The microRNA pathway regulates the temporal pattern of Notch signaling in Drosophila follicle cells

Development

Volumn 138, Issue 9, 2011, Pages 1737-1745

  Poulton, John S ^a,c   Huang, Yi Chun ^a   Smith, Laila ^a   Sun, Jianjun ^a,d   Leake, Nicholas ^a   Schleede, Justin ^b,e   Stevens, Leslie M ^b   Deng, Wu Min ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

^c UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^d GEOPHYSICAL LABORATORY   (United States)

^e UNIVERSITY OF WISCONSIN MADISON   (United States)

Author keywords

Developmental timing; Drosophila; miRNA; Mitotic to endocycle switch; Oogenesis

Indexed keywords

MICRORNA; NOTCH RECEPTOR;

ANIMAL CELL; ARTICLE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL FUNCTION; CONTROLLED STUDY; DROSOPHILA; MUTATION; NONHUMAN; OOCYTE DEVELOPMENT; OVARY FOLLICLE CELL; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN DOMAIN; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DOWN-REGULATION; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEMALE; GENE EXPRESSION REGULATION; MEMBRANE PROTEINS; MICRORNAS; OOGENESIS; OVARIAN FOLLICLE; RECEPTORS, NOTCH; REPRESSOR PROTEINS; RNA HELICASES; SIGNAL TRANSDUCTION;

EID: 79955456131     PISSN: 09501991     EISSN: 14779129     Source Type: Journal    
DOI: 10.1242/dev.059352     Document Type: Article

References (58)

