Global regulation of mRNA translation and stability in the early Drosophila embryo by the Smaug RNA-binding protein

Genome Biology

Volumn 15, Issue 1, 2014, Pages

  Chen, Linan ^a   Dumelie, Jason G ^a   Li, Xiao ^a   Cheng, Matthew H K ^a   Yang, Zhiyong ^a   Laver, John D ^a   Siddiqui, Najeeb U ^a,c   Westwood, J Timothy ^b   Morris, Quaid ^a   Lipshitz, Howard D ^a   Smibert, Craig A ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

6 PHOSPHOFRUCTOKINASE; ADENOSINE TRIPHOSPHATASE; BICAUDAL C PROTEIN; CHAPERONIN CONTAINING TCP1; FAT DROPLET; HEXOKINASE; MESSENGER RNA; POLYCOMB REPRESSIVE COMPLEX 2; REGULATORY PARTICLE NONATPASE 7; RNA BINDING PROTEIN; SMAUG PROTEIN; SU(Z)12 PROTEIN; UNCLASSIFIED DRUG; EDETIC ACID; GLYCOLYTIC ENZYME; PHOSOPHOFRUCTOKINASE; PUROMYCIN; RNA 18S; DROSOPHILA PROTEIN; HEAT SHOCK PROTEIN; HSP83 PROTEIN, DROSOPHILA; NANOS PROTEIN, DROSOPHILA; REPRESSOR PROTEIN; SMG PROTEIN, DROSOPHILA;

ARTICLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DROSOPHILA; EMBRYO; GENE REPRESSION; METABOLIC REGULATION; NONHUMAN; POLYSOME; PROTEIN DEGRADATION; PROTEIN FOLDING; PROTEIN RNA BINDING; RNA STABILITY; RNA TRANSLATION; TRANSLATION REGULATION; DNA RNA HYBRIDIZATION; DOWN REGULATION; GENE EXPRESSION REGULATION; GENE LOCATION; GENE TARGETING; IMMUNOPRECIPITATION; LIPID STORAGE; MICROARRAY ANALYSIS; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN STABILITY; REVERSE TRANSCRIPTION; RNA ANALYSIS; TRANSCRIPTION INITIATION; WILD TYPE; ALLELE; ANIMAL; EMBRYOLOGY; FEMALE; GENETIC EPIGENESIS; GENETICS; METABOLISM; NONMAMMALIAN EMBRYO;

ALLELES; ANIMALS; DROSOPHILA; DROSOPHILA PROTEINS; EMBRYO, NONMAMMALIAN; EPIGENESIS, GENETIC; FEMALE; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HEAT-SHOCK PROTEINS; IMMUNOPRECIPITATION; REPRESSOR PROTEINS; RNA, MESSENGER; RNA-BINDING PROTEINS;

EID: 84891687085     PISSN: None     EISSN: 1474760X     Source Type: Journal    
DOI: 10.1186/gb-2014-15-1-r4     Document Type: Article

References (90)

1. Tadros W, Lipshitz HD. The maternal-to-zygotic transition: a play in two acts. Development 2009, 136:3033-3042. 10.1242/dev.033183, 19700615.
2. Hamatani T, Carter MG, Sharov AA, Ko MS. Dynamics of global gene expression changes during mouse preimplantation development. Dev Cell 2004, 6:117-131. 10.1016/S1534-5807(03)00373-3, 14723852.
3. Giraldez AJ, Mishima Y, Rihel J, Grocock RJ, Van Dongen S, Inoue K, Enright AJ, Schier AF. Zebrafish MiR-430 promotes deadenylation and clearance of maternal mRNAs. Science 2006, 312:75-79. 10.1126/science.1122689, 16484454.
4. De Renzis S, Elemento O, Tavazoie S, Wieschaus EF. Unmasking activation of the zygotic genome using chromosomal deletions in the Drosophila embryo. PLoS Biol 2007, 5:e117. 10.1371/journal.pbio.0050117, 1854917, 17456005.
