The nucleolar protein Viriato/Nol12 is required for the growth and differentiation progression activities of the Dpp pathway during Drosophila eye development

Developmental Biology

Volumn 377, Issue 1, 2013, Pages 154-165

  Marinho, Joana ^a,b   Martins, Torcato ^a   Neto, Marta ^a,c   Casares, Fernando ^c   Pereira, Paulo S ^a  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF COIMBRA   (Portugal)

^c UNIVERSIDAD PABLO DE OLAVIDE   (Spain)

Author keywords

Cell proliferation; Dpp TGFbeta; Drosophila; Photoreceptor differentiation; Viriato Nol12

Indexed keywords

DECAPENTAPLEGIC PROTEIN; DROSOPHILA PROTEIN; NUCLEAR PROTEIN; NUCLEOLAR PROTEIN VIRIATO; SMAD PROTEIN; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 2; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; DIFFERENTIATION; DOWN REGULATION; DROSOPHILA; EYE DEVELOPMENT; GENE EXPRESSION; GENE INTERACTION; GENE TARGETING; GENETIC SCREENING; GROWTH; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RNA INTERFERENCE; SIGNAL TRANSDUCTION;

EID: 84876321493     PISSN: 00121606     EISSN: 1095564X     Source Type: Journal    
DOI: 10.1016/j.ydbio.2013.02.003     Document Type: Article

References (47)

