Abstract
Over the last two decades it has become clear that RNA is much more than just a boring intermediate in protein expression. Ancient RNAs still appear in the core information metabolism and comprise a surprisingly large component in bacterial gene regulation. A common theme with these types of mostly small RNAs is their reliance of conserved secondary structures. Large scale sequencing projects, on the other hand, have profoundly changed our understanding of eukaryotic genomes. Pervasively transcribed, they give rise to a plethora of large and evolutionarily extremely flexible noncoding RNAs that exert a vastly diverse array of molecule functions. In this chapter we provide a—necessarily incomplete—overview of the current state of comparative analysis of noncoding RNAs, emphasizing computational approaches as a means to gain a global picture of the modern RNA world.
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References
Kapranov P, Willingham AT, Gingeras TR (2007) Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 8:413–423
Carninci P, FANTOM Consortium (2005) The transcriptional landscape of the mammalian genome. Science 309:1559–1563
ENCODE Project Consortium (2012) An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74
Derrien T, Johnson R, Bussotti G, Tanzer A, Djebali S, Tilgner H, Guernec G, Martin D, Merkel A, Knowles DG, Lagarde J, Veeravalli L, Ruan X, Ruan Y, Lassmann T, Carninci P, Brown JB, Lipovich L, Gonzalez JM, Thomas M, Davis CA, Shiekhattar R, Gingeras TR, Hubbard TJ, Notredame C, Harrow J, Guigó R (2012) The GENCODE v7 catalog of human long noncoding RNAs: analysis of their gene structure, evolution, and expression. Genome Res 22:1775–1789
Clark MB, Amaral PP, Schlesinger FJ, Dinger ME, Taft RJ, Rinn JL, Ponting CP, Stadler PF, Morris KJ, Morillon A, Rozowsky JS, Gerstein M, Wahlestedt C, Hayashizaki Y, Carninci P, Gingeras TR, Mattick JS (2011) The reality of pervasive transcription. PLoS Biol 9:e1000625
Tisseur M, Kwapisz M, Morillon A (2011) Pervasive transcription – lessons from yeast. Biochimie 93:1889–1896
Wu J, Delneri D, O’Keefe RT (2012) Non-coding RNAs in Saccharomyces cerevisiae: what is the function? Biochem Soc Trans 40:907–911
Leong HS, Dawson K, Wirth C, Li Y, Wirth Y, Smith DL, Wilkinson CRM, Miller CJ (2014) A global non-coding RNA system modulates fission yeast protein levels in response to stress. Nat Commun 5:3947
Xuan H, Zhang L, Liu X, Han G, Li J, Li X, Liu A, Liao M, Zhang S (2015) PLNlncRbase: a resource for experimentally identified lncRNAs in plants. Gene 573:328–332
Woehle C, Kusdian G, Radine C, Graur D, Landan G, Gould SB (2014) The parasite Trichomonas vaginalis expresses thousands of pseudogenes and long non-coding RNAs independently from functional neighbouring genes. BMC Genomics 15:906
Sharma CM, Hoffmann S, Darfeuille F, Reignier J, Findeiß S, Sittka A, Chabas S, Reiche K, Hackermüller J, Reinhardt RR, Stadler PF, Vogel J (2010) The primary transcriptome of the major human pathogen Helicobacter pylori. Nature 464:250–255
Lybecker M, Bilusic I, Raghavan R (2014) Pervasive transcription: detecting functional RNAs in bacteria. Transcription 5:e944039
Wade JT, Grainger DC (2014) Pervasive transcription: illuminating the dark matter of bacterial transcriptomes. Nat Rev Microbiol 12:647–653
Perkel JM (2013) Visiting “noncodarnia”. BioTechniques 54(6):303–304
Mercer TR, Dinger ME, Mattick JS (2009) Long non-coding RNAs: insights into functions. Nat Rev Genet 10(3):155–159
Wassarman KM, Repoila F, Rosenow C, Storz G, Gottesman S (2001) Identification of novel small RNAs using comparative genomics and microarrays. Genes Dev. 15(13):1637–1651
Marz M, Gruber AR, Siederdissen CH, Amman F, Badelt S, Bartschat S, Bernhart SH, Beyer S, Kehr W, Lorenz R, Tanzer A, Yusuf D, Tafer H, Hofacker IL, Stadler PF (2011) Animal snoRNAs and scaRNAs with exceptional structures. RNA Biol 8:938–946
Bompfünewerer AF, Flamm C, Fried C, Fritzsch G, Hofacker IL, Lehmann J, Missal K, Mosig A, Müller B, Prohaska SJ, Stadler BMR, Stadler PF, Tanzer A, Washietl S, Witwer C (2005) Evolutionary patterns of non-coding RNAs. Theory Biosci. 123:301–369
The Athanasius F. Bompfünewerer RNA Consortium, Backofen R, Flamm C, Fried C, Fritzsch G, Hackermüller J, Hertel J, Hofacker IL, Missal K, Mosig SJ, Prohaska A, Rose D, Stadler PF, Tanzer A, Washietl S, Sebastian W (2007) RNAs everywhere: genome-wide annotation of structured RNAs. J Exp Zool B: Mol Dev Evol 308B:1–25
Hertel J, Stadler PF (2015) The expansion of animal microRNA families revisited. Life 5:905–920
Brown JW, Echeverria M, Qu LH (2003) Plant snoRNAs: functional evolution and new modes of gene expression. Trends Plant Sci 8:42–49
Kehr S, Bartschat S, Tafer H, Stadler PF, Hertel J (2014) Matching of soulmates: coevolution of snoRNAs and their targets. Mol Biol Evol 31:455–467
Jorjani H, Kehr S, Jedlinski DJ, Gumienny R, Hertel J, Stadler PF, Zavolan M, Gruber AR (2016) An updated human snoRNAome. Nucleic Acids Res 44(11):5068–5082
Bhattacharya DP, Bartschat S, Kehr S, Hertel J, Grosse I, Stadler PF (2016) Phylogenetic distribution of plant snoRNA families. BMC Genomics 17:969
Gorodkin J, Ruzzo WL (2014) RNA sequence, structure, and function: computational and bioinformatic methods. In: Methods in molecular biology, vol 1097. Humana Press/Springer, New York
Fontana W, Stadler PF, Bornberg-Bauer EG, Griesmacher T, Hofacker IL, Tacker M, Tarazona P, Weinberger ED, Schuster P (1993) RNA folding landscapes and combinatory landscapes. Phys Rev E 47:2083–2099