5. Ferg M, Sanges R, Gehrig J, Kiss J, Bauer M, Lovas A, Szabo M, Yang L, Straehle U, Pankratz MJ, Olasz F, Stupka E, Muller F. The TATA-binding protein regulates maternal mRNA degradation and differential zygotic transcription in zebrafish. EMBO J 2007, 26:3945-3956. 10.1038/sj.emboj.7601821, 1950726, 17703193.
6. Lecuyer E, Yoshida H, Parthasarathy N, Alm C, Babak T, Cerovina T, Hughes TR, Tomancak P, Krause HM. Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 2007, 131:174-187. 10.1016/j.cell.2007.08.003, 17923096.
7. Mathavan S, Lee SGP, Mak A, Miller LD, Murthy KRK, Govindarajan KR, Tong Y, Wu YL, Lam SH, Yang H, Ruan YJ, Korzh V, Gong ZY, Liu ET, Lufkin T. Transcriptome analysis of zebrafish embryogenesis using microarrays. PLoS Genetics 2005, 1:260-276. 1193535, 16132083.
8. Qin X, Ahn S, Speed TP, Rubin GM. Global analyses of mRNA translational control during early Drosophila embryogenesis. Genome Biol 2007, 8:R63. 10.1186/gb-2007-8-4-r63, 1896012, 17448252.
9. Tadros W, Goldman AL, Babak T, Menzies F, Vardy L, Orr-Weaver T, Hughes TR, Westwood JT, Smibert CA, Lipshitz HD. SMAUG is a major regulator of maternal mRNA destabilization in Drosophila and its translation is activated by the PAN GU kinase. Dev Cell 2007, 12:143-155. 10.1016/j.devcel.2006.10.005, 17199047.
10. Bushati N, Stark A, Brennecke J, Cohen SM. Temporal reciprocity of miRNAs and their targets during the maternal-to-zygotic transition in Drosophila. Curr Biol 2008, 18:501-506. 10.1016/j.cub.2008.02.081, 18394895.
11. Benoit B, He CH, Zhang F, Votruba SM, Tadros W, Westwood JT, Smibert CA, Lipshitz HD, Theurkauf WE. An essential role for the RNA-binding protein Smaug during the Drosophila maternal-to-zygotic transition. Development 2009, 136:923-932. 10.1242/dev.031815, 2727558, 19234062.
12. Thomsen S, Anders S, Janga SC, Huber W, Alonso CR. Genome-wide analysis of mRNA decay patterns during early Drosophila development. Genome Biol 2010, 11:R93. 10.1186/gb-2010-11-9-r93, 2965385, 20858238.
13. Bazzini AA, Lee MT, Giraldez AJ. Ribosome profiling shows that miR-430 reduces translation before causing mRNA decay in zebrafish. Science 2012, 336:233-237. 10.1126/science.1215704, 3547538, 22422859.
14. Smibert CA, Wilson JE, Kerr K, Macdonald PM. Smaug protein represses translation of unlocalized nanos mRNA in the Drosophila embryo. Genes Dev 1996, 10:2600-2609. 10.1101/gad.10.20.2600, 8895661.
15. Dahanukar A, Walker JA, Wharton RP. Smaug, a novel RNA-binding protein that operates a translational switch in Drosophila. Mol Cell 1999, 4:209-218. 10.1016/S1097-2765(00)80368-8, 10488336.
16. 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, 5:1535-1547. 10.1017/S1355838299991392, 1369876, 10606265.
17. 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, 10:614-621. 10.1038/nsb956, 12858164.
18. Baez MV, Boccaccio GL. Mammalian Smaug is a translational repressor that forms cytoplasmic foci similar to stress granules. J Biol Chem 2005, 280:43131-43140. 10.1074/jbc.M508374200, 16221671.
19. Green JB, Gardner CD, Wharton RP, Aggarwal AK. RNA recognition via the SAM domain of Smaug. Mol Cell 2003, 11:1537-1548. 10.1016/S1097-2765(03)00178-3, 12820967.
20. Aviv T, Lin Z, Ben-Ari G, Smibert CA, Sicheri F. Sequence-specific recognition of RNA hairpins by the SAM domain of Vts1p. Nat Struct Mol Biol 2006, 13:168-176. 10.1038/nsmb1053, 16429151.
