Use of a coenzyme by the glmS ribozymeriboswitch suggests primordial expansion of RNA chemistry by small molecules

Philosophical Transactions of the Royal Society B: Biological Sciences

Volumn 366, Issue 1580, 2011, Pages 2942-2948

  Ferré D'amaré, Adrian R ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

Catalytic RNA; Enzymatic cofactor; RNA world

Indexed keywords

AMINO ACID; BACTERIUM; CATALYST; CHEMICAL BINDING; ENZYME ACTIVITY;

BACTERIA (MICROORGANISMS);

BACTERIAL PROTEIN; COMPONENT S, GLUTAMATE MUTASE PROTEIN, BACTERIA; DRUG DERIVATIVE; GLUCOSAMINE; GLUCOSAMINE 6 PHOSPHATE; GLUCOSAMINE 6-PHOSPHATE; GLUCOSE 6 PHOSPHATE; GLUTAMINE FRUCTOSE 6 PHOSPHATE AMINOTRANSFERASE; RIBOZYME; RNA;

AMINOACYLATION; ARTICLE; BACTERIUM; BINDING SITE; CATALYSIS; CHEMISTRY; COENZYME; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME SPECIFICITY; GENETICS; RIBOSWITCH; RNA CLEAVAGE; RNA SPLICING;

ALLOSTERIC SITE; BACTERIA; BACTERIAL PROTEINS; CATALYSIS; CATALYTIC DOMAIN; COENZYMES; ENZYME ACTIVATION; GLUCOSAMINE; GLUCOSE-6-PHOSPHATE; GLUTAMINE-FRUCTOSE-6-PHOSPHATE TRANSAMINASE (ISOMERIZING); RIBOSWITCH; RNA; RNA CLEAVAGE; RNA SPLICING; RNA, CATALYTIC; SUBSTRATE SPECIFICITY; TRANSFER RNA AMINOACYLATION;

EID: 80052939924     PISSN: 09628436     EISSN: 14712970     Source Type: Journal    
DOI: 10.1098/rstb.2011.0131     Document Type: Review

References (54)

