Regulation and function of maternal mRNA destabilization during early Drosophila development

Differentiation

Volumn 75, Issue 6, 2007, Pages 482-506

  Semotok, Jennifer L ^a,c   Lipshitz, Howard D ^a,b,c  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

Drosophila; Early embryo; Maternal transcripts; mRNA stability; Posttranscriptional control; RNA localization; Translational regulation

Indexed keywords

MESSENGER RNA;

DROSOPHILA MELANOGASTER; EMBRYO DEVELOPMENT; GENE SILENCING; MESSENGER RNA SYNTHESIS; NONHUMAN; OOCYTE DEVELOPMENT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN METABOLISM; PROTEIN PROCESSING; PROTEIN STABILITY; REVIEW; RNA DEGRADATION; STRUCTURAL HOMOLOGY; TRANSLATION REGULATION; VITELLINE MEMBRANE;

ANIMALIA;

EID: 34447309787     PISSN: 03014681     EISSN: 14320436     Source Type: Journal    
DOI: 10.1111/j.1432-0436.2007.00178.x     Document Type: Review

References (218)

1. Al-Atia, G.R., Fruscoloni, P. Jacobs-Lorena, M. (1985) Translational regulation of mRNAs for ribosomal proteins during early Drosophila development. Biochemistry 24 : 5798 5803.
2. Andrei, M.A., Ingelfinger, D., Heintzmann, R., Achsel, T., Rivera-Pomar, R. Luhrmann, R. (2005) A role for eIF4E and eIF4E-transporter in targeting mRNPs to mammalian processing bodies. RNA 11 : 717 727.
3. Andrulis, E.D., Werner, J., Nazarian, A., Erdjument-Bromage, H., Tempst, P. Lis, J.T. (2002) The RNA processing exosome is linked to elongating RNA polymerase II in Drosophila. Nature 420 : 837 841.
4. Aravin, A.A., Lagos-Quintana, M., Yalcin, A., Zavolan, M., Marks, D., Snyder, B., Gaasterland, T., Meyer, J. Tuschl, T. (2003) The small RNA profile during Drosophila melanogaster development. Dev cell 5 : 337 350.
5. Aravin, A.A., Naumova, N.M., Tulin, A.V., Vagin, V.V., Rozovsky, Y.M. Gvozdev, V.A. (2001) Double-stranded RNA-mediated silencing of genomic tandem repeats and transposable elements in the D. melanogaster germline. Curr Biol 11 : 1017 1027.
6. Arbeitman, M.N., Furlong, E.E., Imam, F., Johnson, E., Null, B.H., Baker, B.S., Krasnow, M.A., Scott, M.P., Davis, R.W. White, K.P. (2002) Gene expression during the life cycle of Drosophila melanogaster. Science 297 : 2270 2275.
7. Asaoka-Taguchi, M., Yamada, M., Nakamura, A., Hanyu, K. Kobayashi, S. (1999) Maternal PUMILIO acts together with Nanos in germline development in Drosophila embryos. Nat Cell Biol 1 : 431 437.
8. Aviv, T., Lin, Z., Ben-Ari, G., Smibert, C.A. Sicheri, F. (2006) Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol 13 : 168 176.
9. Aviv, T., Lin, Z., Lau, S., Rendl, L.M., Sicheri, F. Smibert, C.A. (2003) The RNA-binding SAM domain of SMAUG defines a new family of posttranscriptional regulators. Nat Struct Biol 10 : 614 621.
10. Baez, M.V. Boccaccio, G.L. (2005) Mammalian SMAUG is a translational repressor that forms cytoplasmic foci similar to stress granules. J Biol Chem 280 : 43131 43140.
11. Barreau, C., Paillard, L. Osborne, H.B. (2005) AU-rich elements and associated factors: are there unifying principles? Nucleic Acids Res 33 : 7138 7150.
12. Bashirullah, A., Cooperstock, R.L. Lipshitz, H.D. (2001) Spatial and temporal control of RNA stability. Proc Natl Acad Sci USA 98 : 7025 7028.
13. Bashirullah, A., Halsell, S.R., Cooperstock, R.L., Kloc, M., Karaiskakis, A., Fisher, W.W., Fu, W., Hamilton, J.K., Etkin, L.D. Lipshitz, H.D. (1999) Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J 18 : 2610 2620.
14. Behm-Ansmant, I. Izaurralde, E. (2006) Quality control of gene expression: a stepwise assembly pathway for the surveillance complex that triggers nonsense-mediated mRNA decay. Genes Dev 20 : 391 398.
15. Behm-Ansmant, I., Rehwinkel, J., Doerks, T., Stark, A., Bork, P. Izaurralde, E. (2006) mRNA degradation by miRNAs and GW182 requires both CCR4:NOT deadenylase and DCP1:DCP2 decapping complexes. Genes Dev 20 : 1885 1898.
16. Benoit, B., Mitou, G., Chartier, A., Temme, C., Zaessinger, S., Wahle, E., Busseau, I. Simonelig, M. (2005) An essential cytoplasmic function for the nuclear poly(A) binding protein, PABP2, in poly(A) tail length control and early development in Drosophila. Dev Cell 9 : 511 522.
17. Bergsten, S.E. Gavis, E.R. (1999) Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development (Cambridge, UK) 126 : 659 669.
18. Bilen, J., Liu, N., Burnett, B.G., Pittman, R.N. Bonini, N.M. (2006) MicroRNA pathways modulate polyglutamine-induced neurodegeneration. Mol Cell 24 : 157 163.
19. Brengues, M., Teixeira, D. Parker, R. (2005) Movement of eukaryotic mRNAs between polysomes and cytoplasmic processing bodies. Science 310 : 486 489.
20. Brennecke, J., Hipfner, D.R., Stark, A., Russell, R.B. 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.
21. Cairrao, F., Arraiano, C. Newbury, S. (2005) Drosophila gene tazman, an orthologue of the yeast exosome component Rrp44p/Dis3, is differentially expressed during development. Dev Dyn 232 : 733 737.
22. Caponigro, G., Muhlrad, D. Parker, R. (1993) A small segment of the MAT alpha 1 transcript promotes mRNA decay in Saccharomyces cerevisiae: a stimulatory role for rare codons. Mol Cell Biol 13 : 5141 5148.
