In this feature article, we provide a side-by-side introduction for two research fields: quantum chemical calculations of molecular interaction in nucleic acids and RNA structural bioinformatics. Our main aim is to demonstrate that these research areas, while largely separated in contemporary literature, have substantial potential to complement each other that could significantly contribute to our understanding of the exciting world of nucleic acids. We identify research questions amenable to the combined application of modern ab initio methods and bioinformatics analysis of experimental structures while also assessing the limitations of these approaches. The ultimate aim is to attain valuable physicochemical insights regarding the nature of the fundamental molecular interactions and how they shape RNA structures, dynamics, function, and evolution.

Institute of Biophysics Academy of Sciences of the Czech Republic Královopolská 135 61265 Brno Czech Republic

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Kruger K, Grabowski PJ, Zaug AJ, Sands J, Gottschling DE, Cech TR. Cell. 1982;31:147–157. PubMed

Guerrier-Takada C, Gardiner K, Marsh T, Pace N, Altman S. Cell. 1983;35:849–857. PubMed

Wahl MC, Will CL, Luhrmann R. Cell. 2009;136:701–718. PubMed

Frank J, Zhu J, Penczek P, Li YH, Srivastava S, Verschoor A, Radermacher M, Grassucci R, Lata RK, Agrawal RK. Nature. 1995;376:441–444. PubMed

Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JHD, Noller HF. Science. 2001;292:883–896. PubMed

Wimberly BT, Brodersen DE, Clemons WM, Morgan-Warren RJ, Carter AP, Vonrhein C, Hartsch T, Ramakrishnan V. Nature. 2000;407:327–339. PubMed

Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. Science. 2000;289:905–920. PubMed

Ramakrishnan V, Moore PB. Curr. Opin. Struc. Biol. 2001;11:144–154. PubMed

Mitra K, Frank J. Annu. Rev. Bioph. Biom. 2006;35:299–317. PubMed

Korostelev A, Ermolenko DN, Noller HF. Curr. Opin. Chem. Biol. 2008;12:674–683. PubMed PMC

Halic M, Becker T, Pool MR, Spahn CMT, Grassucci RA, Frank J, Beckmann R. Nature. 2004;427:808–814. PubMed

Egea PF, Stroud RM, Walter P. Curr. Opin. Struc. Biol. 2005;15:213–220. PubMed

Catania F, Gao X, Scofield DG. J. Hered. 2009;100:591–596. PubMed PMC

Gesteland RF, Cech TR, Atkins JF. The RNA World. New York: Cold Spring Harbor Laboratory Press: Cold Spring Harbor; 2006.

Birney E, Stamatoyannopoulos JA, Dutta A, et al. Nature. 2007;447:799–816. PubMed PMC

Carninci P. Trends Genet. 2006;22:501–510. PubMed

Pheasant M, Mattick JS. Genome Res. 2007;17:1245–1253. PubMed

Fire A, Xu SQ, Montgomery MK, Kostas SA, Driver SE, Mello CC. Nature. 1998;391:806–811. PubMed

Hobza P, Selzle HL, Schlag EW. J. Phys. Chem. 1996;100:18790–18794.

Hobza P, Selzle HL, Schlag EW. Chem. Rev. 1994;94:1767–1785.

Zhao Y, Truhlar DG. Accounts Chem. Res. 2008;41:157–167. PubMed

Cieplak P, Dupradeau FY, Duan Y, Wang JM. J. Phys.- Condens. Mat. 2009;21 Art. No. 333102. PubMed PMC

Ponder JW, Wu CJ, Ren PY, Pande VS, Chodera JD, Schnieders MJ, Haque I, Mobley DL, Lambrecht DS, DiStasio RA, Head-Gordon M, Clark GNI, Johnson ME, Head-Gordon T. J. Phys. Chem. B. 2010;114:2549–2564. PubMed PMC

Cornell WD, Cieplak P, Bayly CI, Gould IR, Merz KM, Ferguson DM, Spellmeyer DC, Fox T, Caldwell JW, Kollman PA. J. Am. Chem. Soc. 1995;117:5179–5197.