Schuster P, Fontana W, Stadler PF, Hofacker IL (1994) From sequences to shapes and back: a case study in RNA secondary structures. Proc R Soc Lond B 255:279–284
Nussinov R, Pieczenik G, Griggs JR, Kleitman DJ (1978) Algorithms for loop matchings. SIAM J Appl Math 35(1):68–82
Zuker M, Stiegler P (1981) Optimal computer folding of large RNA sequences using thermodynamics and auxilary information. Nucleic Acids Res 9(1):133–147
Zuker M (1989) On finding all suboptimal foldings of an RNA molecule. Science 244:48–52
Wuchty S, Fontana W, Hofacker IL, Schuster P (1999) Complete suboptimal folding of RNA and the stability of secondary structures. Biopolymers 49:145–165
McCaskill JS (1990) The equilibrium partition function and base pair binding probabilities for RNA secondary structure. Biopolymers 29(6–7):1105–1119
Ding Y, Lawrence CE (2001) Statistical prediction of single-stranded regions in RNA secondary structure and application to predicting effective antisense target sites and beyond. Nucleic Acids Res 29(5):1034–1046
Hofacker IL, Fekete M, Stadler PF (2002) Secondary structure prediction for aligned RNA sequences. J Mol Biol 319:1059–1066
Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinf 9:474
Knudsen B, Hein J (2003) Pfold: RNA secondary structure prediction using stochastic context-free grammars. Nucleic Acids Res 31(13):3423–3428
Sükösd Z, Knudsen B, Kjems J, Pedersen CN (2012) PPfold 3.0: fast RNA secondary structure prediction using phylogeny and auxiliary data. Bioinformatics 28:2691–2692
Seemann SE, Gorodkin J, Backofen R (2008) Unifying evolutionary and thermodynamic information for RNA folding of multiple alignments. Nucleic Acids Res 36(20):6355–6362
Klein RJ, Misulovin Z, Eddy SR (2002) Noncoding RNA genes identified in AT-rich hyperthermophiles. Proc Natl Acad Sci USA 99:7542–7547
Larsson P, Hinas A, Ardell DH, Kirsebom LA, Virtanen A, Söderbom F (2008) De novo search for non-coding RNA genes in the AT-rich genome of Dictyostelium discoideum: performance of Markov-dependent genome feature scoring. Genome Res 18:888–899
Haerty W, Ponting CP (2015) Unexpected selection to retain high GC content and splicing enhancers within exons of multiexonic lncRNA loci. RNA 21:333–346
Washietl S, Hofacker IL (2004) Consensus folding of aligned sequences as a new measure for the detection of functional RNAs by comparative genomics. J Mol Biol 342:19–30
Washietl S, Hofacker IL, Stadler PF (2005) Fast and reliable prediction of noncoding RNAs. Proc Natl Acad Sci USA 102:2454–2459
Clote P, Ferré F, Kranakis E, Krizanc D (2005) Structural RNA has lower folding energy than random RNA of the same dinucleotide frequency. RNA 11:578–591
Workman C, Krogh A (1999) No evidence that mRNAs have lower folding free energies than random sequences with the same dinucleotide distribution. Nucleic Acids Res 27:4816–4822
Altschul SF, Erickson BW (1985) Significance of nucleotide sequence alignment: a method for random sequence permutation that preserves dinucleotide and codon usage. Mol Biol Evol 2:526–538
Fitch WM (1983) Random sequences. J Mol Biol 163:171–176
Kandel D, Matias Y, Unger R, Winker P (1996) Shuffling biological sequences. Discr Appl Math 71:171–185
Jiang M, Anderson J, Gillespie J, Joel M (2008) uShuffle: a useful tool for shuffling biological sequences while preserving the k-let counts. BMC Bioinformatics 9:192
Gruber AR, Findeiß S, Washietl S, Hofacker IL, Stadler PF (2010) RNAz 2.0: improved noncoding RNA detection. Pac Symp Biocomput 15:69–79
Soldatov RA, Vinogradova SV, Mironov AA (2014) RNASurface: fast and accurate detection of locally optimal potentially structured RNA segments. Bioinformatics 30:457–463
Washietl S (2005) Prediction of structured non-coding RNAs by comparative sequence analysis. PhD thesis, Univsity of Vienna
van Nimwegen E, Crutchfield JP, Huynen M (1999) Neutral evolution of mutational robustness. Proc Natl Acad Sci USA 96:9716–9720
Wagner A, Stadler PF (1999) Viral RNA and evolved mutational robustness. J Exp Zool MDE 285:119–127
Ancel LW, Fontana W (2000) Plasticity, evolvability, and modularity in RNA. J Exp Zool MDE 288:242–283
Borenstein E, Ruppin E (2006) Direct evolution of genetic robustness in microRNA. Proc Natl Acad Sci USA 103:6593–6598
Pei S, Anthony JS, Meyer MM (2015) Sampled ensemble neutrality as a feature to classify potential structured RNAs. BMC Genomics 16:35
Gruber AR, Bernhart SH, Hofacker IL, Washietl S (2008) Strategies for measuring evolutionary conservation of RNA secondary structures. BMC Bioinf 9:122
Salari R, Kimchi-Sarfaty C, Gottesman MM, Przytycka TM (2013) Sensitive measurement of single-nucleotide polymorphism-induced changes of RNA conformation: application to disease studies. Nucleic Acids Res 41:44–53
Sabarinathan R, Tafer H, Seemann SE, Hofacker IL, Stadler PF, Gorodkin J (2013) RNAsnp: efficient detection of local RNA secondary structure changes induced by SNPs. Hum Mut 34:546–556
Gardner PP, Wilm A, Washietl S (2005) A benchmark of multiple sequence alignment programs upon structural RNAs. Nucleic Acids Res 33:2433–2439
Parsch J, Braverman JM, Stephan W (2000) Comparative sequence analysis and patterns of covariation in RNA secondary structures. Genetics 154:909–921
Coventry A, Kleitman DJ, Berger B (2004) MSARI: multiple sequence alignments for statistical detection of RNA secondary structure. Proc Natl Acad Sci USA 101:12102–12107
di Bernardo D, Down T, Hubbard T (2003) ddbRNA: detection of conserved secondary structures in multiple alignments. Bioinformatics 19:1606–1611