23. Caponigro, G. Parker, R. (1996) mRNA turnover in yeast promoted by the MATalpha1 instability element. Nucleic Acids Res 24 : 4304 4312.
24. Caudy, A.A., Ketting, R.F., Hammond, S.M., Denli, A.M., Bathoorn, A.M., Tops, B.B., Silva, J.M., Myers, M.M., Hannon, G.J. Plasterk, R.H. (2003) A micrococcal nuclease homologue in RNAi effector complexes. Nature 425 : 411 414.
25. Caudy, A.A., Myers, M., Hannon, G.J. Hammond, S.M. (2002) FRAGILE X-RELATED PROTEIN and VIG associate with the RNA interference machinery. Genes Dev 16 : 2491 2496.
26. Cereghino, G.P., Atencio, D.P., Saghbini, M., Beiner, J. Scheffler, I.E. (1995) Glucose-dependent turnover of the mRNAs encoding succinate dehydrogenase peptides in Saccharomyces cerevisiae: sequence elements in the 5′ untranslated region of the Ip mRNA play a dominant role. Mol Biol Cell 6 : 1125 1143.
27. Chang, T.C., Yamashita, A., Chen, C.Y., Yamashita, Y., Zhu, W., Durdan, S., Kahvejian, A., Sonenberg, N. Shyu, A.B. (2004) UNR, a new partner of poly(A)-binding protein, plays a key role in translationally coupled mRNA turnover mediated by the c-fos major coding-region determinant. Genes Dev 18 : 2010 2023.
28. Chen, C.Y. Shyu, A.B. (1995) AU-rich elements: characterization and importance in mRNA degradation. Trends Biochem Sci 20 : 465 470.
29. Chernokalskaya, E., Dubell, A.N., Cunningham, K.S., Hanson, M.N., Dompenciel, R.E. Schoenberg, D.R. (1998) A polysomal ribonuclease involved in the destabilization of albumin mRNA is a novel member of the peroxidase gene family. RNA 4 : 1537 1548.
30. Cho, P.F., Gamberi, C., Cho-Park, Y.A., Cho-Park, I.B., Lasko, P. Sonenberg, N. (2006) Cap-dependent translational inhibition establishes two opposing morphogen gradients in Drosophila embryos. Curr Biol 16 : 2035 2041.
31. Ciapa, B. Chiri, S. (2000) Egg activation: upstream of the fertilization calcium signal. Biol Cell 92 : 215 233.
32. Coller, J. Parker, R. (2004) Eukaryotic mRNA decapping. Annu Rev Biochem 73 : 861 890.
33. Conti, E. Izaurralde, E. (2005) Nonsense-mediated mRNA decay: molecular insights and mechanistic variations across species. Curr Opin Cell Biol 17 : 316 325.
34. Cook, H.A., Koppetsch, B.S., Wu, J. Theurkauf, W.E. (2004) The Drosophila SDE3 homolog ARMITAGE is required for oskar mRNA silencing and embryonic axis specification. Cell 116 : 817 829.
35. Cooperstock, R.L. (2002) Mechanisms of transcript regulation in the early Drosophila embryo: degradation, localization and translational regulation. Ph.D. Thesis, Department of Molecular and Medical Genetics, University of Toronto, Toronto.
36. Cougot, N., Babajko, S. Seraphin, B. (2004) Cytoplasmic foci are sites of mRNA decay in human cells. J Cell Biol 165 : 31 40.
37. Cunningham, K.S., Dodson, R.E., Nagel, M.A., Shapiro, D.J. Schoenberg, D.R. (2000) Vigilin binding selectively inhibits cleavage of the vitellogenin mRNA 3′-untranslated region by the mRNA endonuclease polysomal ribonuclease 1. Proc Natl Acad Sci USA 97 : 12498 12502.
38. Dahanukar, A., Walker, J.A. Wharton, R.P. (1999) SMAUG, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol Cell 4 : 209 218.
39. Dalby, B. Glover, D.M. (1993) Discrete sequence elements control posterior pole accumulation and translational repression of maternal cyclin B RNA in Drosophila. EMBO J 12 : 1219 1227.
40. Davis, C.A., Monnier, J.M. Nick, H.S. (2001) A coding region determinant of instability regulates levels of manganese superoxide dismutase mRNA. J Biol Chem 276 : 37317 37326.
41. Decker, C.J. Parker, R. (1993) A turnover pathway for both stable and unstable mRNAs in yeast: evidence for a requirement for deadenylation. Genes Dev 7 : 1632 1643.
42. de la Cruz, B.J., Prieto, S. Scheffler, I.E. (2002) The role of the 5′ untranslated region (UTR) in glucose-dependent mRNA decay. Yeast 19 : 887 902.
43. Delaunay, J., Le Mee, G., Ezzeddine, N., Labesse, G., Terzian, C., Capri, M. Ait-Ahmed, O. (2004) The Drosophila BRUNO paralogue Bru-3 specifically binds the EDEN translational repression element. Nucleic Acids Res 32 : 3070 3082.
44. Denli, A.M., Tops, B.B., Plasterk, R.H., Ketting, R.F. Hannon, G.J. (2004) Processing of primary microRNAs by the microprocessor complex. Nature 432 : 231 235.
45. Deshpande, G., Calhoun, G. Schedl, P. (2005) Drosophila ARGONAUTE-2 is required early in embryogenesis for the assembly of centric/centromeric heterochromatin, nuclear division, nuclear migration, and germ-cell formation. Genes Dev 19 : 1680 1685.
46. Deshpande, G., Calhoun, G. Schedl, P. (2006) The Drosophila FRAGILE X PROTEIN, dFMR1, is required during early embryogenesis for pole cell formation and the rapid nuclear division cycles. Genetics 174 : 1287 1298.
47. Ding, D., Parkhurst, S.M., Halsell, S.R. Lipshitz, H.D. (1993) Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Mol Cell Biol 13 : 3773 3781.
48. Doane, W.W. (1960) Completion of meiosis in uninseminated eggs of Drosophila melanogaster. Science 132 : 677 678.
49. Dompenciel, R.E., Garnepudi, V.R. Schoenberg, D.R. (1995) Purification and characterization of an estrogen-regulated Xenopus liver polysomal nuclease involved in the selective destabilization of albumin mRNA. J Biol Chem 270 : 6108 6118.