21. Johnson PE, Donaldson LW. RNA recognition by the Vts1p SAM domain. Nat Struct Mol Biol 2006, 13:177-178. 10.1038/nsmb1039, 16429155.
22. Oberstrass FC, Lee A, Stefl R, Janis M, Chanfreau G, Allain FHT. Shape-specific recognition in the structure of the Vts1p SAM domain with RNA. Nat Struct Mol Biol 2006, 13:160-167. 10.1038/nsmb1038, 16429156.
23. Rendl LM, Bieman MA, Smibert CA. S. cerevisiae Vts1p induces deadenylation-dependent transcript degradation and interacts with the Ccr4p-Pop2p-Not deadenylase complex. RNA 2008, 14:1328-1336. 10.1261/rna.955508, 2441989, 18469165.
24. Rendl LM, Bieman MA, Vari HK, Smibert CA. The eIF4E-binding protein Eap1p functions in Vts1p-mediated transcript decay. PLoS One 2012, 7:e47121. 10.1371/journal.pone.0047121, 3468468, 23071728.
25. Nelson MR, Leidal AM, Smibert CA. Drosophila Cup is an eIF4E-binding protein that functions in Smaug-mediated translational repression. EMBO J 2004, 23:150-159. 10.1038/sj.emboj.7600026, 1271664, 14685270.
26. Pinder BD, Smibert CA. microRNA-independent recruitment of Argonaute 1 to nanos mRNA through the Smaug RNA-binding protein. EMBO Rep 2013, 14:80-86. 10.1038/embor.2012.192, 3537145, 23184089.
27. Hammell CM. The microRNA-argonaute complex: a platform for mRNA modulation. RNA Biol 2008, 5:123-127. 10.4161/rna.5.3.6570, 18698153.
28. 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, 15:284-294. 10.1016/j.cub.2005.01.048, 15723788.
29. 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, 281:25124-25133. 10.1074/jbc.M604802200, 16793774.
30. Zaessinger S, Busseau I, Simonelig M. Oskar allows nanos mRNA translation in Drosophila embryos by preventing its deadenylation by Smaug/CCR4. Development 2006, 133:4573-4583. 10.1242/dev.02649, 17050620.
31. Semotok JL, Luo H, Cooperstock RL, Karaiskakis A, Vari HK, Smibert CA, Lipshitz HD. Drosophila maternal Hsp83 mRNA destabilization is directed by multiple SMAUG recognition elements in the open reading frame. Mol Cell Biol 2008, 28:6757-6772. 10.1128/MCB.00037-08, 2573300, 18794360.
32. Rouget C, Papin C, Boureux A, Meunier AC, Franco B, Robine N, Lai EC, Pelisson A, Simonelig M. Maternal mRNA deadenylation and decay by the piRNA pathway in the early Drosophila embryo. Nature 2010, 467:1128-1132. 10.1038/nature09465, 20953170.
33. Semotok JL, Lipshitz HD. Regulation and function of maternal mRNA destabilization during early Drosophila development. Differentiation 2007, 75:482-506. 10.1111/j.1432-0436.2007.00178.x, 17509066.
34. Wang C, Lehmann R. Nanos is the localized posterior determinant in Drosophila. Cell 1991, 66:637-647. 10.1016/0092-8674(91)90110-K, 1908748.
35. Bergsten S, Gavis E. Role for mRNA localization in translational activation but not spatial restriction of nanos RNA. Development 1999, 126:659-669.
36. Ding D, Parkhurst SM, Halsell SR, Lipshitz HD. Dynamic Hsp83 RNA localization during Drosophila oogenesis and embryogenesis. Mol Cell Biol 1993, 13:3773-3781. 359859, 7684502.
37. Bashirullah A, Halsell SR, Cooperstock RL, Kloc M, Karaiskakis A, Fisher WW, Fu W, Hamilton JK, Etkin LD, Lipshitz HD. Joint action of two RNA degradation pathways controls the timing of maternal transcript elimination at the midblastula transition in Drosophila melanogaster. EMBO J 1999, 18:2610-2620. 10.1093/emboj/18.9.2610, 1171340, 10228172.
