Abstract
Escherichia coli tmRNA functions uniquely as both tRNA and mRNA and possesses structural elements similar to canonical tRNAs. To test whether this mimicry extends to post-transcriptional modification, the technique of combined liquid chromatography/ electrospray ionization mass spectrometry (LC/ESIMS) and sequence data were used to determine the molecular masses of all oligonucleotides produced by RNase T1 hydrolysis with a mean error of 0.1 Da. Thus, this allowed for the detection, chemical characterization and sequence placement of modified nucleotides which produced a change in mass. Also, chemical modifications were used to locate mass-silent modifications. The native E.coli tmRNA contains two modified nucleosides, 5-methyluridine and pseudouridine. Both modifications are located within the proposed tRNA-like domain, in a seven-nucleotide loop mimicking the conserved sequence of T loops in canonical tRNAs. Although tmRNA acceptor branches (acceptor stem and T stem-loop) utilize different architectural rules than those of canonical tRNAs, their conformations in solution may be very similar. A comparative structural and functional analysis of unmodified tmRNA made by in vitro transcription and native E.coli tmRNA suggests that one or both of these post-transcriptional modifications may be required for optimal stability of the acceptor branch which is needed for efficient aminoacylation.
MeSH Terms
Base Composition
Base Sequence
Chromatography, Liquid
Escherichia coli/genetics
Mass Spectrometry
Models, Molecular
Molecular Sequence Data
Molecular Weight
Nucleic Acid Conformation
Oligonucleotides/chemistry
Pseudouridine/chemistry
RNA Processing, Post-Transcriptional/genetics
RNA, Bacterial/chemistry,metabolism
RNA, Transfer/chemistry,genetics
Ribonuclease T1/metabolism
Uridine/analogs & derivatives,chemistry
Chemicals
Oligonucleotides
RNA, Bacterial
tmRNA
Pseudouridine
ribothymidine
RNA, Transfer
Ribonuclease T1
Uridine
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Felden B
Howard Hughes Medical Institute, University of Utah, Salt Lake City, UT 84112, USA.
Hanawa K
Atkins J F
Himeno H
Muto A
Gesteland R F
McCloskey J A
Crain P F
References (34)
34 references, click to expand
-
Preparation and enzymatic hydrolysis of DNA and RNA for mass spectrometry.
Methods Enzymol. 1990;193:782-90
PMID: 1706062
-
Electrospray ionization for mass spectrometry of large biomolecules.
Science. 1989 Oct 6;246(4926):64-71
PMID: 2675315
-
The T-arm of tRNA is a substrate for tRNA (m5U54)-methyltransferase.
Biochemistry. 1991 Mar 26;30(12):2999-3002
PMID: 2007136
-
Identity elements of Escherichia coli tRNA(Ala).
J Mol Recognit. 1991 Jul-Dec;4(4):129-32
PMID: 1799462
-
Four newly located pseudouridylate residues in Escherichia coli 23S ribosomal RNA are all at the peptidyltransferase center: analysis by the application of a new sequencing technique.
Biochemistry. 1993 Sep 21;32(37):9754-62
PMID: 8373778
-
A novel method for the determination of post-transcriptional modification in RNA by mass spectrometry.
Nucleic Acids Res. 1993 Sep 25;21(19):4577-85
PMID: 8233793
-
High-level expression and rapid purification of tRNA (m5U54)-methyltransferase.
Protein Expr Purif. 1994 Apr;5(2):149-52
PMID: 8054847
-
tRNA-like structures in 10Sa RNAs of Mycoplasma capricolum and Bacillus subtilis.
Nucleic Acids Res. 1994 Aug 25;22(16):3392-6
PMID: 7521527
-
A tRNA-like structure is present in 10Sa RNA, a small stable RNA from Escherichia coli.
Proc Natl Acad Sci U S A. 1994 Sep 27;91(20):9223-7
PMID: 7524073
-
C-terminal extension of truncated recombinant proteins in Escherichia coli with a 10Sa RNA decapeptide.
J Biol Chem. 1995 Apr 21;270(16):9322-6
PMID: 7536743
-
Purification, cloning, and properties of the tRNA psi 55 synthase from Escherichia coli.
