2D meets 4G: G-quadruplexes in RNA secondary structure prediction

IEEE/ACM Transactions on Computational Biology and Bioinformatics

Volumn 10, Issue 4, 2013, Pages 832-844

  Lorenz, Ronny ^a   Bernhart, Stephan H ^b   Qin, Jing ^b,c   Siederdissen, Christian Honer Zu ^a   Tanzer, Andrea ^a,d   Amman, Fabian ^a   Hofacker, Ivo L ^a,e   Stadler, Peter F ^a,b,c,e,f  

^a UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF LEIPZIG   (Germany)

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

^d CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^e UNIVERSITY OF COPENHAGEN   (Denmark)

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

Author keywords

Dynamic programming; RNA folding; ViennaRNA Package

Indexed keywords

COMBINATORIAL THEORY; DYNAMIC PROGRAMMING ALGORITHM; ENERGY PARAMETERS; PROTEIN-CODING; RNA FOLDING; RNA SECONDARY STRUCTURE PREDICTION; SECONDARY STRUCTURES; STRUCTURAL ELEMENTS;

DYNAMIC PROGRAMMING;

RNA;

GUANINE QUADRUPLEX; MESSENGER RNA;

5' UNTRANSLATED REGION; ARTICLE; BIOLOGY; CHEMISTRY; CONFORMATION; GENETICS; HUMAN; METABOLISM; NUCLEOTIDE SEQUENCE; RNA FOLDING; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; THERMODYNAMICS;

5' UNTRANSLATED REGIONS; BASE SEQUENCE; COMPUTATIONAL BIOLOGY; G-QUADRUPLEXES; HUMANS; NUCLEIC ACID CONFORMATION; RNA FOLDING; RNA, MESSENGER; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, RNA; THERMODYNAMICS;

EID: 84884395122     PISSN: 15455963     EISSN: None     Source Type: Journal    
DOI: 10.1109/TCBB.2013.7     Document Type: Article

References (75)

