 2008. The TEAD/TEF family protein Scalloped mediates transcriptional output of the Hippo growth-regulatory pathway. Dev Cell 14: 388-398.
52. Xu T, Rubin GM. 1993. Analysis of genetic mosaics in developing and adult Drosophila tissues. Development 117: 1223-1237. (Pubitemid 23154489)
53. Yang Y, Xu S, Xia L, Wang J, Wen S, Jin P, Chen D. 2009. The bantam microRNA is associated with drosophila fragile X mental retardation protein and regulates the fate of germline stem cells. PLoS Genet 5: e1000444. doi: 10.1371/journal. pgen.1000444.
54. Zhang J, Smolen GA, Haber DA. 2008. Negative regulation of YAP by LATS1 underscores evolutionary conservation of the Drosophila Hippo pathway. Cancer Res 68: 2789-2794. (Pubitemid 351556277)
55. Zhang L, Ren F, Zhang Q, Chen Y, Wang B, Jiang J. 2008. The TEAD/TEF family of transcription factor Scalloped mediates Hippo signaling in organ size control. Dev Cell 14: 377-387.
56. Zhang L, Yue T, Jiang J. 2009. Hippo signaling pathway and organ size control. Fly (Austin) 3: 68-73.
57. Zhao B, Ye X, Yu J, Li L, Li W, Li S, Yu J, Lin JD, Wang CY, Chinnaiyan AM, et al. 2008. TEAD mediates YAP-dependent gene induction and growth control. Genes & Dev 22: 1962-1971. (Pubitemid 352008643)
58. Zirin JD, Mann RS. 2004. Differing strategies for the establishment and maintenance of teashirt and homothorax repression in the Drosophila wing. Development 131: 5683-5693.