Role of tautomerism in RNA biochemistry

RNA

Volumn 21, Issue 1, 2015, Pages 1-13

  Singh, Vipender ^a,b   Fedeles, Bogdan I ^a,b   Essigmann, John M ^a,b  

^a Department of Chemistry ^*  (United States)

^b Massachusetts Institute of Technology Cambridge   (United States)

Author keywords

Riboswitches; Ribozymes; RNA; Tautomerism

Indexed keywords

NUCLEIC ACID; NUCLEIC ACID BASE; RIBOZYME; RNA; APTAMER; RIBOSWITCH;

BIOCHEMISTRY; CATALYSIS; DNA REPLICATION; HUMAN; MOLECULAR RECOGNITION; REVIEW; RIBOSWITCH; TAUTOMER; BINDING SITE; BIOCATALYSIS; CHEMICAL STRUCTURE; CHEMISTRY; ISOMERISM; OXIDATION REDUCTION REACTION;

APTAMERS, NUCLEOTIDE; BINDING SITES; BIOCATALYSIS; ISOMERISM; MODELS, MOLECULAR; OXIDATION-REDUCTION; RIBOSWITCH; RNA; RNA, CATALYTIC;

EID: 84920512700     PISSN: 13558382     EISSN: 14699001     Source Type: Journal    
DOI: 10.1261/rna.048371.114     Document Type: Review

References (106)