Seemann SE, Richter AS, Gorodkin J, Backofen R (2010) Hierarchical folding of multiple sequence alignments for the prediction of structures and RNA-RNA interactions. Algorithms Mol Biol 5:22
Seemann SE, Mirza AH, Hansen C, Bang-Berthelsen CH, Garde C, Christensen-Dalsgaard M, Torarinsson E, Yao Z, Workman C, Pociot H, Nielsen F, Tommerup N, Ruzzo WL, Gorodkin J (2017) The identification and functional annotation of RNA structures conserved in vertebrates. Genome Res 27(8):1371–1383
Lindgreen S, Gardner PP, Krogh A (2006) Measuring covariation in RNA alignments: physical realism improves information measures. Bioinformatics 22:2988–2995
Menzel P, Seemann SE, Gorodkin J (2012) RILogo: visualizing RNA-RNA interactions. Bioinformatics 28(19):2523–2526
Piskol R, Stephan W (2011) Selective constraints in conserved folded RNAs of Drosophilid and Hominid genomes. Mol Biol Evol 28:1519–1529
Kusumi J, Ichinose M, Takefu M, Piskol R, Stephan W, Iizuka M (2016) A model of compensatory molecular evolution involving multiple sites in RNA molecules. J Theor Biol 388:96–107
Ponjavic J, Ponting CP, Lunter G (2007) Functionality or transcriptional noise? Evidence for selection within long noncoding RNAs. Genome Res 17:556–565
Pang KC, Frith MC, Mattick JS (2006) Rapid evolution of noncoding RNAs: lack of conservation does not mean lack of function. Trends Genet 22:1–5
Marques AC, Ponting CP (2009) Catalogues of mammalian long noncoding RNAs: modest conservation and incompleteness. Genome Biol 10:R124
Guttman M, Amit I, Garber M, French C, Lin MF, Feldser D, Huarte M, Zuk O, Carey BW, Cassady JP, Cabili MN, Jaenisch R, Mikkelsen TS, Jacks T, Hacohen N, Bernstein BE, Kellis M, Regev A, Rinn JL, Lander ES (2009) Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature 458:223–227
Managadze D, Lobkovsky AE, Wolf YI, Shabalina SA, Rogozin IB, Koonin EV (2013) The vast, conserved mammalian lincRNome. PLoS Comput Biol 9:e1002917
Hüttenhofer A, Schattner P, Polacek N (2005) Non-coding RNAs: hope or hype? Trends Genet 21:289–297
Palazzo AF, Lee ES (2015) Non-coding RNA: what is functional and what is junk? Front Genet 6:2
Johnsson P, Lipovich L, Grandér D, Morris KV (2014) Evolutionary conservation of long non-coding RNAs: sequence, structure, function. Biochim Biophys Acta 1840:1063–1071
Schüler A, Ghanbarian AT, Hurst LD (2014) Purifying selection on splice-related motifs, not expression level nor RNA folding, explains nearly all constraint on human lincRNAs. Mol Biol Evol 31:3164–3183
Mercer TR, Mattick JS (2013) Structure and function of long noncoding RNAs in epigenetic regulation. Nat Struct Mol Biol 20:300–307
Smith MA, Gesell T, Stadler PF, Mattick JS (2013) Widespread purifying selection on RNA structure in mammals. Nucleic Acids Res 41:8220–8236
Hezroni H, Koppstein D, Schwartz MG, Avrutin A, Bartel DP, Ulitsky I (2015) Principles of long noncoding RNA evolution derived from direct comparison of transcriptomes in 17 species. Cell 11:1110–1122
Washietl S, Kellis M, Garber M (2014) Evolutionary dynamics and tissue specificity of human long noncoding RNAs in six mammals. Genome Res 24:616–628
Kutter C, Watt S, Stefflova K, Wilson MD, Goncalves A, Ponting CP, Odom DT, Marques AC (2012) Rapid turnover of long noncoding RNAs and the evolution of gene expression. PLoS Genet 8:e1002841
Necsulea A, Soumillon M, Warnefors M, Liechti A, Daish T, Zeller U, Baker J, Grützner F, Kaessmann H (2014) The evolution of lncRNA repertoires and expression patterns in tetrapods. Nature 505:635–640
Ward M, McEwan C, Mill JD, Janitz M (2015) Conservation and tissue-specific transcription patterns of long noncoding RNAs. J Hum Transcr 1:2–9
Ulitsky I, Shkumatava A, Jan CH, Sive H, Bartel DP (2011) Conserved function of lincRNAs in vertebrate embryonic development despite rapid sequence evolution. Cell 147:1537–1550
Young RS, Marques AC, Tibbit C, Haerty W, Bassett AR, Liu JL, Ponting CP (2012) Identification and properties of 1,119 candidate lincRNA loci in the Drosophila melanogaster genome. Genome Biol Evol 4:427–442
Nitsche A, Rose D, Fasold M, Reiche K, Stadler PF (2015) Comparison of splice sites reveals that long non-coding RNAs are evolutionarily well conserved. RNA 21:801–812
Eng L, Coutinho G, Nahas S, Yeo G, Tanouye R, Babaei M, Dörk T, Burge C, Gatti RA (2004) Nonclassical splicing mutations in the coding and noncoding regions of the ATM gene: maximum entropy estimates of splice junction strengths. Hum Mutat 23:67–76
Canzler S, Stadler PF, Hertel J (2016) U6 snRNA intron insertion occurred multiple times during fungi evolution. RNA Biol 13:119–127
Louhichi A, Fourati A, Rebaï A (2011) IGD: a resource for intronless genes in the human genome. Gene 488:35–40
Nakaya HI, Amaral PP, Louro R, Lopes A, Fachel AA, Moreira YB, El-Jundi TA, da Silva AM, Reis EM, Verjovski-Almeida S (2007) Genome mapping and expression analyses of human intronic noncoding RNAs reveal tissue-specific patterns and enrichment in genes related to regulation of transcription. Genome Biol 8:R43
Louro R, Nakaya HI, Amaral PP, Festa F, Sogayar MC, da Silva AM, Verjovski-Almeida S, Reis EM (2007) Androgen responsive intronic non-coding RNAs. BMC Biol 5:4
Louro R, El-Jundi T, Nakaya HI, Reis EM, Verjovski-Almeida S (2008) Conserved tissue expression signatures of intronic noncoding RNAs transcribed from human and mouse loci. Genomics 92:18–25
Engelhardt J, Stadler PF (2012) Hidden treasures in unspliced EST data. Theory Biosci 131:49–57.