50. Edgar, B.A. Datar, S.A. (1996) Zygotic degradation of two maternal Cdc25 mRNAs terminates Drosophila's early cell cycle program. Genes Dev 10 : 1966 1977.
51. Edgar, B.A. Schubiger, G. (1986) Parameters controlling transcriptional activation during early Drosophila development. Cell 44 : 871 877.
52. Elbashir, S.M., Lendeckel, W. Tuschl, T. (2001) RNA interference is mediated by 21- and 22-nucleotide RNAs. Genes Dev 15 : 188 200.
53. Elfring, L.K., Axton, J.M., Fenger, D.D., Page, A.W., Carminati, J.L. Orr-Weaver, T.L. (1997) Drosophila PLUTONIUM protein is a specialized cell cycle regulator required at the onset of embryogenesis. Mol Biol Cell 8 : 583 593.
54. Fenger, D.D., Carminati, J.L., Burney-Sigman, D.L., Kashevsky, H., Dines, J.L., Elfring, L.K. Orr-Weaver, T.L. (2000) PAN GU: a protein kinase that inhibits S phase and promotes mitosis in early Drosophila development. Development (Cambridge, UK) 127 : 4763 4774.
55. Ferraiuolo, M.A., Basak, S., Dostie, J., Murray, E.L., Schoenberg, D.R. Sonenberg, N. (2005) A role for the eIF4E-binding protein 4E-T in P-body formation and mRNA decay. J Cell Biol 170 : 913 924.
56. Filipowicz, W. (2005) RNAi: the nuts and bolts of the RISC machine. Cell 122 : 17 20.
57. Foe, V.E. Alberts, B.M. (1983) Studies of nuclear and cytoplasmic behaviour during the five mitotic cycles that precede gastrulation in Drosophila embryogenesis. J Cell Sci 61 : 31 70.
58. Fontes, A.M., Riedl, A. Jacobs-Lorena, M. (2001) Developmental regulation of an instability element from the Drosophila fushi tarazu mRNA. Genesis 30 : 59 64.
59. Forrest, K.M. Gavis, E.R. (2003) Live imaging of endogenous RNA reveals a diffusion and entrapment mechanism for nanos mRNA localization in Drosophila. Curr Biol 13 : 1159 1168.
60. Forstemann, K., Tomari, Y., Du, T., Vagin, V.V., Denli, A.M., Bratu, D.P., Klattenhoff, C., Theurkauf, W.E. Zamore, P.D. (2005) Normal microRNA maturation and germ-line stem cell maintenance requires LOQUACIOUS, a double-stranded RNA-binding domain protein. PLoS Biol 3 : e236.
61. Galewsky, S. Schulz, R.A. (1992) Drop out: a third chromosome maternal-effect locus required for formation of the Drosophila cellular blastoderm. Mol Reprod Dev 32 : 331 338.
62. Galiana-Arnoux, D., Dostert, C., Schneemann, A., Hoffmann, J.A. Imler, J.L. (2006) Essential function in vivo for DICER-2 in host defense against RNA viruses in drosophila. Nat Immunol 7 : 590 597.
63. Gallie, D.R. (1991) The cap and poly(A) tail function synergistically to regulate mRNA translational efficiency. Genes Dev 5 : 2108 2116.
64. Gallie, D.R. (1998) A tale of two termini: a functional interaction between the termini of an mRNA is a prerequisite for efficient translation initiation. Gene 216 : 1 11.
65. Gallouzi, I.E., Parker, F., Chebli, K., Maurier, F., Labourier, E., Barlat, I., Capony, J.P., Tocque, B. Tazi, J. (1998) A novel phosphorylation-dependent RNase activity of GAP-SH3 binding protein: a potential link between signal transduction and RNA stability. Mol Cell Biol 18 : 3956 3965.
66. Gamberi, C., Peterson, D.S., He, L. Gottlieb, E. (2002) An anterior function for the Drosophila posterior determinant PUMILIO. Development (Cambridge, UK) 129 : 2699 2710.
67. Gatfield, D. Izaurralde, E. (2004) Nonsense-mediated messenger RNA decay is initiated by endonucleolytic cleavage in Drosophila. Nature 429 : 575 578.
68. Gerber, A.P., Luschnig, S., Krasnow, M.A., Brown, P.O. Herschlag, D. (2006) Genome-wide identification of mRNAs associated with the translational regulator PUMILIO in Drosophila melanogaster. Proc Natl Acad Sci USA 103 : 4487 4492.
69. Giraldez, A.J., Mishima, Y., Rihel, J., Grocock, R.J., Van Dongen, S., Inoue, K., Enright, A.J. Schier, A.F. (2006) Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 312 : 75 79.
70. Goldstrohm, A.C., Hook, B.A., Seay, D.J. Wickens, M. (2006) PUF proteins bind Pop2p to regulate messenger RNAs. Nat Struct Mol Biol 13 : 533 539.
71. Goldstrohm, A.C., Seay, D.J., Hook, B.A. Wickens, M. (2007) PUF protein-mediated deadenylation is catalyzed by Ccr4p. J Biol Chem 282 : 109 114.
72. Grafi, G. Galili, G. (1993) Induction of cytoplasmic factors that bind to the 3′ AU-rich region of human interferon beta mRNA during early development of Xenopus laevis. FEBS Lett 336 : 403 407.
73. Graham, A.C., Kiss, D.L. Andrulis, E.D. (2006) Differential distribution of exosome subunits at the nuclear lamina and in cytoplasmic foci. Mol Biol Cell 17 : 1399 1409.
74. Grosset, C., Chen, C.Y., Xu, N., Sonenberg, N., Jacquemin-Sablon, H. Shyu, A.B. (2000) A mechanism for translationally coupled mRNA turnover: interaction between the poly(A) tail and a c-fos RNA coding determinant via a protein complex. Cell 103 : 29 40.
75. Harris, A.N. Macdonald, P.M. (2001) AUBERGINE encodes a Drosophila polar granule component required for pole cell formation and related to eIF2C. Development (Cambridge, UK) 128 : 2823 2832.
