Computational biology of RNA interactions

Wiley Interdisciplinary Reviews: RNA

Volumn 4, Issue 1, 2013, Pages 107-120

  Dieterich, Christoph ^a   Stadler, Peter F ^b,c,d,e,f,g  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b UNIVERSITY OF LEIPZIG   (Germany)

^c MAX PLANCK INSTITUTE FOR MATHEMATICS IN THE SCIENCES   (Germany)

^d FRAUNHOFER INSTITUTE FOR CELL THERAPY AND IMMUNOLOGY   (Germany)

^e UNIVERSITY OF VIENNA   (Austria)

^f UNIVERSITY OF COPENHAGEN   (Denmark)

^g SANTA FE INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MESSENGER RNA; NUCLEIC ACID; NUCLEOTIDE; PROTEIN; RIBOSOME RNA; RNA; SMALL INTERFERING RNA; SMALL NUCLEOLAR RNA; TRANSFER RNA;

ALGORITHM; ANALYTIC METHOD; BACTERIUM; BASE PAIRING; BIOINFORMATICS; COMPUTATIONAL FLUID DYNAMICS; CROSS LINKING; IN VITRO STUDY; IN VIVO STUDY; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MOLECULE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MICROARRAY; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SECONDARY STRUCTURE; PROTEIN TARGETING; REVIEW; RNA SEQUENCE; RNA STRUCTURE; SEQUENCE ANALYSIS; THERMODYNAMICS;

BASE PAIRING; COMPUTATIONAL BIOLOGY; HUMANS; NUCLEIC ACID CONFORMATION; RNA;

EID: 84871429429     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1147     Document Type: Review

References (102)

