Physics-based RNA structure prediction

Xiaojun Xu; Shi-Jie Chen

doi:10.1007/s41048-015-0001-4

Volume 1 Issue 1

Turn off MathJax

Article Contents

Article Navigation > Biophysics Reports > 2015 > 1(1): 2-13

Xiaojun Xu, Shi-Jie Chen. Physics-based RNA structure prediction. Biophysics Reports, 2015, 1(1): 2-13. doi: 10.1007/s41048-015-0001-4

Citation:

Xiaojun Xu, Shi-Jie Chen. Physics-based RNA structure prediction. Biophysics Reports, 2015, 1(1): 2-13. doi: 10.1007/s41048-015-0001-4

Xiaojun Xu, Shi-Jie Chen. Physics-based RNA structure prediction. Biophysics Reports, 2015, 1(1): 2-13. doi: 10.1007/s41048-015-0001-4

Citation:

Xiaojun Xu, Shi-Jie Chen. Physics-based RNA structure prediction. Biophysics Reports, 2015, 1(1): 2-13. doi: 10.1007/s41048-015-0001-4

PDF (1684 KB)

Physics-based RNA structure prediction

doi: 10.1007/s41048-015-0001-4

Xiaojun Xu^1,2,3,
Shi-Jie Chen^{1,2,3
,
,}

1 Department of Physics, University of Missouri, Columbia, MO 65211, USA
2 Department of Biochemistry, University of Missouri, Columbia, MO 65211, USA
3 Informatics Institute, University of Missouri, Columbia, MO 65211, USA

Funds:

More Information

Corresponding author: Shi-Jie Chen
Received Date: 10 January 2015
Rev Recd Date: 16 February 2015
Publish Date: 31 August 2015

Abstract

Abstract

Despite the success of RNA secondary structure prediction for simple, short RNAs, the problem of predicting RNAs with long-range tertiary folds remains. Furthermore, RNA 3D structure prediction is hampered by the lack of the knowledge about the tertiary contacts and their thermodynamic parameters. Low-resolution structural modeling enables us to estimate the conformational entropies for a number of tertiary folds through rigorous statistical mechanical calculations. The models lead to 3D tertiary folds at coarse-grained level. The coarse-grained structures serve as the initial structures for all-atom molecular dynamics refinement to build the final all-atom 3D structures. In this paper, we present an overview of RNA computational models for secondary and tertiary structures' predictions and then focus on a recently developed RNA statistical mechanical model—the Vfold model. The main emphasis is placed on the physics behind the models, including the treatment of the non-canonical interactions in secondary and tertiary structure modelings, and the correlations to RNA functions.
- RNA,
- Vfold,
- 2D structure prediction,
- 3D structure prediction,
- Tertiary motif

FullText(HTML)

References(156)

References

参考文献

Xu X, Chen S-J (2012) Kinetic mechanism of conformational switch between bistable RNA hairpins. J Am Chem Soc 134:12499-12507

Ding Y, Lawrence CE (2003) A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res 31:7280-7301

Aalberts DP, Hodas NO (2010) A two-length-scale polymer theory for RNA loop free energies and helix stacking. RNA 16:1350-1355

Xu X, Zhao P, Chen S-J (2014) Vfold: a web server for RNA structure and folding thermodynamics prediction. PLoS ONE 9:e107504

Andersen ES (2010) Prediction and design of DNA and RNA structures. New Biotechnol 27:184-192

Ding F, Sharma S, Chalasani P, Demidov VV, Broude NE, Dokholyan NV (2008) Ab initio RNA folding by discrete molecular dynamics: from structure prediction to folding mechanisms. RNA 14:1164-1173

Zhang J, Lin M, Chen R, Wang W, Liang J (2008) Discrete state model and accurate estimation of loop entropy of RNA secondary structures. J Chem Phys 128:125107

Andronescu MS, Pop C, Condon A (2010a) Improved free energy parameters for RNA pseudoknotted secondary structure prediction. RNA 16:26-42

Dirks RM, Pierce NA (2003) A partition function algorithm for nucleic acid secondary structure including pseudoknots. J Comput Chem 24:1664-1677

Zhao Y, Huang Y, Gong Z, Wang Y, Man J, Xiao Y (2012) Automated and fast building of three-dimensional RNA structures. Sci Rep 2:734

