Analysis of RNA interference lines identifies new functions of maternally-expressed genes involved in embryonic patterning in drosophila melanogaster

G3: Genes, Genomes, Genetics

Volumn 5, Issue 6, 2015, Pages 1025-1034

  Liu, Niankun ^a   Lasko, Paul ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Embryonic patterning; Germ plasm; Localized mRNAs; Oogenesis; Pole cells

Indexed keywords

INITIATION FACTOR 4G; INITIATION FACTOR 5; DROSOPHILA PROTEIN;

ARTICLE; CELL COUNT; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; EMBRYO; EMBRYO PATTERN FORMATION; FEMALE; GENE EXPRESSION; NONHUMAN; OOCYTE DEVELOPMENT; POLAR BODY; RNA INTERFERENCE; UBIQUITINATION; ANIMAL; CYTOLOGY; EMBRYO DEVELOPMENT; EMBRYOLOGY; GENE; GENE EXPRESSION REGULATION; GENE LOCUS; GENE SILENCING; GENETICS; METABOLISM; MORPHOGENESIS; NONMAMMALIAN EMBRYO; OVARY; PHENOTYPE;

DROSOPHILA MELANOGASTER; MAMMALIA;

ANIMALS; BODY PATTERNING; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EMBRYONIC DEVELOPMENT; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE KNOCKDOWN TECHNIQUES; GENES, INSECT; GENETIC LOCI; OOGENESIS; OVARY; PHENOTYPE; RNA INTERFERENCE;

EID: 84930833898     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.115.017517     Document Type: Article

References (51)