Rinn JL, Euskirchen G, Bertone P, Martone R, Luscombe NM, Hartman S, Harrison PM, Nelson FK, Miller P, Gerstein M, Weissman S, Snyder M (2003) The transcriptional activity of human chromosome 22. Genes Dev 17:529–540
Reis EM, Nakaya HI, Louro R, Canavez FC, Flatschart AV, Almeida GT, Egidio CM, Paquola AC, Machado AA, Festa F, Yamamoto D, Alvarenga R, da Silva CC, Brito GC, Simon SD, Moreira-Filho CA, Leite KR, Camara-Lopes LH, Campos FS, Gimba E, Vignal GM, El-Dorry H, Sogayar MC, Barcinski MA, da Silva AM, Verjovski-Almeida S (2004) Antisense intronic non-coding RNA levels correlate to the degree of tumor differentiation in prostate cancer. Oncogene 23:6684–6692
Beckedorff FC, Ayupe AC, Crocci-Souza R, Amaral MS, Nakaya HI, Soltys DT, Menck CFM, Reis EM, Verjovski-Almeida S (2013) The intronic long noncoding RNA ANRASSF1 recruits PRC2 to the RASSF1A promoter, reducing the expression of RASSF1A and increasing cell proliferation. PLoS Genet 9:e1003705
Sasaki YTF, Ideue T, Sano M, Mituyama T, Hirose T (2009) MENε/β noncoding RNAs are essential for structural integrity of nuclear paraspeckles. Proc Natl Acad Sci USA 106:2525–2530
Sunwoo H, Dinger ME, Wilusz JE, Amaral PP, Mattick JS, Spector DL (2009) MEN ε/β nuclear-retained non-coding RNAs are up-regulated upon muscle differentiation and are essential components of paraspeckles. Genome Res 19:347–359
Mao YS, Sunwoo H, Zhang B, Spector DL (2011) Direct visualization of the co-transcriptional assembly of a nuclear body by noncoding RNAs. Nat Cell Biol 13:95–101
Stadler PF (2010) Evolution of the long non-coding RNAs MALAT1 and MENβ/ε. In: Ferreira CE, Miyano S, Stadler PF (eds.) Advances in bioinformatics and computational biology, 5th brazilian symposium on bioinformatics. Lecture notes in computer science, vol 6268. Springer, Heidelberg, pp 1–12
Chung S, Nakagawa H, Uemura M, Piao L, Ashikawa K, Hosono N, Takata R, Akamatsu S, Kawaguchi T, Morizono T, Tsunoda T, Daigo Y, Matsuda K, Kamatani N, Nakamura Y, Kubo M (2011) Association of a novel long non-coding RNA in 8q24 with prostate cancer susceptibility. Cancer Sci 102:245–252
Hackermüller J, Reiche K, Otto C, Hösler N, Blumert C, Brocke-Heidrich K, Böhlig L, Nitsche A, Kasack K, Ahnert P, Krupp W, Engeland K, Stadler PF, Horn F (2014) Cell cycle, oncogenic and tumor suppressor pathways regulate numerous long and macro non-protein coding RNAs. Genome Biol 15:R48
Kapranov P, St Laurent G, Raz T, Ozsolak F, Reynolds CP, Sorensen PH, Reaman G, Milos P, Arceci RJ, Thompson JF, Triche TJ (2010) The majority of total nuclear-encoded non-ribosomal RNA in a human cell is ‘dark matter’ un-annotated RNA. BMC Biol 8:149
Seidl CIM, Stricker SH, Barlow DP (2006) The imprinted Air ncRNA is an atypical RNAPII transcript that evades splicing and escapes nuclear export. EMBO J 25:1–11
Stricker SH, Steenpass L, Pauler FM, Santoro F, Latos PA, Huang R, Koerner MV, Sloane MA, Warczok KE, Barlow DP (2008) Silencing and transcriptional properties of the imprinted Airn ncRNA are independent of the endogenous promoter. EMBO J 27:3116–3128
Redrup L, Branco MR, Perdeaux ER, Krueger C, Lewis A, Santos F, Nagano T, Cobb BS, Fraser P, Reik W (2009) The long noncoding RNA Kcnq1ot1 organises a lineage-specific nuclear domain for epigenetic gene silencing. Development 136:525–530
Mercer TR, Wilhelm D, Dinger ME, Soldà G, Korbie DJ, Glazov EA, Truong V, Schwenke M, Simons C, Matthaei KI, Saint R, Koopman P, Mattick JS (2011) Expression of distinct RNAs from 3’ untranslated regions. Nucleic Acids Res 39:2393–2403
Engelhardt J, Stadler PF (2015) Evolution of the unspliced transcriptome. BMC Evol Biol 15:166
Menzel P, Gorodkin J, Stadler PF (2009) The tedious task of finding homologous non-coding RNA genes. RNA 15:2075–2082
Nawrocki EP, Burge SW, Bateman A, Daub J, Eberhardt RY, Eddy SR, Floden EW, Gardner PP, Jones TA, Tate J, Finn RD (2015) Rfam 12.0: updates to the RNA families database. Nucl Acids Res 43:D130–D137
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410
Hertel J, de Jong D, Marz M, Rose D, Tafer H, Tanzer A, Schierwater B, Stadler PF (2009) Non-coding RNA annotation of the genome of Trichoplax adhaerens. Nucleic Acids Res 37:1602–1615
Menzel P, Stadler PF, Gorodkin J (2011) maxAlike: maximum-likelihood based sequence reconstruction with application to improved primer design for unknown sequences. Bioinformatics 27:317–325
Xie M, Mosig A, Qi X, Li Y, Stadler PF, Chen J-L (2008) Size variation and structural conservation of vertebrate telomerase RNA. J Biol Chem 283:2049–2059
Lu Y, Sze S-H (2009) Improving accuracy of multiple sequence alignment algorithms based on alignment of neighboring residues. Nucl. Acids Res 37:463–472
Bussotti G, Raineri E, Erb I, Zytnicki M, Wilm A, Beaudoing E, Bucher P, Notredame C (2011) BlastR-fast and accurate database searches for non-coding RNAs. Nucleic Acids Res 39:6886–6895