1. Ferré-D'Amaré, A. R. 2010 The glmS ribozyme: use of a small molecule coenzyme by a gene-regulatory RNA. Q. Rev. Biophys. 43, 423-447. (doi:10.1017/S0033583510000144)
2. Winkler, W. C., Nahvi, A., Roth, A., Collins, J. A. & Breaker, R. R. 2004 Control of gene expression by a natural metabolite-responsive ribozyme. Nature 428, 281-286. (doi:10.1038/nature02362)
3. Collins, J. A., Irnov, I., Baker, S. & Winkler, W. C. 2007 Mechanism of mRNA destabilization by the glmS ribozyme. Genes Dev. 21, 3356-3368. (doi:10.1101/gad.1605307)
4. Milewski, S. 2002 Glucosamine-6-phosphate synthase- the multi-facets enzyme. Biochem. Biophys. Acta 1597, 173-192. (doi:10.1016/S0167-4838(02)00318-7)
5. Klein, D. J. & Ferré-D'Amaré, A. R. 2006 Structural basis of glmS ribozyme activation by glucosamine-6-phosphate. Science 313, 1752-1756. (doi:10.1126/science.1129666)
6. Klein, D. J., Wilkinson, S. R., Been, M. D. & Ferré- D'Amaré, A. R. 2007 Requirement of helix P2.2 and nucleotide G1 for positioning of the cleavage site and cofactor of the glmS ribozyme. J. Mol. Biol. 373, 178-189. (doi:10.1016/j.jmb.2007.07.062)
7. Klein, D. J., Been, M. D. & Ferré-D'Amaré, A. R. 2007 Essential role of an active-site guanine in glmS ribozyme catalysis. J. Am. Chem. Soc. 129, 14858-14859. (doi:10.1021/ja0768441)
8. Cochrane, J. C., Lipchock, S. V. & Strobel, S. A. 2007 Structural investigation of the GlmS ribozyme bound to its catalytic cofactor. Chem. Biol. 14, 97-105. (doi:10.1016/j.chembiol.2006.12.005)
9. Cochrane, J. C., Lipchock, S. V., Smith, K. D. & Strobel, S. A. 2009 Structural and chemical basis for glucosamine 6-phosphate binding and activation of the glmS ribozyme. Biochemistry 48, 3239-3246. (doi:10.1021/ bi802069p)
10. Hampel, K. J. & Tinsley, M. M. 2006 Evidence for preorganization of the glmS ribozyme ligand binding pocket. Biochemistry 45, 7861-7871. (doi:10.1021/bi060337z)
11. Tinsley, R. A., Furchak, J. R. & Walter, N. G. 2007 Trans-acting glmS catalytic riboswitch: locked and loaded. RNA 13, 468-477. (doi:10.1261/rna.341807)
12. McCarthy, T. J., Plog, M. A., Floy, S. A., Jansen, J. A., Soukup, J. K. & Soukup, G. A. 2005 Ligand requirements for glmS ribozyme self-cleavage. Chem. Biol. 12, 1221-1226. (doi:10.1016/j.chembiol.2005.09.006)
13. Edwards, T. E., Klein, D. J. & Ferré-D'Amaré, A. R. 2007 Riboswitches: small-molecule recognition by gene regulatory RNAs. Curr. Opin. Struct. Biol. 17, 273-279. (doi:10.1016/j.sbi.2007.05.004)
14. Zhang, J., Lau, M. W. & Ferré-D'Amaré, A. R. 2010 Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 49, 9123-9131. (doi:10.1021/bi1012645)
15. Ellington, A. D. & Szostak, J. W. 1990 In vitro selection of RNA molecules that bind specific ligands. Nature 346, 818-822. (doi:10.1038/346818a0)
16. Wachter, A. 2010 Riboswitch-mediated control of gene expression in eukaryotes. RNA Biol. 7, 67-76. (doi:10.4161/rna.7.1.10489)
17. Lee, E. R., Baker, J. L., Weinberg, Z., Sudarsan, N. & Breaker, R. R. 2010 An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 329, 845-848. (doi:10.1126/science.1190713)
18. Loh, E. et al. 2009 A trans-acting riboswitch controls expression of the virulence regulator PrfA in Listeria monocytogenes. Cell 139, 770-779. (doi:10.1016/j.cell.2009.08.046)
19. Edwards, T. E. & Ferré-D'Amaré, A. R. 2006 Crystal structures of the thi-box riboswitch bound to thiamine pyrophosphate analogs reveal adaptive RNA-small molecule recognition. Structure 14, 1459-1468. (doi:10.1016/j.str.2006.07.008)
20. Lang, K., Rieder, R. & Micura, R. 2007 Ligand-induced folding of the thiM TPP riboswitch investigated by a structure-based fluorescence spectroscopic approach. Nucleic Acids Res. 35, 5370-5378. (doi:10.1093/nar/ gkm580)
21. Klein, D., Edwards, T. & Ferré-D'Amaré, A. 2009 Cocrystal structure of a class I preQ1 riboswitch reveals a pseudoknot recognizing an essential hypermodified nucleobase. Nat. Struct. Mol. Biol. 16, 343-344. (doi:10.1038/nsmb.1563)
22. Rieder, U., Kreutz, C. & Micura, R. 2010 Folding of a transcriptionally acting preQ1 riboswitch. Proc. Natl Acad. Sci. USA 107, 10804-10809. (doi:10.1073/pnas.0914925107)
23. Kulshina, N., Baird, N. J. & Ferré-D'Amaré, A. R. 2009 Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat Struct. Mol. Biol. 16, 1212-1217. (doi:10.1038/nsmb.1701)
24. Baird, N. J., Kulshina, N. & Ferré-D'Amaré, A. R. 2010 Riboswitch function: flipping the switch or tuning the dimmer? RNA Biol. 7, 328-332. (doi:10.4161/rna.7.3.11932)
25. Xiao, H., Edwards, T. E. & Ferré-D'Amaré, A. R. 2008 Structural basis for specific, high-affinity tetracycline binding by an in vitro evolved aptamer and artificial riboswitch. Chem. Biol. 15, 1125-1137. (doi:10.1016/j. chembiol.2008.09.004)
26. Ferré-D'Amaré, A. R. & Scott, W. G. 2010 Small selfcleaving ribozymes. Cold Spring Harb. Perspect. Biol. 2, a003574. (doi:10.1101/cshperspect.a003574)
27. Nakano, S., Cerrone, A. L. & Bevilacqua, P. C. 2003 Mechanistic characterization of the HDV genomic ribozyme: classifying the catalytic and structural metal ion sites within a multichannel reaction mechanism. Biochemistry 42, 2982-2994. (doi:10.1021/bi026815x)