1. Archambault, V., X. Zhao, H. White-Cooper, A. T. Carpenter, and D. M. Glover, 2007 Mutations in Drosophila Greatwall/Scant reveal its roles in mitosis and meiosis and interdependence with Polo kinase. PLoS Genet. 3: e200.
2. Asaoka-Taguchi, M., M. Yamada, A. Nakamura, K. Hanyu, and S. Kobayashi, 1999 Maternal Pumilio acts together with Nanos in germline development in Drosophila embryos. Nat. Cell Biol. 1: 431-437.
3. Barišić-Jäger, E., I. Krȩcioch, S. Hosiner, S. Antic, and S. Dorner, 2013 HPat a decapping activator interacting with the miRNA effector complex. PLoS ONE 8: e71680.
4. Chen, F., M. Barkett, K. T. Ram, A. Quintanilla, and I. K. Hariharan, 1997 Biological characterization of Drosophila Rapgap1, a GTPase activating protein for Rap1. Proc. Natl. Acad. Sci. USA 94: 12485-12490.
5. Chicoine, J., P. Benoit, C. Gamberi, M. Paliouras, M. Simonelig et al., 2007 Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev. Cell 13: 691-704.
6. Christerson, L. B., and D. McKearin, 1994 orb is required for anteroposterior and dorsoventral patterning during Drosophila oogenesis. Genes Dev. 8: 614-628.
7. Dubin-Bar, D., A. Bitan, A. Bakhrat, S. Amsalem, and U. Abdu, 2011 Drosophila javelin-like encodes a novel microtubule-associated protein and is required for mRNA localization during oogenesis. Development 138: 4661-4671.
8. Erdélyi, M., A.-M. Michon, A. Guichet, J. B. Glotzer, and A. Ephrussi, 1995 Requirement for Drosophila cytoplasmic tropomyosin in oskar mRNA localization. Nature 377: 524-527.
9. Fire, A., S. Xu, M. K. Montgomery, S. A. Kostas, S. E. Driver et al., 1998 Potent and specific genetic interference by double-stranded RNA in Caenorhaebditis elegans. Nature 391: 806-811.
10. Fisher, B., R. Weiszmann, E. Frise, A. Hammonds, P. Tomancak et al., 2012 BDGP in situ homepage. Available at: http://insitu.fruitfly.org. Accessed: April 17, 2015
11. Gao, M., T. C. Thomson, T. M. Creed, S. Tu, S. N. Loganathan et al., 2015 Glycolytic enzymes localize to ribonucleoprotein granules in Drosophila germ cells, bind Tudor and protect them from transposable elements. EMBO Rep. 16: 379-386.
12. González-Reyes, A., H. Elliott, and D. St Johnston, 1995 Polarization of both major body axes in Drosophila by gurken-torpedo signalling. Nature 375: 654-658.
13. Graveley, B. R., A. N. Brooks, J. W. Carlson, M. O. Duff, J. M. Landolin et al., 2011 The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479.
14. Handler, D., K. Meixner, M. Pizka, K. Lauss, C. Schmied et al., 2013 The genetic makeup of the Drosophila piRNA pathway. Mol. Cell 50: 762-777.
15. Igreja, C., and E. Izaurralde, 2011 CUP promotes deadenylation and inhibits decapping of mRNA targets. Genes Dev. 25: 1955-1967.
16. Jacobs, H. W., J. A. Knoblich, and C. F. Lehner, 1998 Drosophila Cyclin B3 is required for female fertility and is dispensable for mitosis like Cyclin B. Genes Dev. 12: 3741-3751.
17. Jäger, E., and S. Dorner, 2010 The decapping activator HPat is a novel factor co-purifying with GW182 from Drosophila cells. RNA Biol. 7: 381-385.
18. Kim, J.-H., K. W. Park, E.-W. Lee, W.-S. Jang, J. Seo et al., 2014 Suppression of PPARg through MKRN1-mediated ubiquitination and degradation prevents adipocyte differentiation. Cell Death Differ. 21: 594-603.
19. Kobayashi, S., R. Amikura, A. Nakamura, and P. F. Lasko, 1999 Techniques for analyzing protein and RNA distribution in Drosophila ovaries and embryos at structural and ultrastructural resolution, pp. 426-445 in Advances in molecular biology: a comparative methods approach to the study of oocytes and embryos, edited by J. Richter. Oxford University Press, Oxford, UK.
20. Kugler, J.-M., and P. Lasko, 2009 Localization, anchoring and translational control of oskar, gurken, bicoid, and nanos mRNA during Drosophila oogenesis. Fly (Austin) 3: 15-28.
21. Kugler, J.-M., J. S. Woo, B. H. Oh, and P. Lasko, 2010 Regulation of Drosophila Vasa in vivo through paralogous cullin-RING E3 ligase specificity receptors. Mol. Cell. Biol. 30: 1769-1782.
22. Lécuyer, E., H. Yoshida, N. Parthasarathy, C. Alm, T. Babak et al., 2007 Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
23. Lehmann, R., and C. Nüsslein-Volhard, 1986 Abdominal segmentation, pole cell formation and embryonic polarity require the localized activity of oskar, a maternal gene in Drosophila. Cell 47: 141-152.
24. Liu, N., D. A. Dansereau, and P. Lasko, 2003 Fat facets interacts with Vasa in the Drosophila pole plasm and protects it from degradation. Curr. Biol. 13: 1905-1909.
25. Manseau, L., and T. Schüpbach, 1989 cappuccino and spire: two unique maternal-effect loci requires for both the anteroposterior and dorsoventral patterns of the Drosophila embryo. Genes Dev. 3: 1437-1452.
26. Martinho, R. G., P. S. Kunwar, J. Casanova, and R. Lehmann, 2004 A noncoding RNA is required for the repression of RNApolII-dependent transcription in primordial germ cells. Curr. Biol. 14: 159-165.