Andronescu MS, Condon A, Hoos HH, Mathews DH, Murphy KP (2010b) Computational approaches for RNA energy parameter estimation. RNA 16:2304-2318

Ennifar E, Yusupov M,Walter P,Marquet R, Ehresmann B, Ehresmann C, Dumas P (1999) The crystal structure of the dimerization initiation site of genomic HIV-1 RNA reveals an extended duplex with two adenine bulges. Structure 7:1439-1449

Zuker M (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406-3415

Argaman L, Altuvia S (2000) fhlA repression by OxyS RNA: kissing complex formation at two sites results in a stable antisensetarget RNA complex. J Mol Biol 300:1101-1112

Ennifar E, Walter P, Ehresmann B, Ehresmann C, Dumas P (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat Struct Biol 8:1064-1068

Ferro DR, Hermans J (1971) A different best rigid-body molecular fit routine. Acta Crystallogr A 33:345-347

Frellsen J, Moltke I, Thiim M, Mardia KV, Ferkinghoff-Borg J, Hamelryck T (2009) A probabilistic model of RNA conformational space. PLoS Comput Biol 5:e1000406

Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3 UTRs via Alu elements. Nature 470:284-288

Bachellerie JP, Cavaille J, Huttenhofer A (2002) The expanding snoRNA world. Biochimie 84:774-790

Grosberg AY, Khokhlov A (1994) Statistical physics of macromolecules. AIP Press, New York

Bartel DP (2009) MicroRNAs: target recognition and regulatory functions. Cell 136:215-233

Gutell RR, Lee JC, Connone JJ (2002) The accuracy of ribosomal RNA comparative structure models. Curr Opin Struct Biol 12:301-310

Bellaousov S, Reuter JS, Seetin MG, Methews DH (2013) RNAstructure: web servers for RNA secondary structure prediction and analysis. Nucleic Acids Res 41:W471-W474

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

Bernhart SH, Hofacker IL, Will S, Gruber AR, Stadler PF (2008) RNAalifold: improved consensus structure prediction for RNA alignments. BMC Bioinformatics 11:474

Havgaard JH, Lyngso RB, Gorodkin J (2005) The FOLDALIGN web server for pairwise structural RNA alignment and mutual motif search. Nucleic Acids Res 33:W650-W653

Bindewald E, Shapiro BA (2006) RNA secondary structure prediction from sequence alignments using a network of k-nearest neighbor classifiers. RNA 12:342-352

He S, Su H, Liu C, Skogerbo G, He H, He D, Zhu X, Liu T, Zhao Y, Chen R (2008) MicroRNA-encoding long non-coding RNAs. BMC Genom 9:236

Bossi L, Figueroa-Bossi N (2007) A small RNA downregulates LamB maltoporin in Salmonella. Mol Microbiol 65:799-810

Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429-3431

Cao S, Chen S-J (2005) PredictingRNAfolding thermodynamics with a reduced chain representation model. RNA 11:1884-1897

Hofacker IL, Fekete M, Stadler PF (2002) Secondary structure prediction for aligned RNA sequences. J Mol Biol 319:1059-1066

Izzo JA, Kim N, Elmetwaly S, Schlick T (2011) RAG: an update to the RNA-As-Graphs resource. BMC Bioinformatics 31:219

Cao S, Chen S-J (2006) Predicting RNA pseudoknot folding thermodynamics. Nucleic Acids Res 34:2634-2652

Jonikas MA, Radmer RJ, Laederach A, Das R, Pearlman S, Herschlag D, Altman RB (2009) Coarse-grained modeling of large RNA molecules with knowledge-based potentials and structural filters. RNA 15:189-199

Jossinet F, Ludwig TE, Westhof E (2010) Assemble: an interactive graphical tool to analyze and build RNA architectures at the 2D and 3D levels. Bioinformatics 26:2057-2059

Cao S, Chen S-J (2009) Predicting structures and stabilities for H-type pseudoknots with interhelix loops. RNA 15:696-706

Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278-1284

Cao S, Chen S-J (2011a) Structure and stability of RNA/RNA kissing complex: with application of HIV dimerization initiation signal. RNA 17:2130-2143