Ornstein RL, Rein R, Breen DL, Macelroy RD. Biopolymers. 1978;17:2341–2360. PubMed

Langlet J, Claverie P, Caron F, Boeuve JC. Int. J. Quant. Chem. 1981;20:299–338.

Forner W, Otto P, Ladik J. Chem. Phys. 1984;86:49–56.

Gresh N, Pullman B. Int. J. Quant. Chem. 1985;(Suppl. 12):49–56.

Aida M, Nagata C. Int. J. Quant. Chem. 1986;29:1253–1261.

Hobza P, Sandorfy C. J. Am. Chem. Soc. 1987;109:1302–1307.

Anwander EHS, Probst MM, Rode BM. Biopolymers. 1990;29:757–769. PubMed

Colson AO, Besler B, Close DM, Sevilla MD. J. Phys. Chem. 1992;96:661–668.

Hobza P, Sponer J, Polasek M. J. Am. Chem. Soc. 1995;117:792–798.

Sponer J, Leszczynski J, Hobza P. J. Phys. Chem. 1996;100:5590–5596.

Hobza P, Sponer J. Chem. Rev. 1999;99:3247–3276. PubMed

Sponer J, Leszczynski J, Hobza P. Biopolymers. 2001;61:3–31. PubMed

Sponer J, Gabb HA, Leszczynski J, Hobza P. Biophys. J. 1997;73:76–87. PubMed PMC

Sponer J, Hobza P. J. Phys. Chem. 1994;98:3161–3164.

Sponer J, Hobza P. J. Am. Chem. Soc. 1994;116:709–714.

Hobza P, Sponer J. J. Am. Chem. Soc. 2002;124:11802–11808. PubMed

Leininger ML, Nielsen IMB, Colvin ME, Janssen CL. J. Phys. Chem. A. 2002;106:3850–3854.

Jurecka P, Hobza P. J. Am. Chem. Soc. 2003;125:15608–15613. PubMed

Sponer J, Jurecka P, Hobza P. J. Am. Chem. Soc. 2004;126:10142–10151. PubMed

Sponer J, Jurecka P, Marchan I, Luque FJ, Orozco M, Hobza P. Chem.- Eur. J. 2006;12:2854–2865. PubMed

Sponer J, Riley KE, Hobza P. Phys. Chem. Chem. Phys. 2008;10:2595–2610. PubMed

Perez A, Marchan I, Svozil D, Sponer J, Cheatham TE, Laughton CA, Orozco M. Biophys. J. 2007;92:3817–3829. PubMed PMC

Cheatham TE, Cieplak P, Kollman PA. J. Biomol. Struct. Dyn. 1999;16:845–862. PubMed

Mackerell AD. J. Comput. Chem. 2004;25:1584–1604. PubMed

Prive GG, Yanagi K, Dickerson RE. J. Mol. Biol. 1991;217:177–199. PubMed

Suzuki M, Amano N, Kakinuma J, Tateno M. J. Mol. Biol. 1997;274:421–435. PubMed

Leontis NB, Stombaugh J, Westhof E. Nucleic Acids Res. 2002;30:3497–3531. PubMed PMC

Stombaugh J, Zirbel CL, Westhof E, Leontis NB. Nucleic Acids Res. 2009;37:2294–2312. PubMed PMC

de Vries MS, Hobza P. Annu. Rev. Phys. Chem. 2007;58:585–612. PubMed

Voet D, Voet JG, Pratt CW. Fundamentals of Biochemistry. 3rd. Wiley & Sons, Inc; 2008.

Svozil D, Hobza P, Sponer J. J. Phys. Chem. B. 2010;114:1191–1203. PubMed

Mathews DH, Sabina J, Zuker M, Turner DH. J. Mol. Biol. 1999;288:911–940. PubMed

SantaLucia J. Proc. Natl. Acad. Sci. U. S. A. 1998;95:1460–1465. PubMed PMC

Ditzler MA, Otyepka M, Sponer J, Walter NG. Accounts Chem. Res. 2010;43:40–47. PubMed PMC

Banas P, Jurecka P, Walter NG, Sponer J, Otyepka M. Methods. 2009;49:202–216. PubMed PMC

Sponer J, Lankas F. Computational Studies of RNA and DNA. Dordrecht: Springer; 2006.

