Using RNA inverse folding to identify IRES-like structural subdomains

RNA Biology

Volumn 10, Issue 12, 2013, Pages 1842-1852

  Dotu, Ivan ^a   Lozano, Gloria ^b   Clote, Peter ^a   Martinez Salas, Encarnacion ^b  

^a BOSTON COLLEGE   (United States)

^b CSIC   (Spain)

Author keywords

Inverse folding; IRES elements; RNA structural domains; SHAPE analysis; Translation control

Indexed keywords

MESSENGER RNA; PROTEIN TAF6; TATA BINDING PROTEIN ASSOCIATED FACTOR; UNCLASSIFIED DRUG;

5' UNTRANSLATED REGION; ALGORITHM; AMINO ACID SEQUENCE; ARTICLE; CODON USAGE; DNA BINDING; DROSOPHILA MELANOGASTER; GENETIC CODE; INTERNAL RIBOSOME ENTRY SITE; NONHUMAN; PROTEIN DOMAIN; PROTEIN MOTIF; RNA FOLDING; RNA SEQUENCE; RNA STRUCTURE; START CODON; TISSUE CULTURE CELL; TRANSLATION INITIATION;

INVERSE FOLDING; IRES ELEMENTS; RNA STRUCTURAL DOMAINS; SHAPE ANALYSIS; TRANSLATION CONTROL;

ALGORITHMS; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; GENE EXPRESSION REGULATION; MODELS, MOLECULAR; NUCLEIC ACID CONFORMATION; PICORNAVIRIDAE; REGULATORY SEQUENCES, RIBONUCLEIC ACID; REPRODUCIBILITY OF RESULTS; RIBOSOMES; RNA FOLDING; RNA, MESSENGER; TATA-BINDING PROTEIN ASSOCIATED FACTORS; TRANSCRIPTION FACTOR TFIID;

EID: 84893121503     PISSN: 15476286     EISSN: 15558584     Source Type: Journal    
DOI: 10.4161/rna.26994     Document Type: Article

References (61)