1. The ENCODE Project Consortium. Identification and analysis of functional elements in 1% of the human genome by the ENCODE pilot project. Nature 2007, 447: 799-816.
2. Nussinov R, Jacobson AB. Fast algorithm for predicting the secondary structure of single stranded RNA. Proc Natl Acad Sci U S A 1980, 77:6309-6313.
3. Zuker M, Sankoff D. RNA secondary structures and their prediction. Bull Math Biol 1984, 46:591-621.
4. Freier SM, Kierzek R, Jaeger JA, Sugimoto N, Caruthers MH, Neilson T, Turner DH. Improved free-energy parameters for predictions of RNA duplex stability. Proc Natl Acad Sci U S A 1986, 83:9373-9377.
5. Nussinov R, Piecznik G, Griggs JR, Kleitman DJ. Algorithms for loop matching. SIAM J Appl Math 1978, 35:68-82.
6. Waterman MS, Smith TF. RNA secondary structure: a complete mathematical analysis. Math Biosci 1978, 42:257-266.
7. Lorenz R, Bernhart SH, Höner zu Siederdissen C, Tafer H, Flamm C, Stadler PF, Hofacker IL. ViennaRNA Package 2.0. Alg Mol Biol 2011, 6:26.
8. Rivas E, Lang R, Eddy SR. A range of complex probabilistic models for RNA secondary structure prediction that includes the nearest-neighbor model and more. RNA 2012, 18:193-212.
9. McCaskill JS. The equilibrium partition function and base pair binding probabilities for RNA secondary structure. Biopolymers 1990, 29:1105-1119.
10. Mückstein U, Tafer H, Hackermüller J, Bernhard SB, Stadler PF, Hofacker IL. Thermodynamics of RNA-RNA binding. Bioinformatics 2006, 22:1177-1182.
11. Mückstein U, Tafer H, Bernhard SH, Hernandez-Rosales M, Vogel J, Stadler PF, Hofacker IL. Translational control by RNA-RNA interaction: Improved computation of RNA-RNA binding thermodynamics. In: Elloumi M, Küng J, Linial M, Murphy RF, Schneider K, Toma C, eds. BioInformatics Research and Development-BIRD 2008, Vol. 13 Comm Comp Inf Sci Berlin: Springer; 2008.
12. Hofacker IL, Fontana W, Stadler PF, Bonhoeffer LS, Tacker M, Schuster P. Fast folding and comparison of RNA secondary structures. Monatsh Chem 1994, 125:167-188.
13. Tacker M, Stadler PF, Bornberg-Bauer EG, Hofacker IL, Schuster P. Algorithm independent properties of RNA structure prediction. Eur Biophy J 1996, 25: 115-130.
14. Ding Y, Lawrence CE. A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res 2003, 31:7280-7301.
15. Hofacker IL, Fekete M, Stadler PF. Secondary structure prediction for aligned RNA sequences. J Mol Biol 2002, 319:1059-1066.
16. Markham NR, Zuker M. UNAFold: software for nucleic acid folding and hybridization. Methods Mol Biol 2008, 453:3-31.
17. Fabian MR, Sonenberg N, Filipowicz W. Regulation of mRNA translation and stability by microRNAs. Annu Rev Biochem 2010, 79:351-379.
18. Narberhaus F, Vogel J. Sensory and regulatory RNAs in prokaryotes: a new german research focus. RNA Biol 2007, 4:160-164.
19. Sharma C, Darfeuille F, Plantinga T, Vogel J. A small RNA regulates multiple ABC transporter mRNAs by targeting C/A-rich elements inside and upstream of ribosome-binding sites. Genes & Dev 2007, 21: 2804-2817.
20. Majdalani N, Hernandez D, Gottesman S. Regulation and mode of action of the second small RNA activator of RpoS translation, RprA. Mol Microbiol 2002, 46:813-826.
21. Dimitrov RA, Zuker M. Prediction of hybridization and melting for double-stranded nucleic acids. Biophys J 2004, 87:215-226.
22. Bernhart SH, Tafer H, Mückstein U, Flamm C, Stadler PF, Hofacker IL. Partition function and base pairing probabilities of RNA heterodimers. Algor Mol Biol 2006, 1:3.
23. Dirks RM, Bois JS, Schaeffer JM, Winfree E, Pierce NA. Thermodynamic analysis of interacting nucleic acid strands. SIAM Rev 2007, 49:65-88.
24. Zadeh JN, Steenberg CD, Bois JS, Wolfe BR, Pierce MB, Khan AR, Dirks RM, Pierce NA. NUPACK: analysis and design of nucleic acid systems. J Comput Chem 2011, 32:170-173.
25. Busch A, Richter A, Backofen R. IntaRNA: efficient prediction of bacterial sRNA targets incorporating target site accessibility and seed regions. Bioinformatics 2008, 24:2849-2856.
26. Tafer H, Kehr S, Hertel J, Stadler PF. RNAsnoop: efficient target prediction for box H/ACA snoRNAs. Bioinformatics 2010, 26:610-616.