Tomasi J, Mennucci B, Cammi R. Chem. Rev. 2005;105:2999–3093. PubMed

Florian J, Sponer J, Warshel A. J. Phys. Chem. B. 1999;103:884–892.

Klamt A, Schuurmann G. J. Chem. Soc.-Perkin Trans. 1993;2:799–805.

Bachs M, Luque FJ, Orozco M. J. Comput. Chem. 1994;15:446–454.

Luque FJ, Curutchet C, Munoz-Muriedas J, Bidon-Chanal A, Soteras I, Morreale A, Gelpi JL, Orozco M. Phys. Chem. Chem. Phys. 2003;5:3827–3836.

Sponer JE, Reblova K, Mokdad A, Sychrovsky V, Leszczynski J, Sponer J. J. Phys. Chem. B. 2007;111:9153–9164. PubMed

Mladek A, Sharma P, Mitra A, Bhattacharyya D, Sponer J, Sponer JE. J. Phys. Chem. B. 2009;113:1743–1755. PubMed

Soteras I, Forti F, Orozco M, Luque FJ. J. Phys. Chem. B. 2009;113:9330–9334. PubMed

Soteras I, Orozco M, Luque FJ. J. Comput .- Aided Mol. Des. 2010;24:281–291. PubMed

Curutchet C, Orozco M, Luque FJ. J. Comput. Chem. 2001;22:1180–1193.

Soteras I, Curutchet C, Bidon-Chanal A, Orozco M, Luque FJ. J. Mol. Struct.-Theochem. 2005;727:29–40.

Ribeiro RF, Marenich AV, Cramer CJ, Truhlar DG. J. Comput .- Aided Mol. Des. 2010;24:317–333. PubMed

Marenich AV, Olson RM, Kelly CP, Cramer CJ, Truhlar DG. J. Chem. Theory Comput. 2007;3:2011–2033. PubMed

Marenich AV, Cramer CJ, Truhlar DG. J. Phys. Chem. B. 2009;113:6378–6396. PubMed

Marenich AV, Cramer CJ, Truhlar DG. J. Chem. Theory Comput. 2009;5:2447–2464. PubMed

Klamt A, Diedenhofen M. J. Comput .- Aided Mol. Des. 2010;24:357–360. PubMed

Klamt A, Jonas V, Burger T, Lohrenz JCW. J. Phys. Chem. A. 1998;102:5074–5085.

Richardson JS, Schneider B, Murray LW, Kapral GJ, Immormino RM, Headd JJ, Richardson DC, Ham D, Hershkovits E, Williams LD, Keating KS, Pyle AM, Micallef D, Westbrook J, Berman HM. RNA. 2008;14:465–481. PubMed PMC

Svozil D, Kalina J, Omelka M, Schneider B. Nucleic Acids Res. 2008;36:3690–3706. PubMed PMC

Svozil D, Sponer JE, Marchan I, Perez A, Cheatham TE, Forti F, Luque FJ, Orozco M, Sponer J. J. Phys. Chem. B. 2008;112:8188–8197. PubMed

Millen AL, Manderville RA, Wetmore SD. J. Phys. Chem. B. 2010;114:4373–4382. PubMed

Palamarchuk GV, Shishkin OV, Gorb L, Leszczynski J. J. Biomol. Struct. Dyn. 2009;26:653–661. PubMed

MacKerell AD. J. Phys. Chem. B. 2009;113:3235–3244. PubMed PMC

Foloppe N, Hartmann B, Nilsson L, MacKerell AD. Biophys. J. 2002;82:1554–1569. PubMed PMC

Foloppe N, Nilsson L, MacKerell AD. Biopolymers. 2001;61:61–76. PubMed

Hocquet A, Leulliot N, Ghomi M. J. Phys. Chem. B. 2000;104:4560–4568.