1. Martínez-Salas E, Pacheco A, Serrano P, Fernandez N. New insights into internal ribosome entry site elements relevant for viral gene expression. J Gen Virol 2008; 89:611-26; PMID:18272751; http://dx.doi.org/10.1099/vir.0. 83426-0
2. Filbin ME, Kieft JS. Toward a structural understanding of IRES RNA function. Curr Opin Struct Biol 2009; 19:267-76; PMID:19362464; http://dx.doi.org/10.1016/j.sbi.2009.03.005
3. Spriggs KA, Bushell M, Willis AE. Translational regulation of gene expression during conditions of cell stress. Mol Cell 2010; 40:228-37; PMID:20965418; http://dx.doi.org/10.1016/j.molcel.2010.09.028
4. Liwak U, Faye MD, Holcik M. Translation control in apoptosis. Exp Oncol 2012; 34:218-30; PMID:23070007
5. Komar AA, Hatzoglou M. Cellular IRES-mediated translation: the war of ITAFs in pathophysiological states. Cell Cycle 2011; 10:229-40; PMID:21220943; http://dx.doi.org/10.4161/cc.10.2.14472
6. Martínez-Salas E. The impact of RNA structure on picornavirus IRES activity. Trends Microbiol 2008; 16:230-7; PMID:18420413; http://dx.doi.org/10. 1016/j.tim.2008.01.013
7. Fernández N, Fernandez-Miragall O, Ramajo J, García- Sacristán A, Bellora N, Eyras E, Briones C, Martínez-Salas E. Structural basis for the biological relevance of the invariant apical stem in IRES-mediated translation. Nucleic Acids Res 2011; 39:8572-85; PMID:21742761; http://dx.doi.org/10.1093/nar/gkr560
8. Domingo E, Escarmis C, Martinez MA, Martinez-Salas E, Mateu MG. Foot-and-mouth disease virus populations are quasispecies. Curr Top Microbiol Immunol 1992; 176:33-47; PMID:1318185; http://dx.doi.org/10.1007/978-3-642- 77011-1-3
9. Pacheco A, Martinez-Salas E. Insights into the biology of IRES elements through riboproteomic approaches. J Biomed Biotechnol 2010; 2010:458927; PMID:20150968; http://dx.doi.org/10.1155/2010/458927
10. Fernández N, García-Sacristán A, Ramajo J, Briones C, Martínez-Salas E. Structural analysis provides insights into the modular organization of picornavirus IRES. Virology 2011; 409:251-61; PMID:21056890; http://dx.doi.org/10.1016/j.virol.2010.10.013
11. López de Quinto S, Martínez-Salas E. Conserved structural motifs located in distal loops of aphthovirus internal ribosome entry site domain 3 are required for internal initiation of translation. J Virol 1997; 71:4171-5; PMID:9094703
12. Fernández-Miragall O, Martínez-Salas E. Structural organization of a viral IRES depends on the integrity of the GNRA motif. RNA 2003; 9:1333-44; PMID:14561883; http://dx.doi.org/10.1261/rna.5950603
13. Robertson ME, Seamons RA, Belsham GJ. A selection system for functional internal ribosome entry site (IRES) elements: analysis of the requirement for a conserved GNRA tetraloop in the encephalomyocarditis virus IRES. RNA 1999; 5:1167-79; PMID:10496218; http://dx.doi.org/10.1017/S1355838299990301
14. Fernández-Miragall O, Ramos R, Ramajo J, Martínez-Salas E. Evidence of reciprocal tertiary interactions between conserved motifs involved in organizing RNA structure essential for internal initiation of translation. RNA 2006; 12:223-34; PMID:16373480; http://dx.doi.org/10.1261/rna.2153206
15. Jung S, Schlick T. Candidate RNA structures for domain 3 of the foot-and-mouth-disease virus internal ribosome entry site. Nucleic Acids Res 2013; 41:1483-95; PMID:23275533; http://dx.doi.org/10.1093/nar/gks1302
16. Schnall-Levin M, Chindelevitch L, Berger B. In WW Cohen, A McCallum, SR Roweis (ed.) International Conference on Machine Learning 2008; volume 307. ACM International Conference Proceedings Series.
17. Bailor MH, Sun X, Al-Hashimi HM. Topology links RNA secondary structure with global conformation, dynamics, and adaptation. Science 2010; 327:202-6; PMID:20056889; http://dx.doi.org/10.1126/science.1181085
18. Gruber AR, Lorenz R, Bernhart SH, Neuböck R, Hofacker IL. The Vienna RNA websuite. Nucleic Acids Res 2008; 36(Web Server issue):W70-4; PMID:18424795; http://dx.doi.org/10.1093/nar/gkn188
19. Busch A, Backofen R. INFO-RNA - a fast approach to inverse RNA folding. Bioinformatics 2006; 22:1823-31; PMID:16709587; http://dx.doi.org/10.1093/ bioinformatics/btl194
20. Andronescu M, Fejes AP, Hutter F, Hoos HH, Condon A. A new algorithm for RNA secondary structure design. J Mol Biol 2004; 336:607-24; PMID:15095976; http://dx.doi.org/10.1016/j.jmb.2003.12.041
21. Taneda A. MODENA: a multi-objective RNA inverse folding. Adv Appl Bioinform Chem 2011; 4:1-12; PMID:21918633
22. Zadeh JN, Wolfe BR, Pierce NA. Nucleic acid sequence design via efficient ensemble defect optimization. J Comput Chem 2011; 32:439-52; PMID:20717905; http://dx.doi.org/10.1002/jcc.21633