Cao S, Chen S-J (2011b) Physics-based de novo prediction of RNA 3D structures. J Phys Chem B 115:4216-4226

Kim N, Laing C, Elmetwaly S, Jung S, Curuksu J, Schlick T (2014) Graph-based sampling for approximating global helical topologies of RNA. Proc Natl Acad Sci USA 111:4079-4084

Cao S, Chen S-J (2012a) Predicting kissing interactions in microRNA-target complex and assessment of microRNA activity. Nucleic Acids Res 40:4681-4690

Kladwang W, VanLang CC, Cordero P, Das R (2011) Understanding the errors of SHAPE-directed RNA structure modeling. Biochemistry 50:8049-8056

Cao S, Chen S-J (2012b) A domain-based model for predicting large and complex pseudoknotted structures. RNA Biol 9:201-212

Laing C, Schlick T (2011) Computational approaches to RNA structure prediction, analysis, and design. Curr Opin Struct Biol 21:306-318

Cao S, Xu X, Chen S-J (2014) Predicting structure and stability for RNA complexes with intermolecular loop-loop base pairing. RNA 20:835-845

Laughrea M, Jette L (1994) A 19-Nucleotide sequence upstream of the 5' major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA. Biochemistry 33:13464-13474

Case DA, Cheatham TE, Darden T, Gohlke H, Luo R, Merz KM, Onufriev A, Simmerling C, Wang B, Woods RJ (2005) The Amber biomolecular simulation programs. J Comput Chem 26:1668-1688

Leonard CW, Hajdin CE, Karabiber F, Mathews DH, Favorov OV, Dokholyan NV, Weeks KM (2013) Principles for understanding the accuracy of SHAPE-directed RNA structure modeling. Biochemistry 52:588-595

Chen SJ (2008) RNA folding: conformational statistics, folding kinetics, and ion electrostatics. Annu Rev Biophys 37:197-214

Li Z, Scheraga HA (1987) Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc Natl Acad Sci USA 84:6611-6615

Curuksu J, Zacharias M (2009) Enhanced conformational sampling of nucleic acids by a new Hamiltonian replica exchange molecular dynamics approach. J Chem Phys 130:104110

Liu F, Tong H, Ou-Yang Z (2006) Force unfolding single RNAs. Biophys J 90:1895-1902

Das R, Baker D (2007) Automated de novo prediction of nativelike RNA tertiary structures. Proc Natl Acad Sci USA 104:14664-14669

Das R, Kudaravalli M, Jonikas M, Laederach A, Fong R, Schwans JP, Baker D, Piccirilli JA, Altman RB, Herschlag D (2008) Structural inference of native and partially folded RNA by high-throughput contact mapping. Proc Natl Acad Sci USA 105:4144-4149

Das R, Karanicolas J, Baker D (2010) Atomic accuracy in predicting and designing noncanonical RNA structure. Nat Methods 7:291-294

Low JT, Weeks KM (2010) SHAPE-directed RNA secondary structure prediction. Methods 52:150-158

Deigan KE, Li TW, Mathews DH, Weeks KM (2009) Accurate SHAPE-directed RNA structure determination. Proc Natl Acad Sci USA 106:97-102 des Cloizeaux J (1974) Lagrangian theory for a self-avoiding random chain. Phys Rev A 10:1665-1669

Martinez HM, Maizel JV Jr, Shapiro BA (2008) RNA2D3D: a program for generating, viewing, and comparing 3-dimensional models of RNA. J Biomol Struct Dyn 25:669-683

Ding Y, Lawrence CE (2003) A statistical sampling algorithm for RNA secondary structure prediction. Nucleic Acids Res 31:7280-7301

Mathews DH, Turner DH (2002) Dynalign: an algorithm for finding the secondary structure common to two RNA sequences. J Mol Biol 317:191-203

Ding F, Sharma S, Chalasani P, Demidov VV, Broude NE, Dokholyan NV (2008) Ab initio RNA folding by discrete molecular dynamics: from structure prediction to folding mechanisms. RNA 14:1164-1173

Mathews DH, Turner DH (2006) Prediction of RNA secondary structure by free energy minimization. Curr Opin Struct Biol 16:270-278

