RNA quaternary structure and global symmetry

Trends in Biochemical Sciences

Volumn 40, Issue 4, 2015, Pages 211-220

  Jones, Christopher P ^a   Ferré D'Amaré, Adrian R ^a  

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

Author keywords

Bacteriophage 29 pRNA; C di AMP riboswitch; Cooperativity; FMN riboswitch; Glycine riboswitch; X ray crystallography

Indexed keywords

CYCLIC AMP; FLAVINE MONONUCLEOTIDE; GLYCINE; PROHEAD RNA; RNA; UNCLASSIFIED DRUG; RIBOSWITCH;

BACTERIOPHAGE; BASE PAIRING; BETA TURN; CHIRALITY; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DIMERIZATION; FUSOBACTERIUM NUCLEATUM; LIGAND BINDING; MOLECULAR EVOLUTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN MOTIF; PROTEIN QUATERNARY STRUCTURE; PROTEIN RNA BINDING; REVIEW; RIBOSWITCH; RNA STABILITY; RNA STRUCTURE; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CONFORMATION; HUMAN;

ANIMALS; HUMANS; MODELS, BIOLOGICAL; NUCLEIC ACID CONFORMATION; RIBOSWITCH; RNA;

EID: 84925302778     PISSN: 09680004     EISSN: 13624326     Source Type: Journal    
DOI: 10.1016/j.tibs.2015.02.004     Document Type: Review

References (91)