Mosig A, Sameith K, Stadler PF (2005) fragrep: efficient search for fragmented patterns in genomic sequences. Geno Prot Bioinfo 4:56–60
Weinberg Z, Ruzzo WL (2004) Exploiting conserved structure for faster annotation of non-coding RNAs without loss of accuracy. Bioinformatics 20:i334–i341
Weinberg Z, Ruzzo WL (2006) Sequence-based heuristics for faster annotation of non-coding RNA families. Bioinformatics 22:35–39
Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res 25:955–964
Macke TJ, Ecker DJ, Gutell RR, Gautheret D, Case DA, Sampath R (2001) RNAMotif, an RNA secondary structure definition and search algorithm. Nucl Acids Res 29:4724–4735
Billoud B, Kontic M, Viari A (1996) Palingol: a declarative programming language to describe nucleic acids’ secondary structures and to scan sequence database. Nucl Acids Res 24:1395–1403
Gautheret D, Major F, Cedergren R (1990) Pattern searching/alignment with RNA primary and secondary structures: an effective descriptor for tRNA. Comput Appl Biosci 6:325–331
Dsouza M, Larsen N, Overbeek R (1997) Searching for patterns in genomic data. Trends Genet 13:497–498
Reeder J, Reeder J, Giegerich R (2007) Locomotif: from graphical motif description to RNA motif search. Bioinformatics 23:i392–i400
Gautheret D, Lambert A (2001) Direct RNA motif definition and identification from multiple sequence alignments using secondary structure profiles. J Mol Biol 313:1003–1011
Freyhult EK, Bollback JP, Gardner PP (2007) Exploring genomic dark matter: a critical assessment of the performance of homology search methods on noncoding RNA. Genome Res 17:117–125
Finn RD, Coggill P, Eberhardt RY, Eddy SR, Mistry J, Mitchell AL, Potter SC, Punta M, Qureshi M, Sangrador-Vegas A, Salazar GA, Tate J, Bateman A (2016) The Pfam protein families database: towards a more sustainable future. Nucleic Acids Res 44(D1):D279–D285
Giegerich R (2014) Introduction to stochastic context free grammars. Methods Mol Biol 1097:85–106
Sükösd Z, Andersen ES, Lyngsø R (2014) SCFGs in RNA secondary structure prediction RNA secondary structure prediction: a hands-on approach. Methods Mol Biol 1097:143–162
Nawrocki EP, Eddy SR (2013) Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics 29:2933–2935
Nawrocki EP (2014) Annotating functional RNAs in genomes using Infernal. Methods Mol Biol 1097:163–197
Anthon C, Tafer H, Havgaard JH, Thomsen B, Hedegaard J, Seemann SE, Pundhir S, Kehr S, Bartschat S, Nielsen M, Nielsen RO, Fredholm M, Stadler PF, Gorodkin J (2014) Structured RNAs and synteny regions in the pig genome. BMC Genomics 15:459
Eggenhofer F, Hofacker IL, Siederdissen CH (2016) RNAlien - unsupervised RNA family model construction. Nucl Acids Res 44:8433–8441
Gesell T, Washietl S (2008) Dinucleotide controlled null models for comparative RNA gene prediction. BMC Bioinf 9:248
Washietl S, Hofacker IL, Lukasser M, Hüttenhofer A, Stadler PF (2005) Mapping of conserved RNA secondary structures predicts thousands of functional non-coding RNAs in the human genome. Nat Biotech 23:1383–1390
Rivas E, Eddy SR (2001) Noncoding RNA gene detection using comparative sequence analysis. BMC Bioinf 2:8
Pedersen JS, Bejerano G, Siepel A, Rosenbloom K, Lindblad-Toh K, Lander ES, Kent J, Miller W, Haussler D (2006) Identification and classification of conserved RNA secondary structures in the human genome. PLoS Comput Biol 2(4):e33
Parker BJ, Moltke I, Roth A, Washietl S, Wen J, Kellis M, Breaker R, Pedersen JS (2011) New families of human regulatory RNA structures identified by comparative analysis of vertebrate genomes. Genome Res 21(11):1929–1943
Wang AX, Ruzzo WL, Tompa M (2007) How accurately is ncRNA aligned within whole-genome multiple alignments? BMC Bioinf 8:417
Gorodkin J, Stricklin SL, Stormo GD (2001) Discovering common stem-loop motifs in unaligned RNA sequences. Nucleic Acids Res 29:2135–2144
Havgaard JH, Torarinsson E, Gorodkin J (2007) Fast pairwise structural RNA alignments by pruning of the dynamical programming matrix. PLoS Comput Biol 3(10):1896–1908
Sundfeld D, Havgaard JH, de Melo AC, Gorodkin J (2016) Foldalign 2.5: multithreaded implementation for pairwise structural RNA alignment. Bioinformatics 22:1238–1240
Mathews DH, Turner DH (2002) Dynalign: an algorithm for finding the secondary structure common to two RNA sequences. J Mol Biol 317:191–203
Fu Y, Sharma G, Mathews DH (2014) Dynalign II: common secondary structure prediction for RNA homologs with domain insertions. Nucleic Acids Res 42:13939–13948
Will S, Missal K, Hofacker IL, Stadler PF, Backofen R (2007) Inferring non-coding RNA families and classes by means of genome-scale structure-based clustering. PLoS Comput Biol 3:e65
Will S, Joshi T, Hofacker IL, Stadler PF, Backofen R (2012) LocARNA-P: accurate boundary prediction and improved detection of structured RNAs for genome-wide screens. RNA 18:900–914
Sankoff D (1985) Simultaneous solution of the RNA folding, alignment and protosequence problems. SIAM J Appl Math 45:810–825