1. Ambrus, A. M. and Frolov, M. V. (2010). Mutation of the DEAD-box helicase belle downregulates the cyclin-dependent kinase inhibitor Dacapo. Cell Cycle 9, 1016-1020.
2. Ambrus, A. M., Nicolay, B. N., Rasheva, V. I., Suckling, R. J. and Frolov, M. V. (2007). dE2F2-independent rescue of proliferation in cells lacking an activator dE2F1. Mol. Cell. Biol. 27, 8561-8570.
3. Aravin, A. A., Hannon, G. J. and Brennecke, J. (2007). The Piwi-piRNA pathway provides an adaptive defense in the transposon arms race. Science 318, 761-764.
4. Artavanis-Tsakonas, S., Matsuno, K. and Fortini, M. E. (1995). Notch signaling. Science 268, 225-232.
5. Baker, N. E. (2007). Patterning signals and proliferation in Drosophila imaginal discs. Curr. Opin. Genet. Dev. 17, 287-293.
6. Bartel, D. P. (2009). MicroRNAs: target recognition and regulatory functions. Cell 136, 215-233.
7. Bender, M., Turner, F. R. and Kaufman, T. C. (1987). A development genetic analysis of the gene regulator of postbithorax in Drosophila melanogaster. Dev. Biol. 119, 418-432.
8. Brennecke, J., Hipfner, D. R., Stark, A., Russell, R. B. and Cohen, S. M. (2003). bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113, 25-36.
9. Calvi, B. R., Lilly, M. A. and Spradling, A. C. (1998). Cell cycle control of chorion gene amplification. Genes Dev. 12, 734-744.
10. Caygill, E. E. and Johnston, L. A. (2008). Temporal regulation of metamorphic processes in Drosophila by the let-7 and miR-125 heterochronic microRNAs. Curr. Biol. 18, 943-950.
11. Cordle, J., Johnson, S., Tay, J. Z., Roversi, P., Wilkin, M. B., de Madrid, B. H., Shimizu, H., Jensen, S., Whiteman, P., Jin, B. et al. (2008). A conserved face of the Jagged/Serrate DSL domain is involved in Notch trans-activation and cisinhibition. Nat. Struct. Mol. Biol. 15, 849-857.
12. Cox, D. N., Chao, A., Baker, J., Chang, L., Qiao, D. and Lin, H. (1998). A novel class of evolutionarily conserved genes defined by piwi are essential for stem cell self-renewal. Genes Dev. 12, 3715-3727.
13. de Celis, J. F. and Bray, S. (1997). Feed-back mechanisms affecting Notch activation at the dorsoventral boundary in the Drosophila wing. Development 124, 3241-3251.
14. de Celis, J. F., Mari-Beffa, M. and Garcia-Bellido, A. (1991). Cell-autonomous role of Notch, an epidermal growth factor homologue, in sensory organ differentiation in Drosophila. Proc. Natl. Acad. Sci. USA 88, 632-636.
15. de Celis, J. F., Tyler, D. M., de Celis, J. and Bray, S. J. (1998). Notch signalling mediates segmentation of the Drosophila leg. Development 125, 4617-4626.
16. 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.
17. Fiuza, U. M., Klein, T., Martinez Arias, A. and Hayward, P. (2010). Mechanisms of ligand-mediated inhibition in Notch signaling activity in Drosophila. Dev. Dyn. 239, 798-805.
18. Golic, K. G. (1991). Site-specific recombination between homologous chromosomes in Drosophila. Science 252, 958-961.
19. Inui, M., Martello, G. and Piccolo, S. (2010). MicroRNA control of signal transduction. Nat. Rev. Mol. Cell Biol. 11, 252-263.
20. Johnstone, O., Deuring, R., Bock, R., Linder, P., Fuller, M. T. and Lasko, P. (2005). Belle is a Drosophila DEAD-box protein required for viability and in the germ line. Dev. Biol. 277, 92-101.
21. Jones, W. K. and Rawls, J. M., Jr (1988). Genetic and molecular mapping of chromosome region 85A in Drosophila melanogaster. Genetics 120, 733-742.
22. Klein, T., Brennan, K. and Arias, A. M. (1997). An intrinsic dominant negative activity of serrate that is modulated during wing development in Drosophila. Dev. Biol. 189, 123-134.
23. Klusza, S. and Deng, W. M. (2011). At the crossroads of differentiation and proliferation: precise control of cell-cycle changes by multiple signaling pathways in Drosophila follicle cells. BioEssays 33, 124-134.
24. Kwon, C., Han, Z., Olson, E. N. and Srivastava, D. (2005). MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc. Natl. Acad. Sci. USA 102, 18986-18991.
25. Lai, E. C., Tam, B. and Rubin, G. M. (2005). Pervasive regulation of Drosophila Notch target genes by GY-box-, Brd-box-, and K-box-class microRNAs. Genes Dev. 19, 1067-1080.
26. Lee, T. and Luo, L. (1999). Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22, 451-461.
27. Lee, Y. S., Nakahara, K., Pham, J. W., Kim, K., He, Z., Sontheimer, E. J. and Carthew, R. W. (2004). Distinct roles for Drosophila Dicer-1 and Dicer-2 in the siRNA/miRNA silencing pathways. Cell 117, 69-81.
28. Li, Y. and Baker, N. E. (2004). The roles of cis-inactivation by Notch ligands and of neuralized during eye and bristle patterning in Drosophila. BMC Dev. Biol. 4, 5.
29. 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.