1. Amore G., Casares F. Size matters: the contribution of cell proliferation to the progression of the specification Drosophila eye gene regulatory network. Dev. Biol. 2010, 344:569-577.
2. Bakal C., Linding R., Llense F., Heffern E., Martin-Blanco E., Pawson T., Perrimon N. Phosphorylation networks regulating JNK activity in diverse genetic backgrounds. Science 2008, 322:453-456.
3. Baryshnikova A., Costanzo M., Kim Y., Ding H., Koh J., Toufighi K., Youn J.-Y., Ou J., San Luis B.-J., Bandyopadhyay S., Hibbs M., Hess D., Gingras A.-C., Bader G.D., Troyanskaya O.G., Brown G.W., Andrews B., Boone C., Myers C.L. Quantitative analysis of fitness and genetic interactions in yeast on a genome scale. Nat. Meth. 2010, 7:1017-1024.
4. Bessa J., Gebelein B., Pichaud F., Casares F., Mann R.S. Combinatorial control of Drosophila eye development by eyeless, homothorax, and teashirt. Genes Dev. 2002, 16:2415-2427.
5. Blackman R.K., Sanicola M., Raftery L.A., Gillevet T., Gelbart W.M. An extensive 3' cis-regulatory region directs the imaginal disk expression of decapentaplegic, a member of the TGF-beta family in Drosophila. Development 1991, 111:657-666.
6. Brummel T., Abdollah S., Haerry T.E., Shimell M.J., Merriam J., Raftery L., Wrana J.L., O'Connor M.B. The Drosophila activin receptor baboon signals through dSmad2 and controls cell proliferation but not patterning during larval development. Genes Develop. 1999, 13:98-111.
7. Chanut F., Heberlein U. Role of decapentaplegic in initiation and progression of the morphogenetic furrow in the developing Drosophila retina. Development 1997, 124:559-567.
8. Chen X., Hiller M., Sancak Y., Fuller M.T. Tissue-specific TAFs counteract Polycomb to turn on terminal differentiation. Science 2005, 310:869-872.
9. Costanzo M., Baryshnikova A., Myers C.L., Andrews B., Boone C. Charting the genetic interaction map of a cell. Curr. Opin. Biotechnol. 2011, 22:66-74.
10. Crickmore M.A., Mann R.S. Hox control of organ size by regulation of morphogen production and mobility. Science 2006, 313:63-68.
11. Dixon S.J., Costanzo M., Baryshnikova A., Andrews B., Boone C. Systematic mapping of genetic interaction networks. Annu Rev. Genet. 2009, 43:601-625.
12. Djebali S., Davis C.A., Merkel A., Dobin A., Lassmann T., Mortazavi A., Tanzer A., Lagarde J., Lin W., Schlesinger F., Xue C., Marinov G.K., Khatun J., Williams B.A., Zaleski C., Rozowsky J., Roder M., Kokocinski F., Abdelhamid R.F., Alioto T., Antoshechkin I., Baer M.T., Bar N.S., Batut P., Bell K., Bell I., Chakrabortty S., Chen X., Chrast J., Curado J., Derrien T., Drenkow J., Dumais E., Dumais J., Duttagupta R., Falconnet E., Fastuca M., Fejes-Toth K., Ferreira P., Foissac S., Fullwood M.J., Gao H., Gonzalez D., Gordon A., Gunawardena H., Howald C., Jha S., Johnson R., Kapranov P., King B., Kingswood C., Luo O.J., Park E., Persaud K., Preall J.B., Ribeca P., Risk B., Robyr D., Sammeth M., Schaffer L., See L.H., Shahab A., Skancke J., Suzuki A.M., Takahashi H., Tilgner H., Trout D., Walters N., Wang H., Wrobel J., Yu Y., Ruan X., Hayashizaki Y., Harrow J., Gerstein M., Hubbard T., Reymond A., Antonarakis S.E., Hannon G., Giddings M.C., Ruan Y., Wold B., Carninci P., Guigo R., Gingeras T.R. Landscape of transcription in human cells. Nature 2012, 489:101-108.
13. Firth L.C., Baker N.E. Retinal determination genes as targets and possible effectors of extracellular signals. Dev. Biol. 2009, 327:366-375.
14. Horn T., Sandmann T., Fischer B., Axelsson E., Huber W., Boutros M. Mapping of signaling networks through synthetic genetic interaction analysis by RNAi. Nat. Meth. 2011, 8:341-346.
15. Jonikas M.C., Collins S.R., Denic V., Oh E., Quan E.M., Schmid V., Weibezahn J., Schwappach B., Walter P., Weissman J.S., Schuldiner M. Comprehensive characterization of genes required for protein folding in the endoplasmic reticulum. Science 2009, 323:1693-1697.
16. Kumar J.P. My what big eyes you have: how the Drosophila retina grows. Dev. Neurobiol. 2011, 71:1133-1152.
17. Lecuit T., Brook W.J., Ng M., Calleja M., Sun H., Cohen S.M. Two distinct mechanisms for long-range patterning by Decapentaplegic in the Drosophila wing. Nature 1996, 381:387-393.
18. Lecuit T., Cohen S.M. Dpp receptor levels contribute to shaping the Dpp morphogen gradient in the Drosophila wing imaginal disc. Development 1998, 125:4901-4907.
19. Li Z., Lee I., Moradi E., Hung N.J., Johnson A.W., Marcotte E.M. Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 2009, 7:e1000213.
20. Mani R., Onge R.P., Hartman J.L., Giaever G., Roth F.P. Defining genetic interaction. Proc. Natl. Acad. Sci. U.S.A. 2008, 105:3461-3466.
21. Mao Y., Freeman M. Fasciclin 2, the Drosophila orthologue of neural cell-adhesion molecule, inhibits EGF receptor signalling. Development 2009, 136:473-481.
22. Marinho J., Casares F., Pereira P.S. The Drosophila Nol12 homologue viriato is a dMyc target that regulates nucleolar architecture and is required for dMyc-stimulated cell growth. Development 2011, 138:349-357.