1. K. Paeschke, T. Simonsson, J. Postberg, D. Rhodes, and H.J. Lipps, "Telomere End-Binding Proteins Control the Formation of GQuadruplex DNA Structures in Vivo," Nature Structural Molecular Biology, vol. 12, pp. 847-854, 2005. (Pubitemid 41486707)
2. J.E. Johnson, J.S. Smith, M.L. Kozak, and F.B. Johnson, "In Vivo Veritas: Using Yeast to Probe the Biological Functions of GQuadruplexes," Biochimie, vol. 90, pp. 1250-1263, 2008.
3. H.M. Wong, L. Payet, and J.L. Huppert, "Function and Targeting of G-Quadruplexes," Current Opinion Molecular Therapeutics, vol. 11, pp. 146-155, 2009.
4. A. Baral, P. Kumar, R. Halder, P. Mani, V.K. Yadav, A. Singh, S.K. Das, and S. Chowdhury, "Quadruplex-Single Nucleotide Polymorphisms (Quad-SNP) Influence Gene Expression Difference among Individuals," Nucleic Acids Research, vol. 40, pp. 3800-3811, 2012.
5. D. Gomez, A. Guédin, J.L. Mergny, B. Salles, J.F. Riou, M.P. Teulade-Fichou, and P. Calsou, "A G-Quadruplex Structure within the 5'-UTR of TRF2 mRNA Represses Translation in Human Cells," Nucleic Acids Research, vol. 38, pp. 7187-7198, 2010.
6. M.J. Morris and S. Basu, "An Unusually Stable G-Quadruplex within the 5'-UTR of the MT3 Matrix Metalloproteinase mRNA Represses Translation in Eukaryotic Cells," Biochemistry, vol. 48, pp. 5313-5319, 2009.
7. L. Menon and M.R. Mihailescu, "Interactions of the G Quartet Forming Semaphorin 3F RNA with the RGG Box Domain of the Fragile X Protein Family," Nucleic Acids Research, vol. 35, pp. 5379-5392, 2007. (Pubitemid 47423912)
8. M. Bensaid, M. Melko, E.G. Bechara, L. Davidovic, A. Berretta, M.V. Catania, J. Gecz, E. Lalli, and B. Bardoni, "FRAXEAssociated Mental Retardation Protein (FMR2) Is an RNABinding Protein with High Affinity for G-Quartet RNA Forming Structure," Nucleic Acids Research, vol. 37, pp. 1269-1279, 2009.
9. A. Bugaut and S. Balasubramanian, "5'-UTR RNA G-Quadruplexes: Translation Regulation and Targeting," Nucleic Acids Research, vol. 40, pp. 4727-4741, 2012.
10. A. Arora and B. Suess, "An RNA G-Quadruplex in the 3' UTR of the Proto-Oncogene PIM1 Represses Translation," RNA Biology, vol. 8, pp. 802-805, 2011.
11. J.L. Huppert, A. Bugaut, S. Kumari, and S. Balasubramanian, "GQuadruplexes: The Beginning and End of UTRs," Nucleic Acids Research, vol. 36, pp. 6260-6268, 2008.
12. J.D. Beaudoin and J.P. Perreault, "5'-UTR G-Quadruplex Structures Acting as Translational Repressors," Nucleic Acids Research, vol. 38, pp. 7022-7036, 2010.
13. M. Wieland and J.S. Hartig, "RNA Quadruplex-Based Modulation of Gene Expression," Chemistry Biology, vol. 14, pp. 757-763, 2007. (Pubitemid 47081424)
14. G.G. Jayaraj, S. Pandey, V. Scaria, and S. Maiti, "Potential GQuadruplexes in the Human Long Non-Coding Transcriptome," RNA Biology, vol. 9, pp. 81-86, 2012.
15. B. Luke and J. Lingner, "TERRA: Telomeric Repeat-Containing RNA," EMBO J., vol. 28, pp. 2503-2510, 2009.
16. A.Y. Zhang, A. Bugaut, and S. Balasubramanian, "A Sequence-Independent Analysis of the Loop Length Dependence of Intramolecular RNA G-Quadruplex Stability and Topology," Biochemistry, vol. 50, pp. 7251-7258, 2011.
17. M. Webba da Silva, "Geometric Formalism for DNA Quadruplex Folding," Chemistry, vol. 13, pp. 9738-9745, 2007. (Pubitemid 350279686)
18. D.H. Zhang and G.Y. Zhi, "Structure Monomorphism of RNA GQuadruplex That Is Independent of Surrounding Condition," J. Biotechnology, vol. 150, pp. 6-10, 2010.
19. J. Eddy and N. Maizels, "Gene Function Correlates with Potential for G4 DNA Formation in the Human Genome," Nucleic Acids Research, vol. 34, pp. 3887-3896, 2006. (Pubitemid 44391004)
20. J.L. Huppert and S. Balasubramanian, "Prevalence of Quadruplexes in the Human Genome," Nucleic Acids Research, vol. 33, pp. 2908-2916, 2005. (Pubitemid 41511230)