Havgaard JH, Gorodkin J (2014) RNA structural alignments, part I: sankoff-based approaches for structural alignments. Methods Mol Biol 1097:275–290
Yao Z, Weinberg Z, Ruzzo WL (2006) CMfinder–a covariance model based RNA motif finding algorithm. Bioinformatics 22(4):445–452
Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P (1994) Fast folding and comparison of RNA secondary structures. Monatsh Chem 125:167–188
Bailey TL, Elkan C (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc Int Conf Intell Syst Mol Biol 2:28–36
Ruzzo WL Gorodkin J (2014) De novo discovery of structured ncRNA motifs in genomic sequences. Methods Mol Biol 1097:303–318
Puton T, Kozlowski LP, Rother KM, Bujnicki JM (2013) CompaRNA: a server for continuous benchmarking of automated methods for RNA secondary structure prediction. Nucleic Acids Res 41(7):4307–4323
Puton T, Kozlowski LP, Rother KM, Bujnicki JM (2014) CompaRNA: a server for continuous benchmarking of automated methods for RNA secondary structure prediction. Nucleic Acids Res 42(8):5403–5406
Will S, Yu M, Berger B (2013) Structure-based whole-genome realignment reveals many novel noncoding RNAs. Genome Res 23:1018–1027
Torarinsson E, Sawera M, Havgaard JH, Fredholm M, Gorodkin J (2006) Thousands of corresponding human and mouse genomic regions unalignable in primary sequence contain common RNA structure. Genome Res 16:885–889
Weinberg Z, Barrick JE, Yao Z, Roth A, Kim JN, Gore J, Wang JX, Lee ER, Block KF, Sudarsan N, Neph S, Tompa M, Ruzzo WL, Breaker RR (2007) Identification of 22 candidate structured RNAs in bacteria using the CMfinder comparative genomics pipeline. Nucleic Acids Res 35:4809–4819
The ENCODE Project Consortium (2007) Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 447:799–816
Torarinsson E, Yao Z, Wiklund ED, Bramsen JB, Hansen C, Kjems J, Tommerup N, Ruzzo WL, Gorodkin J (2008) Comparative genomics beyond sequence-based alignments: RNA structures in the ENCODE regions. Genome Res 18:242–251
Ulveling D, Francastel C, Hubé F (2011) When one is better than two: RNA with dual functions. Biochimie 93:633–644
Leygue E (2007) Steroid receptor RNA activator (SRA1): unusual bifaceted gene products with suspected relevance to breast cancer. Nucl Recept Signal 5:e006
Rivas E, Clements J, Eddy SR (2017) A statistical test for conserved RNA structure shows lack of evidence for structure in lncRNAs. Nat Methods 14(1):45–48
Jenny A, Hachet O, Závorszky P, Cyrklaff A, Weston MD, Johnston DS, Erdélyi M, Ephrussi A (2006) A translation-independent role of oskar RNA in early Drosophila oogenesis. Development 133:2827–2833
Weill L, James L, Ulryck N, Chamond N, Herbreteau CH, Ohlmann T, Sargueil B (2010) A new type of IRES within gag coding region recruits three initiation complexes on HIV-2 genomic RNA. Nucleic Acids Res 38:1367–1381
Kumari, P, Sampath K (2015) cncRNAs: bi-functional RNAs with protein coding and non-coding functions. Semin Cell Dev Biol 47–48:40–51
Neuhaus K, Landstorfer R, Simon S, Schober S, Wright PR, Smith C, Backofen R, Wecko R, Keim DA, Scherer S (2017) Differentiation of ncRNAs from small mRNAs in Escherichia coli O157:H7 EDL933 (EHEC) by combined RNAseq and RIBOseq - ryhB encodes the regulatory RNA RyhB and a peptide, RyhP. BMC Genomics 18(1):216
Pedersen JS, Meyer IM, Forsberg R, Simmonds P, Hein J (2004) A comparative method for finding and folding RNA secondary structures within protein-coding regions. Nucleic Acids Res 32:4925–4936
Meyer IM, Miklós I (2005) Statistical evidence for conserved, local secondary structure in the coding regions of eukaryotic mRNAs and pre-mRNAs. Nucleic Acids Res 33:6338–6348
Findeiß S, Engelhardt J, Prohaska SP, Stadler PF (2011) Protein-coding structured RNAs: a computational survey of conserved RNA secondary structures overlapping coding regions in drosophilids. Biochimie 93:2019–2023
Stoletzki N (2008) Conflicting selection pressures on synonymous codon use in yeast suggest selection on mRNA secondary structures. BMC Evol Biol 8:224
Lin MF, Kheradpour P, Washietl S, Parker BJ, Pedersen JS, Kellis M (2011) Locating protein-coding sequences under selection for additional, overlapping functions in 29 mammalian genomes. Genome Res 21:1916–1928
Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Roy Stat Soc Ser B 57:289–300
Babak T, Blencowe BJ, Hughes TR (2007) Considerations in the identification of functional RNA structural elements in genomic alignments. BMC Bioinf 8:33
Anandam P, Torarinsson E, Ruzzo WL (2009) Multiperm: shuffling multiple sequence alignments while approximately preserving dinucleotide frequencies. Bioinformatics 25:668–669
Washietl S, Pedersen JS, Korbel JO, Gruber A, Hackermüller J, Hertel J, Lindemeyer M, Reiche K, Stocsits C, Tanzer A, Ucla C, Wyss C, Antonarakis SE, Denoeud F, Lagarde J, Drenkow J, Kapranov P, Gingeras TR, Guigó R, Snyder M, Gerstein MB, Reymond A, Hofacker IL, Stadler PF (2007) Structured RNAs in the ENCODE selected regions of the human genome. Gen Res 17:852–864
