The Solution Structure of a RNA Pentadecamer Comprising the Anticodon Loop and Stem of Yeast TRNAPhe. A 500 MHz 1H-n.m.r. Study

Overview

Journal Biochem J

Specialty Biochemistry

Date 1984 Aug 1

PMID 6089745

Citations 14

Authors

G M Clore

A M Gronenborn

E A PIPER

L W McLaughlin

E Graeser

J H VAN Boom

Affiliations

Soon will be listed here.

Abstract

A 500 MHz 1H-n.m.r. study on the semi-synthetic RNA pentadecamer 5'-r(C-A-G-A-Cm-U-Gm-A-A-Y-A-psi-m5C-U-G) comprising the anticodon loop and stem (residues 28-42) of yeast tRNAPhe is presented. By using pre-steady-state nuclear-Overhauser-effect measurements all exchangeable and non-exchangeable base proton resonances, all H1' ribose resonances and all methyl proton resonances are assigned and over 70 intra- and inter-nucleotide interproton distances determined. From the distance data the solution structure of the pentadecamer is solved by model-building. It is shown that the pentadecamer adopts a hairpin-loop structure in solution with the loop in a 3'-stacked conformation. This structure is both qualitatively and quantitatively remarkably similar to that of the anticodon loop and stem found in the crystal structures of tRNAPhe with an overall root-mean-square difference of 0.12 nm between the interproton distances determined by n.m.r. and X-ray crystallography. The hairpin-loop solution structure of the pentadecamer is very stable with a 'melting' temperature of 53 degrees C in 500 mM-KCl, and the structural features responsible for this high stability are discussed. Interaction of the pentadecamer with the ribotrinucleoside diphosphate UpUpC, one of the codons for the amino acid phenylalanine, results only in minor perturbations in the structure of the pentadecamer, and the 3'-stacked conformation of the loop is preserved. The stability of the pentadecamer-UpUpC complex (K approximately 2.5 X 10(4) M-1 at 0 degrees C) is approximately an order of magnitude greater than that of the tRNAPhe-UpUpC complex.

Citing Articles

Selectivity of stop codon recognition in translation termination is modulated by multiple conformations of GTS loop in eRF1.

Wong L, Li Y, Pillay S, Frolova L, Pervushin K Nucleic Acids Res. 2012; 40(12):5751-65.

PMID: 22383581 PMC: 3384315. DOI: 10.1093/nar/gks192.

Programmed translational -1 frameshifting on hexanucleotide motifs and the wobble properties of tRNAs.

Licznar P, Mejlhede N, Prere M, Wills N, Gesteland R, Atkins J EMBO J. 2003; 22(18):4770-8.

PMID: 12970189 PMC: 212731. DOI: 10.1093/emboj/cdg465.

tRNA recognition by tRNA-guanine transglycosylase from Escherichia coli: the role of U33 in U-G-U sequence recognition.

Nonekowski S, Garcia G RNA. 2001; 7(10):1432-41.

PMID: 11680848 PMC: 1370187.

Molecular dynamics of the anticodon domain of yeast tRNA(Phe): codon-anticodon interaction.

Lahiri A, Nilsson L Biophys J. 2000; 79(5):2276-89.

PMID: 11053108 PMC: 1301116. DOI: 10.1016/S0006-3495(00)76474-5.

Pleiotropic effects of intron removal on base modification pattern of yeast tRNAPhe: an in vitro study.

Jiang H, Motorin Y, Jin Y, Grosjean H Nucleic Acids Res. 1997; 25(14):2694-701.

PMID: 9207014 PMC: 146816. DOI: 10.1093/nar/25.14.2694.

References

Crick F . Codon--anticodon pairing: the wobble hypothesis. J Mol Biol. 1966; 19(2):548-55. DOI: 10.1016/s0022-2836(66)80022-0. View

Gronenborn A, Clore G, Kimber B . An investigation into the solution structures of two self-complementary DNA oligomers, 5'-d(C-G-T-A-C-G) and 5'-d(A-C-G-C-G-C-G-T), by means of nuclear-Overhauser-enhancement measurements. Biochem J. 1984; 221(3):723-36. PMC: 1144102. DOI: 10.1042/bj2210723. View

Uhlenbeck O, Borer P, Dengler B, Tinoco Jr I . Stability of RNA hairpin loops: A 6 -C m -U 6 . J Mol Biol. 1973; 73(4):483-96. DOI: 10.1016/0022-2836(73)90095-8. View