27. Alkan C, Karakoc E, Nadeau J, Sahinalp S, Zhang K. RNA-RNA interaction prediction and antisense RNA target search. J Comput Biol 2006, 13:267-282.
28. Chitsaz H, Salari R, Sahinalp SC, Backofen R. A partition function algorithm for interacting nucleic acid strands. Bioinformatics 2009, 25:i365-i373.
29. Huang FWD, Qin J, Reidys CM, Stadler PF. Partition function and base pairing probabilities for RNA-RNA interaction prediction. Bioinformatics 2009, 25: 2646-2654.
30. Huang FWD, Qin J, Reidys CM, Stadler PF. Target prediction and a statistical sampling algorithm for RNA-RNA interaction. Bioinformatics 2010, 26:175-181.
31. Hofacker IL, Priwitzer B, Stadler PF. Prediction of locally stable RNA secondary structures for genome-wide surveys. Bioinformatics 2004, 20:191-198.
32. Bernhart S, Hofacker IL, Stadler PF. Local RNA base pairing probabilities in large sequences. Bioinformatics 2006, 22:614-615.
33. Bompfünewerer AF, Backofen R, Berhart SH, Hertel J, Hofacker IL, Stadler PF, Will S. Variations on RNA folding and alignment: Lessons from Benasque. J Math Biol 2008, 56:129-144.
34. Tjaden B. TargetRNA: a tool for predicting targets of small RNA action in bacteria. Nucleic Acids Res 2008, 36:109-113.
35. Eggenhofer F, Tafer H, Stadler PF, Hofacker IL. RNApredator: fast accessibility-based prediction of sRNA targets. Nucleic Acids Res 2011, 39: W149-W154.
36. Tafer H, Ammann F, Eggenhoffer F, Stadler PF, Hofacker IL. Fast accessibility-based prediction of RNA-RNA interactions. Bioinformatics 2011, 27: 1934-1940.
37. Richter AS, Schleberger C, Backofen R, Steglich C. Seed-based INTARNA prediction combined with GFP-reporter system identifies mRNA targets of the small RNA Yfr1. Bioinformatics 2010, 26:1-5.
38. H. Chitsaz R. Backofen S. C. Sahinalp birna: Fast RNA-RNA binding sites prediction. Proceedings of the 9th Workshop on Algorithms in Bioinformatics (WABI), 2009, 25-36.
39. Brodersen P, Voinnet O. Revisiting the principles of microRNA target recognition and mode of action. Nat Rev Mol Cell Biol 2009, 10:141-148.
40. Holen T, Amarzguioui M, Wiiger MT, Babaie E, Prydz H. Positional effects of short interfering RNAs targeting the human coagulation trigger Tissue Factor. Nucleic Acids Res 2002, 30:1757-1766.
41. Patzel V, Rutz S, Dietrich I, Köberle C, Scheffold A, Kaufmann S. Design of siRNAs producing unstructured guide-RNAs results in improved RNA interference efficiency. Nat Biotechnol 2005, 23:1440-1444.
42. Ui-Tei K, Nishi K, Takahashi T, Nagasawa T. Thermodynamic control of small RNA-mediated gene silencing. Front Genet 2012, 3:101.
43. Tafer H, Ameres SL, Obernosterer G, Gebeshuber CA, Schroeder R, Martinez J, Hofacker IL. The impact of target site accessibility on the design of effective siRNAs. Nat Biotechnol 2008, 26:578-583.
44. Hofacker IL, Tafer H. Designing optimal siRNA based on target site accessibility. Methods Mol Biol 2010, 623:137-154.
45. Thomas M, Lieberman J, Lal A. Desperately seeking microRNA targets. Nat Struct Mol Biol 2010, 17: 1169-1174.
46. Witkos TM, Koscianska E, Krzyzosiak WJ. Practical aspects of microRNA target prediction. Curr Mol Med 2011, 11:93-109.
47. Tan Gana NH, Victoriano AFB, Okamoto T. Evaluation of online miRNA resources for biomedical applications. Genes Cells 2012, 17:11-27.
48. Lewis BP, Burge CB, Bartel DP. Conserved seed pairing, often flanked by adenosines, indicates that thousands of human genes are microRNA targets. Cell 2005, 120:15-20.
49. Krek A, Grün D, Poy MN, Wolf R, Rosenberg L, Epstein EJ, MacMenamin P, da Piedade I, Gunsalus KC, Stoffel M, et al. Combinatorial microRNA target predictions. Nat Genet 2005, 37:495-500.
50. John B, Enright AJ, Aravin A, Tuschl T, Sander C, Marks DS. Human microRNA targets. PLoS Biol 2004, 2:e363.
51. Alexiou P, Maragkakis M, Papadopoulos GL, Reczko M, Hatzigeorgiou AG. Lost in translation: an assessment and perspective for computational microRNA target identification. Bioinformatics 2009, 25:3049-3055.
52. Rigoutsos I. New tricks for animal microRNAs: targeting of amino acid coding regions at conserved and nonconserved sites. Cancer Res 2009, 69:3245-3248.