1. Alkorta I, Elguero J, Liebman JF. 2006. The annular tautomerism of imidazoles and pyrazoles: the possible existence of nonaromatic forms. Struct Chem 17: 439-444.
2. Antonov L. 2014. Tautomerism-methods and theories. Wiley, New York.
3. Baker JW, Ingold CK, Thorpe JF. 1924. XXXVI. -Ring-chain tautomerism. Part IX. The mutarotation of the sugars. J Chem Soc Trans 125: 268-291.
4. Bakker JM, Compagnon I, Meijer G, von Helden G,Kabeláč M, Hobza P, de Vries MS. 2004. The mid-IR absorption spectrum of gas-phase clusters of the nucleobases guanine and cytosine. Phys Chem Chem Phys 6: 2810-2815.
5. Batey RT, Gilbert SD, Montange RK. 2004. Structure of a natural gua-nine- responsive riboswitch complexed with the metabolite hypoxanthine. Nature 432: 411-415.
6. Bebenek K, Pedersen LC, Kunkel TA. 2011. Replication infidelity via a mismatch with Watson-Crick geometry. Proc Natl Acad Sci 108: 1862-1867.
7. Bensaude O, Dreyfus M, Dodin G, Dubois JE. 1977. Intramolecular nondissociative proton transfer in aqueous solutions of tautomeric heterocycles: a temperature-jump kinetic study. J Am Chem Soc 99: 4438-4446.
8. Bevilacqua PC, Yajima R. 2006. Nucleobase catalysis in ribozyme mechanism. Curr Opin Chem Biol 10: 455-464.
9. Bevilacqua PC, Brown TS, Nakano S, Yajima R. 2004. Catalytic roles for proton transfer and protonation in ribozymes. Biopolymers 73: 90-109.
10. Björk GR, Durand JMB, Hagervall TG, Leipuviene R, Lundgren HK, Nilsson K, Chen P, Qian Q, Urbonavičius J. 1999. Transfer RNA modification: influence on translational frameshifting and metabolism. FEBS Lett 452: 47-51.
11. Breaker RR. 2011. Prospects for riboswitch discovery and analysis. Mol Cell 43: 867-879.
12. Brown RD, Godfrey PD, McNaughton D, Pierlot AP. 1989. Tautomers of cytosine by microwave spectroscopy. JAmChem Soc 111: 2308-2310.
13. Chi YI, Martick M, Lares M, Kim R, Scott WG, Kim SH. 2008. Capturing hammerhead ribozyme structures in action by modulating general base catalysis. PLoS Biol 6: e234.
14. Cochrane JC, Strobel SA. 2008a. Catalytic strategies of self-cleaving ribozymes. Acc Chem Res 41: 1027-1035.
15. Cochrane JC, Strobel SA. 2008b. Riboswitch effectors as protein enzyme cofactors. RNA 14: 993-1002.
16. Cochrane JC, Lipchock SV, Strobel SA. 2007. Structural investigation of the GlmS ribozyme bound to its catalytic cofactor. Chem Biol 14: 97-105.
17. Collins JA, Irnov I, Baker S, Winkler WC. 2007. Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev 21: 3356-3368.
18. Colominas C, Luque FJ, Orozco M. 1996. Tautomerism and protonation of guanine and cytosine. Implications in the formation of hy-drogen- bonded complexes. J Am Chem Soc 118: 6811-6821.
19. Czerwoniec A,Dunin-HorkawiczS, Purta E,KaminskaKH,KasprzakJM, Bujnicki JM, Grosjean H, Rother K. 2009.MODOMICS:a database of RNA modification pathways. 2008 update. Nucleic Acids Res 37: D118-D121.
20. Das SR, Piccirilli JA. 2005. General acid catalysis by the hepatitis ä virus ribozyme. Nat Chem Biol 1: 45-52.
21. Davis JH, Dunican BF, Strobel SA. 2011. glmS Riboswitch binding to the glucosamine-6-phosphate α-anomer shifts the pKa toward neutrality. Biochemistry 50: 7236-7242.
22. Demeshkina N, Jenner L, Westhof E, Yusupov M, Yusupova G. 2012. A new understanding of the decoding principle on the ribosome. Nature 484: 256-259.
23. Donghi D, Schnabl J. 2011. Multiple roles of metal ions in large ribozymes. Met Ions Life Sci 9: 197-234.
24. Fedor MJ. 2000. Structure and function of the hairpin ribozyme. J Mol Biol 297: 269-291.
25. Ferre-D'Amare AR, Scott WG. 2010. Small self-cleaving ribozymes. Cold Spring Harb Perspect Biol 2: a003574.
26. Gilbert W. 1986. Origin of life: the RNA world. Nature 319: 618.
27. Gilbert SD, Mediatore SJ, Batey RT. 2006a. Modified pyrimidines specifically bind the purine riboswitch. J Am Chem Soc 128: 14214-14215.
28. Gilbert SD, Stoddard CD, Wise SJ, Batey RT. 2006b. Thermodynamic and kinetic characterization of ligand binding to the purine riboswitch aptamer domain. J Mol Biol 359: 754-768.
