Smaug: An unexpected journey into the mechanisms of post-transcriptional regulation

Fly

Volumn 7, Issue 3, 2013, Pages 142-145

  Pinder, Benjamin D ^a   Smibert, Craig A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

Author keywords

Argonaute; Drosophila; Embryo; Nanos; Smaug; Translational control

Indexed keywords

ARGONAUTE PROTEIN; DROSOPHILA PROTEIN; MESSENGER RNA; REPRESSOR PROTEIN; RNA BINDING PROTEIN;

ANIMAL; DROSOPHILA; EMBRYO; FEMALE; GENETICS; METABOLISM; NANOS; NOTE; SMAUG; TRANSLATIONAL CONTROL;

ARGONAUTE; DROSOPHILA; EMBRYO; NANOS; SMAUG; TRANSLATIONAL CONTROL;

ANIMALS; ARGONAUTE PROTEINS; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; REPRESSOR PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84879908339     PISSN: 19336934     EISSN: 19336942     Source Type: Journal    
DOI: 10.4161/fly.24336     Document Type: Article

References (30)

1. Smibert CA, Wilson JE, Kerr K, Macdonald PM. Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 1996; 10:2600-9. PMID:8895661; http://dx.doi.org/10.1101/gad.10.20.2600
2. Smibert CA, Lie YS, Shillinglaw W, Henzel WJ, Macdonald PM. Smaug, a novel and conserved protein, contributes to repression of nanos mRNA translation in vitro. RNA 1999; 5:1535-47. PMID:10606265; http://dx.doi.org/10.1017/S1355838299991392
3. Dahanukar A, Walker JA, Wharton RP. Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol Cell 1999; 4:20918. PMID:10488336; http://dx.doi.org/10.1016/S1097-2765(00)80368-8
4. Aviv T, Lin Z, Lau S, Rendl LM, Sicheri F, Smibert CA. The RNA-binding SAM domain of Smaug defines a new family of post-transcriptional regulators. Nat Struct Biol 2003; 10:614-21. PMID:12858164; http://dx.doi.org/10.1038/nsb956
5. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, et al. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 2007; 12:143-55. PMID:17199047; http://dx.doi.org/10.1016/j.devcel.2006.10.005
6. Green JB, Gardner CD, Wharton RP, Aggarwal AK. RNA recognition via the SAM domain of Smaug. Mol Cell 2003; 11:1537-48. PMID:12820967; http://dx.doi.org/10.1016/S1097-2765(03)00178-3
7. Baez MV, Boccaccio GL. Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J Biol Chem 2005; 280:43131-40. PMID:16221671; http://dx.doi.org/10.1074/jbc.M508374200
8. Rendl LM, Bieman MA, Smibert CAS. S. cerevisiae Vts1p induces deadenylation-dependent transcript degradation and interacts with the Ccr4p-Pop2pNot deadenylase complex. RNA 2008; 14:1328-36. PMID:18469165; http://dx.doi.org/10.1261/rna.955508
9. Hammell CM. The microRNA-argonaute complex: a platform for mRNA modulation. RNA Biol 2008; 5:123-7. PMID:18698153; http://dx.doi.org/10.4161/rna.5.3.6570
10. Pinder BD, Smibert CA. microRNA-independent recruitment of Argonaute 1 to nanos mRNA through the Smaug RNA-binding protein. EMBO Rep 2013; 14:80-6. PMID:23184089; http://dx.doi.org/10.1038/embor.2012.192
11. Dahanukar A, Wharton RP. The Nanos gradient in Drosophila embryos is generated by translational regulation. Genes Dev 1996; 10:2610-20. PMID:8895662; http://dx.doi.org/10.1101/gad.10.20.2610
12. Djuranovic S, Nahvi A, Green R. A parsimonious model for gene regulation by miRNAs. Science 2011; 331:550-3. PMID:21292970; http://dx.doi.org/10.1126/science.1191138
13. Elkayam E, Kuhn CD, Tocilj A, Haase AD, Greene EM, Hannon GJ, et al. The structure of human argonaute-2 in complex with miR-20a. Cell 2012; 150:100-10. PMID:22682761; http://dx.doi.org/10.1016/j.cell.2012.05.017
14. Leung AK, Young AG, Bhutkar A, Zheng GX, Bosson AD, Nielsen CB, et al. Genome-wide identification of Ago2 binding sites from mouse embryonic stem cells with and without mature microRNAs. Nat Struct Mol Biol 2011; 18:237-44. PMID:21258322; http://dx.doi.org/10.1038/nsmb.1991