Mathews DH, Disney MD, Childs JL, Schroeder SJ, Zuker M, Turner DH (2004) Incorporating chemical modification constraints into a dynamic programming algorithm for prediction of RNA secondary structure. Proc Natl Acad Sci USA 101:7287-7292

Dirks RM, Pierce NA (2003) A partition function algorithm for nucleic acid secondary structure including pseudoknots. J Comput Chem 24:1664-1677

Meng Y, Aalberts DP (2013) Free energy cost of stretching mRNA hairpin loops inhibits small RNA binding. Biophys J 104:482-487

Minary P, Tuckerman ME, Martyna GJ (2004) Long time molecular dynamics for enhanced conformational sampling in biomolecular systems. Phys Rev Lett 93:150201

Ennifar E, Walter P, Ehresmann B, Ehresmann C, Dumas P (2001) Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat Struct Biol 8:1064-1068

Muriaux D, De Rocquigny H, Roques BP, Paoletti J (1996a) NCp7 activates HIV-1Lai RNA dimerization by converting a transient loop-loop complex into a stable dimer. J Biol Chem 271:33686-33692

Ferro DR, Hermans J (1971) A different best rigid-body molecular fit routine. Acta Crystallogr A 33:345-347

Frellsen J, Moltke I, Thiim M, Mardia KV, Ferkinghoff-Borg J, Hamelryck T (2009) A probabilistic model of RNA conformational space. PLoS Comput Biol 5:e1000406

Muriaux D, Fosse P, Paoletti J (1996b) A kissing complex together with a stable dimer is involved in the HIV-1 Lai RNA dimerization process in vitro. Biochemistry 35:5075-5082

Paillart JC, Shehu-Xhilaga M, Marquet R, Mak J (2004) Dimerization of retroviral RNA genomes: an inseparable pair. Nat Rev Microbiol 2:461-472

Gong C, Maquat LE (2011) lncRNAs transactivate STAU1-mediated mRNA decay by duplexing with 3 UTRs via Alu elements. Nature 470:284-288

Parisien M, Major F (2008) The MC-Fold and MC-Sym pipeline infers RNA structure from sequence data. Nature 452:51-55

Grosberg AY, Khokhlov A (1994) Statistical physics of macromolecules. AIP Press, New York

Gutell RR, Lee JC, Connone JJ (2002) The accuracy of ribosomal RNA comparative structure models. Curr Opin Struct Biol 12:301-310

Pasquali S, Derreumaux P (2010) HiRE-RNA: a high resolution coarse-grained energy model for RNA. J Phys Chem B 114:11957-11966

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

Havgaard JH, Lyngso RB, Gorodkin J (2005) The FOLDALIGN web server for pairwise structural RNA alignment and mutual motif search. Nucleic Acids Res 33:W650-W653

Rahman JA, Tully JC (2002) Puddle-skimming: an efficient sampling of multidimensional configuration space. J Chem Phys 116:8750-8760

He S, Su H, Liu C, Skogerbo G, He H, He D, Zhu X, Liu T, Zhao Y, Chen R (2008) MicroRNA-encoding long non-coding RNAs. BMC Genom 9:236

Repoila F, Majdalani N, Gottesman S (2003) Small non-coding RNAs, co-ordinators of adaptation processes in Escherichia coli: the RpoS paradigm. Mol Microbiol 48:855-861

Hofacker IL (2003) Vienna RNA secondary structure server. Nucleic Acids Res 31:3429-3431

Rother K, Rother M, Boniecki M, Puton T, Bujnicki JM (2011) RNA and protein 3D structure modeling: similarities and differences. J Mol Model 17:2325-2336

Hofacker IL, Fekete M, Stadler PF (2002) Secondary structure prediction for aligned RNA sequences. J Mol Biol 319:1059-1066

Sato K, Hamada M, Asai K, Mituyama T (2009) CENTROIDFOLD: a web server for RNA secondary structure prediction. Nucleic Acids Res 37:W277-W280

Izzo JA, Kim N, Elmetwaly S, Schlick T (2011) RAG: an update to the RNA-As-Graphs resource. BMC Bioinformatics 31:219

Schmidt M, Zheng P, Delihas N (1995) Secondary structures of Escherichia coli antisense micF RNA, the 5'-end of the target ompF mRNA, and the RNA/RNA duplex. Biochemistry 34:3621-3631