1. Goodsell D.S., Olson A.J. Structural symmetry and protein function. Annu. Rev. Biophys. Biomol. Struct. 2000, 29:105-153.
2. Watson J.D., Crick F.H. Molecular structure of nucleic acids; a structure for deoxyribose nucleic acid. Nature 1953, 171:737-738.
3. Robertus J.D., et al. Structure of yeast phenylalanine tRNA at 3Å resolution. Nature 1974, 250:546-551.
4. Cate J.H., et al. Crystal structure of a group I ribozyme domain: principles of RNA packing. Science 1996, 273:1678-1685.
5. Ferré-D'Amaré A.R., et al. Crystal structure of a hepatitis delta virus ribozyme. Nature 1998, 395:567-574.
6. Rupert P.B., Ferré-D'Amaré A.R. Crystal structure of a hairpin ribozyme-inhibitor complex with implications for catalysis. Nature 2001, 410:780-786.
7. Pley H.W., et al. Three-dimensional structure of a hammerhead ribozyme. Nature 1994, 372:68-74.
8. Ban N., et al. The complete atomic structure of the large ribosomal subunit at 2.4Å resolution. Science 2000, 289:905-920.
9. Schluenzen F., et al. Structure of functionally activated small ribosomal subunit at 3.3 ångströms resolution. Cell 2000, 102:615-623.
10. Yusupov M.M., et al. Crystal structure of the ribosome at 5.5Å resolution. Science 2001, 292:883-896.
11. Wimberly B.T., et al. Structure of the 30S ribosomal subunit. Nature 2000, 407:327-339.
12. Bashan A., et al. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell 2003, 11:91-102.
13. Mujeeb A., et al. Structure of the dimer initiation complex of HIV-1 genomic RNA. Nat. Struct. Biol. 1998, 5:432-436.
14. Marino J.P., et al. Bent helix formation between RNA hairpins with complementary loops. Science 1995, 268:1448-1454.
15. Guo P., et al. Inter-RNA interaction of phage phi29 pRNA to form a hexameric complex for viral DNA transportation. Mol. Cell 1998, 2:149-155.
16. Neidle S., Balasubramanian S. Quadruplex Nucleic Acids 2006, RSC.
17. Grabow W.W., et al. The right angle (RA) motif: a prevalent ribosomal RNA structural pattern found in group I introns. J. Mol. Biol. 2012, 424:54-67.
18. Chworos A., et al. Building programmable jigsaw puzzles with RNA. Science 2004, 306:2068-2072.
19. Geary C., et al. RNA nanostructures. A single-stranded architecture for cotranscriptional folding of RNA nanostructures. Science 2014, 345:799-804.
20. Moore M.D., Hu W.S. HIV-1 RNA dimerization: it takes two to tango. AIDS Rev. 2009, 11:91-102.
21. Ennifar E., et al. Crystal structures of coaxially stacked kissing complexes of the HIV-1 RNA dimerization initiation site. Nat. Struct. Biol. 2001, 8:1064-1068.
22. Simpson A.A., et al. Structure of the bacteriophage ϕ29 DNA packaging motor. Nature 2000, 408:745-750.
23. Guo P.X., et al. A small viral RNA is required for in vitro packaging of bacteriophage phi 29 DNA. Science 1987, 236:690-694.
24. Ding F., et al. Structure and assembly of the essential RNA ring component of a viral DNA packaging motor. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7357-7362.
25. Zhang J., et al. Ribozymes and riboswitches: modulation of RNA function by small molecules. Biochemistry 2010, 49:9123-9131.
26. Serganov A. The long and the short of riboswitches. Curr. Opin. Struct. Biol. 2009, 19:251-259.
27. Breaker R.R. Riboswitches and the RNA world. Cold Spring Harb. Perspect. Biol. 2012, 4:a003566.
28. Dann C.E., et al. Structure and mechanism of a metal-sensing regulatory RNA. Cell 2007, 130:878-892.
29. Winkler W.C., et al. An mRNA structure that controls gene expression by binding FMN. Proc. Natl. Acad. Sci. U.S.A. 2002, 99:15908-15913.
30. Mandal M., et al. A glycine-dependent riboswitch that uses cooperative binding to control gene expression. Science 2004, 306:275-279.
31. Baker J.L., et al. Widespread genetic switches and toxicity resistance proteins for fluoride. Science 2012, 335:233-235.
32. Grundy F.J., Henkin T.M. tRNA as a positive regulator of transcription antitermination in B. subtilis. Cell 1993, 74:475-482.
33. Mironov A.S., et al. Sensing small molecules by nascent RNA: a mechanism to control transcription in bacteria. Cell 2002, 111:747-756.