Gralla J, Crothers D . Free energy of imperfect nucleic acid helices. II. Small hairpin loops. J Mol Biol. 1973; 73(4):497-511. DOI: 10.1016/0022-2836(73)90096-x. View

Arnott S, Hukins D, Dover S, Fuller W, Hodgson A . Structures of synthetic polynucleotides in the A-RNA and A'-RNA conformations: x-ray diffraction analyses of the molecular conformations of polyadenylic acid--polyuridylic acid and polyinosinic acid--polycytidylic acid. J Mol Biol. 1973; 81(2):107-22. DOI: 10.1016/0022-2836(73)90183-6. View

Kim S, Sussman J . pi turn is a conformational pattern in RNA loops and bends. Nature. 1976; 260(5552):645-6. DOI: 10.1038/260645a0. View

QUIGLEY G, Rich A . Structural domains of transfer RNA molecules. Science. 1976; 194(4267):796-806. DOI: 10.1126/science.790568. View

Jack A, Ladner J, Klug A . Crystallographic refinement of yeast phenylalanine transfer RNA at 2-5A resolution. J Mol Biol. 1976; 108(4):619-49. DOI: 10.1016/s0022-2836(76)80109-x. View

Ezra F, Lee C, Kondo N, Danyluk S, Sarma R . Conformational properties of purine-pyrimidine and pyrimidine-purine dinucleoside monophosphates. Biochemistry. 1977; 16(9):1977-87. DOI: 10.1021/bi00628a035. View

10.

Sussman J, Holbrook S, Warrant R, Church G, Kim S . Crystal structure of yeast phenylalanine transfer RNA. I. Crystallographic refinement. J Mol Biol. 1978; 123(4):607-30. DOI: 10.1016/0022-2836(78)90209-7. View

11.

Holbrook S, Sussman J, Warrant R, Kim S . Crystal structure of yeast phenylalanine transfer RNA. II. Structural features and functional implications. J Mol Biol. 1978; 123(4):631-60. DOI: 10.1016/0022-2836(78)90210-3. View

12.

Hingerty B, Brown R, Jack A . Further refinement of the structure of yeast tRNAPhe. J Mol Biol. 1978; 124(3):523-34. DOI: 10.1016/0022-2836(78)90185-7. View

13.

Labuda D, Porschke D . Multistep mechanism of codon recognition by transfer ribonucleic acid. Biochemistry. 1980; 19(16):3799-805. DOI: 10.1021/bi00557a023. View

14.

Early T, Kearns D, Hillen W, Wells R . A 300- and 600-MHz proton nuclear magnetic resonance investigation of a 12 base pair deoxyribonucleic acid restriction fragment: relaxation behavior of the low-field resonances in water. Biochemistry. 1981; 20(13):3756-64. DOI: 10.1021/bi00516a014. View

15.

Porschke D, Labuda D . Codon-induced transfer ribonucleic acid association: quantitative analysis by sedimentation equilibrium. Biochemistry. 1982; 21(1):53-6. DOI: 10.1021/bi00530a010. View

16.

DICKERSON R, Drew H . Kinematic model for B-DNA. Proc Natl Acad Sci U S A. 1981; 78(12):7318-22. PMC: 349257. DOI: 10.1073/pnas.78.12.7318. View

17.

Hare D, Reid B . Direct assignment of the dihydrouridine-helix imino proton resonances in transfer ribonucleic acid nuclear magnetic resonance spectra by means of the nuclear Overhauser effect. Biochemistry. 1982; 21(8):1835-42. DOI: 10.1021/bi00537a020. View

18.

Pardi A, Morden K, Patel D, Tinoco Jr I . Kinetics for exchange of imino protons in the d(C-G-C-G-A-A-T-T-C-G-C-G) double helix and in two similar helices that contain a G . T base pair, d(C-G-T-G-A-A-T-T-C-G-C-G), and an extra adenine, d(C-G-C-A-G-A-A-T-T-C-G-C-G). Biochemistry. 1982; 21(25):6567-74. DOI: 10.1021/bi00268a038. View

19.

Roy S, Redfield A . Assignment of imino proton spectra of yeast phenylalanine transfer ribonucleic acid. Biochemistry. 1983; 22(6):1386-90. DOI: 10.1021/bi00275a010. View

20.

Reid D, Salisbury S, Bellard S, Shakked Z, Williams D . Proton nuclear Overhauser effect study of the structure of a deoxyoligonucleotide duplex in aqueous solution. Biochemistry. 1983; 22(8):2019-25. DOI: 10.1021/bi00277a044. View