29. Gilbert SD, Reyes FE, Edwards AL, Batey RT. 2009. Adaptive ligand binding by the purine riboswitch in the recognition of guanine and adenine analogs. Structure 17: 857-868.
30. Gong B, Chen JH, Chase E, Chadalavada DM, Yajima R, Golden BL, Bevilacqua PC, Carey PR. 2007. Direct measurement of a pKa near neutrality for the catalytic cytosine in the genomic HDV ribozyme using Raman crystallography. J Am Chem Soc 129: 13335-13342.
31. Gong B, Chen JH, Yajima R, Chen Y, Chase E, Chadalavada DM, Golden BL, Carey PR, Bevilacqua PC. 2009. Raman crystallography of RNA. Methods 49: 101-111.
32. Gong B, Klein DJ, Ferré-D'Amaré AR, Carey PR. 2011. The glmS ribozyme tunes the catalytically critical pKa of its coenzyme glucos-amine- 6-phosphate. J Am Chem Soc 133: 14188-14191.
33. Griffiths AJ. 1995. Natural plasmids of filamentous fungi. Microbiol Rev 59: 673-685.
34. Hamm P, Zanni M. 2011. Concepts and methods of 2D infrared spectroscopy,1st ed. Cambridge University Press, Cambridge, New York, UK, New York.
35. Hammann C, Luptak A, Perreault J, de la Peña M. 2012. The ubiquitous hammerhead ribozyme. RNA 18: 871-885.
36. Han J, Burke JM. 2005. Model for general acid-base catalysis by the hammerhead ribozyme: pH-activity relationships of G8 and G12 variants at the putative active site. Biochemistry 44: 7864-7870.
37. Hiley SL, Sood VD, Fan J, Collins RA. 2002. 4-Thio-U cross-linking identifies the active site of the VS ribozyme. EMBO J 21: 4691-4698.
38. Hiller DA, Strobel SA. 2011. The chemical versatility of RNA. Philos Trans R Soc Lond B Biol Sci 366: 2929-2935.
39. Huang F, Bugg CW, Yarus M. 2000. RNA-catalyzed CoA, NAD, and FAD synthesis from phosphopantetheine, NMN, and FMN. Biochemistry 39: 15548-15555.
40. Jaworski A. 1990. Infrared spectra and tautomerism of 5-fluorocytosine, 5-bromocytosine and 5-iodocytosine. Matrix isolation and theoretical AB initio studies. J Mol Struct 223: 63-92.
41. Jones PR. 1963. Ring-chain tautomerism. Chem Rev 63: 461-487.
42. Jones FD, Strobel SA. 2003. Ionization of a critical adenosine residue in the Neurospora Varkud Satellite ribozyme active site. Biochemistry 42: 4265-4276.
43. Klein DJ, Ferré-D'Amaré AR. 2006. Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313: 1752-1756.
44. Klein DJ, Been MD, Ferré-D'Amaré AR. 2007. Essential role of an ac-tive- site guanine in glmS ribozyme catalysis. J Am Chem Soc 129: 14858-14859.
45. Kühne RO, Schaffhauser T, Wokaun A, Ernst RR. 1979. Study of transient chemical reactions by NMR. Fast stopped-flow Fourier transform experiments. J Magn Reson 1969 35: 39-67.
46. Kuzmin YI, Da Costa CP, Fedor MJ. 2004. Role of an active site guanine in hairpin ribozyme catalysis probed by exogenous nucleobase rescue. J Mol Biol 340: 233-251.
47. Laar C. 1886. Ueber die Hypothese der wechselnden Bindung. Ber Dtsch Chem Ges 19: 730-741.
48. Lafontaine DA, Wilson TJ, Norman DG, Lilley DM. 2001. The A730 loop is an important component of the active site of the VS ribozyme. J Mol Biol 312: 663-674.
49. Lafontaine DA, Wilson TJ, Zhao ZY, Lilley DMJ. 2002. Functional group requirements in the probable active site of the VS ribozyme. J Mol Biol 323: 23-34.
50. Legault P, Pardi A. 1997. Unusual dynamics and pKa shift at the active site of a lead-dependent ribozyme. J Am Chem Soc 119: 6621-6628.
51. Li D, Fedeles BI, Singh V, Peng CS, Silvestre KJ, Simi A, Simpson J, Tokmakoff A, Essigmann JM. 2014. Tautomerism provides a molecular explanation for the mutagenic properties of the anti-HIV nucleoside 5-aza-5,6-dihydro-2? -deoxycytidine. Proc Natl Acad Sci 111: E3252-E3259.
52. Lilley DMJ. 2004. The Varkud satellite ribozyme. RNA 10: 151-158.
53. Lippert B, Gupta D. 2009. Promotion of rare nucleobase tautomers by metal binding. Dalton Trans 4619-4634.
54. Mandal M, Breaker RR. 2004. Adenine riboswitches and gene activation by disruption of a transcription terminator. Nat Struct Mol Biol 11: 29-35.