76. Hatfield, S.D., Shcherbata, H.R., Fischer, K.A., Nakahara, K., Carthew, R.W. Ruohola-Baker, H. (2005) Stem cell division is regulated by the microRNA pathway. Nature 435 : 974 978.
77. Heifetz, Y., Yu, J. Wolfner, M.F. (2001) Ovulation triggers activation of Drosophila oocytes. Dev Biol 234 : 416 424.
78. Hennigan, A.N. Jacobson, A. (1996) Functional mapping of the translation-dependent instability element of yeast MATalpha1 mRNA. Mol Cell Biol 16 : 3833 3843.
79. Herrick, D.J. Ross, J. (1994) The half-life of c-myc mRNA in growing and serum-stimulated cells: influence of the coding and 3′ untranslated regions and role of ribosome translocation. Mol Cell Biol 14 : 2119 2128.
80. Hollien, J. Weissman, J.S. (2006) Decay of endoplasmic reticulum-localized mRNAs during the unfolded protein response. Science 313 : 104 107.
81. Horner, V.L., Czank, A., Jang, J.K., Singh, N., Williams, B.C., Puro, J., Kubli, E., Hanes, S.D., McKim, K.S., Wolfner, M.F. Goldberg, M.L. (2006) The Drosophila calcipressin sarah is required for several aspects of egg activation. Curr Biol 16 : 1441 1446.
82. Hsu, C.L. Stevens, A. (1993) Yeast cells lacking 5′- ->3′ exoribonuclease 1 contain mRNA species that are poly(A) deficient and partially lack the 5′ cap structure. Mol Cell Biol 13 : 4826 4835.
83. Ishizuka, A., Siomi, M.C. Siomi, H. (2002) A Drosophila FRAGILE X PROTEIN interacts with components of RNAi and ribosomal proteins. Genes Dev 16 : 2497 2508.
84. Ito, J. Jacobs-Lorena, M. (2001) Functional mapping of destabilizing elements in the protein-coding region of the Drosophila fushi tarazu mRNA. J Biol Chem 276 : 23525 23530.
85. Jeske, M., Meyer, S., Temme, C., Freudenreich, D. Wahle, E. (2006) Rapid ATP-dependent deadenylation of nanos mRNA in a cell-free system from Drosophila embryos. J Biol Chem 281 : 25124 25133.
86. Jiang, F., Ye, X., Liu, X., Fincher, L., McKearin, D. Liu, Q. (2005) DICER-1 and R3D1-L catalyze microRNA maturation in Drosophila. Genes Dev 19 : 1674 1679.
87. Jing, Q., Huang, S., Guth, S., Zarubin, T., Motoyama, A., Chen, J., Di Padova, F., Lin, S.C., Gram, H. Han, J. (2005) Involvement of microRNA in AU-rich element-mediated mRNA instability. Cell 120 : 623 634.
88. Johnson, P.E. Donaldson, L.W. (2006) RNA recognition by the Vts1p SAM domain. Nat Struct Mol Biol 13 : 177 178.
89. Kataoka, Y., Takeichi, M. Uemura, T. (2001) Developmental roles and molecular characterization of a Drosophila homologue of Arabidopsis ARGONAUTE1, the founder of a novel gene superfamily. Genes Cells 6 : 313 325.
90. Kavi, H.H., Fernandez, H.R., Xie, W. Birchler, J.A. (2005) RNA silencing in Drosophila. FEBS Lett 579 : 5940 5949.
91. Kennerdell, J.R., Yamaguchi, S. Carthew, R.W. (2002) RNAi is activated during Drosophila oocyte maturation in a manner dependent on AUBERGINE and SPINDLE-E. Genes Dev 16 : 1884 1889.
92. Koprunner, M., Thisse, C., Thisse, B. Raz, E. (2001) A zebrafish nanos-related gene is essential for the development of primordial germ cells. Genes Dev 15 : 2877 2885.
93. Kwon, C., Han, Z., Olson, E.N. Srivastava, D. (2005) MicroRNA1 influences cardiac differentiation in Drosophila and regulates Notch signaling. Proc Natl Acad Sci USA 102 : 18986 18991.
94. Lai, E.C., Tomancak, P., Williams, R.W. Rubin, G.M. (2003) Computational identification of Drosophila microRNA genes. Genome Biol 4 : R42.
95. Leaman, D., Chen, P.Y., Fak, J., Yalcin, A., Pearce, M., Unnerstall, U., Marks, D.S., Sander, C., Tuschl, T. Gaul, U. (2005) Antisense-mediated depletion reveals essential and specific functions of microRNAs in Drosophila development. Cell 121 : 1097 1108.
96. Lee, Y., Ahn, C., Han, J., Choi, H., Kim, J., Yim, J., Lee, J., Provost, P., Radmark, O., Kim, S. Kim, V.N. (2003b) The nuclear RNase III DROSHA initiates microRNA processing. Nature 425 : 415 419.
97. Lee, Y.S., Nakahara, K., Pham, J.W., Kim, K., He, Z., Sontheimer, E.J. Carthew, R.W. (2004) Distinct roles for Drosophila DICER-1 and DICER-2 in the siRNA/miRNA silencing pathways. Cell 117 : 69 81.
98. Lee, L.A., Van Hoewyk, D. Orr-Weaver, T.L. (2003a) The Drosophila cell cycle kinase PAN GU forms an active complex with PLUTONIUM and GNU to regulate embryonic divisions. Genes Dev 17 : 2979 2991.
99. Lemm, I. Ross, J. (2002) Regulation of c-myc mRNA decay by translational pausing in a coding region instability determinant. Mol Cell Biol 22 : 3959 3969.
100. Lieberfarb, M.E., Chu, T., Wreden, C., Theurkauf, W., Gergen, J.P. Strickland, S. (1996) Mutations that perturb poly(A)-dependent maternal mRNA activation block the initiation of development. Development (Cambridge, UK) 122 : 579 588.
101. Li, X. Carthew, R.W. (2005) A microRNA mediates EGF receptor signaling and promotes photoreceptor differentiation in the Drosophila eye. Cell 123 : 1267 1277.
