Modeling the binding specificity of the RNA-binding protein GLD-1 suggests a function of coding region-located sites in translational repression

RNA

Volumn 19, Issue 10, 2013, Pages 1317-1326

  Brümmer, Anneke ^a   Kishore, Shivendra ^a   Subasic, Deni ^b   Hengartner, Michael ^b   Zavolan, Mihaela ^a  

^a UNIVERSITY OF BASEL   (Switzerland)

^b UNIVERSITY OF ZURICH   (Switzerland)

Author keywords

Accessibility; Binding site prediction; GLD 1; RNA binding protein (RBP); Stabilization; Translation repression

Indexed keywords

MESSENGER RNA; PROTEIN GLD 1; RNA BINDING PROTEIN; UNCLASSIFIED DRUG;

ACCURACY; ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; IMMUNOPRECIPITATION; NONHUMAN; POLYSOME; PREDICTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CROSS LINKING; PROTEIN FUNCTION; TRANSLATION REGULATION;

ACCESSIBILITY; BINDING SITE PREDICTION; GLD-1; RNA-BINDING PROTEIN (RBP); STABILIZATION; TRANSLATION REPRESSION;

ANIMALS; BINDING SITES; CAENORHABDITIS ELEGANS; CAENORHABDITIS ELEGANS PROTEINS; GENE EXPRESSION REGULATION; IMMUNOPRECIPITATION; MODELS, THEORETICAL; OPEN READING FRAMES; PROTEIN BINDING; PROTEIN BIOSYNTHESIS; RNA, MESSENGER;

EID: 84884677366     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.037531.112     Document Type: Article

References (41)