27. Mohn, F., G. Sienski, D. Handler, and J. Brennecke, 2014 The Rhino-Deadlock-Cutoff complex licenses noncanonical transcription of dualstrand piRNA clusters in Drosophila. Cell 157: 1364-1379.
28. Mummery-Widmer, J. L., M. Yamazaki, T. Stoeger, M. Novatchkova, S. Bhalerao et al., 2009 Genome-wide analysis of Notch signalling in Drosophila melanogaster. Nature 458: 987-992.
29. Nakamura, A., R. Amikura, M. Mukai, S. Kobayashi, and P. F. Lasko, 1996 Requirement for a noncoding RNA in Drosophila polar granules for germ cell establishment. Science 274: 2075-2079.
30. Ni, J.-Q., R. Zhou, B. Czech, L.-P. Liu, L. Holderbaum et al., 2011 A genome-scale shRNA resource for transgenic RNAi in Drosophila. Nat. Methods 8: 405-407.
31. Nishihara, T., L. Zekri, J. E. Braun, and E. Izaurralde, 2013 miRISC recruits decapping factors to miRNA targets to enhance their degradation. Nucleic Acids Res. 41: 8692-8705.
32. Nüsslein-Volhard, C., E. Wieschaus, and H. Kluding, 1984 Mutations affecting the pattern of the larval cuticle in Drosophila melanogaster. Rouxs Arch. Dev. Biol. 193: 267-282.
33. Nüsslein-Volhard, C., H.-G. Frohnhöfer, and R. Lehmann, 1987 Determination of anteroposterior polarity in Drosophila. Science 238: 1675-1681.
34. Page, S. L., K. S. McKim, B. Deneen, T. L. van Hook, and R. S. Hawley, 2000 Genetic studies of mei-P26 reveal a link between the processes that control germ cell proliferation in both sexes and those that control meiotic exchange in Drosophila. Genetics 155: 1757-1772.
35. Parisi, M., and H. Lin, 1999 The Drosophila pumilio gene encodes two functional protein isoforms that play multiple roles in germline development, gonadogenesis, oogenesis and embryogenesis. Genetics 153: 235-250.
36. Perrimon, N., and M. Gans, 1983 Clonal analysis of the tissue specificity of recessive female sterile mutations of Drosophila melanogaster using a dominant female sterile mutation Fs(1)K1237. Dev. Biol. 100: 365-373.
37. Perrimon, N., L. Engstrom, and A. P. Mahowald, 1984 The effects of zygotic lethal mutations on female germ-line functions in Drosophila. Dev. Biol. 105: 404-414.
38. Perrimon, N., L. Engstrom, and A. P. Mahowald, 1989 Zygotic lethals with specific maternal effect phenotypes in Drosophila melanogaster. I. Loci on the X chromosome. Genetics 121: 333-352.
39. Petrella, L. N., T. Smith-Leiker, and L. Cooley, 2007 The Ovhts polyprotein is cleaved to produce fusome and ring canal proteins required for Drosophila oogenesis. Development 134: 703-712.
40. Pradhan, S. J., K. R. Nesler, S. F. Rosen, Y. Kato, A. Nakamura et al., 2012 The conserved P body component HPat/Pat1 negatively regulates synaptic terminal growth at the larval Drosophila neuromuscular junction. J. Cell Sci. 125: 6105-6116.
41. Robertson, S. E., T. C. Dockendorff, J. L. Leatherman, D. L. Faulkner, and T. A. Jongens, 1999 germ cell-less is required only during the establishment of the germ cell lineage of Drosophila and has activities which are dependent and independent of its localization to the nuclear envelope. Dev. Biol. 215: 288-297.
42. Roth, S., F. S. Neuman-Silberberg, G. Barcelo, and T. Schüpbach, 1995 cornichon and the EGF receptor signalling process are necessary for both anterior-posterior and dorsal-ventral pattern formation in Drosophila. Cell 81: 967-978.
43. Rouget, C., C. Papin, A. Boureux, A. C. Meunier, B. Franco et al., 2010 Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 467: 1128-1132.
44. Sato, K., Y. Hayashi, Y. Ninomiya, S. Shigenobu, K. Arita et al., 2007 Maternal Nanos represses hid/skl-dependent apoptosis to maintain the germ line in Drosophila embryos. Proc. Natl. Acad. Sci. USA 104: 7455-7460.
45. Schüpbach, T., and E. Wieschaus, 1986 Maternal-effect mutations altering the anterior-posterior pattern of the Drosophila embryo. Rouxs Arch. Dev. Biol. 195: 302-317.
46. Schüpbach, T., and E. Wieschaus, 1989 Female sterile mutations on the second chromosome of Drosophila melanogaster. I. Maternal effect mutations. Genetics 121: 101-117.
47. Schüpbach, T., and E. Wieschaus, 1991 Female sterile mutations on the second chromosome of Drosophila melanogaster. II. Mutations blocking oogenesis or altering egg morphology. Genetics 129: 1119-1136.
48. Syrjänen, L., M. E. Tolvanen, M. Hilvo, D. Vullo, F. Carta et al., 2013 Characterization, bioinformatic analysis and dithiocarbamate inhibition studies of two new a-carbonic anhydrases, CAH1 and CAH2, from the fruit fly Drosophila melanogaster. Bioorg. Med. Chem. 21: 1516-1521.
49. Tadros, W., A. L. Goldman, T. Babak, F. Menzies, L. Vardy et al., 2007 SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev. Cell 12: 143-155.
50. Wehr, K., A. Swan, and T. Schüpbach, 2006 Deadlock, a novel protein of Drosophila, is required for germline maintenance, fusome morphogenesis and axial patterning in oogenesis and associates with centrosomes in the early embryo. Dev. Biol. 294: 406-417.
51. Zaessinger, S., I. Busseau, and M. Simonelig, 2006 Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 133: 4573-4583.