55. Mandal M, Boese B, Barrick JE, Winkler WC, Breaker RR. 2003. Riboswitches control fundamental biochemical pathways in Bacillus subtilis and other bacteria. Cell 113: 577-586.
56. Martick M, Scott WG. 2006. Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126: 309-320.
57. Mata S, Cortijo V, CaminatiW, Alonso JL, Sanz ME, López JC, Blanco S. 2010. Tautomerism and microsolvation in 2-hydroxypyridine/2- pyridone. J Phys Chem A 114: 11393-11398.
58. McCarthy TJ, Plog MA, Floy SA, Jansen JA, Soukup JK, Soukup GA. 2005. Ligand requirements for glmS ribozyme self-cleavage. Chem Biol 12: 1221-1226.
59. McCown PJ, Winkler WC, Breaker RR. 2012. Mechanism and distribution of glmS ribozymes. Methods Mol Biol 848: 113-129.
60. McKay DB. 1996. Structure and function of the hammerhead ribozyme: an unfinished story. RNA 2: 395-403.
61. Milewski S. 2002. Glucosamine-6-phosphate synthase-the multi-facets enzyme. Biochim Biophys Acta 1597: 173-192.
62. Minkin VI, Garnovskii AD, Elguero J, Katritzky AR, Denisko OV. 2000.The tautomerism of heterocycles: five-membered rings with two or more heteroatoms. Adv Heterocycl Chem 76: 157-323.
63. Mons M, Dimicoli I, Piuzzi F, Tardivel B, Elhanine M. 2002.Tautomerism of the DNA base guanine and its methylated derivatives as studied by gas-phase infrared and ultraviolet spectroscopy. J Phys Chem A 106: 5088-5094.
64. Moreno M, Miller WH. 1990. On the tautomerization reaction 2-pyridone Equilibrium 2-hydroxypyridine: an ab initio study. Chem Phys Lett 171: 475-479.
65. Nakano S, Chadalavada DM, Bevilacqua PC. 2000. General acid-base catalysis in the mechanism of a hepatitis ä virus ribozyme. Science 287: 1493-1497.
66. Nir E, Plützer C, Kleinermanns K, de Vries M. 2002. Properties of isolated DNA bases, base pairs and nucleosides examined by laser spectroscopy. Eur Phys J D 20: 317-329.
67. Nissen P, Hansen J, Ban N, Moore PB, Steitz TA. 2000. The structural basis of ribosome activity in peptide bond synthesis. Science 289: 920-930.
68. Peng CS, Tokmakoff A. 2012. Identification of lactam-lactim tautomers of aromatic heterocycles in aqueous solution using 2D IR spectroscopy. J Phys Chem Lett 3: 3302-3306.
69. Peng CS, Jones KC, Tokmakoff A. 2011. Anharmonic vibrational modes of nucleic acid bases revealed by 2D IR spectroscopy. J Am Chem Soc 133: 15650-15660.
70. Peng CS, Baiz CR, Tokmakoff A. 2013. Direct observation of groundstate lactam-lactim tautomerization using temperature-jump transient R spectroscopy. Proc Natl Acad Sci 110: 9243-9248.
71. Perrotta AT, Wadkins TS, Been MD. 2006. Chemical rescue, multiple ionizable groups, and general acid-base catalysis in the HDV genomic ribozyme. RNA 12: 1282-1291.
72. Pinard R, Hampel KJ, Heckman JE, Lambert D, Chan PA, Major F, Burke JM. 2001. Functional involvement of G8 in the hairpin ribozyme cleavage mechanism. EMBO J 20: 6434-6442.
73. Prudent JR, Uno T, Schultz PG. 1994. Expanding the scope of RNA catalysis. Science 264: 1924-1927.
74. Ravindranathan S, Butcher SE, Feigon J. 2000. Adenine protonation in domain B of the hairpin ribozyme. Biochemistry 39: 16026-16032.
75. Roth A, Breaker RR. 2009. The structural and functional diversity of me-tabolite- binding riboswitches. Annu Rev Biochem 78: 305-334.
76. Ruffner DE, Stormo GD, Uhlenbeck OC. 1990. Sequence requirements of the hammerhead RNA self-cleavage reaction. Biochemistry 29: 10695-10702.
77. Rupert PB, Ferré-D'Amaré AR. 2001. Crystal structure of a hairpin ribo-zyme- inhibitor complex with implications for catalysis. Nature 410: 780-786.
78. Sato O, Cui A, Matsuda R, Tao J, Hayami S. 2007. Photo-induced valence tautomerism in Co complexes. Acc Chem Res 40: 361-369.
79. Saville BJ, Collins RA. 1990. A site-specific self-cleavage reaction performed by a novel RNA in Neurospora mitochondria. Cell 61: 685-696.
80. Sayle RA. 2010. So you think you understand tautomerism? J Comput Aided Mol Des 24: 485-496.