34. Ren A., Patel D.J. c-di-AMP binds the ydaO riboswitch in two pseudo-symmetry-related pockets. Nat. Chem. Biol. 2014, 10:780-786.
35. Gao A., Serganov A. Structural insights into recognition of c-di-AMP by the ydaO riboswitch. Nat. Chem. Biol. 2014, 10:787-792.
36. Jones C.P., Ferré-D'Amaré A.R. Crystal structure of a c-di-AMP riboswitch reveals an internally pseudo-dimeric RNA. EMBO J. 2014, 33:2692-2703.
37. Serganov A., et al. Coenzyme recognition and gene regulation by a flavin mononucleotide riboswitch. Nature 2009, 458:233-237.
38. Butler E.B., et al. Structural basis of cooperative ligand binding by the glycine riboswitch. Chem. Biol. 2011, 18:293-298.
39. Huang L., et al. Structural insights into ligand recognition by a sensing domain of the cooperative glycine riboswitch. Mol. Cell 2010, 40:774-786.
40. Bloomfield V.A., et al. Nucleic Acids: Structures, Properties, and Functions 2000, University Science Books.
41. Janin J., Chothia C. The structure of protein-protein recognition sites. J. Biol. Chem. 1990, 265:16027-16030.
42. Levy E.D., Teichmann S. Structural, evolutionary, and assembly principles of protein oligomerization. Prog. Mol. Biol. Transl. Sci. 2013, 117:25-51.
43. Vitreschak A.G., et al. Regulation of riboflavin biosynthesis and transport genes in bacteria by transcriptional and translational attenuation. Nucleic Acids Res. 2002, 30:3141-3151.
44. Deigan K.E., Ferré-D'Amaré A.R. Riboswitches: discovery of drugs that target bacterial gene-regulatory RNAs. Acc. Chem. Res. 2011, 44:1329-1338.
45. Ott E., et al. The RFN riboswitch of Bacillus subtilis is a target for the antibiotic roseoflavin produced by Streptomyces davawensis. RNA Biol. 2009, 6:276-280.
46. Lee E.R., et al. Roseoflavin is a natural antibacterial compound that binds to FMN riboswitches and regulates gene expression. RNA Biol. 2009, 6:187-194.
47. Chan C.W., et al. Structure and function of the T-loop structural motif in noncoding RNAs. Wiley Interdiscip. Rev. RNA 2013, 4:507-522.
48. Zhang J., Ferré-D'Amaré A.R. Co-crystal structure of a T-box riboswitch stem I domain in complex with its cognate tRNA. Nature 2013, 500:363-366.
49. Jaeger L., et al. The UA_handle: a versatile submotif in stable RNA architectures. Nucleic Acids Res. 2009, 37:215-230.
50. Ellington A.D., Szostak J.W. In vitro selection of RNA molecules that bind specific ligands. Nature 1990, 346:818-822.
51. Sudarsan N., et al. Thiamine pyrophosphate riboswitches are targets for the antimicrobial compound pyrithiamine. Chem. Biol. 2005, 12:1325-1335.
52. Sudarsan N., et al. Tandem riboswitch architectures exhibit complex gene control functions. Science 2006, 314:300-304.
53. Ames T.D., Breaker R.R. Bacterial aptamers that selectively bind glutamine. RNA Biol. 2011, 8:82-89.
54. Trausch J.J., et al. The structure of a tetrahydrofolate-sensing riboswitch reveals two ligand binding sites in a single aptamer. Structure 2011, 19:1413-1423.
55. Nissen P., et al. RNA tertiary interactions in the large ribosomal subunit: the A-minor motif. Proc. Natl. Acad. Sci. U.S.A. 2001, 98:4899-4903.
56. Ruff K.M., Strobel S.A. Ligand binding by the tandem glycine riboswitch depends on aptamer dimerization but not double ligand occupancy. RNA 2014, 20:1775-1788.
57. Corrigan R.M., Grundling A. Cyclic di-AMP: another second messenger enters the fray. Nat. Rev. Microbiol. 2013, 11:513-524.
58. Nelson J.W., et al. Riboswitches in eubacteria sense the second messenger c-di-AMP. Nat. Chem. Biol. 2013, 9:834-839.
59. Block K.F., et al. Evidence for widespread gene control function by the ydaO riboswitch candidate. J. Bacteriol. 2010, 192:3983-3989.
60. Ferré-D'Amaré A.R., et al. A general module for RNA crystallization. J. Mol. Biol. 1998, 279:621-631.
61. Hendrix R.W. Symmetry mismatch and DNA packaging in large bacteriophages. Proc. Natl. Acad. Sci. U.S.A. 1978, 75:4779-4783.
62. Monod J., et al. On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 1965, 12:88-118.