21. Y. Zhao, Z. Du, and N. Li, "Extensive Selection for the Enrichment of G4 DNA Motifs in Transcriptional Regulatory Regions of Warm Blooded Animals," FEBS Letters, vol. 581, pp. 1951-1956, 2007. (Pubitemid 46670122)
22. A. Verma, K. Halder, R. Halder, V.K. Yadav, P. Rawal, R.K. Thakur, F. Mohd, A. Sharma, and S. Chowdhury, "G-Quadruplex DNA Motifs as Conserved Cis-Regulatory Elements," J. Medicinal Chemistry, vol. 51, pp. 5641-5649, 2008.
23. O. Kikin, L. D'Antonio, and P.S. Bagga, "QGRS Mapper: A Web-Based Server for Predicting G-Quadruplexes in Nucleotide Sequences," Nucleic Acids Research, vol. 34, pp. W676-W682, 2006. (Pubitemid 44529856)
24. A.K. Todd, "Bioinformatics Approaches to Quadruplex Sequence Location," Methods, vol. 43, pp. 246-251, 2007. (Pubitemid 47633212)
25. O. Stegle, L. Payet, J.-L. Mergny, D.J.C. MacKay, and J.L. Huppert, "Predicting and Understanding the Stability of G-Quadruplexes," Bioinformatics, vol. 25, pp. i374-i382, 2009.
26. R. Lorenz, S.H. Bernhart, F. Externbrink, J. Qin, C. Höner zu Siederdissen, F. Amman, I.L. Hofacker, and P.F. Stadler, "RNA Folding Algorithms with G-Quadruplexes," Proc. Brazilian Symp. Bioinformatics (BSB '12), M.C.P. de Souto and M.G. Kann, eds., pp. 49-60, 2012.
27. J.L. Mergny and L. Lacroix, "UV Melting of G-Quadruplexes," Current Protocols in Nucleic Acid Chemistry, Unit 17.1, Wiley, 2009.
28. A. Bugaut and S. Balasubramanian, "A Sequence-Independent Study of the Influence of Short Loop Lengths on the Stability and Topology of Intramolecular DNA G-Quadruplexes," Biochemistry, vol. 47, pp. 689-697, 2008. (Pubitemid 351195440)
29. D.H. Zhang, T. Fujimoto, S. Saxena, H.Q. Yu, D. Miyoshi, and N. Sugimoto, "Monomorphic RNA G-Quadruplex and Polymorphic DNA G-Quadruplex Structures Responding to Cellular Environmental Factors," Biochemistry, vol. 49, pp. 4554-4563, 2010.
30. A. Guédin, A. De Cian, J. Gros, L. Lacroix, and J.L. Mergny, "Sequence Effects in Single-Base Loops for Quadruplexes," Biochimie, vol. 90, pp. 686-696, 2008.
31. A. Guédin, J. Gros, A. Patrizia, and J.-L. Mergny, "How Long Is Too Long? Effects of Loop Size on G-Quadruplex Stability," Nucleic Acids Research, vol. 38, pp. 7858-7868, 2010.
32. C.T. Lauhon and J.W. Szostak, "RNA Aptamers that Bind Flavin and Nicotinamide Redox Cofactors," J. Am. Chemical Soc., vol. 117, pp. 1246-1257, 1995.
33. A. Joachimi, A. Benz, and J.S. Hartig, "A Comparison of DNA and RNA Quadruplex Structures and Stabilities," Bioorganic Medicinal Chemistry, vol. 17, pp. 6811-6815, 2009.
34. R. Lorenz, S.H. Bernhart, C. Höner zu Siederdissen, H. Tafer, C. Flamm, P.F. Stadler, and I.L. Hofacker, "ViennaRNA Package 2.0," Algorithms Molecular Biology, vol. 6, article 26, 2011.
35. P. Schuster, W. Fontana, P.F. Stadler, and I.L. Hofacker, "From Sequences to Shapes and Back: A Case Study in RNA Secondary Structures," Proc. Royal Soc. London B, vol. 255, pp. 279-284, 1994. (Pubitemid 24102288)
36. R. Giegerich, B. Voss, and M. Rehmsmeier, "Abstract Shapes of RNA," Nucleic Acids Research, vol. 32, pp. 4843-4851, 2004. (Pubitemid 39429688)
37. P. Flajolet and R. Sedgewick, Analytic Combinatorics. Cambridge Univ. Press, 2009.
38. I.L. Hofacker, P. Schuster, and P.F. Stadler, "Combinatorics of RNA Secondary Structures," Discrete Applied Math., vol. 88, pp. 207-237, 1998. (Pubitemid 128379054)
39. D.H. Mathews, M.D. Disney, J.L. Childs, S.J. Schroeder, M. Zuker, and D.H. Turner, "Incorporating Chemical Modification Constraints into a Dynamic Programming Algorithm for Prediction of RNA Secondary Structure," Proc. Nat'l Academy Sciences USA, vol. 101, pp. 7287-7292, 2004. (Pubitemid 38638025)
40. M. Zuker and P. Stiegler, "Optimal Computer Folding of Large RNA Sequences Using Thermodynamics and Auxiliary Information," Nucleic Acids Research, vol. 9, pp. 133-148, 1981.
41. J.S. McCaskill, "The Equilibrium Partition Function and Base Pair Binding Probabilities for RNA Secondary Structure," Biopolymers, vol. 29, pp. 1105-1119, 1990. (Pubitemid 20145703)