102. Li, Y., Wang, F., Lee, J.A. Gao, F.B. (2006) MicroRNA-9a ensures the precise specification of sensory organ precursors in Drosophila. Genes Dev 20 : 2793 2805.
103. Lin, M.D., Fan, S.J., Hsu, W.S. Chou, T.B. (2006) Drosophila decapping protein 1, dDcp1, is a component of the oskar mRNP complex and directs its posterior localization in the oocyte. Dev Cell 10 : 601 613.
104. Liu, X., Jiang, F., Kalidas, S., Smith, D. Liu, Q. (2006) DICER-2 and R2D2 coordinately bind siRNA to promote assembly of the siRISC complexes. RNA 12 : 1514 1520.
105. Liu, Q., Rand, T.A., Kalidas, S., Du, F., Kim, H.E., Smith, D.P. Wang, X. (2003) R2D2, a bridge between the initiation and effector steps of the Drosophila RNAi pathway. Science 301 : 1921 1925.
106. Liu, J., Rivas, F.V., Wohlschlegel, J., Yates, J.R. IIIrd., Parker, R. Hannon, G.J. (2005) A role for the P-body component GW182 in microRNA function. Nat Cell Biol 7 : 1261 1266.
107. Lykke-Andersen, J. (2002) Identification of a human decapping complex associated with hUpf proteins in nonsense-mediated decay. Mol Cell Biol 22 : 8114 8121.
108. Mahowald, A.P. (2001) Assembly of the Drosophila germ plasm. Int Rev Cytol 203 : 187 213.
109. Mahowald, A.P., Goralski, T.J. Caulton, J.H. (1983) In vitro activation of Drosophila eggs. Dev Biol 98 : 437 445.
110. Matthews, K.A., Miller, D.F. Kaufman, T.C. (1989) Developmental distribution of RNA and protein products of the Drosophila alpha-tubulin gene family. Dev Biol 132 : 45 61.
111. Megosh, H.B., Cox, D.N., Campbell, C. Lin, H. (2006) The role of PIWI and the miRNA machinery in Drosophila germline determination. Curr Biol 16 : 1884 1894.
112. Meister, G. Tuschl, T. (2004) Mechanisms of gene silencing by double-stranded RNA. Nature 431 : 343 349.
113. Menon, K.P., Sanyal, S., Habara, Y., Sanchez, R., Wharton, R.P., Ramaswami, M. Zinn, K. (2004) The translational repressor PUMILIO regulates presynaptic morphology and controls postsynaptic accumulation of translation factor eIF-4E. Neuron 44 : 663 676.
114. Merrill, P.T., Sweeton, D. Wieschaus, E. (1988) Requirements for autosomal gene activity during precellular stages of Drosophila melanogaster. Development (Cambridge, UK) 104 : 495 509.
115. Meyer, W.J., Schreiber, S., Guo, Y., Volkmann, T., Welte, M.A. Muller, H.A. (2006) Overlapping functions of ARGONAUTE proteins in patterning and morphogenesis of Drosophila embryos. PLoS Genet 2 : e134.
116. Meyer, S., Temme, C. Wahle, E. (2004) Messenger RNA turnover in eukaryotes: pathways and enzymes. Crit Rev Biochem Mol Biol 39 : 197 216.
117. Miyoshi, K., Tsukumo, H., Nagami, T., Siomi, H. Siomi, M.C. (2005) Slicer function of Drosophila ARGONAUTES and its involvement in RISC formation. Genes Dev 19 : 2837 2848.
118. Morris, J.Z., Hong, A., Lilly, M.A. Lehmann, R. (2005) twin, a CCR4 homolog, regulates cyclin poly(A) tail length to permit Drosophila oogenesis. Development (Cambridge, UK) 132 : 1165 1174.
119. Muhlrad, D., Decker, C.J. Parker, R. (1994) Deadenylation of the unstable mRNA encoded by the yeast MFA2 gene leads to decapping followed by 5′->3′ digestion of the transcript. Genes Devt 8 : 855 866.
120. Muhlrad, D. Parker, R. (1992) Mutations affecting stability and deadenylation of the yeast MFA2 transcript. Genes Dev 6 : 2100 2111.
121. Mukherjee, D., Gao, M., O'Connor, J.P., Raijmakers, R., Pruijn, G., Lutz, C.S. Wilusz, J. (2002) The mammalian exosome mediates the efficient degradation of mRNAs that contain AU-rich elements. Embo J 21 : 165 174.
122. Munroe, D. Jacobson, A. (1990) Tales of poly(A): a review. Gene 91 : 151 158.
123. Murata, Y. Wharton, R.P. (1995) Binding of PUMILIO to maternal hunchback mRNA is required for posterior patterning in Drosophila embryos. Cell 80 : 747 756.
124. Myers, F.A., Francis-Lang, H. Newbury, S.F. (1995) Degradation of maternal string mRNA is controlled by proteins encoded on maternally contributed transcripts. Mech Dev 51 : 217 226.
125. Nakamura, A., Amikura, R., Hanyu, K. Kobayashi, S. (2001) Me31B silences translation of oocyte-localizing RNAs through the formation of cytoplasmic RNP complex during Drosophila oogenesis. Development (Cambridge, UK) 128 : 3233 3242.
126. Nelson, M.R., Leidal, A.M. Smibert, C.A. (2004) Drosophila Cup is an eIF4E-binding protein that functions in SMAUG-mediated translational repression. Embo J 23 : 150 159.
127. Nguyen, H.T. Frasch, M. (2006) MicroRNAs in muscle differentiation: lessons from Drosophila and beyond. Curr Opin Genet Dev 16 : 533 539.
128. Oberstrass, F.C., Lee, A., Stefl, R., Janis, M., Chanfreau, G. Allain, F.H. (2006) Shape-specific recognition in the structure of the Vts1p SAM domain with RNA. Nat Struct Mol Biol 13 : 160 167.
129. Okamura, K., Ishizuka, A., Siomi, H. Siomi, M.C. (2004) Distinct roles for ARGONAUTE proteins in small RNA-directed RNA cleavage pathways. Genes Dev 18 : 1655 1666.
130. Olsen, P.H. Ambros, V. (1999) The lin-4 regulatory RNA controls developmental timing in Caenorhabditis elegans by blocking LIN-14 protein synthesis after the initiation of translation. Dev Biol 216 : 671 680.