38. Tusher VG, Tibshirani R, Chu G. Significance analysis of microarrays applied to the ionizing radiation response. Proc Natl Acad Sci U S A 2001, 98:5116-5121. 10.1073/pnas.091062498, 33173, 11309499.
39. Grolleau A, Bowman J, Pradet-Balade B, Puravs E, Hanash S, Garcia-Sanz JA, Beretta L. Global and specific translational control by rapamycin in T cells uncovered by microarrays and proteomics. J Biol Chem 2002, 277:22175-22184. 10.1074/jbc.M202014200, 11943782.
40. Johannes G, Carter MS, Eisen MB, Brown PO, Sarnow P. Identification of eukaryotic mRNAs that are translated at reduced cap binding complex eIF4F concentrations using a cDNA microarray. Proc Natl Acad Sci U S A 1999, 96:13118-13123. 10.1073/pnas.96.23.13118, 23910, 10557283.
41. Kuhn KM, DeRisi JL, Brown PO, Sarnow P. Global and specific translational regulation in the genomic response of Saccharomyces cerevisiae to a rapid transfer from a fermentable to a nonfermentable carbon source. Mol Cell Biol 2001, 21:916-927. 10.1128/MCB.21.3.916-927.2001, 86682, 11154278.
42. Clark IE, Wyckoff D, Gavis ER. Synthesis of the posterior determinant Nanos is spatially restricted by a novel cotranslational regulatory mechanism. Curr Biol 2000, 10:1311-1314. 10.1016/S0960-9822(00)00754-5, 11069116.
43. Li X, Quon G, Lipshitz HD, Morris Q. Predicting in vivo binding sites of RNA-binding proteins using mRNA secondary structure. RNA 2010, 16:1096-1107. 10.1261/rna.2017210, 2874161, 20418358.
44. Foat BC, Stormo GD. Discovering structural cis-regulatory elements by modeling the behaviors of mRNAs. Mol Syst Biol 2009, 5:268. 2683727, 19401680.
45. Ray D, Kazan H, Cook KB, Weirauch MT, Najafabadi HS, Li X, Gueroussov S, Albu M, Zheng H, Yang A, Na H, Irimia M, Matzat LH, Dale RK, Smith SA, Yarosh CA, Kelly SM, Nabet B, Mecenas D, Li W, Laishram RS, Qiao M, Lipshitz HD, Piano F, Corbett AH, Carstens RP, Frey BJ, Anderson RA, Lynch KW, Penalva LO, Lei EP, Fraser AG, Blencowe BJ, Morris QD, Hughes TR. A compendium of RNA-binding motifs for decoding gene regulation. Nature 2013, 499:172-177. 10.1038/nature12311, 23846655.
46. Ray D, Kazan H, Chan ET, Pena Castillo L, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 2009, 27:667-670. 10.1038/nbt.1550, 19561594.
47. Kazan H, Ray D, Chan ET, Hughes TR, Morris Q. RNAcontext: a new method for learning the sequence and structure binding preferences of RNA-binding proteins. PLoS Computat Biol 2010, 6:e1000832.
48. Riordan DP, Herschlag D, Brown PO. Identification of RNA recognition elements in the Saccharomyces cerevisiae transcriptome. Nucleic Acids Res 2011, 39:1501-1509. 10.1093/nar/gkq920, 3045596, 20959291.
49. Storey JD, Tibshirani R. Statistical significance for genomewide studies. Proc Natl Acad Sci U S A 2003, 100:9440-9445. 10.1073/pnas.1530509100, 170937, 12883005.
50. Fly-FISH. [http://fly-fish.ccbr.utoronto.ca/].
51. Huang DW, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009, 37:1-13. 10.1093/nar/gkn923, 2615629, 19033363.
52. Huang DW, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009, 4:44-57.
53. Hartl FU, Bracher A, Hayer-Hartl M. Molecular chaperones in protein folding and proteostasis. Nature 2011, 475:324-332. 10.1038/nature10317, 21776078.