Rose DR, Hackermüller J, Washietl S, Findeiß S, Reiche K, Hertel J, Stadler PF, Prohaska SJ (2007) Computational RNomics of drosophilids. BMC Genomics 8:406
Theis C, Zirbel CL, Siederdissen CHZ, Anthon C, Hofacker IL, Nielsen H, Gorodkin J (2015) RNA 3D modules in genome-wide predictions of RNA 2D structure. PLoS ONE 10(10):e0139900
Zhang XH-F, Leslie CS, Chasin LA (2005) Computational searches for splicing signals. Methods 37:292–305
Hiller M, Findeiß S, Lein S, Marz M, Nickel C, Rose D, Schulz C, Backofen R, Prohaska SJ, Reuter G, Stadler PF (2009) Conserved introns reveal novel transcripts in Drosophila melanogaster. Genome Res 19:1289–1300
Rose D, Hiller M, Schutt K, Hackermüller J, Backofen R, Stadler PF (2011) Computational discovery of human coding and non-coding transcripts with conserved splice sites. Bioinformatics 27:1894–1900
Kingsford C, Ayanbule K, Salzberg SL (2007) Rapid, accurate, computational discovery of Rho-independent transcription terminators illuminates their relationship to DNA uptake. Genome Biol 8:R22
Naville M, Ghuillot-Gaudeffroy A, Marchais A, Gautheret D (2011) ARNold: a web tool for the prediction of Rho-independent transcription terminators. RNA Biol 8:11–13
Pichon C, Felden B (2003) Intergenic sequence inspector: searching and identifying bacterial RNAs. Bioinformatics 19:1707–1709
Livny J, Fogel MA, Davis BM, Waldor MK (2005) sRNAPredict: an integrative computational approach to identify sRNAs in bacterial genomes. Nucleic Acids Res 13:4096–4105
Pichon C, du Merle L, Caliot M, Trieu-Cuot P, La Bouguénec C (2012) An in silico model for identification of small RNAs in whole bacterial genomes: characterization of antisense RNAs in pathogenic Escherichia coli and Streptococcus agalactiae strains. Nucl Acids Res 40:2846–2861
Arnedo J, Romero-Zaliz R, Zwir I, del Val C (2014) A multiobjective method for robust identification of bacterial small non-coding RNAs. Bioinformatics 30:2875–2882
Marchais A, Naville M, Bohn C, Bouloc P, Gautheret D (2009) Single-pass classification of all noncoding sequences in a bacterial genome using phylogenetic profiles. Genome Res 19:1084–1092
Ott A, Idali A, Marchais A, Gautheret D (2012) NAPP: the nucleic acid phylogenetic profile database. Nucl Acids Res 40:D205–D209
Weinberg Z, Perreault J, Meyer MM, Breaker RR (2009) Exceptional structured noncoding RNAs revealed by bacterial metagenome analysis. Nature 462(7273):656–659
Roth A, Weinberg Z, Chen AG, Kim PB, Ames TD, Breaker RR (2014) A widespread self-cleaving ribozyme class is revealed by bioinformatics. Nat Chem Biol 10(1):56–60
Weinberg Z, Kim PB, Chen TH, Li S, Harris KA, Lunse CE, Breaker RR (2015) New classes of self-cleaving ribozymes revealed by comparative genomics analysis. Nat Chem Biol 11(8):606–610
Pain A, Ott A, Amine H, Rochat T, Bouloc P, Gautheret D (2015) An assessment of bacterial small RNA target prediction programs. RNA Biol 12(5):509–513
Lai D, Meyer IM (2016) A comprehensive comparison of general RNA-RNA interaction prediction methods. Nucleic Acids Res 44(7):e61
Umu SU, Gardner PP (2017) A comprehensive benchmark of RNA-RNA interaction prediction tools for all domains of life. Bioinformatics 33(7):988–996
Gerlach W, Giegerich R (2006) GUUGle: a utility for fast exact matching under RNA complementary rules including G-U base pairing. Bioinformatics 22(6):762–764
Tjaden B, Goodwin SS, Opdyke JA, Guillier M, Fu DX, Gottesman S, Storz G (2006) Target prediction for small, noncoding RNAs in bacteria. Nucleic Acids Res 34(9):2791–802
Wenzel A, Akbasli E, Gorodkin J (2012) RIsearch: fast RNA-RNA interaction search using a simplified nearest-neighbor energy model. Bioinformatics 28(21):2738–2746
Rehmsmeier M, Steffen P, Höchsmann M, Giegerich R (2004) Fast and effective prediction of microRNA/target duplexes. RNA 10(10):1507–1517
Alkan C, Karakoç E, Nadeau JH, Sahinalp SC, Zhang K (2006) RNA-RNA interaction prediction and antisense RNA target search. J Comput Biol 13(2):267–282
Dimitrov RA, Zuker M (2004) Prediction of hybridization and melting for double-stranded nucleic acids. Biophys J 87(1):215–226
Bernhart SH, Tafer H, Muckstein U, Flamm C, Stadler PF, Hofacker IL (2006) Partition function and base pairing probabilities of RNA heterodimers. Algorithms Mol Biol 1(1):3
Mückstein U, Tafer H, Hackermuller J, Bernhart SH, Stadler PF, Hofacker IL (2006) Thermodynamics of RNA-RNA binding. Bioinformatics 22:1177–1182
Bernhart SH, Mückstein U, Hofacker IL (2011) RNA accessibility in cubic time. Algorithms Mol Biol 6(1):3
Busch A, Richter AS, Backofen R (2008) IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 24(24):2849–2856
Wright PR, Georg J, Mann M, Sorescu DA, Richter AS, Lott S, Kleinkauf R, Hess WR, Backofen R (2014) CopraRNA and IntaRNA: predicting small RNA targets, networks and interaction domains. Nucleic Acids Res 42(Web Server issue):W119–W123. PRW, JG and MM contributed equally to this work.