53. Fröhlich KS, Vogel J. Activation of gene expression by small RNA. Curr Opin Microbiol 2009, 12:674-682.
54. Geissmann T, Touati D. Hfq, a new chaperoning role: binding to messenger RNA determines access for small RNA regulator. EMBO J 2004, 23:396-405.
55. Nakama M, Kawakami K, Kajitani T, Urano T, Murakami Y. DNA-RNA hybrid formation mediates RNAi-directed heterochromatin formation. Genes Cells 2012, 17:218-233.
56. Qi X, Xie M, Brown AF, Bley CJ, Podlevsky JD, Chen JJ-L. RNA/DNA hybrid binding affinity determines telomerase template-translocation efficiency. EMBO J 2012, 31:150-161.
57. Tadigotla VR, O Maoiléidigh D, Sengupta AM, Epshtein V, Ebright RH, Nudler E, Ruckenstein AE. Thermodynamic and kinetic modeling of transcriptional pausing. Proc Natl Acad Sci U S A 2006, 103: 4439-4444.
58. Howard JA, Delmas S, Ivančić-Baće I, Bolt EL. Helicase dissociation and annealing of RNA-DNA hybrids by Escherichia coli Cas3 protein. Biochem J 2011, 439: 85-95.
59. Sugimoto N, Nakano S, Katoh M, Matsumura A, Nakamuta H, Ohmichi T, Yoneyama M, Sasaki M. Thermodynamic parameters to predict stability of RNA/DNA hybrid duplexes. Biochemistry 1995, 34: 11211-11216.
60. Chu C, Qu K, Zhong FL, Artandi SE, Chang HY. Genomic maps of long noncoding RNA occupancy reveal principles of RNA-chromatin interactions. Mol Cell 2011, 44:667-678.
61. Simon MD, Wang CI, Kharchenko PV, West JA, Chapman BA, Alekseyenko AA, Borowsky ML, Kuroda MI, Kingston RE. The genomic binding sites of a noncoding RNA. Proc Natl Acad Sci U S A 2011, 108: 20497-20502.
62. Plum GE, Pilch DS, Singleton SF, Breslauer KJ. Nucleic acid hybridization: triplex stability and energetics. Annu Rev Biophys Biomol Structure 1995, 24: 319-350.
63. Roberts RW, Crothers DM. Prediction of the stability of DNA triplexes. Proc Natl Acad Sci U S A 1996, 93: 4320-4325.
64. Tabaska JE, Cary RB, Gabow HN, Stormo GD. An RNA folding method capable of identifying pseudoknots and base triples. Bioinformatics 1998, 14:691-699.
65. Baltz AG, Munschauer M, Schwanhäusser B, Vasile A, Murakawa Y, Schueler M, Youngs N, Penfold-Brown D, Drew K, Milek M, et al. The mRNA-bound proteome and its global occupancy profile on protein-coding transcripts. Mol Cell 2012, 46:674-690.
66. Castello A, Fischer B, Eichelbaum K, Horos R, Beckmann BM, Strein C, Davey NE, Humphreys DT, Preiss T, Steinmetz LM, et al. Insights into RNA biology from an atlas of mammalian mRNA-binding proteins. Cell 2012, 149:1393-1406.
67. Scherrer T, Mittal N, Janga SC, Gerber AP. A screen for RNA-binding proteins in yeast indicates dual functions for many enzymes. PLoS One 2010, 5:e15499.
68. Hunter S, Jones P, Mitchell A, Apweiler R, Attwood TK, Bateman A, Bernard T, Binns D, Bork P, Burge S, et al. Interpro in 2011: new developments in the family and domain prediction database. Nucleic Acids Res 2012, 40:D306-D312.
69. Puton T, Kozlowski L, Tuszynska I, Rother K, Bujnicki JM. Computational methods for prediction of protein-RNA interactions. J Struct Biol 2012, 179:261-268.
70. Kudla G, Granneman S, Hahn D, Beggs JD, Tollervey D. Cross-linking, ligation, and sequencing of hybrids reveals RNA-RNA interactions in yeast. Proc Natl Acad Sci U S A 2011, 108:10010-10015.
71. Serganov A, Patel DJ. Towards deciphering the principles underlying an mRNA recognition code. Curr Opin Struct Biol 2008, 18:120-129.
72. Teplova M, Malinina L, Darnell JC, Song J, Lu M, Abagyan R, Musunuru K, Teplov A, Burley SK, Darnell RB, et al. Protein-RNA and protein-protein recognition by dual kh1/2 domains of the neuronal splicing factor nova-1. Structure 2011, 19:930-944.
73. Eddy SR, Durbin R. RNA sequence analysis using covariance models. Nucleic Acids Res 1994, 22: 2079-2088.
74. Nawrocki EP, Kolbe DL, Eddy SR. Infernal 1.0: inference of RNA alignments. Bioinformatics 2009, 25: 1335-1337.
75. 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 Comput Biol 2010, 6:e1000832.
76. Hiller M, Pudimat R, Busch A, Backofen R. Using RNA secondary structures to guide sequence motif finding towards single-stranded regions. Nucleic Acids Res 2006, 34:e117.
77. Ray D, Kazan H, Chan ET, Pea 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.