42. R.E. Bruccoleri and G. Heinrich, "An Improved Algorithm for Nucleic Acid Secondary Structure Display," Computer Application Biosciences, vol. 4, pp. 167-173, 1988. (Pubitemid 18072033)
43. C.B. Do, D.A. Woods, and S. Batzoglou, "CONTRAfold: RNA Secondary Structure Prediction without Physics-Based Models," Bioinformatics, vol. 22, no. 14, pp. e90-e98, 2006. (Pubitemid 44288277)
44. S. Kumari, A. Bugaut, J.L. Huppert, and S. Balasubramanian, "An RNA G-Quadruplex in the 5'UTR of the NRAS Proto-Oncogene Modulates Translation," Nat'l Chemical Biology, vol. 3, pp. 218-221, 2007. (Pubitemid 46440536)
45. I.L. Hofacker, B. Priwitzer, and P.F. Stadler, "Prediction of Locally Stable RNA Secondary Structures for Genome-Wide Surveys," Bioinformatics, vol. 20, pp. 191-198, 2004.
46. S. Bernhart, I.L. Hofacker, and P.F. Stadler, "Local RNA Base Pairing Probabilities in Large Sequences," Bioinformatics, vol. 22, pp. 614-615, 2006. (Pubitemid 43372823)
47. S.H. Bernhart, H. Tafer, U. Mü ckstein, C. Flamm, P.F. Stadler, and I.L. Hofacker, "Partition Function and Base Pairing Probabilities of RNA Heterodimers," Algorithms Molecular Biology, vol. 1, article 3, 2006.
48. U. Mü ckstein, H. Tafer, J. Hackermü ller, S.B. Bernhard, P.F. Stadler, and I.L. Hofacker, "Thermodynamics of RNA-RNA Binding," Bioinformatics, vol. 22, pp. 1177-1182, 2006. (Pubitemid 43779008)
49. A. Busch, A. Richter, and R. Backofen, "IntaRNA: Efficient Prediction of Bacterial sRNA Targets Incorporating Target Site Accessibility and Seed Regions," Bioinformatics, vol. 24, pp. 2849-2856, 2008.
50. M. Rehmsmeier, P. Steffen, M. Höchsmann, and R. Giegerich, "Fast and Effective Prediction of MicroRNA/Target Duplexes," RNA, vol. 10, pp. 1507-1517, 2004. (Pubitemid 39288185)
51. K. Ito, S. Go, M. Komiyama, and Y. Xu, "Inhibition of Translation by Small RNA-Stabilized mRNA Structures in Human Cells," J. Am. Chemical Soc., vol. 133, pp. 19153-19159, 2011.
52. H. Tafer, F. Ammann, F. Eggenhoffer, P.F. Stadler, and I.L. Hofacker, "Fast Accessibility-Based Prediction of RNA-RNA Interactions," Bioinformatics, vol. 27, pp. 1934-1940, 2011.
53. D. Pervouchine, "IRIS: Intermolecular RNA Interaction Search," Proc. Int'l Conf. Genome Informatics, vol. 15, pp. 92-101, 2004.
54. C. Alkan, E. Karakoc, J. Nadeau, S. Sahinalp, and K. Zhang, "RNA-RNA Interaction Prediction and Antisense RNA Target Search," J. Computational Biology, vol. 13, pp. 267-282, 2006.
55. H. Chitsaz, R. Salari, S. Sahinalp, and R. Backofen, "A Partition Function Algorithm for Interacting Nucleic Acid Strands," Bioinformatics, vol. 25, pp. i365-i373, 2009.
56. F.W.D. Huang, J. Qin, C.M. Reidys, and P.F. Stadler, "Partition Function and Base Pairing Probabilities for RNA-RNA Interaction Prediction," Bioinformatics, vol. 25, pp. 2646-2654, 2009.
57. F.W.D. Huang, J. Qin, C.M. Reidys, and P.F. Stadler, "Target Prediction and a Statistical Sampling Algorithm for RNA-RNA Interaction," Bioinformatics, vol. 26, pp. 175-181, 2010.
58. I.L. Hofacker, M. Fekete, and P.F. Stadler, "Secondary Structure Prediction for Aligned RNA Sequences," J. Molecular Biology, vol. 319, pp. 1059-1066, 2002. (Pubitemid 34729418)
59. S.H. Bernhart, I.L. Hofacker, S. Will, A.R. Gruber, and P.F. Stadler, "RNAalifold: Improved Consensus Structure Prediction for RNA Alignments," BMC Bioinformatics, vol. 9, article 474, 2008.
60. S.W. Burge, J. Daub, R. Eberhardt, J. Tate, L. Barquist, E.P. Nawrocki, S.R. Eddy, P.P. Gardner, and A. Bateman, "Rfam 11.0: 10 Years of RNA Families," Nucleic Acids Research, vol. 41, pp. D226-D232, 2012.