23. Garcia-Martin JA, Clote P, Dotu I. RNAiFOLD: a constraint programming algorithm for rna inverse folding and molecular design. J Bioinform Comput Biol 2013; 11:1350001; PMID:23600819; http://dx.doi.org/10.1142/S0219720013500017
24. Hisatake K, Ohta T, Takada R, Guermah M, Horikoshi M, Nakatani Y, Roeder RG. Evolutionary conservation of human TATA-binding-polypeptide-associated factors TAFII31 and TAFII80 and interactions of TAFII80 with other TAFs and with general transcription factors. Proc Natl Acad Sci U S A 1995; 92:8195-9; PMID:7667268; http://dx.doi.org/10.1073/pnas.92.18.8195
25. Shao H, Revach M, Moshonov S, Tzuman Y, Gazit K, Albeck S, Unger T, Dikstein R. Core promoter binding by histone-like TAF complexes. Mol Cell Biol 2005; 25:206-19; PMID:15601843; http://dx.doi.org/10.1128/MCB.25.1.206-219.2005
26. Scheer E, Delbac F, Tora L, Moras D, Romier C. TFIID TAF6-TAF9 complex formation involves the HEAT repeat-containing C-terminal domain of TAF6 and is modulated by TAF5 protein. J Biol Chem 2012; 287:27580-92; PMID:22696218; http://dx.doi.org/10.1074/jbc.M112.379206
27. nd, Tjian R. TAF4 nucleates a core subcomplex of TFIID and mediates activated transcription from a TATA-less promoter. Proc Natl Acad Sci U S A 2006; 103:12347-52; PMID:16895980; http://dx.doi.org/10.1073/pnas.0605499103
28. Martínez-Salas E, Piñeiro D, Fernández N. Alternative Mechanisms to Initiate Translation in Eukaryotic mRNAs. Comp Funct Genomics 2012; 2012:391546; PMID:22536116; http://dx.doi.org/10.1155/2012/391546
29. Herbreteau CH, Weill L, Décimo D, Prévôt D, Darlix JL, Sargueil B, Ohlmann T. HIV-2 genomic RNA contains a novel type of IRES located downstream of its initiation codon. Nat Struct Mol Biol 2005; 12:1001-7; PMID:16244661; http://dx.doi.org/10.1038/nsmb1011
30. Henis-Korenblit S, Shani G, Sines T, Marash L, Shohat G, Kimchi A. The caspase-cleaved DAP5 protein supports internal ribosome entry site-mediated translation of death proteins. Proc Natl Acad Sci U S A 2002; 99:5400-5; PMID:11943866; http://dx.doi.org/10.1073/pnas.082102499
31. Du X, Wang J, Zhu H, Rinaldo L, Lamar KM, Palmenberg AC, Hansel C, Gomez CM. Second cistron in CACNA1A gene encodes a transcription factor mediating cerebellar development and SCA6. Cell 2013; 154:118-33; PMID:23827678; http://dx.doi.org/10.1016/j.cell.2013.05.059
32. Burkart C, Fan JB, Zhang DE. Two independent mechanisms promote expression of an N-terminal truncated USP18 isoform with higher DeISGylation activity in the nucleus. J Biol Chem 2012; 287:4883-93; PMID:22170061; http://dx.doi.org/10.1074/jbc. M111.255570
33. Martínez-Salas E. Internal ribosome entry site biology and its use in expression vectors. Curr Opin Biotechnol 1999; 10:458-64; PMID:10508627; http://dx.doi.org/10.1016/S0958-1669(99)00010-5
34. Fernández-Miragall O, López de Quinto S, Martínez-Salas E. Relevance of RNA structure for the activity of picornavirus IRES elements. Virus Res 2009; 139:172-82; PMID:18692097; http://dx.doi.org/10.1016/j.virusres.2008.07.009
35. Birney E, Stamatoyannopoulos JA, Dutta A, Guigó R, Gingeras TR, Margulies EH, Weng Z, Snyder M, Dermitzakis ET, Thurman RE, et al.; ENCODE Project Consortium; NISC Comparative Sequencing Program; Baylor College of Medicine Human Genome Sequencing Center; Washington University Genome Sequencing Center; Broad Institute; Children's Hospital Oakland Research Institute. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007; 447:799-816; PMID:17571346; http://dx.doi.org/10.1038/nature05874
36. Clark MB, Amaral PP, Schlesinger FJ, Dinger ME, Taft RJ, Rinn JL, Ponting CP, Stadler PF, Morris KV, Morillon A, et al. The reality of pervasive transcription. PLoS Biol 2011; 9:e1000625, discussion e1001102; PMID:21765801; http://dx.doi.org/10.1371/journal.pbio.1000625
37. van Bakel H, Nislow C, Blencowe BJ, Hughes TR. Most "dark matter" transcripts are associated with known genes. PLoS Biol 2010; 8:e1000371; PMID:20502517; http://dx.doi.org/10.1371/journal.pbio.1000371
38. Xue C, Li F, He T, Liu GP, Li Y, Zhang X. Classification of real and pseudo microRNA precursors using local structure-sequence features and support vector machine. BMC Bioinformatics 2005; 6:310; PMID:16381612; http://dx.doi.org/10.1186/1471-2105-6-310
39. Ng KL, Mishra SK. De novo SVM classification of precursor microRNAs from genomic pseudo hairpins using global and intrinsic folding measures. Bioinformatics 2007; 23:1321-30; PMID:17267435; http://dx.doi.org/10.1093/ bioinformatics/btm026
40. Tjaden B. Prediction of small, noncoding RNAs in bacteria using heterogeneous data. J Math Biol 2008; 56:183-200; PMID:17354017; http://dx.doi.org/10.1007/s00285-007-0079-5