Florian J, Strajbl M, Warshel A. J. Am. Chem. Soc. 1998;120:7959–7966.

Sychrovsky V, Vokacova Z, Sponer J, Spackova N, Schneider B. J. Phys. Chem. B. 2006;110:22894–22902. PubMed

Reed AE, Curtiss LA, Weinhold F. Chem. Rev. 1988;88:899–926.

Bader RFW. Atoms in Molecules. A Quantum Theory. Oxford: Clarendon Press; 1990.

Hobza P, Sponer J, Cubero E, Orozco M, Luque FJ. J. Phys. Chem. B. 2000;104:6286–6292.

Guerra CF, Bickelhaupt FM. Angew. Chem. Int. Ed. 2002;41:2092–2095. PubMed

Sponer J, Zgarbova M, Jurecka P, Riley KE, Sponer JE, Hobza P. J. Chem. Theory Comput. 2009;5:1166–1179. PubMed

Hesselmann A, Jansen G, Schutz M. J. Am. Chem. Soc. 2006;128:11730–11731. PubMed

Gresh N. J. Comput. Chem. 1995;16:856–882.

Gresh N, Sponer JE, Spackova N, Leszczynski J, Sponer J. J. Phys. Chem. B. 2003;107:8669–8681.

Gresh N, Sponer J. J. Phys. Chem. B. 1999;103:11415–11427.

Jeziorski B, Moszynski R, Szalewicz K. Chem. Rev. 1994;94:1887–1930.

Hesselmann A, Jansen G, Schutz M. J. Chem. Phys. 2005;122:014103. PubMed

Mattick JS. J. Exp. Biol. 2007;210:1526–1547. PubMed

Beniaminov A, Westhof E, Krol A. RNA. 2008;14:1270–1275. PubMed PMC

Mokdad A, Krasovska MV, Sponer J, Leontis NB. Nucleic Acids Res. 2006;34:1326–1341. PubMed PMC

Leontis NB, Westhof E. RNA. 2001;7:499–512. PubMed PMC

Nissen P, Ippolito JA, Ban N, Moore PB, Steitz TA. Proc. Natl. Acad. Sci. U. S. A. 2001;98:4899–4903. PubMed PMC

Tamura M, Holbrook SR. J. Mol. Biol. 2002;320:455–474. PubMed

Gagnon MG, Steinberg SV. RNA. 2002;8:873–877. PubMed PMC

Noller HF. Science. 2005;309:1508–1514. PubMed

Swart M, Guerra CF, Bickelhaupt FM. J. Am. Chem. Soc. 2004;126:16718–16719. PubMed

Perez A, Sponer J, Jurecka P, Hobza P, Luque FJ, Orozco M. Chem. Eur. J. 2005;11:5062–5066. PubMed

Acosta-Silva C, Branchadell V, Bertran J, Oliva A. J. Phys. Chem. B. 2010;114:10217–10227. PubMed

Vertessy BG, Toth J. Accounts Chem. Res. 2009;42:97–106. PubMed PMC

Krokan HE, Drablos F, Slupphaug G. Oncogene. 2002;21:8935–8948. PubMed

Parisien M, Major F. Nature. 2008;452:51–55. PubMed

Das R, Karanicolas J, Baker D. Nat. Methods. 2010;7:291–294. PubMed PMC

Mathews DH, Turner DH. Curr. Opin. Struc. Biol. 2006;16:270–278. PubMed

Deigan KE, Li TW, Mathews DH, Weeks KM. Proc. Natl. Acad. Sci. U. S. A. 2009;106:97–102. PubMed PMC

Mathews D, Disney M, Childs J, Schroeder S, Zuker M, Turner D. Proc. Natl. Acad. Sci. U. S. A. 2004;101:7287–7292. PubMed PMC

Eddy SR, Durbin R. Nucleic Acids Res. 1994;22:2079–2088. PubMed PMC

Gardner PP, Giegerich R. BMC Bioinformatics. 2004;5 Art. No. 140. PubMed PMC

Michel F, Westhof E. J. Mol. Biol. 1990;216:585–610. PubMed

Massire C, Jaeger L, Westhof E. J. Mol. Biol. 1998;279:773–793. PubMed

Michel F, Costa M, Massire C, Westhof E. Methods Enzymol. 2000;317:491–510. PubMed