131. Orban, T.I. Izaurralde, E. (2005) Decay of mRNAs targeted by RISC requires XRN1, the Ski complex, and the exosome. RNA 11 : 459 469.
132. Osborne, H.B., Gautier-Courteille, C., Graindorge, A., Barreau, C., Audic, Y., Thuret, R., Pollet, N. Paillard, L. (2005) Post-transcriptional regulation in Xenopus embryos: role and targets of EDEN-BP. Biochem Soc Trans 33 : 1541 1543.
133. Page, A.W. Orr-Weaver, T.L. (1996) The Drosophila genes GRAUZONE and CORTEX are necessary for proper female meiosis. J Cell Sci 109 (Pt 7) : 1707 1715.
134. Page, A.W. Orr-Weaver, T.L. (1997) Activation of the meiotic divisions in Drosophila oocytes. Dev Biol 183 : 195 207.
135. Paillard, L. Osborne, H.B. (2003) East of EDEN was a poly(A) tail. Biol Cell 95 : 211 219.
136. Pal-Bhadra, M., Bhadra, U. Birchler, J.A. (2002) RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol Cell 9 : 315 327.
137. Pal-Bhadra, M., Leibovitch, B.A., Gandhi, S.G., Rao, M., Bhadra, U., Birchler, J.A. Elgin, S.C. (2004) Heterochromatic silencing and HP1 localization in Drosophila are dependent on the RNAi machinery. Science 303 : 669 672.
138. Paste, M., Huez, G. Kruys, V. (2003) Deadenylation of interferon-beta mRNA is mediated by both the AU-rich element in the 3′-untranslated region and an instability sequence in the coding region. Eur J Biochem 270 : 1590 1597.
139. Pastori, R.L., Moskaitis, J.E. Schoenberg, D.R. (1991) Estrogen-induced ribonuclease activity in Xenopus liver. Biochemistry 30 : 10490 10498.
140. Patel, R.C. Jacobs-Lorena, M. (1992) Cis-acting sequences in the 5′-untranslated region of the ribosomal protein A1 mRNA mediate its translational regulation during early embryogenesis of Drosophila. J Biol Chem 267 : 1159 1164.
141. Pazman, C., Mayes, C.A., Fanto, M., Haynes, S.R. Mlodzik, M. (2000) Rasputin, the Drosophila homologue of the RasGAP SH3 binding protein, functions in ras- and Rho-mediated signaling. Development (Cambridge, UK) 127 : 1715 1725.
142. Petersen, C.P., Bordeleau, M.E., Pelletier, J. Sharp, P.A. (2006) Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21 : 533 542.
143. Pierrat, B., Lacroute, F. Losson, R. (1993) The 5′ untranslated region of the PPR1 regulatory gene dictates rapid mRNA decay in yeast. Gene 131 : 43 51.
144. Pillai, R.S., Bhattacharyya, S.N., Artus, C.G., Zoller, T., Cougot, N., Basyuk, E., Bertrand, E. Filipowicz, W. (2005) Inhibition of translational initiation by Let-7 MicroRNA in human cells. Science 309 : 1573 1576.
145. Raijmakers, R., Schilders, G. Pruijn, G.J. (2004) The exosome, a molecular machine for controlled RNA degradation in both nucleus and cytoplasm. Eur J Cell Biol 83 : 175 183.
146. Rand, T.A., Ginalski, K., Grishin, N.V. Wang, X. (2004) Biochemical identification of ARGONAUTE 2 as the sole protein required for RNA-induced silencing complex activity. Proc Natl Acad Sci USA 101 : 14385 14389.
147. Rehwinkel, J., Behm-Ansmant, I., Gatfield, D. Izaurralde, E. (2005) A crucial role for GW182 and the DCP1:DCP2 decapping complex in miRNA-mediated gene silencing. RNA 11 : 1640 1647.
148. Rehwinkel, J., Natalin, P., Stark, A., Brennecke, J., Cohen, S.M. Izaurralde, E. (2006) Genome-wide analysis of mRNAs regulated by DROSHA and ARGONAUTE proteins in Drosophila melanogaster. Mol Cell Biol 26 : 2965 2975.
149. Richter, J.D. (1999) Cytoplasmic polyadenylation in development and beyond. Microbiol Mol Biol Rev 63 : 446 456.
150. Riedl, A. Jacobs-Lorena, M. (1996) Determinants of Drosophila fushi tarazu mRNA instability. Mol Cell Biol 16 : 3047 3053.
151. Rodgers, N.D., Wang, Z. Kiledjian, M. (2002) Characterization and purification of a mammalian endoribonuclease specific for the alpha-globin mRNA. J Biol Chem 277 : 2597 2604.
152. Roux, M.M., Townley, I.K., Raisch, M., Reade, A., Bradham, C., Humphreys, G., Gunaratne, H.J., Killian, C.E., Moy, G., Su, Y.H., Ettensohn, C.A., Wilt, F., Vacquier, V.D., Burke, R.D., Wessel, G. Foltz, K.R. (2006) A functional genomic and proteomic perspective of sea urchin calcium signaling and egg activation. Dev Biol 300 : 416 433.
153. Sachs, A. (1990) The role of poly(A) in the translation and stability of mRNA. Curr Opin Cell Biol 2 : 1092 1098.
154. Sachs, A.B., Sarnow, P. Hentze, M.W. (1997) Starting at the beginning, middle, and end: translation initiation in eukaryotes. Cell 89 : 831 838.
155. Saito, K., Ishizuka, A., Siomi, H. Siomi, M.C. (2005) Processing of pre-microRNAs by the DICER-1-LOQUACIOUS complex in Drosophila cells. PLoS Biol 3 : e235.
156. Saito, K., Nishida, K.M., Mori, T., Kawamura, Y., Miyoshi, K., Nagami, T., Siomi, H. Siomi, M.C. (2006) Specific association of Piwi with rasiRNAs derived from retrotransposon and heterochromatic regions in the Drosophila genome. Genes Dev 20 : 2214 2222.
157. Salles, F.J., Lieberfarb, M.E., Wreden, C., Gergen, J.P. Strickland, S. (1994) Coordinate initiation of Drosophila development by regulated polyadenylation of maternal messenger RNAs. Science 266 : 1996 1999.