28. Das, S. R. & Piccirilli, J. A. 2005 General acid catalysis by the hepatitis delta virus ribozyme. Nat. Chem. Biol. 1, 45-52. (doi:10.1038/nchembio703)
29. Bevilacqua, P. C. & Yajima, R. 2006 Nucleobase catalysis in ribozyme mechanism. Curr. Opin. Chem. Biol. 10, 455-464. (doi:10.1016/j.cbpa.2006.08.014)
30. Rupert, P. B. & Ferré-D'Amaré, A. R. 2001 Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 410, 780-786. (doi:10.1038/35071009)
31. Rupert, P. B., Massey, A. P., Sigurdsson, S. T. & Ferré- D'Amaré, A. R. 2002 Transition state stabilization by a catalytic RNA. Science 298, 1421-1424. (doi:10.1126/ science.1076093)
32. Guo, M., Spitale, R. C., Volpini, R., Krucinska, J., Cristalli, G., Carey, P. R. & Wedekind, J. E. 2009 Direct Raman measurement of an elevated base pKa in the active site of a small ribozyme in a precatalytic conformation. J. Am. Chem. Soc. 131, 12908-12909. (doi:10.1021/ja9060883)
33. A. R. 2004 The hairpin ribozyme. Biopolymers 73, 71-78. (doi:10.1002/bip.10516)
34. Martick, M. & Scott, W. G. 2006 Tertiary contacts distant from the active site prime a ribozyme for catalysis. Cell 126, 309-320. (doi:10.1016/j.cell.2006.06.036)
35. Bevilacqua, P. C. 2003 Mechanistic considerations for general acid-base catalysis by RNA: revisiting the mechanism of the hairpin ribozyme. Biochemistry 42, 2259-2265. (doi:10.1021/bi027273m)
36. Wilson, T. J., Li, N.-S., Lu, J., Frederiksen, J. K., Piccirilli, J. A. & Lilley, D. M. J. 2010 Nucleobase-mediated general acid-base catalysis in the Varkud satellite ribozyme. Proc. Natl Acad. Sci. USA 107, 11 751-11 756. (doi:10.1073/pnas.1004255107)
37. Ferré-D'Amaré, A. R., Zhou, K. & Doudna, J. A. 1998 Crystal structure of a hepatitis delta virus ribozyme. Nature 395, 567-574. (doi:10.1038/26912)
38. Banás, P., Walter, N. G., Sponer, J. & Otyepka, M. 2010 Protonation states of the key active site residues and structural dynamics of the glmS riboswitch as revealed by molecular dynamics. J. Phys. Chem. B 114, 8701-8712. (doi:10.1021/jp9109699)
39. Xin, Y. & Hamelberg, D. 2010 Deciphering the role of glucosamine-6-phosphate in the riboswitch action of glmS ribozyme. RNA 16, 2455-2463. (doi:10.1261/ rna.2334110)
40. Wilson, D. S. & Szostak, J. W. 1999 In vitro selection of functional nucleic acids. Annu. Rev. Biochem. 68, 611-647. (doi:10.1146/annurev.biochem.68.1.611)
41. Chen, X., Li, N. & Ellington, A. D. 2007 Ribozyme catalysis of metabolism in the RNA world. Chem. Biodivers. 4, 633-655. (doi:10.1002/cbdv.200790055)
42. Meli, M., Vergne, J. & Maurel, M.-C. 2003 In vitro selection of adenine-dependent hairpin ribozymes. J. Biol. Chem. 278, 9835-9842. (doi:10.1074/jbc.M213058200)
43. Tsukiji, S., Pattnaik, S. B. & Suga, H. 2003 An alcohol dehydrogenase ribozyme. Nat. Struct. Biol. 10, 713-717. (doi:10.1038/nsb964)
44. White, H. B. 1976 Coenzymes as fossils of an earlier metabolic state. J. Mol. Evol. 7, 101-104. (doi:10.1007/BF01732468)
45. A. R. 2003 RNA-modifying enzymes. Curr. Opin. Struct. Biol. 13, 49-55. (doi:10.1016/ S0959-440X(02)00002-7)
46. Hoang, C., Chen, J., Vizthum, C. A., Kandel, J. M., Hamilton, C. S., Mueller, E. G. & Ferré-D'Amaré, A. R. 2006 Crystal structure of pseudouridine synthase RluA: indirect sequence readout through proteininduced RNA structure. Mol. Cell 24, 535-545. (doi:10.1016/j.molcel.2006.09.017)
47. Noller, H. F. 2010 Evolution of protein synthesis from an RNA world. Cold Spring Harb. Perspect. Biol. 2, a003681. (doi:10.1101/cshperspect.a003681)
48. Koizumi, M., Soukup, G. A., Kerr, J. N. & Breaker, R. R. 1999 Allosteric selection of ribozymes that respond to the second messengers cGMP and cAMP. Nat. Struct. Biol. 6, 1062-1071. (doi:10.1038/14947)
49. Benner, S. A., Kim, H.-J. & Yang, Z. 2010 Setting the stage: the history, chemistry, and geobiology behind RNA. Cold Spring Harb. Perspect. Biol. 2, a003541. (doi:10.1101/cshperspect.a003541)
50. Orgel, L. E. 1968 Evolution of the genetic apparatus. J. Mol. Biol. 38, 381-393. (doi:10.1016/0022-2836(68)90393-8)
51. White, H. B. I. 1982 Evolution of coenzymes and the origin of pyridine nucleotides. In The pyridine nucleotide coenzymes (eds J. Everse, B. Anderson & K.-S. You), pp. 1-17. New York: Academic Press.
52. Maizels, N. & Weiner, A. M. 1993 The genomic tag hypothesis: modern viruses as molecular fossils of ancient strategies for genome replication. In The RNA world (eds R. F. Gesteland & J. F. Atkins), pp. 577-602. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
53. Wong, J. T. 1991 Origin of genetically encoded protein synthesis: a model based on selection for RNA peptidation. Orig. Life Evol. Biosph. 21, 165-176. (doi:10.1007/BF01809445)
54. Xiao, H., Murakami, H., Suga, H. & Ferré-D'Amaré, A. R. 2008 Structural basis of specific tRNA aminoacylation by a small in vitro selected ribozyme. Nature 454, 358-361. (doi:10.1038/nature07033)