78. Meyer F, Kurtz S, Backofen R, Will S, Beckstette M. Structator: fast index-based search for RNA sequence-structure patterns. BMC Bioinform 2011, 12:214.
79. Hackermüller J, Meisner N-C, Auer M, Jaritz M, Stadler PF. The effect of RNA secondary structures on RNA-ligand binding and the modifier RNA mechanism: a quantitative model. Gene 2005, 345:3-12.
80. Brennan CM, Steitz JA. HuR and mRNA stability. Cell Mol Life Sci 2001, 58:266-277.
81. 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.
82. Forties RA, Bundschuh R. Modeling the interplay of single-stranded binding proteins and nucleic acid secondary structure. Bioinformatics 2010, 26:61-67.
83. Licatalosi DD, Mele A, Fak JJ, Ule J, Kayikci M, Chi SW, Clark TA, Schweitzer AC, Blume JE, Wang X, et al. Hits-clip yields genome-wide insights into brain alternative RNA processing. Nature 2008, 456:464-469.
84. Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jr. Jungkamp A-C, Munschauer M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by par-clip. Cell 2010, 141: 129-141.
85. Mukherjee N, Corcoran DL, Nusbaum JD, Reid DW, Georgiev S, Hafner M, Ascano M, Jr. Tuschl T, Ohler U, Keene JD. Integrative regulatory mapping indicates that the RNA-binding protein hur couples pre-mRNA processing and mRNA stability. Mol Cell 2011, 43:327-339.
86. Corcoran DL, Georgiev S, Mukherjee N, Gottwein E, Skalsky RL, Keene JD, Ohler U. Paralyzer: definition of RNA binding sites from par-clip short-read sequence data. Genome Biol 2011, 12:R79.
87. Lebedeva S, Jens M, Theil K, Schwanhäusser B, Selbach M, Landthaler M, Rajewsky N. Transcriptome-wide analysis of regulatory interactions of the RNA-binding protein hur. Mol Cell 2011, 43:340-352.
88. Goodarzi H, Najafabadi HS, Oikonomou P, Greco TM, Fish L, Salavati R, Cristea IM, Tavazoie S. Systematic discovery of structural elements governing stability of mammalian messenger RNAs. Nature 2012, 485: 264-268.
89. Ellington AE, Szostak JW. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346:818-822.
90. Kenan DJ, Tsai DE, Keene JD. Exploring molecular diversity with combinatorial shape libraries. Trends Biochem Sci 1994, 19:57-64.
91. Kang KN, Lee YS. RNA aptamers: a review of recent trends and applications. Adv Biochem Eng Biotechnol (Epub ahead of print; 2012).
92. Hoinka J, Zotenko E, Friedman A, Sauna ZE, Przytycka TM. Identification of sequence-structure RNA binding motifs for selex-derived aptamers. Bioinformatics 2012, 28:i215-i223.
93. Riccitelli NJ, Lupták A. Computational discovery of folded RNA domains in genomes and in vitro selected libraries. Methods 2010, 52:133-140.
94. Barrick JE, Breaker RR. The distributions, mechanisms and structures of metabolite-binding riboswitches. Genome Biol 2007, 8:239.
95. Hofacker IL, Flamm C, Heine C, Wolfinger MT, Scheuermann G, Stadler PF. BarMap: RNA folding on dynamics energy landscapes. RNA 2010, 16: 1308-1316.
96. Meyer MM, Hammond MC, Salinas Y, Roth A, Sudarsan N, Breaker RR. Challenges of ligand identification for riboswitch candidates. RNA Biol 2011, 8: 5-10.
97. Beisel CL, Smolke CD. Design principles for riboswitch function. PLoS Comput Biol 2009, 5:e1000363.
98. Kozomara A, Griffiths-Jones S. mirbase: integrating microRNA annotation and deep-sequencing data. Nucleic Acids Res 2011, 39:D152-D157.
99. Vergoulis T, Vlachos IS, Alexiou P, Georgakilas G, Maragkakis M, Reczko M, Gerangelos S, Koziris N, Dalamagas T, Hatzigeorgiou AG. Tarbase 6.0: capturing the exponential growth of miRNA targets with experimental support. Nucleic Acids Res 2012, 40: D222-D229.
100. Cook KB, Kazan H, Zuberi K, Morris Q, Hughes TR. Rbpdb: a database of RNA-binding specificities. Nucleic Acids Res 2011, 39:D301-D308.
101. Yang J-H, Li J-H, Shao P, Zhou H, Chen Y-Q, Qu L-H. starbase: a database for exploring microRNA-mRNA interaction maps from argonaute clip-seq and degradome-seq data. Nucleic Acids Res 2011, 39: D202-D209.
102. Anders G, Mackowiak SD, Jens M, Maaskola J, Kuntzagk A, Rajewsky N, Landthaler M, Dieterich C. dorina: a database of RNA interactions in post-transcriptional regulation. Nucleic Acids Res 2012, 40: D180-D186.