A Wingless and Notch double-repression mechanism regulates G1-S transition in the Drosophila wing

EMBO Journal

Volumn 27, Issue 11, 2008, Pages 1633-1645

  Herranz, Héctor ^a   Pérez, Lidia ^a   Martín, Francisco A ^b   Milán, Marco ^a  

^a INSTITUCIÓ CATALANA DE RECERCA I ESTUDIS AVANÇATS ICREA   (Spain)

^b CENTRO DE BIOLOGÍA MOLECULAR SEVERO OCHOA   (Spain)

Author keywords

Bantam; dMyc; E2F; Micro RNA

Indexed keywords

MICRORNA; NOTCH RECEPTOR; TRANSCRIPTION FACTOR E2F; WNT1 PROTEIN; BANTAM MICRORNA, DROSOPHILA; DIMINUTIVE PROTEIN, DROSOPHILA; DNA BINDING PROTEIN; DROSOPHILA PROTEIN; NOTCH PROTEIN, DROSOPHILA; ONCOPROTEIN; REPRESSOR PROTEIN; TRANSCRIPTION FACTOR; WINGLESS PROTEIN, DROSOPHILA;

ARTICLE; BANTAM GENE; CELL CYCLE G1 PHASE; CELL CYCLE PHASE; CELL CYCLE PROGRESSION; CELL CYCLE REGULATION; CELL CYCLE S PHASE; CELL PROLIFERATION; CONTROLLED STUDY; DMYC GENE; DROSOPHILA; FORELIMB; GENE EXPRESSION; MOLECULE; NONHUMAN; ONCOGENE; PRIMORDIUM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; ANIMAL; CYTOLOGY; DROSOPHILA MELANOGASTER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM;

ANIMALS; DNA-BINDING PROTEINS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; G1 PHASE; MICRORNAS; PROTO-ONCOGENE PROTEINS; RECEPTORS, NOTCH; REPRESSOR PROTEINS; S PHASE; TRANSCRIPTION FACTORS; WING;

EID: 44649171784     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2008.84     Document Type: Article

References (47)