63. Wolynes P.G. Symmetry and the energy landscapes of biomolecules. Proc. Natl. Acad. Sci. U.S.A. 1996, 93:14249-14255.
64. Baird N.J., Ferré-D'Amaré A.R. Idiosyncratically tuned switching behavior of riboswitch aptamer domains revealed by comparative small-angle X-ray scattering analysis. RNA 2010, 16:598-609.
65. Baird N.J., Ferré-D'Amaré A.R. Modulation of quaternary structure and enhancement of ligand binding by the K-turn of tandem glycine riboswitches. RNA 2013, 19:167-176.
66. Klein D.J., et al. The kink-turn: a new RNA secondary structure motif. EMBO J. 2001, 20:4214-4221.
67. Kladwang W., et al. Automated RNA structure prediction uncovers a kink-turn linker in double glycine riboswitches. J. Am. Chem. Soc. 2012, 134:1404-1407.
68. Sherman E.M., et al. An energetically beneficial leader-linker interaction abolishes ligand-binding cooperativity in glycine riboswitches. RNA 2012, 18:496-507.
69. Oppenheimer-Shaanan Y., et al. c-di-AMP reports DNA integrity during sporulation in Bacillus subtilis. EMBO Rep. 2011, 12:594-601.
70. Corrigan R.M., et al. Systematic identification of conserved bacterial c-di-AMP receptor proteins. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:9084-9089.
71. Sureka K., et al. The cyclic dinucleotide c-di-AMP is an allosteric regulator of metabolic enzyme function. Cell 2014, 158:1389-1401.
72. Huynh T.N., et al. An HD-domain phosphodiesterase mediates cooperative hydrolysis of c-di-AMP to affect bacterial growth and virulence. Proc. Natl. Acad. Sci. U.S.A. 2015, 112:E747-E756.
73. Zhang J., et al. Global analysis of riboswitches by small-angle X-ray scattering and calorimetry. Biochim. Biophys. Acta 2014, 1839:1020-1029.
74. Sudarsan N., et al. Riboswitches in eubacteria sense the second messenger cyclic di-GMP. Science 2008, 321:411-413.
75. Lee E.R., et al. An allosteric self-splicing ribozyme triggered by a bacterial second messenger. Science 2010, 329:845-848.
76. Kulshina N., et al. Recognition of the bacterial second messenger cyclic diguanylate by its cognate riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1212-1217.
77. Smith K.D., et al. Structural basis of ligand binding by a c-di-GMP riboswitch. Nat. Struct. Mol. Biol. 2009, 16:1218-1223.
78. Smith K.D., et al. Structural basis of differential ligand recognition by two classes of bis-(3'-5')-cyclic dimeric guanosine monophosphate-binding riboswitches. Proc. Natl. Acad. Sci. U.S.A. 2011, 108:7757-7762.
79. Janin J., et al. Protein-protein interaction and quaternary structure. Q. Rev. Biophys. 2008, 41:133-180.
80. Levy E.D., et al. Assembly reflects evolution of protein complexes. Nature 2008, 453:1262-1265.
81. Pitt J.N., Ferré-D'Amaré A.R. Rapid construction of empirical RNA fitness landscapes. Science 2010, 330:376-379.
82. Lau M.W., Ferré-D'Amaré A.R. An in vitro evolved glmS ribozyme has the wild-type fold but loses coenzyme dependence. Nat. Chem. Biol. 2013, 9:805-810.
83. Barrick J.E., Breaker R.R. The distributions, mechanisms, and structures of metabolite-binding riboswitches. Genome Biol. 2007, 8:R239.
84. Geary C., et al. Promoting RNA helical stacking via A-minor junctions. Nucleic Acids Res. 2011, 39:1066-1080.
85. Rossmann M.G. Structure of viruses: a short history. Q. Rev. Biophys. 2013, 46:133-180.
86. Monod J., et al. Allosteric proteins and cellular control systems. J. Mol. Biol. 1963, 6:306-329.
87. Svedberg T. Mass and size of protein molecules. Nature 1929, 123:871.
88. Perutz M.F., et al. Three-dimensional Fourier synthesis of horse oxyhaemoglobin at 2.8Å resolution: (1) X-ray analysis. Nature 1968, 219:29-32.
89. Lee A.J., Crothers D.M. The solution structure of an RNA loop-loop complex: the ColE1 inverted loop sequence. Structure 1998, 6:993-1005.
90. Leontis N.B., Westhof E. Geometric nomenclature and classification of RNA base pairs. RNA 2001, 7:499-512.
91. Bolton W., Perutz M.F. Three dimensional fourier synthesis of horse deoxyhaemoglobin at 2.8 Ångström units resolution. Nature 1970, 228:551-552.