Brown JW, Birmingham A, Griffiths PE, Jossinet F, Kachouri-Lafond R, Knight R, Lang BF, Leontis N, Steger G, Stombaugh J, Westhof E. RNA. 2009;15:1623–1631. PubMed PMC

Reblova K, Spackova N, Stefl R, Csaszar K, Koca J, Leontis NB, Sponer J. Biophys. J. 2003;84:3564–3582. PubMed PMC

Reblova K, Strelcova Z, Kulhanek P, Besscova I, Mathews DH, Van Nostrand K, Yildirim I, Turner DH, Sponer J. J. Chem. Theory Comput. 2010;6:910–929. PubMed PMC

Sponer J, Mokdad A, Sponer JE, Spackova N, Leszczynski J, Leontis NB. J. Mol. Biol. 2003;330:967–978. PubMed

Freier SM, Sugimoto N, Sinclair A, Alkema D, Neilson T, Kierzek R, Caruthers MH, Turner DH. Biochemistry. 1986;25:3214–3219. PubMed

Yildirim I, Turner DH. Biochemistry. 2005;44:13225–13234. PubMed PMC

Kopitz H, Zivkovic A, Engels JW, Gohlke H. ChemBioChem. 2008;9:2619–2622. PubMed

Yildirim I, Stern HA, Sponer J, Spackova N, Turner DH. J. Chem. Theory Comput. 2009;5:2088–2100. PubMed PMC

Koller AN, Bozilovic J, Engels JW, Gohlke H. Nucleic Acids Res. 2010;38:3133–3146. PubMed PMC

Kool ET. Annu. Rev. Biochemistry. 2002;71:191–219. PubMed

Krueger AT, Kool ET. Curr. Opin. Chem. Biol. 2007;11:588–594. PubMed PMC

Sarver M, Zirbel CL, Stombaugh J, Mokdad A, Leontis NB. J. Math. Biol. 2008;56:215–252. PubMed PMC

Nozinovic S, Furtig B, Jonker HRA, Richter C, Schwalbe H. Nucleic Acids Res. 2010;38:683–694. PubMed PMC

Leontis NB, Lescoute A, Westhof E. Curr. Opin. Struc. Biol. 2006;16:279–287. PubMed PMC

Lescoute A, Leontis NB, Massire C, Westhof E. Nucleic Acids Res. 2005;33:2395–2409. PubMed PMC

Lescoute A, Westhof E. RNA. 2006;12:83–93. PubMed PMC

Laing C, Schlick T. J. Mol. Biol. 2009;390:547–559. PubMed PMC

Klein DJ, Schmeing TM, Moore PB, Steitz TA. EMBO J. 2001;20:4214–4221. PubMed PMC

Razga F, Koca J, Sponer J, Leontis NB. Biophys. J. 2005;88:3466–3485. PubMed PMC

Reblova K, Razga F, Li W, Gao HX, Frank J, Sponer J. Nucleic Acids Res. 2010;38:1325–1340. PubMed PMC

Correll CC, Freeborn B, Moore PB, Steitz TA. Cell. 1997;91:705–712. PubMed

Correll CC, Munishkin A, Chan YL, Ren Z, Wool IG, Steitz TA. Proc. Natl. Acad. Sci. U. S. A. 1998;95:13436–13441. PubMed PMC

Correll CC, Wool IG, Munishkin A. J. Mol. Biol. 1999;292:275–287. PubMed

Parisien M, Cruz JA, Westhof E, Major F. RNA. 2009;15:1875–1885. PubMed PMC

Shankar N, Kennedy SD, Chen G, Krugh TR, Turner DH. Biochemistry. 2006;45:11776–11789. PubMed PMC

Lee JC, Gutell RR, Russell R. J. Mol. Biol. 2006;360:978–988. PubMed

Nasalean L, Stombaugh J, Zirbel C, Leontis N, Walter NG, Woodson S, Batey RT. Non-Protein Coding RNAs. 2009;13:1–26.