158. Schneider, M.D., Najand, N., Chaker, S., Pare, J.M., Haskins, J., Hughes, S.C., Hobman, T.C., Locke, J. Simmonds, A.J. (2006) GAWKY is a component of cytoplasmic mRNA processing bodies required for early Drosophila development. J Cell Biol 174 : 349 358.
159. Schultz, R.M. (1993) Regulation of zygotic gene activation in the mouse. Bioessays 15 : 531 538.
160. Schultz, R.M. (2002) The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Hum Reprod Update 8 : 323 331.
161. Seago, J.E., Chernukhin, I.V. Newbury, S.F. (2001) The Drosophila gene twister, an orthologue of the yeast helicase SKI2, is differentially expressed during development. Mech Dev 106 : 137 141.
162. Semotok, J.L., Cooperstock, R.L., Pinder, B.D., Vari, H.K., Lipshitz, H.D. Smibert, C.A. (2005) SMAUG recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 15 : 284 294.
163. Sen, G.L. Blau, H.M. (2006) A brief history of RNAi: the silence of the genes. FASEB J 20 : 1293 1299.
164. Seydoux, G. Fire, A. (1994) Soma-germline asymmetry in the distributions of embryonic RNAs in Caenorhabditis elegans. Development (Cambridge, UK) 120 : 2823 2834.
165. Shamanski, F.L. Orr-Weaver, T.L. (1991) The Drosophila PLUTONIUM and PAN GU genes regulate entry into S phase at fertilization. Cell 66 : 1289 1300.
166. Sheth, U. Parker, R. (2003) Decapping and decay of messenger RNA occur in cytoplasmic processing bodies. Science 300 : 805 808.
167. Shyu, A.B., Belasco, J.G. Greenberg, M.E. (1991) Two distinct destabilizing elements in the c-fos message trigger deadenylation as a first step in rapid mRNA decay. Genes Dev 5 : 221 231.
168. Shyu, A.B., Greenberg, M.E. Belasco, J.G. (1989) The c-fos transcript is targeted for rapid decay by two distinct mRNA degradation pathways. Genes Dev 3 : 60 72.
169. Smibert, C.A., Lie, Y.S., Shillinglaw, W., Henzel, W.J. Macdonald, P.M. (1999) SMAUG, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 5 : 1535 1547.
170. Smibert, C.A., Wilson, J.E., Kerr, K. Macdonald, P.M. (1996) SMAUG protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 10 : 2600 2609.
171. Sokol, N.S. Ambros, V. (2005) Mesodermally expressed Drosophila microRNA-1 is regulated by Twist and is required in muscles during larval growth. Genes Dev 19 : 2343 2354.
172. Sonoda, J. Wharton, R.P. (1999) Recruitment of Nanos to hunchback mRNA by PUMILIO. Genes Dev 13 : 2704 2712.
173. Sonoda, J. Wharton, R.P. (2001) Drosophila brain tumor is a translational repressor. Genes Dev 15 : 762 773.
174. Sontheimer, E.J. (2005) Assembly and function of RNA silencing complexes. Nat Rev Mol Cell Biol 6 : 127 138.
175. Spradling, A. (1993a) Developmental genetics of oogenesis. In : Bate, M. Arias, A.M. eds. The development of Drosophila melanogaster. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, pp. 1 70.
176. Spradling, A.C. (1993b) Germline cysts: communes that work. Cell 72 : 649 651.
177. Surdej, P. Jacobs-Lorena, M. (1998) Developmental regulation of bicoid mRNA stability is mediated by the first 43 nucleotides of the 3′ untranslated region. Mol Cell Biol 18 : 2892 2900.
178. Tadros, W., Goldman, A.L., Babak, T., Menzies, F., Vardy, L., Orr-Weaver, T., Hughes, T.R., Westwood, J.T., Smibert, C.A. Lipshitz, H.D. (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.
179. Tadros, W., Houston, S.A., Bashirullah, A., Cooperstock, R.L., Semotok, J.L., Reed, B.H. Lipshitz, H.D. (2003) Regulation of maternal transcript destabilization during egg activation in Drosophila. Genetics 164 : 989 1001.
180. Tadros, W. Lipshitz, H.D. (2005) Setting the stage for development: mRNA translation and stability during oocyte maturation and egg activation in Drosophila. Dev Dyn 232 : 593 608.
181. Takeo, S., Tsuda, M., Akahori, S., Matsuo, T. Aigaki, T. (2006) The calcineurin regulator sra plays an essential role in female meiosis in Drosophila. Curr Biol 16 : 1435 1440.
182. Tang, G. (2005) siRNA and miRNA: an insight into RISCs. Trends Biochem Sci 30 : 106 114.
183. Tarun, S.Z. Jr. Sachs, A.B. (1995) A common function for mRNA 5′ and 3′ ends in translation initiation in yeast. Genes Dev 9 : 2997 3007.
184. Teleman, A.A., Maitra, S. Cohen, S.M. (2006) Drosophila lacking microRNA miR-278 are defective in energy homeostasis. Genes Dev 20 : 417 422.
185. Temme, C., Zaessinger, S., Meyer, S., Simonelig, M. Wahle, E. (2004) A complex containing the CCR4 and CAF1 proteins is involved in mRNA deadenylation in Drosophila. Embo J 23 : 2862 2871.
186. Tharun, S. Parker, R. (1999) Analysis of mutations in the yeast mRNA decapping enzyme. Genetics 151 : 1273 1285.
187. Theurkauf, W.E., Smiley, S., Wong, M.L. Alberts, B.M. (1992) Reorganization of the cytoskeleton during Drosophila oogenesis: implications for axis specification and intercellular transport. Development (Cambridge, UK) 115 : 923 936.
188. Tierney, M.J. Medcalf, R.L. (2001) Plasminogen activator inhibitor type 2 contains mRNA instability elements within exon 4 of the coding region. Sequence homology to coding region instability determinants in other mRNAs. J Biol Chem 276 : 13675 13684.