41. Lagesen K, Hallin P, Rødland EA, Staerfeldt HH, Rognes T, Ussery DW. RNAmmer: consistent and rapid annotation of ribosomal RNA genes. Nucleic Acids Res 2007; 35:3100-8; PMID:17452365; http://dx.doi.org/10.1093/nar/gkm160
42. Lowe TM, Eddy SR. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 1997; 25:955-64; PMID:9023104
43. Schattner P, Brooks AN, Lowe TM. The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucleic Acids Res 2005; 33(Web Server issue):W686-9; PMID:15980563; http://dx.doi.org/10.1093/nar/gki366
44. Freyhult E, Edvardsson S, Tamas I, Moulton V, Poole AM. Fisher: a program for the detection of H/ACA snoRNAs using MFE secondary structure prediction and comparative genomics - assessment and update. BMC Res Notes 2008; 1:49; PMID:18710502; http://dx.doi.org/10.1186/1756-0500-1-49
45. Tafer H, Kehr S, Hertel J, Hofacker IL, Stadler PF. RNAsnoop: efficient target prediction for H/ACA snoRNAs. Bioinformatics 2010; 26:610-6; PMID:20015949; http://dx.doi.org/10.1093/bioinformatics/btp680
46. Chang TH, Huang HD, Wu LC, Yeh CT, Liu BJ, Horng JT. Computational identification of riboswitches based on RNA conserved functional sequences and conformations. RNA 2009; 15:1426-30; PMID:19460868; http://dx.doi.org/10.1261/ rna.1623809
47. Singh P, Bandyopadhyay P, Bhattacharya S, Krishnamachari A, Sengupta S. Riboswitch detection using profile hidden Markov models. BMC Bioinformatics 2009; 10:325; PMID:19814811; http://dx.doi.org/10.1186/1471-2105-10-325
48. Naville M, Ghuillot-Gaudeffroy A, Marchais A, Gautheret D. ARNold: a web tool for the prediction of Rho-independent transcription terminators. RNA Biol 2011; 8:11-3; PMID:21282983; http://dx.doi.org/10.4161/rna.8.1.13346
49. Nawrocki EP, Kolbe DL, Eddy SR. Infernal 1.0: inference of RNA alignments. Bioinformatics 2009; 25:1335-7; PMID:19307242; http://dx.doi.org/10. 1093/bioinformatics/btp157
50. Zytnicki M, Gaspin C, Schiex T. Darn: a weighted constraint solver for RNA motif localization. Constraints 2008; 13:91-109; http://dx.doi.org/10.1007/ s10601-007-9033-9
51. Gruber AR, Neuböck R, Hofacker IL, Washietl S. The RNAz web server: prediction of thermodynamically stable and evolutionarily conserved RNA structures. Nucleic Acids Res 2007; 35(Web Server issue):W335-8; PMID:17452347; http://dx.doi.org/10.1093/nar/gkm222
52. Parker BJ, Moltke I, Roth A, Washietl S, Wen J, Kellis M, Breaker R, Pedersen JS. New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes. Genome Res 2011; 21:1929-43; PMID:21994249; http://dx.doi.org/10.1101/gr.112516.110
53. Hoeppner MP, Gardner PP, Poole AM. Comparative analysis of RNA families reveals distinct repertoires for each domain of life. PLoS Comput Biol 2012; 8:e1002752; PMID:23133357; http://dx.doi.org/10.1371/journal.pcbi.1002752
54. Burge SW, Daub J, Eberhardt R, Tate J, Barquist L, Nawrocki EP, Eddy SR, Gardner PP, Bateman A. Rfam 11.0: 10 years of RNA families. Nucleic Acids Res 2013; 41(Database issue):D226-32; PMID:23125362; http://dx.doi.org/10.1093/nar/ gks1005
55. Rubin GM, Hong L, Brokstein P, Evans-Holm M, Frise E, Stapleton M, Harvey DA. A Drosophila complementary DNA resource. Science 2000; 287:2222-4; PMID:10731138; http://dx.doi.org/10.1126/science.287.5461.2222
56. Martínez-Salas E, Sáiz JC, Dávila M, Belsham GJ, Domingo E. A single nucleotide substitution in the internal ribosome entry site of foot-and-mouth disease virus leads to enhanced cap-independent translation in vivo. J Virol 1993; 67:3748-55; PMID:8389904
57. López de Quinto S, Sáiz M, de la Morena D, Sobrino F, Martínez-Salas E. IRES-driven translation is stimulated separately by the FMDV 3′-NCR and poly(A) sequences. Nucleic Acids Res 2002; 30:4398-405; PMID:12384586; http://dx.doi.org/10.1093/nar/gkf569
58. Karabiber F, McGinnis JL, Favorov OV, Weeks KM. QuShape: rapid, accurate, and best-practices quantification of nucleic acid probing information, resolved by capillary electrophoresis. RNA 2013; 19:63-73; PMID:23188808; http://dx.doi.org/10.1261/rna.036327.112
59. Zarringhalam K, Meyer MM, Dotu I, Chuang JH, Clote P. Integrating chemical footprinting data into RNA secondary structure prediction. PLoS One 2012; 7:e45160; PMID:23091593; http://dx.doi.org/10.1371/journal.pone.0045160
60. Darty K, Denise A, Ponty Y. VARNA: Interactive drawing and editing of the RNA secondary structure. Bioinformatics 2009; 25:1974-5; PMID:19398448; http://dx.doi.org/10.1093/bioinformatics/btp250
61. McGinnis JL, Duncan CD, Weeks KM. High-throughput SHAPE and hydroxyl radical analysis of RNA structure and ribonucleo-protein assembly. Methods Enzymol 2009; 468:67-89; PMID:20946765; http://dx.doi.org/10.1016/S0076-6879(09) 68004-6