Jaeger L, Verzemnieks EJ, Geary C. Nucleic Acids Res. 2009;37:215–230. PubMed PMC

Besseova I, Otyepka M, Reblova K, Sponer J. Phys. Chem. Chem. Phys. 2009;11:10701–10711. PubMed

Sponer JE, Spackova N, Kulhanek P, Leszczynski J, Sponer J. J. Phys. Chem. A. 2005;109:2292–2301. PubMed

Sponer JE, Spackova N, Leszczynski J, Sponer J. J. Phys. Chem. B. 2005;109:11399–11410. PubMed

Sponer JE, Leszczynski J, Sychrovsky V, Sponer J. J. Phys. Chem. B. 2005;109:18680–18689. PubMed

Sharma P, Sponer JE, Sponer J, Sharma S, Bhattacharyya D, Mitra A. J. Phys. Chem. B. 2010;114:3307–3320. PubMed

Sharma P, Mitra A, Sharma S, Singh H, Bhattacharyya D. J. Biomol. Struct. Dyn. 2008;25:709–732. PubMed

Oliva R, Tramontano A, Cavallo L. RNA. 2007;13:1427–1436. PubMed PMC

Oliva R, Cavallo L, Tramontano A. Nucleic Acids Res. 2006;34:865–879. PubMed PMC

Sharma P, Chawla M, Sharma S, Mitra A. RNA. 2010;16:942–957. PubMed PMC

Luisi B, Orozco M, Sponer J, Luque FJ, Shakked Z. J. Mol. Biol. 1998;279:1123–1136. PubMed

Vlieghe D, Sponer J, Van Meervelt L. Biochemistry. 1999;38:16443–16451. PubMed

Zirbel CL, Sponer JE, Sponer J, Stombaugh J, Leontis NB. Nucleic Acids Res. 2009;37:4898–4918. PubMed PMC

Sponer J, Kypr J. J. Biomol. Struct. Dyn. 1993;11:277–292. PubMed

Morgado CA, Jurecka P, Svozil D, Hobza P, Sponer J. J. Chem. Theory Comput. 2009;5:1524–1544. PubMed

Spackova N, Berger I, Egli M, Sponer J. J. Am. Chem. Soc. 1998;120:6147–6151.

Siegfried NA, Metzger SL, Bevilacqua PC. Biochemistry. 2007;46:172–181. PubMed

Siegfried NA, Kierzek R, Bevilacqua PC. J. Am. Chem. Soc. 2010;132:5342–5344. PubMed

Meneni SR, Shell SM, Gao L, Jurecka P, Lee W, Sponer J, Zou Y, Chiarelli MP, Cho BP. Biochemistry. 2007;46:11263–11278. PubMed

Devoe H, Tinoco I. J. Mol. Biol. 1962;4:500–517. PubMed

Kudritskaya ZG, Danilov VI. J. Theor. Biol. 1976;59:303–318. PubMed

Aida M. J. Theor. Biol. 1988;130:327–335. PubMed

Ninio J. Biochimie. 2006;88:963–992. PubMed

Blanchard SC, Kim HD, Gonzalez RL, Puglisi JD, Chu S. Proc. Natl. Acad. Sci. U. S. A. 2004;101:12893–12898. PubMed PMC

Frank J, Spahn CMT. Rep. Prog. Phys. 2006;69:1383–1417.

Spirin AS. FEBS Lett. 2002;514:2–10. PubMed

Prive GG, Heinemann U, Chandrasegaran S, Kan LS, Kopka ML, Dickerson RE. Science. 1987;238:498–504. PubMed

Ennifar E, Yusupov M, Walter P, Marquet R, Ehresmann B, Ehresmann C, Dumas P. Structure. 1999;7:1439–1449. PubMed

Wu M, Turner DH. Biochemistry. 1996;35:9677–9689. PubMed

Santalucia J, Turner DH. Biochemistry. 1993;32:12612–12623. PubMed

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