23. Mohr S., Bakal C., Perrimon N. Genomic screening with RNAi: results and challenges. Ann. Rev. Biochem. 2010, 79:37-64.
24. Murali T., Pacifico S., Yu J., Guest S., Roberts G.G., Finley R.L. DroID 2011: a comprehensive, integrated resource for protein, transcription factor, RNA and gene interactions for Drosophila. Nucl. Acids Res. 2011, 39:D736-743.
25. Nellen D., Burke R., Struhl G., Basler K. Direct and long-range action of a DPP morphogen gradient. Cell 1996, 85:357-368.
26. Oeffinger M., Zenklusen D., Ferguson A., Wei K.E., El Hage A., Tollervey D., Chait B.T., Singer R.H., Rout M.P. Rrp17p is a eukaryotic exonuclease required for 5' end processing of Pre-60S ribosomal RNA. Mol. Cell. 2009, 36:768-781.
27. Ostrin E.J., Li Y., Hoffman K., Liu J., Wang K., Zhang L., Mardon G., Chen R. Genome-wide identification of direct targets of the Drosophila retinal determination protein Eyeless. Genome Res. 2006, 16:466-476.
28. Pappu K.S., Chen R., Middlebrooks B.W., Woo C., Heberlein U., Mardon G. Mechanism of hedgehog signaling during Drosophila eye development. Development 2003, 130:3053-3062.
29. Peng W.T., Robinson M.D., Mnaimneh S., Krogan N.J., Cagney G., Morris Q., Davierwala A.P., Grigull J., Yang X., Zhang W., Mitsakakis N., Ryan O.W., Datta N., Jojic V., Pal C., Canadien V., Richards D., Beattie B., Wu L.F., Altschuler S.J., Roweis S., Frey B.J., Emili A., Greenblatt J.F., Hughes T.R. A panoramic view of yeast noncoding RNA processing. Cell 2003, 113:919-933.
30. Peterson A.J., Jensen P.A., Shimell M., Stefancsik R., Wijayatonge R., Herder R., Raftery L.A., O'Connor M.B. R-Smad competition controls activin receptor output in Drosophila. PLoS One 2012, 7:e36548.
31. Phillips P.C. Epistasis - the essential role of gene interactions in the structure and evolution of genetic systems. Nat. Rev. Genet. 2008, 9:855-867.
32. Pichaud F., Casares F. homothorax and iroquois-C genes are required for the establishment of territories within the developing eye disc. Mech. Dev. 2000, 96:15-25.
33. Pignoni F., Zipursky S.L. Induction of Drosophila eye development by decapentaplegic. Development 1997, 124:271-278.
34. Qu J., Bishop J.M. Nucleostemin maintains self-renewal of embryonic stem cells and promotes reprogramming of somatic cells to pluripotency. J. Cell Biol. 2012, 197:731-745.
35. Ranade S.S., Yang-Zhou D., Kong S.W., McDonald E.C., Cook T.A., Pignoni F. Analysis of the Otd-dependent transcriptome supports the evolutionary conservation of CRX/OTX/OTD functions in flies and vertebrates. Dev. Biol. 2008, 315:521-534.
36. Royet J., Finkelstein R. hedgehog, wingless and orthodenticle specify adult head development in Drosophila. Development 1996, 122:1849-1858.
37. Sahasranaman A., Dembowski J., Strahler J., Andrews P., Maddock J., Woolford J.L. Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: role of factors required for 27S pre-rRNA processing. Embo J. 2011, 30:4020-4032.
38. Sander V., Eivers E., Choi R.H., De Robertis E.M. Drosophila Smad2 opposes Mad Signaling during Wing vein development. PLoS One 2010, 5:e10383.
39. Shugo H., Ooshio T., Naito M., Naka K., Hoshii T., Tadokoro Y., Muraguchi T., Tamase A., Uema N., Yamashita T., Nakamoto Y., Suda T., Kaneko S., Hirao A. Nucleostemin in injury-induced liver regeneration. Stem Cells Dev 2012, 21:3044-3054.
40. Sisson J.C., Field C., Ventura R., Royou A., Sullivan W. Lava Lamp, a novel peripheral golgi protein, is required for Drosophila melanogaster cellularization. J. Cell Biol. 2000, 151:905-918.
41. Spencer F.A., Hoffmann F.M., Gelbart W.M. Decapentaplegic: a gene complex affecting morphogenesis in Drosophila melanogaster. Cell 1982, 28:451-461.
42. Tsai R.Y., McKay R.D. A nucleolar mechanism controlling cell proliferation in stem cells and cancer cells. Genes Dev. 2002, 16:2991-3003.
43. van Riggelen J., Yetil A., Felsher D.W. MYC as a regulator of ribosome biogenesis and protein synthesis. Nat. Rev. Cancer 2010, 10:301-309.
44. Wiersdorff V., Lecuit T., Cohen S.M., Mlodzik M. Mad acts downstream of Dpp receptors, revealing a differential requirement for dpp signaling in initiation and propagation of morphogenesis in the Drosophila eye. Development 1996, 122:2153-2162.
45. Woodhouse E.C., Fisher A., Bandle R.W., Bryant-Greenwood B., Charboneau L., Petricoin E.F., Liotta L.A. Drosophila screening model for metastasis: Semaphorin 5c is required for l(2)gl cancer phenotype. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:11463-11468.
46. Yuva-Aydemir Y., Bauke A.-C., Klambt C. Spinster controls Dpp signaling during glial migration in the Drosophila eye. J. Neurosci. 2011, 31:7005-7015.
47. Zecca M., Basler K., Struhl G. Sequential organizing activities of engrailed, hedgehog and decapentaplegic in the Drosophila wing. Development 1995, 121:2265-2278.