Serra MJ, Turner DH (1995) Predicting thermodynamic properties of RNA. Methods Enzymol 259:242-261

Shapiro BA, Yingling YG, Kasprzak W, Bindewald E (2007) Bridging the gap in RNA structure prediction. Curr Opin Struct Biol 17:157-165

Jossinet F, Ludwig TE, Westhof E (2010) Assemble: an interactive graphical tool to analyze and build RNA architectures at the 2D and 3D levels. Bioinformatics 26:2057-2059

Sharma S, Ding F, Dokholyan NV (2008) iFoldRNA: three-dimensionalRNA structure prediction and folding. Bioinformatics 24:1951-1952

Kertesz M, Iovino N, Unnerstall U, Gaul U, Segal E (2007) The role of site accessibility in microRNA target recognition. Nat Genet 39:1278-1284

Shi YZ, Wang FH, Wu YY, Tan ZJ (2014) A coarse-grained model with implicit salt for RNAs: predicting 3D structure, stability and salt effect. J Chem Phys 141:105102

Sim AY, Minary P, Levitt M (2012) Modeling nucleic acids. Curr Opin Struct Biol 22:1-6

Kim N, Laing C, Elmetwaly S, Jung S, Curuksu J, Schlick T (2014) Graph-based sampling for approximating global helical topologies of RNA. Proc Natl Acad Sci USA 111:4079-4084

Sperschneider J, Datta A, Wise MJ (2011) Heuristic RNA pseudoknot prediction including intramolecular kissing hairpins. RNA 17:27-38

Kladwang W, VanLang CC, Cordero P, Das R (2011) Understanding the errors of SHAPE-directed RNA structure modeling. Biochemistry 50:8049-8056

Tan RK, Petrov AS, Harvey SC (2006) YUP: a molecular simulation program for coarse-grained and multiscaled models. J Chem Theory Comput 2:529-540

Laing C, Schlick T (2011) Computational approaches to RNA structure prediction, analysis, and design. Curr Opin Struct Biol 21:306-318

Turner DH, Mathews DH (2010) NNDB: the nearest neighbor parameter database for predicting stability of nucleic acid secondary structure. Nucleic Acids Res 38:D280-D282

Vogel J, Wagner EG (2007) Target identification of small noncoding RNAs in bacteria. Curr Opin Microbiol 10:262-270

Laughrea M, Jette L (1994) A 19-Nucleotide sequence upstream of the 5' major splice donor is part of the dimerization domain of human immunodeficiency virus 1 genomic RNA. Biochemistry 33:13464-13474

Wang R, Alexander RW, VanLoock M, Vladimirov S, Bukhtiyarov Y, Harvey SC, Cooperman BS (1999) Three-dimensional placement of the conserved 530 loop of 16 S rRNA and of its neighboring components in the 30 S subunit. J Mol Biol 286:521-540

Leonard CW, Hajdin CE, Karabiber F, Mathews DH, Favorov OV, Dokholyan NV, Weeks KM (2013) Principles for understanding the accuracy of SHAPE-directed RNA structure modeling. Biochemistry 52:588-595

Wang W, Wang L, Wu J, Gong Q, Shi Y (2013) Hfq-bridged ternary complex is important for translation activation of rpoS by DsrA. Nucleic Acids Res 41:5938-5948

Li Z, Scheraga HA (1987) Monte Carlo-minimization approach to the multiple-minima problem in protein folding. Proc Natl Acad Sci USA 84:6611-6615

Xayaphoummine A, Bucher T, Isambert H (2005) Kinefold web server for RNA/DNA folding path and structure prediction including pseudoknots and knots. Nucleic Acids Res 33:W605-W610

Liu F, Tong H, Ou-Yang Z (2006) Force unfolding single RNAs. Biophys J 90:1895-1902

Xia Z, Gardner DP, Gutell RR, Ren P (2010) Coarse-grained model for simulation of RNA three-dimensional structures. J Phys Chem B 114:13497-13506

Low JT, Weeks KM (2010) SHAPE-directed RNA secondary structure prediction. Methods 52:150-158

Xia Z, Bell DR, Shi Y, Ren P (2013) RNA 3D structure prediction by using a coarse-grained model and experimental data. J Phys Chem B 117:3135-3144