15. Frohn A, Eberl HC, Stöhr J, Glasmacher E, Rüdel S, Heissmeyer V, et al. Dicer-dependent and -independent Argonaute2 protein interaction networks in mammalian cells. Mol Cell Proteomics 2012; 11:1442-56. PMID:22918229; http://dx.doi.org/10.1074/mcp.M112.017756
16. Friend K, Campbell ZT, Cooke A, Kroll-Conner P, Wickens MP, Kimble J. A conserved PUF-Ago-eEF1A complex attenuates translation elongation. Nat Struct Mol Biol 2012; 19:176-83. PMID:22231398; http://dx.doi.org/10.1038/nsmb.2214
17. Smibert CA, Wilson JE, Kerr K, Macdonald PM. Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 1996; 10:2600-9. PMID:8895661; http://dx.doi.org/10.1101/gad.10.20.2600
18. Nelson MR, Leidal AM, Smibert CA. Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO J 2004; 23:150-9. PMID:14685270; http://dx.doi.org/10.1038/sj.emboj.7600026
19. Andrews S, Snowflack DR, Clark IE, Gavis ER. Multiple mechanisms collaborate to repress nanos translation in the Drosophila ovary and embryo. RNA 2011; 17:967-77. PMID:21460235; http://dx.doi.org/10.1261/rna.2478611
20. Jeske M, Moritz B, Anders A, Wahle E. Smaug assembles an ATP-dependent stable complex repressing nanos mRNA translation at multiple levels. EMBO J 2011; 30:90-103. PMID:21081899; http://dx.doi.org/10.1038/emboj.2010.283
21. Igreja C, Izaurralde E. CUP promotes deadenylation and inhibits decapping of mRNA targets. Genes Dev 2011; 25:1955-67. PMID:21937713; http://dx.doi.org/10.1101/gad.17136311
22. Semotok JL, Cooperstock RL, Pinder BD, Vari HK, Lipshitz HD, Smibert CA. Smaug recruits the CCR4/POP2/NOT deadenylase complex to trigger maternal transcript localization in the early Drosophila embryo. Curr Biol 2005; 15:284-94. PMID:15723788; http://dx.doi.org/10.1016/j.cub.2005.01.048
23. Jeske M, Meyer S, Temme C, Freudenreich D, Wahle E. Rapid ATP-dependent deadenylation of nanos mRNA in a cell-free system from Drosophila embryos. J Biol Chem 2006; 281:25124-33. PMID:16793774; http://dx.doi.org/10.1074/jbc.M604802200
24. Zaessinger S, Busseau I, Simonelig M. Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 2006; 133:4573-83. PMID:17050620; http://dx.doi.org/10.1242/dev.02649
25. Semotok JL, Luo H, Cooperstock RL, Karaiskakis A, Vari HK, Smibert CA, et al. Drosophila maternal Hsp83 mRNA destabilization is directed by multiple SMAUG recognition elements in the open reading frame. Mol Cell Biol 2008; 28:6757-72. PMID:18794360; http://dx.doi.org/10.1128/MCB.00037-08
26. Sachs A. Physical and Functional Interactions between the mRNA Cap Structure and the Poly(A) Tail. In: Hershey JWB, Mathews MB, Sonenberg N, eds. Translational control of gene expression. Cold Spring Harbor: Cold Spring Harbor Laboratory Press, 2000:447-65
27. Rouget C, Papin C, Boureux A, Meunier AC, Franco B, Robine N, et al. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010; 467:1128-32. PMID:20953170; http://dx.doi.org/10.1038/nature09465
28. Iwasaki S, Kawamata T, Tomari Y. Drosophila argonaute1 and argonaute2 employ distinct mechanisms for translational repression. Mol Cell 2009; 34:58-67. PMID:19268617; http://dx.doi.org/10.1016/j.molcel.2009.02.010
29. Semotok JL, Lipshitz HD. Regulation and function of maternal mRNA destabilization during early Drosophila development. Differentiation 2007; 75:482-506. PMID:17509066; http://dx.doi.org/10.1111/j.1432-0436.2007.00178.x
30. Nelson MR, Luo H, Vari HK, Cox BJ, Simmonds AJ, Krause HM, et al. A multiprotein complex that mediates translational enhancement in Drosophila. J Biol Chem 2007; 282:34031-8. PMID:17890223; http://dx.doi.org/10.1074/jbc.M706363200