61. T.W. Harris, I. Antoshechkin, T. Bieri, D. Blasiar, J. Chan, W.J. Chen, N. De La Cruz, P. Davis, M. Duesbury, R. Fang, J. Fernandes, M. Han, R. Kishore, R. Lee, H.M.Mü ller, C. Nakamura, P. Ozersky, A. Petcherski, A. Rangarajan, A. Rogers, G. Schindelman, E.M. Schwarz, M.A. Tuli, K. Van Auken, D. Wang, X. Wang, G. Williams, K. Yook, R. Durbin, L.D. Stein, J. Spieth, and P.W. Sternberg, "WormBase: A Comprehensive Resource for Nematode Research," Nucleic Acids Research, vol. 38, pp. D463-D467, 2010.
62. P. McQuilton, S.E.S. Pierre, J. Thurmond and the FlyBase Consortium, "FlyBase 101-The Basics of Navigating FlyBase," Nucleic Acids Research, vol. 40, pp. D706-D714, 2012.
63. P. Flicek, M. Amode, D. Barrell, K. Beal, S. Brent, D. Carvalho-Silva, P. Clapham, G. Coates, S. Fairley, S. Fitzgerald, L. Gil, L. Gordon, M. Hendrix, T. Hourlier, N. Johnson, A.K. Kähäri, D. Keefe, S. Keenan, R. Kinsella, M. Komorowska, G. Koscielny, E. Kulesha, P. Larsson, I. Longden, W. McLaren, M. Muffato, B. Overduin, M. Pignatelli, B. Pritchard, H.S. Riat, G.R. Ritchie, M. Ruffier, M. Schuster, D. Sobral, Y.A. Tang, K. Taylor, S. Trevanion, J. Vandrovcova, S. White, M. Wilson, S.P. Wilder, B.L. Aken, E. Birney, F. Cunningham, I. Dunham, R. Durbin, X.M. Fernández-Suarez, J. Harrow, J. Herrero, T.J. Hubbard, A. Parker, G. Proctor, G. Spudich, J. Vogel, A. Yates, A. Zadissa, and S.M. Searle, "Ensembl 2012," Nucleic Acids Research, vol. 40, pp. D84-D90, 2012.
64. A.R. Quinlan and I.M. Hall, "Bedtools: A Flexible Suite of Utilities for Comparing Genomic Features," Bioinformatics, vol. 26, pp. 841-842, 2010.
65. J. Gros, A. Guédin, J.-L. Mergny, and L. Lacroix, "G-Quadruplex Formation Interferes with P1 Helix Formation in the RNA Component of Telomerase hTERC," ChemBioChem, vol. 9, pp. 2075-2079, 2008.
66. S.C.J. Parker, E.H. Margulies, and T.D. Tullius, "The Relationship between Fine Scale DNA Structure, GC Content, and Functional Elements in 1% of the Human Genome," Genome Informatics, vol. 20, pp. 199-211, 2008.
67. A. Arora, M. Dutkiewicz, V. Scaria, M. Hariharan, S. Maiti, and J. Kurreck, "Inhibition of Translation in Living Eukaryotic Cells by an RNA G-Quadruplex Motif," RNA, vol. 14, pp. 1290-1296, 2008. (Pubitemid 351872187)
68. R. Shahid, A. Bugaut, and S. Balasubramanian, "The BCL-2 5' Untranslated Region Contains an RNA G-Quadruplex-Forming Motif That Modulates Protein Expression," Biochemistry, vol. 49, pp. 8300-8306, 2010.
69. K. Halder, M. Wieland, and J.S. Hartig, "Predictable Suppression of Gene Expression by 5'-UTR-Based RNA Quadruplexes," Nucleic Acids Research, vol. 37, no. 20, pp. 6811-6817, 2009.
70. S. Lammich, F. Kamp, J. Wagner, B. Nuscher, S. Zilow, A.-K. Ludwig, M. Willem, and C. Haass, "Translational Repression of the Disintegrin and Metalloprotease ADAM10 by a Stable GQuadruplex Secondary Structure in Its 5'-Untranslated Region," J. Biological Chemistry, vol. 286, pp. 45063-45072, 2011.
71. M.J. Morris, Y. Negishi, C. Pazsint, J.D. Schonhoft, and S. Basu, "An RNA G-Quadruplex Is Essential for Cap-Independent Translation Initiation in Human VEGF IRES," J. Am. Chemical Soc., vol. 132, pp. 17831-17839, 2010.
72. P.R. Wills, "Potential Pseudoknots in the PrP-Encoding mRNA," J. Theoretical Biology, vol. 159, pp. 523-527, 1992. (Pubitemid 23055514)
73. I. Barrette, G. Poisson, P. Gendron, and F. Major, "Pseudoknots in Prion Protein mRNAs Confirmed by Comparative Sequence Analysis and Pattern Searching," Nucleic Acids Research, vol. 29, pp. 753-758, 2001. (Pubitemid 32124387)
74. P. Cavaliere, B. Pagano, V. Granata, S. Prigent, H. Rezaei, C. Giancola, and A. Zagari, "Cross-Talk between Prion Protein and Quadruplex-Forming Nucleic Acids: A Dynamic Complex Formation," Nucleic Acids Research, vol. 41, pp. 327-339, 2013.
75. J.A. Capra, K. Paeschke, M. Singh, and V.A. Zakian, "GQuadruplex DNA Sequences Are Evolutionarily Conserved and Associated with Distinct Genomic Features in Saccharomyces cerevisiae," PLoS Computational Biology, vol. 6, article e1000861, 2010