Tafer H, Hofacker IL (2008) RNAplex: a fast tool for RNA-RNA interaction search. Bioinformatics 24(22):2657–2663
Chitsaz H, Backofen R, Sahinalp SC (2009) biRNA: fast RNA-RNA binding sites prediction. In: Salzberg S, Warnow T (eds) Proceedings of the 9th workshop on algorithms in bioinformatics (WABI). Lecture notes in computer science, vol. 5724. Springer, Berlin, pp 25–36
Salari R, Backofen R, Sahinalp SC (2009) Fast prediction of RNA-RNA interaction. In: Salzberg S, Warnow T (eds) Proceedings of the 9th Workshop on Algorithms in Bioinformatics (WABI). Lecture Notes in Computer Science, vol 5724. Springer, Berlin, pp 261–272
Salari R, Backofen R, Sahinalp SC (2010) Fast prediction of RNA-RNA interaction. Algorithms Mol Biol 5:5
Pervouchine DD (2004) IRIS: intermolecular RNA interaction search. Genome Inform 15(2):92–101
Chitsaz H, Salari R, Sahinalp SC, Backofen R (2009) A partition function algorithm for interacting nucleic acid strands. Bioinformatics 25(12):i365–i373
Huang FWD, Qin J, Reidys CM, Stadler PF (2009) Partition function and base pairing probabilities for RNA-RNA interaction prediction. Bioinformatics 25(20):2646–2654
Seemann SE, Richter AS, Gesell T, Backofen R, Gorodkin J (2011) PETcofold: predicting conserved interactions and structures of two multiple alignments of RNA sequences. Bioinformatics 27(2):211–219
Li AX, Marz M, Qin J, Reidys CM (2011) RNA-RNA interaction prediction based on multiple sequence alignments. Bioinformatics 27(4):456–463
Schattner P, Brooks AN, Lowe TM (2005) The tRNAscan-SE, snoscan and snoGPS web servers for the detection of tRNAs and snoRNAs. Nucl Acid Res 33:W686–W689
Freyhult E, Edvardsson S, Tamas I, Moulton V, Poole AM (2008) Fisher: a program for the detection of H/ACA snoRNAs using MFE secondary structure prediction and comparative genomics – assessment and update. BMC Res Notes 1:49
Kehr S, Bartschat S, Stadler PF, Tafer H (2011) PLEXY: efficient target prediction for box C/D snoRNAs. Bioinformatics 27:279–280
Tafer H, Kehr S, Hertel J, Stadler PF (2010) RNAsnoop: efficient target prediction for box H/ACA snoRNAs. Bioinformatics 26:610–616
Richter AS, Backofen R (2012) Accessibility and conservation: general features of bacterial small RNA-mRNA interactions? RNA Biol 9(7):954–965
Wright PR, Richter AS, Papenfort K, Mann M, Vogel J, Hess WR, Backofen R, Georg J (2013) Comparative genomics boosts target prediction for bacterial small RNAs. Proc Natl Acad Sci USA 110(37):E3487–E3496
Alkan F,Wenzel A, Palasca O, Kerpedjiev P, Rudebeck AF, Stadler PF, Hofacker IL,Gorodkin J (2017) RIsearch2: suffix array-based large-scale prediction of RNA-RNA interactions and siRNA off-targets. Nucleic Acids Res. 45: e60
Deigan KE, Li TW, Mathews DH, Weeks KM (2009) Accurate SHAPE-directed RNA structure determination. Proc Natl Acad Sci USA 106:97–102
Zarringhalam K, Meyer MM, Dotu I, Chuang JH, Clote P (2012) Integrating chemical footprinting data into RNA secondary structure prediction. PLoS One 7:e45160
Hajdin CE, Bellaousov S, Huggins W, Leonard CW, Mathews DH, Weeks KM (2013) Accurate SHAPE-directed RNA secondary structure modeling, including pseudoknots. Proc Natl Acad Sci USA 110:5498–5503
Cordero P, Kladwang W, VanLang CC, Das R (2012) Quantitative dimethyl sulfate mapping for automated RNA secondary structure inference. Biochemistry 51:7037–7039
Kertesz M, Wan Y, Mazor E, Rinn JL, Nutter RC, Chang HY, Segal E (2010) Genome-wide measurement of RNA secondary structure in yeast. Nature 467:103–107
Wan Y, Qu K, Zhang QC, Flynn RA, Manor O, Ouyang Z, Zhang J, Spitale RC, Snyder MP, Segal E, Chang HY (2014) Landscape and variation of RNA secondary structure across the human transcriptome. Nature 505:706–709
Sükösd Z, Swenson MS, Kjems J, Heitsch CE (2013) Evaluating the accuracy of SHAPE-directed RNA secondary structure predictions. Nucleic Acids Res 41:2807–2816
Lorenz R, Luntzer D, Hofacker IL, Stadler PF, Wolfinger MT (2016) SHAPE directed RNA folding. Bioinformatics 32:145–147
Lorenz R, Hofacker IL, Stadler PF (2016) RNA folding with hard and soft constraints. Algorithms Mol Biol 11:8
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 (2013) A compendium of RNA-binding motifs for decoding gene regulation. Nature 499:172–177
Chu C, Qu K, Zhong FL, Artandi SE, Chang HY (2011) Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 44:667–678
Simon MD (2016) Insight into lncRNA biology using hybridization capture analyses. Biochim Biophys Acta 1859:121–127
Birkedal U, Christensen-Dalsgaard M, Krogh N, Sabarinathan R, Gorodkin J, Nielsen H (2015) Profiling of ribose methylations in RNA by high-throughput sequencing. Angew Chem Int Ed Engl 54(2):451–455
Liu N, Pan T (2016) N6-methyladenosine-encoded epitranscriptomics. Nat Struct Mol Biol 23:98–102
Sibbritt T, Shafik A, Clark SJ, Preiss T (2016) Nucleotide-level profiling of m5C RNA methylation. Methods Mol Biol 1358:269–284
Husain B, Hesler S, Cole JL (2015) Regulation of PKR by RNA: formation of active and inactive dimers. Biochemistry 54:6663–6672
Osman F, Jarrous N, Ben-Asouli Y, Kaempfer R (1999) A cis-acting element in the 3’-untranslated region of human TNF-alpha mRNA renders splicing dependent on the activation of protein kinase PKR. Genes Dev 13:3280–3293
Cohen-Chalamish S, Hasson A, Weinberg D, Namer LS, Banai Y, Osman F, Kaempfer R (2009) Dynamic refolding of IFN-gamma mRNA enables it to function as PKR activator and translation template. Nat Chem Biol 5:896–903
Acknowledgements
This work was funded in part by the German Federal Ministry of Education and Research (BMBF; 031A538B) within the German Network for Bioinformatics Infrastructure (de.NBI), the Deutsche Forschungsgemeinschaft (DFG; BA 2168/11-2, BA2168/3-3, and STA 850/19) within the Priority Programme SPP 1738, the Innovation Fund Denmark (0603-00320B, 5163-00010B), The Danish Council for Independent Research (DFF-4005-00443).
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Backofen, R., Gorodkin, J., Hofacker, I.L., Stadler, P.F. (2018). Comparative RNA Genomics. In: Setubal, J., Stoye, J., Stadler, P. (eds) Comparative Genomics. Methods in Molecular Biology, vol 1704. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7463-4_14
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