81. Schramm VL. 2007. Binding isotope effects: boon and bane. Curr Opin Chem Biol 11: 529-536.
82. Seelig B, Jäschke A. 1999. A small catalytic RNA motif with Diels- Alderase activity. Chem Biol 6: 167-176.
83. Serganov A, Yuan YR, Pikovskaya O, Polonskaia A, Malinina L, Phan AT, Hobartner C, Micura R, Breaker RR, Patel DJ. 2004. Structural basis for discriminative regulation of gene expression by adenine- and guanine-sensing mRNAs. Chem Biol 11: 1729-1741.
84. Shugar D, Kierdaszuk B. 1985. New light on tautomerism of purines and pyrimidines and its biological and genetic implications. J Biosci 8: 657-668.
85. Singh V, Peng CS, Li D, Mitra K, Silvestre KJ, Tokmakoff A, Essigmann JM. 2014. Direct observation of multiple tautomers of oxythiamine and their recognition by the thiamine pyrophosphate riboswitch. ACS Chem Biol 9: 227-236.
86. Sood VD, Collins RA. 2002. Identification of the catalytic subdomain of the VS ribozyme and evidence for remarkable sequence tolerance in the active site loop. J Mol Biol 320: 443-454.
87. Su D, Chan CTY, Gu C, Lim KS, Chionh YH, McBee ME, Russell BS, Babu IR, Begley TJ, Dedon PC. 2014. Quantitative analysis of ribonucleoside modifications in tRNA by HPLC-coupled mass spectrometry. Nat Protoc 9: 828-841.
88. Sudarsan N, Wickiser JK, Nakamura S, Ebert MS, Breaker RR. 2003. An mRNA structure in bacteria that controls gene expression by binding lysine. Genes Dev 17: 2688-2697.
89. Suydam IT, Strobel SA. 2008. Fluorine substituted adenosines as probes of nucleobase protonation in functional RNAs. J Am Chem Soc 130: 13639-13648.
90. Thomas JM, Perrin DM. 2008. Probing general base catalysis in the hammerhead ribozyme. J Am Chem Soc 130: 15467-15475.
91. Thore S, Leibundgut M, Ban N. 2006. Structure of the eukaryotic thiamine pyrophosphate riboswitch with its regulatory ligand. Science 312: 1208-1211.
92. Thore S, Frick C, Ban N. 2008. Structural basis of thiamine pyrophosphate analogues binding to the eukaryotic riboswitch. J Am Chem Soc 130: 8116-8117.
93. Topal MD, Fresco JR. 1976. Complementary base pairing and the origin of substitution mutations. Nature 263: 285-289.
94. Tsukiji S, Pattnaik SB, Suga H. 2003. An alcohol dehydrogenase ribozyme. Nat Struct Mol Biol 10: 713-717.
95. Velikyan I, Acharya S, Trifonova A, Földesi A, Chattopadhyaya J. 2001.
96. The pKa's of 2'-hydroxyl group in nucleosides and nucleotides. J Am Chem Soc 123: 2893-2894.
97. Viladoms J, Fedor MJ. 2012. The glmS ribozyme cofactor is a general acid-base catalyst. J Am Chem Soc 134: 19043-19049.
98. Viladoms J, Scott LG, Fedor MJ. 2011. An active-site guanine participates in glmS ribozyme catalysis in its protonated state. J Am Chem Soc 133: 18388-18396.
99. Wang W, Hellinga HW, Beese LS. 2011. Structural evidence for the rare tautomer hypothesis of spontaneous mutagenesis. Proc Natl Acad Sci 108: 17644-17648.
100. Watson JD, Crick FH. 1953. Genetical implications of the structure of deoxyribonucleic acid. Nature 171: 964-967.
101. Wilcox JL, Bevilacqua PC. 2013. A simple fluorescence method for pKa determination in RNA and DNA reveals highly shifted pKa's. J Am Chem Soc 135: 7390-7393.
102. Wilcox JL, Ahluwalia AK, Bevilacqua PC. 2011. Charged nucleobases and their potential for RNA catalysis. Acc Chem Res 44: 1270-1279.
103. Winkler WC, Cohen-Chalamish S, Breaker RR. 2002a. An mRNA structure that controls gene expression by binding FMN. Proc Natl Acad Sci 99: 15908-15913.
104. Winkler W, Nahvi A, Breaker RR. 2002b. Thiamine derivatives bind messenger RNAs directly to regulate bacterial gene expression. Nature 419: 952-956.
105. Winkler WC, Nahvi A, Sudarsan N, Barrick JE, Breaker RR. 2003. An mRNA structure that controls gene expression by binding S-adenosylmethionine. Nat Struct Biol 10: 701-707.
106. Winkler WC, Nahvi A, Roth A, Collins JA, Breaker RR. 2004. Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428: 281-286.