30. Martin, R., Smibert, P., Yalcin, A., Tyler, D. M., Schafer, U., Tuschl, T. and Lai, E. C. (2009). A Drosophila pasha mutant distinguishes the canonical microRNA and mirtron pathways. Mol. Cell. Biol. 29, 861-870.
31. Micchelli, C. A., Rulifson, E. J. and Blair, S. S. (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.
32. Miller, A. C., Lyons, E. L. and Herman, T. G. (2009). cis-Inhibition of Notch by endogenous Delta biases the outcome of lateral inhibition. Curr. Biol. 19, 1378-1383.
33. Okamura, K., Chung, W. J. and Lai, E. C. (2008). The long and short of inverted repeat genes in animals: microRNAs, mirtrons and hairpin RNAs. Cell Cycle 7, 2840-2845.
34. Poethig, R. S. (2009). Small RNAs and developmental timing in plants. Curr. Opin. Genet. Dev. 19, 374-378.
35. Portin, P. (2002). General outlines of the molecular genetics of the Notch signalling pathway in Drosophila melanogaster: a review. Hereditas 136, 89-96.
36. Poulton, J. S. and Deng, W. M. (2007). Cell-cell communication and axis specification in the Drosophila oocyte. Dev. Biol. 311, 1-10.
37. Rauskolb, C., Correia, T. and Irvine, K. D. (1999). Fringe-dependent separation of dorsal and ventral cells in the Drosophila wing. Nature 401, 476-480.
38. Rougvie, A. E. (2005). Intrinsic and extrinsic regulators of developmental timing: from miRNAs to nutritional cues. Development 132, 3787-3798.
39. Ruby, J. G., Stark, A., Johnston, W. K., Kellis, M., Bartel, D. P. and Lai, E. C. (2007). Evolution, biogenesis, expression, and target predictions of a substantially expanded set of Drosophila microRNAs. Genome Res. 17, 1850-1864.
40. Ruohola, H., Bremer, K. A., Baker, D., Swedlow, J. R., Jan, L. Y. and Jan, Y. N. (1991). Role of neurogenic genes in establishment of follicle cell fate and oocyte polarity during oogenesis in Drosophila. Cell 66, 433-449.
41. Sakamoto, K., Ohara, O., Takagi, M., Takeda, S. and Katsube, K. (2002). Intracellular cell-autonomous association of Notch and its ligands: a novel mechanism of Notch signal modification. Dev. Biol. 241, 313-326.
42. Schuldt, A. J., Adams, J. H., Davidson, C. M., Micklem, D. R., Haseloff, J., St Johnston, D. and Brand, A. H. (1998). Miranda mediates asymmetric protein and RNA localization in the developing nervous system. Genes Dev. 12, 1847-1857.
43. Silver, S. J., Hagen, J. W., Okamura, K., Perrimon, N. and Lai, E. C. (2007). Functional screening identifies miR-315 as a potent activator of Wingless signaling. Proc. Natl. Acad. Sci. USA 104, 18151-18156.
44. Sokol, N. S., Xu, P., Jan, Y. N. and Ambros, V. (2008). Drosophila let-7 microRNA is required for remodeling of the neuromusculature during metamorphosis. Genes Dev. 22, 1591-1596.
45. St Johnston, D., Beuchle, D. and Nusslein-Volhard, C. (1991). Staufen, a gene required to localize maternal RNAs in the Drosophila egg. Cell 66, 51-63.
46. Stark, A., Brennecke, J., Russell, R. B. and Cohen, S. M. (2003). Identification of Drosophila microRNA targets. PLoS Biol. 1, e60.
47. 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.
48. 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.
49. Sun, J., Smith, L., Armento, A. and Deng, W. M. (2008). Regulation of the endocycle/gene amplification switch by Notch and ecdysone signaling. J. Cell Biol. 182, 885-896.
50. Tennessen, J. M. and Thummel, C. S. (2008). Developmental timing: let-7 function conserved through evolution. Curr. Biol. 18, R707-R708.
51. Tien, A. C., Rajan, A. and Bellen, H. J. (2009). A Notch updated. J. Cell Biol. 184, 621-629.
52. Ulvila, J., Parikka, M., Kleino, A., Sormunen, R., Ezekowitz, R. A., Kocks, C. and Ramet, M. (2006). Double-stranded RNA is internalized by scavenger receptor-mediated endocytosis in Drosophila S2 cells. J. Biol. Chem. 281, 14370-14375.
53. Vallejo, D. M., Caparros, E. and Dominguez, M. (2011). Targeting Notch signalling by the conserved miR-8/200 microRNA family in development and cancer cells. EMBO J. 30, 756-769.
54. Wienholds, E. and Plasterk, R. H. (2005). MicroRNA function in animal development. FEBS Lett. 579, 5911-5922.
55. Worringer, K. A., Chu, F. and Panning, B. (2009). The zinc finger protein Zn72D and DEAD box helicase Belle interact and control maleless mRNA and protein levels. BMC Mol. Biol. 10, 33.
56. Wu, L. and Belasco, J. G. (2008). Let me count the ways: mechanisms of gene regulation by miRNAs and siRNAs. Mol. Cell 29, 1-7.
57. 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.
58. Zhou, R., Hotta, I., Denli, A. M., Hong, P., Perrimon, N. and Hannon, G. J. (2008). Comparative analysis of argonaute-dependent small RNA pathways in Drosophila. Mol. Cell 32, 592-599.