189. Till, D.D., Linz, B., Seago, J.E., Elgar, S.J., Marujo, P.E., Elias, M.L., Arraiano, C.M., McClellan, J.A., McCarthy, J.E. Newbury, S.F. (1998) Identification and developmental expression of a 5′-3′ exoribonuclease from Drosophila melanogaster. Mech Dev 79 : 51 55.
190. Tomari, Y., Du, T., Haley, B., Schwarz, D.S., Bennett, R., Cook, H.A., Koppetsch, B.S., Theurkauf, W.E. Zamore, P.D. (2004a) RISC assembly defects in the Drosophila RNAi mutant ARMITAGE. Cell 116 : 831 841.
191. Tomari, Y., Matranga, C., Haley, B., Martinez, N. Zamore, P.D. (2004b) A protein sensor for siRNA asymmetry. Science 306 : 1377 1380.
192. Tourriere, H., Gallouzi, I.E., Chebli, K., Capony, J.P., Mouaikel, J., van der Geer, P. Tazi, J. (2001) RasGAP-associated endoribonuclease G3Bp: selective RNA degradation and phosphorylation-dependent localization. Mol Cell Biol 21 : 7747 7760.
193. Tuschl, T., Zamore, P.D., Lehmann, R., Bartel, D.P. Sharp, P.A. (1999) Targeted mRNA degradation by double-stranded RNA in vitro. Genes Dev 13 : 3191 3197.
194. Vagin, V.V., Sigova, A., Li, C., Seitz, H., Gvozdev, V. Zamore, P.D. (2006) A distinct small RNA pathway silences selfish genetic elements in the germline. Science 313 : 320 324.
195. Vardy, L. Orr-Weaver, T.L. (2007) The Drosophila PNG kinase complex regulates the translation of cyclin B. Dev Cell 12 : 157 166.
196. Vasudevan, S. Peltz, S.W. (2001) Regulated ARE-mediated mRNA decay in Saccharomyces cerevisiae. Mol Cell 7 : 1191 1200.
197. Voeltz, G.K. Steitz, J.A. (1998) AUUUA sequences direct mRNA deadenylation uncoupled from decay during Xenopus early development. Mol Cell Biol 18 : 7537 7545.
198. Wang, Z. Kiledjian, M. (2000a) Identification of an erythroid-enriched endoribonuclease activity involved in specific mRNA cleavage. Embo J 19 : 295 305.
199. Wang, X.H., Aliyari, R., Li, W.X., Li, H.W., Kim, K., Carthew, R., Atkinson, P. Ding, S.W. (2006) RNA interference directs innate immunity against viruses in adult Drosophila. Science 312 : 452 454.
200. Wang, Z. Kiledjian, M. (2000b) The poly(A)-binding protein and an mRNA stability protein jointly regulate an endoribonuclease activity. Mol Cell Biol 20 : 6334 6341.
201. Wang, Z. Kiledjian, M. (2001) Functional link between the mammalian exosome and mRNA decapping. Cell 107 : 751 762.
202. Wells, S.E., Hillner, P.E., Vale, R.D. Sachs, A.B. (1998) Circularization of mRNA by eukaryotic translation initiation factors. Mol Cell 2 : 135 140.
203. Wharton, R.P., Sonoda, J., Lee, T., Patterson, M. Murata, Y. (1998) The PUMILIO RNA-binding domain is also a translational regulator. Mol Cell 1 : 863 872.
204. Wharton, R.P. Struhl, G. (1991) RNA regulatory elements mediate control of Drosophila body pattern by the posterior morphogen nanos. Cell 67 : 955 967.
205. Whitaker, M. (2006) Calcium at fertilization and in early development. Physiol Rev 86 : 25 88.
206. Wickens, M., Bernstein, D.S., Kimble, J. Parker, R. (2002) A PUF family portrait: 3′ UTR regulation as a way of life. Trends Genet 18 : 150 157.
207. Wieschaus, E. Sweeton, D. (1988) Requirements for X-linked zygotic gene activity during cellularization of early Drosophila embryos. Development (Cambridge, UK) 104 : 483 493.
208. Williams, R.W. Rubin, G.M. (2002) ARGONAUTE1 is required for efficient RNA interference in Drosophila embryos. Proc Natl Acad Sci USA 99 : 6889 6894.
209. Wilson, J.E., Connell, J.E. Macdonald, P.M. (1996) AUBERGINE enhances oskar translation in the Drosophila ovary. Development (Cambridge, UK) 122 : 1631 1639.
210. Wilson, T. Treisman, R. (1988) Removal of poly(A) and consequent degradation of c-fos mRNA facilitated by 3′ AU-rich sequences. Nature 336 : 396 399.
211. Wisdom, R. Lee, W. (1991) The protein-coding region of c-myc mRNA contains a sequence that specifies rapid mRNA turnover and induction by protein synthesis inhibitors. Genes Dev 5 : 232 243.
212. Wolke, U., Weidinger, G., Koprunner, M. Raz, E. (2002) Multiple levels of posttranscriptional control lead to germ line-specific gene expression in the zebrafish. Curr Biol 12 : 289 294.
213. Wreden, C., Verrotti, A.C., Schisa, J.A., Lieberfarb, M.E. Strickland, S. (1997) Nanos and PUMILIO establish embryonic polarity in Drosophila by promoting posterior deadenylation of hunchback mRNA. Development (Cambridge, UK) 124 : 3015 3023.
214. Wu, L., Fan, J. Belasco, J.G. (2006) MicroRNAs direct rapid deadenylation of mRNA. Proc Natl Acad Sci USA 103 : 4034 4039.
215. Xu, P., Vernooy, S.Y., Guo, M. Hay, B.A. (2003) The Drosophila microRNA Mir-14 suppresses cell death and is required for normal fat metabolism. Curr Biol 13 : 790 795.
216. Yasuda, G.K. Schubiger, G. (1992) Temporal regulation in the early embryo: is MBT too good to be true? Trends Genet 8 : 124 127.
217. Zaessinger, S., Busseau, I. Simonelig, M. (2006) Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by SMAUG/CCR4. Development (Cambridge, UK) 133 : 4573 4583.
218. Zamore, P.D., Williamson, J.R. Lehmann, R. (1997) The PUMILIO protein binds RNA through a conserved domain that defines a new class of RNA-binding proteins. RNA 3 : 1421 1433.