54. Saeki Y, Tanaka K. Assembly and function of the proteasome. Methods Mol Biol 2012, 832:315-337. 10.1007/978-1-61779-474-2_22, 22350895.
55. Farese RV, Walther TC. Lipid droplets finally get a little R-E-S-P-E-C-T. Cell 2009, 139:855-860. 10.1016/j.cell.2009.11.005, 3097139, 19945371.
56. Beller M, Riedel D, Jansch L, Dieterich G, Wehland J, Jackle H, Kuhnlein RP. Characterization of the Drosophila lipid droplet subproteome. Mol Cell Proteomics 2006, 5:1082-1094. 10.1074/mcp.M600011-MCP200, 16543254.
57. Cermelli S, Guo Y, Gross SP, Welte MA. The lipid-droplet proteome reveals that droplets are a protein-storage depot. Curr Biol 2006, 16:1783-1795. 10.1016/j.cub.2006.07.062, 16979555.
58. Pilkis SJ, Claus TH, Kurland IJ, Lange AJ. 6-Phosphofructo-2-kinase/fructose-2,6-bisphosphatase: a metabolic signaling enzyme. Annu Rev Biochem 1995, 64:799-835. 10.1146/annurev.bi.64.070195.004055, 7574501.
59. Pilkis SJ, el-Maghrabi MR, Claus TH. Hormonal regulation of hepatic gluconeogenesis and glycolysis. Annu Rev Biochem 1988, 57:755-783. 10.1146/annurev.bi.57.070188.003543, 3052289.
60. Simon JA, Kingston RE. Occupying chromatin: Polycomb mechanisms for getting to genomic targets, stopping transcriptional traffic, and staying put. Mol Cell 2013, 49:808-824. 10.1016/j.molcel.2013.02.013, 23473600.
61. Gamberi C, Lasko P. The Bic-C family of developmental translational regulators. Comp Funct Genomics 2012, 2012:141386. 3352585, 22611335.
62. Nelson MR, Luo H, Vari HK, Cox BJ, Simmonds AJ, Krause HM, Lipshitz HD, Smibert CA. A multiprotein complex that mediates translational enhancement in Drosophila. J Biol Chem 2007, 282:34031-34038. 10.1074/jbc.M706363200, 17890223.
63. Gavis ER, Lehmann R. Translational regulation of nanos by RNA localization. Nature 1994, 369:315-318. 10.1038/369315a0, 7514276.
64. 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. 10.1038/emboj.2010.283, 3020108, 21081899.
65. Dahanukar A, Wharton RP. The nanos gradient in Drosophila embryos is generated by translational regulation. Genes Dev 1996, 10:2610-2620. 10.1101/gad.10.20.2610, 8895662.
66. Gavis ER, Curtis D, Lehmann R. Identification of cis-acting sequences that control nanos RNA localization. Dev Biol 1996, 176:36-50. 10.1006/dbio.1996.9996, 8654893.
67. Klein U, Gernold M, Kloetzel PM. Cell-specific accumulation of Drosophila proteasomes (MCP) during early development. J Cell Biol 1990, 111:2275-2282. 10.1083/jcb.111.6.2275, 2116374, 2126012.
68. Reed SI. The ubiquitin-proteasome pathway in cell cycle control. Results Probl Cell Differ 2006, 42:147-181. 10.1007/b136681, 16903211.
69. Sun XH, Tso JY, Lis J, Wu R. Differential regulation of the two glyceraldehyde-3-phosphate dehydrogenase genes during Drosophila development. Mol Cell Biol 1988, 8:5200-5205. 365622, 3149711.
70. Shaw-Lee RL, Lissemore JL, Sullivan DT. Structure and expression of the triose phosphate isomerase (Tpi) gene of Drosophila melanogaster. Mol Gen Genet 1991, 230:225-229. 10.1007/BF00290672, 1720860.
71. Roselli-Rehfuss L, Ye F, Lissemore JL, Sullivan DT. Structure and expression of the phosphoglycerate kinase (Pgk) gene of Drosophila melanogaster. Mol Gen Genet 1992, 235:213-220. 10.1007/BF00279363, 1465095.