RNA. 1995 Mar;1(1):102-12
PMID: 7489483
-
Role of a peptide tagging system in degradation of proteins synthesized from damaged messenger RNA.
Science. 1996 Feb 16;271(5251):990-3
PMID: 8584937
-
tRNA and mRNA both in the same molecule.
Nat Struct Biol. 1996 Jun;3(6):494
PMID: 8646531
-
Phylogenetic analysis of tmRNA secondary structure.
RNA. 1996 Dec;2(12):1306-10
PMID: 8972778
-
Probing the structure of the Escherichia coli 10Sa RNA (tmRNA).
RNA. 1997 Jan;3(1):89-103
PMID: 8990402
-
Matrix-assisted laser desorption/ionization mass spectrometry (MALDI) of endonuclease digests of RNA.
Nucleic Acids Res. 1997 May 15;25(10):1957-64
PMID: 9115363
-
Structural organization of Escherichia coli tmRNA.
Biochimie. 1996;78(11-12):979-83
PMID: 9150875
-
Structure of the acceptor stem of Escherichia coli tRNA Ala: role of the G3.U70 base pair in synthetase recognition.
Nucleic Acids Res. 1997 Jun 1;25(11):2083-90
PMID: 9153306
-
In vitro trans translation mediated by alanine-charged 10Sa RNA.
J Mol Biol. 1997 May 23;268(5):803-8
PMID: 9180372
-
Compilation of tRNA sequences and sequences of tRNA genes.
Nucleic Acids Res. 1998 Jan 1;26(1):148-53
PMID: 9399820
-
The tmRNA Website.
Nucleic Acids Res. 1998 Jan 1;26(1):163-5
PMID: 9399824
-
The tmRNA database (tmRDB).
Nucleic Acids Res. 1998 Jan 1;26(1):166-7
PMID: 9399825
-
The RNA modification database--1998.
Nucleic Acids Res. 1998 Jan 1;26(1):196-7
PMID: 9399834
-
Reaction of pseudouridine and inosine with N-cyclohexyl-N'-beta-(4-methylmorpholinium)ethylcarbodiimide.
Biochemistry. 1971 Sep 28;10(20):3651-7
PMID: 4328867
-
Three-dimensional structure of yeast phenylalanine transfer RNA at 3.0angstroms resolution.
Nature. 1974 Mar 1;248(5443):20-4
PMID: 4594440
-
Small stable RNAs from Escherichia coli: evidence for the existence of new molecules and for a new ribonucleoprotein particle containing 6S RNA.
J Bacteriol. 1978 Feb;133(2):1015-23
PMID: 342486
-
Role of ribothymidine in the thermal stability of transfer RNA as monitored by proton magnetic resonance.
Nucleic Acids Res. 1979 Apr;6(4):1571-81
PMID: 377228
-
Characterization of 10S RNA: a new stable rna molecule from Escherichia coli.
Mol Gen Genet. 1979 Jul 2;174(1):25-32
PMID: 384159
-
A small RNA that complements mutants in the RNA processing enzyme ribonuclease P.
J Mol Biol. 1982 Dec 15;162(3):515-33
PMID: 6187924
-
Purification, structure, and properties of Escherichia coli tRNA pseudouridine synthase I.
J Biol Chem. 1988 Feb 15;263(5):2255-63
PMID: 3276686
-
Crosslinking of the anticodon of P site bound tRNA to C-1400 of E.coli 16S RNA does not require the participation of the 50S subunit.
Nucleic Acids Res. 1988 Jan 11;16(1):165-78
PMID: 3277159
-
Changing the identity of a tRNA by introducing a G-U wobble pair near the 3' acceptor end.
Science. 1988 May 6;240(4853):793-6
PMID: 2452483
-
A simple structural feature is a major determinant of the identity of a transfer RNA.
Nature. 1988 May 12;333(6169):140-5
PMID: 3285220
-
Analysis of RNA hydrolyzates by liquid chromatography-mass spectrometry.
Methods Enzymol. 1990;193:796-824
PMID: 1706064