1. Asano M, Wharton RP (1999) E2F mediates developmental and cell cycle regulation of ORC1 in Drosophila. EMBO J 18: 2435-2448
2. Axelrod JD, Matsuno K, Artavanis-Tsakonas S, Perrimon N (1996) Interaction between wingless and Notch signaling pathways mediated by Dishevelled. Science 271: 1826-1832
3. Baena-Lopez LA, Garcia-Bellido A (2003) Genetic requirements of vestigial in the regulation of Drosophila wing development. Development 130: 197-208
4. Baonza A, Freeman M (2005) Control of cell proliferation in the Drosophila eye by Notch signaling. Dev Cell 8: 529-539
5. Bienz M, Clevers H (2000) Linking colorectal cancer to Wnt signaling. Cell 103: 311-320
6. Blair SS, Brower DL, Thomas JB, Zavortink M (1994) The role of apterous in the control of dorsoventral compartmentalization and PS integrin gene expression in the developing wing of Drosophila. Development 120: 1805-1815
7. Bray SJ (2006) Notch signalling: a simple pathway becomes complex. Nat Rev Mol Cell Biol 7: 678-689
8. 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
9. Buceta J, Herranz H, Canela-Xandri O, Reigada R, Sagues F, Milan M (2007) Robustness and stability of the gene regulatory network involved in DV boundary formation in the Drosophila wing. PLoS ONE 2: e602
10. Clevers H (2006) Wnt/beta-catenin signaling in development and disease. Cell 127: 469-480
11. de Celis JF, Bray S (1997) Feedback mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124: 3241-3251
12. de Celis JF, Garcia-Bellido A, Bray SJ (1996) Activation and function of Notch at the dorsal-ventral boundary of the wing imaginal disc. Development 122: 359-369
13. Diaz-Benjumea FJ, Cohen SM (1993) Interaction between dorsal and ventral cells in the imaginal disc directs wing development in Drosophila. Cell 75: 741-752
14. Diaz-Benjumea FJ, Cohen SM (1995) Serrate signals through Notch to establish a Wingless-dependent organizer at the dorsal/ventral compartment boundary of the Drosophila wing. Development 121: 4215-4225
15. Duman-Scheel M, Johnston LA, Du W (2004) Repression of dMyc expression by Wingless promotes Rbf-induced G1 arrest in the presumptive Drosophila wing margin. Proc Natl Acad Sci USA 101: 3857-3862
16. Dyson N (1998) The regulation of E2F by pRB-family proteins. Genes Dev 12: 2245-2262
17. Firth LC, Baker NE (2005) Extracellular signals responsible for spatially regulated proliferation in the differentiating Drosophila eye. Dev Cell 8: 541-551
18. García-Bellido A, Merriam JR (1971) Parameters of the wing imaginal disc development of Drosophila melanogaster. Dev Biol 24: 61-87
19. Giraldez AJ, Cohen SM (2003) Wingless and Notch signaling provide cell survival cues and control cell proliferation during wing development. Development 130: 6533-6543
20. Giraldez AJ, Perez L, Cohen SM (2002) A naturally occurring alternative product of the mastermind locus that represses notch signalling. Mech Dev 115: 101-105
21. Helms W, Lee H, Ammerman M, Parks AL, Muskavitch MA, Yedvobnick B (1999) Engineered truncations in the Drosophila mastermind protein disrupt Notch pathway function. Dev Biol 215: 358-374
22. Herranz H, Stamataki E, Feiguin F, Milan M (2006) Self-refinement of Notch activity through the transmembrane protein Crumbs: modulation of gamma-secretase activity. EMBO Rep 7: 297-302
23. Irvine K, Wieschaus E (1994) fringe, a boundary specific signalling molecule, mediates interactions between dorsal and ventral cells during Drosophila wing development. Cell 79: 595-606
24. Johnston LA, Edgar BA (1998) Wingless and Notch regulate cell-cycle arrest in the developing Drosophila wing. Nature 394: 82-84
25. Johnston LA, Prober DA, Edgar BA, Eisenman RN, Gallant P (1999) Drosophila myc regulates cellular growth during development. Cell 98: 779-790
26. Johnston LA, Sanders AL (2003) Wingless promotes cell survival but constrains growth during Drosophila wing development. Nat Cell Biol 5: 827-833
27. Klein T, Arias AM (1998) Different spatial and temporal interactions between Notch, wingless, and vestigial specify proximal and distal pattern elements of the wing in Drosophila. Dev Biol 194: 196-212
28. Knoblich JA, Sauer K, Jones L, Richardson H, Saint R, Lehner CF (1994) Cyclin E controls S phase progression and its downregulation during Drosophila embryogenesis is required for the arrest of cell proliferation. Cell 77: 107-120
29. Logan CY, Nusse R (2004) The Wnt signaling pathway in development and disease. Annu Rev Cell Dev Biol 20: 781-810
30. Madhavan MM, Schneiderman HA (1977) Histological analysis of the dynamics of growth of imaginal discs and histoblast nests during the larval development of Drosophila melanogaster. Rouxs Arch Dev Biol 183: 269-305
31. McGuire SE, Mao Z, Davis RL (2004) Spatiotemporal gene expression targeting with the TARGET and gene-switch systems in Drosophila. Sci STKE 2004: pl6
32. Micchelli CA, Rulifson EJ, Blair SS (1997) The function and regulation of cut expression on the wing margin of Drosophila: Notch, Wingless and a dominant negative role for Delta and Serrate. Development 124: 1485-1495
33. Milan M, Campuzano S, Garcia-Bellído A (1996) Cell-cycling and patterned cell proliferation in the wing primordium of Drosophila. Proc Natl Acad Sci USA 93: 640-645
34. Neufeld TP, de la Cruz AF, Johnston LA, Edgar BA (1998) Coordination of growth and cell division in the Drosophila wing. Cell 93: 1183-1193
35. Neumann CJ, Cohen SM (1997) Long-range action of Wingless organizes the dorsal-ventral axis of the Drosophila wing. Development 124: 871-880
36. Neumann CJ, Cohen SM (1998) Boundary formation in the Drosophila wing: the POU-domain protein Nubbin attenuates Notch activity. Science 281: 409-413
37. Nolo R, Abbott LA, Bellen HJ (2000) Senseless, a Zn finger transcription factor, is necessary and sufficient for sensory organ development in Drosophila. Cell 102: 349-362
38. O'Brochta DA, Bryant PJ (1985) A zone of non-proliferating cells at a lineage restriction boundary in Drosophila. Nature 313: 138-141
39. Phillips R, Whittle JRS (1993) wingless expression mediates determination of peripheral nervous system elements in late stages of Drosophila wing disc development. Development 118: 427-438
40. Radtke F, Raj K (2003) The role of Notch in tumorigenesis: oncogene or tumour suppressor? Nat Rev Cancer 3: 756-767
41. Rulifson EJ, Micchelli CA, Axelrod JD, Perrimon N, Blair SS (1996) wingless refines its own expression domain on the Drosophila wing margin. Nature 384: 72-74
42. Sharma VM, Calvo JA, Draheim KM, Cunningham LA, Hermance N, Beverly L, Krishnamoorthy V, Bhasin M, Capobianco AJ, Kelliher MA (2006) Notch1 contributes to mouse T-cell leukemia by directly inducing the expression of c-myc. Mol Cell Biol 26: 8022-8031
43. Strigini M, Cohen SM (2000) Wingless gradient formation in the Drosophila wing. Curr Biol 10: 293-300
44. Wehrli M, Dougan ST, Caldwell K, O'Keefe L, Schwartz S, Vaizel-Ohayon D, Schejter E, Tomlinson A, DiNardo S (2000) arrow encodes an LDL-receptor-related protein essential for Wingless signalling. Nature 407: 527-530
45. Weng AP, Millholland JM, Yashiro-Ohtani Y, Arcangeli ML, Lau A, Wai C, Del Bianco C, Rodriguez CG, Sai H, Tobias J, Li Y, Wolfe MS, Shachaf C, Felsher D, Blacklow SC, Pear WS, Aster JC (2006) c-Myc is an important direct target of Notch1 in T-cell acute lymphoblastic leukemia/lymphoma. Genes Dev 20: 2096-2109
46. Zecca M, Basler K, Struhl G (1996) Direct and long-range action of a Wingless morphogen gradient. Cell 87: 833-844
47. Zecca M, Struhl G (2007) Recruitment of cells into the Drosophila wing primordium by a feed-forward circuit of vestigial autoregulation. Development 134: 3001-3010