72. Shaw-Lee R, Lissemore JL, Sullivan DT, Tolan DR. Alternative splicing of fructose 1,6-bisphosphate aldolase transcripts in Drosophila melanogaster predicts three isozymes. J Biol Chem 1992, 267:3959-3967.
73. Currie PD, Sullivan DT. Structure, expression and duplication of genes which encode phosphoglyceromutase of Drosophila melanogaster. Genetics 1994, 138:352-363. 1206154, 7828819.
74. Currie PD, Sullivan DT. Structure and expression of the gene encoding phosphofructokinase (PFK) in Drosophila melanogaster. J Biol Chem 1994, 269:24679-24687.
75. Tennessen JM, Baker KD, Lam G, Evans J, Thummel CS. The Drosophila estrogen-related receptor directs a metabolic switch that supports developmental growth. Cell Metab 2011, 13:139-148. 10.1016/j.cmet.2011.01.005, 3072597, 21284981.
76. Dworkin MB, Dworkin-Rastl E. Carbon metabolism in early amphibian embryos. Trends Biochem Sci 1991, 16:229-234.
77. Dumollard R, Carroll J, Duchen MR, Campbell K, Swann K. Mitochondrial function and redox state in mammalian embryos. Semin Cell Dev Biol 2009, 20:346-353. 10.1016/j.semcdb.2008.12.013, 19530278.
78. Bartel DP, Chen CZ. Micromanagers of gene expression: the potentially widespread influence of metazoan microRNAs. Nat Rev Genet 2004, 5:396-400.
79. Hummel T, Klambt C. P-element mutagenesis. Methods Mol Biol 2008, 420:97-117. 10.1007/978-1-59745-583-1_6, 18641943.
80. FlyBase. [http://flybase.org/].
81. The Canadian Drosophila Microarray Centre. [http://www.erin.utoronto.ca/~w3flyma/overview.htm].
82. Bernhart SH, Hofacker IL, Stadler PF. Local RNA base pairing probabilities in large sequences. Bioinformatics 2006, 22:614-615. 10.1093/bioinformatics/btk014, 16368769.
83. Lange SJ, Maticzka D, Mohl M, Gagnon JN, Brown CM, Backofen R. Global or local? Predicting secondary structure and accessibility in mRNAs. Nucleic Acids Res 2012, 40:5215-5226. 10.1093/nar/gks181, 3384308, 22373926.
84. Wuchty S, Fontana W, Hofacker IL, Schuster P. Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 1999, 49:145-165. 10.1002/(SICI)1097-0282(199902)49:2<145::AID-BIP4>3.0.CO;2-G, 10070264.
85. Laver JD, Li X, Ancevicius K, Westwood JT, Smibert CA, Morris QD, Lipshitz HD. Genome-wide analysis of Staufen-associated mRNAs identifies secondary structures that confer target specificity. Nucleic Acids Res 2013, 41:9438-9460. 10.1093/nar/gkt702, 3814352, 23945942.
86. Tie F, Prasad-Sinha J, Birve A, Rasmuson-Lestander A, Harte PJ. A 1-megadalton ESC/E(Z) complex from Drosophila that contains Polycomblike and RPD3. Mol Cell Biol 2003, 23:3352-3362. 10.1128/MCB.23.9.3352-3362.2003, 153183, 12697833.
87. Chicoine J, Benoit P, Gamberi C, Paliouras M, Simonelig M, Lasko P. Bicaudal-C recruits CCR4-NOT deadenylase to target mRNAs and regulates oogenesis, cytoskeletal organization, and its own expression. Dev Cell 2007, 13:691-704. 10.1016/j.devcel.2007.10.002, 17981137.
88. Bischof J, Maeda RK, Hediger M, Karch F, Basler K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc Natl Acad Sci U S A 2007, 104:3312-3317. 10.1073/pnas.0611511104, 1805588, 17360644.
89. Worthington Biochemical. [http://www.worthington-biochem.com/HK/assay.html].
90. Edgar R, Domrachev M, Lash AE. Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 2002, 30:207-210. 10.1093/nar/30.1.207, 99122, 11752295.