1. Auweter SD, Oberstrass FC, Allain FH. 2006. Sequence-specific binding of single-stranded RNA: Is there a code for recognition? Nucleic Acids Res 34: 4943-4959. (Pubitemid 44605637)
2. Bartel DP. 2009. MicroRNAs: Target recognition and regulatory functions. Cell 136: 215-233.
3. Bernhart SH, Hofacker IL, Stadler PF. 2006. Local RNA base pairing probabilities in large sequences. Bioinformatics 22: 614-615. (Pubitemid 43372823)
4. Beuck C, Szymczyna BR, Kerkow DE, Carmel AB, Columbus L, Stanfield RL, Williamson JR. 2010. Structure of the GLD-1 homodimerization domain: Insights into STAR protein-mediated translational regulation. Structure 18: 377-389.
5. Biedermann B, Wright J, Senften M, Kalchhauser I, Sarathy G, Lee MH, Ciosk R. 2009. Translational repression of cyclin E prevents precocious mitosis and embryonic gene activation during C. elegans meiosis. Dev Cell 17: 355-364.
6. Darnell RB. 2010. HITS-CLIP: Panoramic views of protein -RNA regulation in living cells. Wiley Interdiscip Rev RNA 1: 266-286.
7. Gaidatzis D, van Nimwegen E, Hausser J, Zavolan M. 2007. Inference of miRNA targets using evolutionary conservation and pathway analysis. BMC Bioinformatics 8: 69.
8. Galarneau A, Richard S. 2009. The STAR RNA binding proteins GLD-1, QKI, SAM68 and SLM-2 bind bipartite RNA motifs. BMC Mol Biol 10: 47.
9. Guo H, Ingolia NT, Weissman JS, Bartel DP. 2010. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 466: 835-840.
10. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M Jr, Jungkamp AC, Munschauer M, et al. 2010. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 141: 129-141.
11. Hausser J, Landthaler M, Jaskiewicz L, Gaidatzis D, Zavolan M. 2009. Relative contribution of sequence and structure features to the mRNA binding of Argonaute/EIF2C-miRNA complexes and the degradation of miRNA targets. Genome Res 19: 2009-2020.
12. Hausser J, Syed AP, Bilen B, Zavolan M. 2013. Analysis of CDS-located miRNA target sites suggests that they can effectively inhibit translation. Genome Res 23: 604-615.
13. Hofacker IL, Tafer H. 2010. Designing optimal siRNA based on target site accessibility. Methods Mol Biol 623: 137-154.
14. Jan E, Motzny CK, Graves LE, Goodwin EB. 1999. The STAR protein, GLD-1, is a translational regulator of sexual identity in Caenorhabditis elegans. EMBO J 18: 258-269. (Pubitemid 29005041)
15. Jungkamp AC, Stoeckius M, Mecenas D, Grün D, Mastrobuoni G, Kempa S, Rajewsky N. 2011. In vivo and transcriptome-wide identification of RNA binding protein target sites. Mol Cell 44: 828-840.
16. Kazan H, Ray D, Chan ET, Hughes TR, Morris Q. 2010. RNAcontext: A new method for learning the sequence and structure binding preferences of RNA-binding proteins. PLoS Comput Biol 6: e1000832.
17. Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E. 2007. The role of site accessibility in microRNA target recognition. Nat Genet 39: 1278-1284. (Pubitemid 47482690)
18. Khorshid M, Rodak C, Zavolan M. 2010. CLIPZ: A database and analysis environment for experimentally determined binding sites of RNAbinding proteins. Nucleic Acids Res 39: D245-D252.
19. Kishore S, Jaskiewicz L, Burger L, Hausser J, Khorshid M, Zavolan M. 2011. A quantitative analysis of CLIP methods for identifying binding sites of RNA-binding proteins. Nat Methods 8: 559 -564.
20. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, Rajewsky N. 2011. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein HuR. Mol Cell 43: 340-352.
21. Lee MH, Schedl T. 2001. Identification of in vivo mRNA targets of GLD-1, a maxi-KH motif containing protein required for C. elegans germ cell development. Genes Dev 15: 2408-2420. (Pubitemid 32899744)
22. Lee MH, Schedl T. 2004. Translation repression by GLD-1 protects its mRNA targets from nonsense-mediated mRNA decay in C. elegans. Genes Dev 18: 1047-1059. (Pubitemid 38620244)
23. Marin VA, Evans TC. 2003. Translational repression of a C. elegans Notch mRNA by the STAR/KH domain protein GLD-1. Development 130: 2623-2632. (Pubitemid 37069579)
24. Mootz D, Ho DM, Hunter CP. 2004. The STAR/Maxi-KH domain protein GLD-1 mediates a developmental switch in the translational control of C. elegans. Development 131: 3263-3272. (Pubitemid 39139874)
25. Petersen CP, Bordeleau ME, Pelletier J, Sharp PA. 2006. Short RNAs repress translation after initiation in mammalian cells. Mol Cell 21: 533-542. (Pubitemid 43228008)
26. Rajewsky N, Vergassola M, Gaul U, Siggia ED. 2002. Computational detection of genomic cis-regulatory modules applied to body patterning in the early Drosophila embryo. BMC Bioinformatics 3: 30.
27. Ray D, Kazan H, Chan ET, Peña Castillo L, Chaudhry S, Talukder S, Blencowe BJ, Morris Q, Hughes TR. 2009. Rapid and systematic analysis of the RNA recognition specificities of RNA-binding proteins. Nat Biotechnol 27: 667- 670.
28. Ryder SP, Frater LA, Abramowitz DL, Goodwin EB, Williamson JR. 2004. RNA target specificity of the STAR/GSG domain post-transcriptional regulatory protein GLD-1. Nat Struct Mol Biol 11: 20-28. (Pubitemid 38173437)
29. Scheckel C, Gaidatzis D, Wright JE, Ciosk R. 2012. Genome-wide analysis of GLD-1-mediated mRNA regulation suggests a role in mRNA storage. PLoS Genet 8: e1002742.
30. Schumacher B, Hanazawa M, Lee MH, Nayak S, Volkmann K, Hofmann ER, Hengartner M, Schedl T, Gartner A. 2005. Translational repression of C. elegans p53 by GLD-1 regulates DNA damage-induced apoptosis. Cell 120: 357-368.
31. Siddharthan R, Siggia ED, van Nimwegen E. 2005. PhyloGibbs: A Gibbs sampling motif finder that incorporates phylogeny. PLoS Comput Biol 1: e67.
32. Sugimoto Y, König J, Hussain S, Zupan B, Curk T, Frye M, Ule J. 2012. Analysis of CLIP and iCLIP methods for nucleotide-resolution studies of protein-RNA interactions. Genome Biol 13: R67.
33. Ule J, Jensen KB, Ruggiu M, Mele A, Ule A, Darnell RB. 2003. CLIP identifies Nova-regulated RNA networks in the brain. Science 302: 1212-1215. (Pubitemid 37421026)
34. van Nimwegen E. 2007. Finding regulatory elements and regulatory motifs: A general probabilistic framework. BMC Bioinformatics 8 Suppl 6: S4.
35. Wang X, Zhao Y, Wong K, Ehlers P, Kohara Y, Jones SJ, Marra MA, Holt RA, Moermann DG, Hansen D. 2009. Identification of genes expressed in the hermaphrodite germ line of C. elegans using SAGE. BMC Genomics 10: 213.
36. Wang X, Juan L, Lv J, Wang K, Sanford JR, Liu Y. 2011. Predicting sequence and structural specificities of RNA binding regions recognized by splicing factor SRSF1. BMC Genomics 12 Suppl 5: S8.
37. Wright JE, Gaidatzis D, Senften M, Farley BM, Westhof E, Ryder SP, Ciosk R. 2011. A quantitative RNA code for mRNA target selection by the germline fate determinant GLD-1. EMBO J 30: 533-545.
38. Xu L, Paulsen J, Yoo Y, Goodwin EB, Strome S. 2001. Caenorhabditis elegans MES-3 is a target of GLD-1 and functions epigenetically in germline development. Genetics 159: 1007-1017. (Pubitemid 34033447)
39. Yeo GW, Coufal NG, Liang TY, Peng GE, Fu XD, Gage FH. 2009. An RNA code for the FOX2 splicing regulator revealed by mapping RNA-protein interactions in stem cells. Nat Struct Mol Biol 16: 130-137.
40. Zhang C, Frias MA, Mele A, Ruggiu M, Eom T, Marney CB, Wang H, Licatalosi DD, Fak JJ, Darnell RB. 2010. Integrative modeling defines the Nova splicing-regulatory network and its combinatorial controls. Science 329: 439-443.
41. Zisoulis DG, Yeo GW, Pasquinelli AE. 2011. Comprehensive identification of miRNA target sites in live animals. Methods Mol Biol 732: 169-185.