Functional TRNAs with Altered 3' Ends

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 1993 Jun 1

PMID 7685277

Citations 26

Authors

M OConnor

N M Willis

L Bossi

R F GESTELAND

J F Atkins

Affiliations

Soon will be listed here.

Abstract

The CCA trinucleotide is a universally conserved feature of the 3' end of tRNAs, where it serves as the site of amino acid attachment. Despite this extreme conservation, we have isolated functional mutants of tRNA(His) and tRNA(Val1) with altered CCA ends. A mutant that leads to de-repression of the histidine biosynthetic operon in Salmonella typhimurium has been characterized and found to have the CCA end of the sole tRNA(His) species mutated to UCA. However, constructed mutants of tRNA(His) with ACA or GCA ends appeared to be nonfunctional in vivo. Mutants of Escherichia coli tRNA(Val1) with GCA or ACA ends were isolated on the basis of their ability to promote frameshifting at a specific sequence. These same tRNA(Val1) mutants also caused read-through of stop codons that were one, or in some instances two, codons downstream of the valine codon decoded by the mutant tRNA. A startling implication of these data is that disruption of interactions between the CCA end of the tRNA and the large ribosomal subunit promotes these aberrant codon-anticodon interactions on the small ribosomal subunit.

Citing Articles

Rare ribosomal RNA sequences from archaea stabilize the bacterial ribosome.

Nissley A, Penev P, Watson Z, Banfield J, Cate J Nucleic Acids Res. 2023; 51(4):1880-1894.

PMID: 36660825 PMC: 9976906. DOI: 10.1093/nar/gkac1273.

Mutational characterization and mapping of the 70S ribosome active site.

dAquino A, Azim T, Aleksashin N, Hockenberry A, Kruger A, Jewett M Nucleic Acids Res. 2020; 48(5):2777-2789.

PMID: 32009164 PMC: 7049736. DOI: 10.1093/nar/gkaa001.

Culmination of a half-century quest reveals insight into mutant tRNA-mediated frameshifting after tRNA departure from the decoding site.

Atkins J Proc Natl Acad Sci U S A. 2018; 115(44):11121-11123.

PMID: 30341222 PMC: 6217412. DOI: 10.1073/pnas.1815837115.

Ribosomal frameshifting and transcriptional slippage: From genetic steganography and cryptography to adventitious use.

Atkins J, Loughran G, Bhatt P, Firth A, Baranov P Nucleic Acids Res. 2016; 44(15):7007-78.

PMID: 27436286 PMC: 5009743. DOI: 10.1093/nar/gkw530.

Ribosomal frameshifting used in influenza A virus expression occurs within the sequence UCC_UUU_CGU and is in the +1 direction.

Firth A, Jagger B, Wise H, Nelson C, Parsawar K, Wills N Open Biol. 2012; 2(10):120109.

PMID: 23155484 PMC: 3498833. DOI: 10.1098/rsob.120109.

References

Moir P, Spiegelberg R, Oliver I, Pringle J, Masters M . Proteins encoded by the Escherichia coli replication terminus region. J Bacteriol. 1992; 174(7):2102-10. PMC: 205826. DOI: 10.1128/jb.174.7.2102-2110.1992. View

Vogel H, Bonner D . Acetylornithinase of Escherichia coli: partial purification and some properties. J Biol Chem. 1956; 218(1):97-106. View

Kopelowitz J, Hampe C, Goldman R, Reches M, Engelberg-Kulka H . Influence of codon context on UGA suppression and readthrough. J Mol Biol. 1992; 225(2):261-9. DOI: 10.1016/0022-2836(92)90920-f. View

Atkins J, Nichols B, Thompson S . The nucleotide sequence of the first externally suppressible--1 frameshift mutant, and of some nearby leaky frameshift mutants. EMBO J. 1983; 2(8):1345-50. PMC: 555281. DOI: 10.1002/j.1460-2075.1983.tb01590.x. View

Davies J, Jones D, Khorana H . A further study of misreading of codons induced by streptomycin and neomycin using ribopolynucleotides containing two nucleotides in alternating sequence as templates. J Mol Biol. 1966; 18(1):48-57. DOI: 10.1016/s0022-2836(66)80075-x. View

Roth J, ANTON D, Hartman P . Histidine regulatory mutants in Salmonella typhimurium. I. Isolation and general properties. J Mol Biol. 1966; 22(2):305-23. DOI: 10.1016/0022-2836(66)90134-3. View

MONRO R, Marcker K . Ribosome-catalysed reaction of puromycin with a formylmethionine-containing oligonucleotide. J Mol Biol. 1967; 25(2):347-50. DOI: 10.1016/0022-2836(67)90146-5. View

MONRO R, Cerna J, Marcker K . Ribosome-catalyzed peptidyl transfer: substrate specificity at the P-site. Proc Natl Acad Sci U S A. 1968; 61(3):1042-9. PMC: 305433. DOI: 10.1073/pnas.61.3.1042. View

Hirsh D, Gold L . Translation of the UGA triplet in vitro by tryptophan transfer RNA's. J Mol Biol. 1971; 58(2):459-68. DOI: 10.1016/0022-2836(71)90363-9. View

10.

Brenner M, Ames B . Histidine regulation in Salmonella typhimurium. IX. Histidine transfer ribonucleic acid of the regulatory mutants. J Biol Chem. 1972; 247(4):1080-8. View

11.

Atkins J, Ryce S . UGA and non-triplet suppressor reading of the genetic code. Nature. 1974; 249(457):527-30. DOI: 10.1038/249527a0. View

12.

Chang A, Cohen S . Construction and characterization of amplifiable multicopy DNA cloning vehicles derived from the P15A cryptic miniplasmid. J Bacteriol. 1978; 134(3):1141-56. PMC: 222365. DOI: 10.1128/jb.134.3.1141-1156.1978. View

13.

Johnston H, Barnes W, Chumley F, Bossi L, Roth J . Model for regulation of the histidine operon of Salmonella. Proc Natl Acad Sci U S A. 1980; 77(1):508-12. PMC: 348301. DOI: 10.1073/pnas.77.1.508. View

14.

Hazelbauer G, Engstrom P, Harayama S . Methyl-accepting chemotaxis protein III and transducer gene trg. J Bacteriol. 1981; 145(1):43-9. PMC: 217242. DOI: 10.1128/jb.145.1.43-49.1981. View

15.

Quiggle K, Kumar G, Ott T, Ryu E, Chladek S . Donor site of ribosomal peptidyltransferase: investigation of substrate specificity using 2'(3')-O-(N-acylaminoacyl)dinucleoside phosphates as models of the 3' terminus of N-acylaminoacyl transfer ribonucleic acid. Biochemistry. 1981; 20(12):3480-5. DOI: 10.1021/bi00515a027. View

16.

Bitner R, KUEMPEL P . P1 transduction map spanning the replication terminus of Escherichia coli K12. Mol Gen Genet. 1981; 184(2):208-12. DOI: 10.1007/BF00272906. View

17.

Chopra I, Shales S, Ward J, Wallace L . Reduced expression of Tn 10-mediated tetracycline resistance in Escherichia coli containing more than one copy of the transposon. J Gen Microbiol. 1981; 126(1):45-54. DOI: 10.1099/00221287-126-1-45. View

18.

Stoker N, Fairweather N, Spratt B . Versatile low-copy-number plasmid vectors for cloning in Escherichia coli. Gene. 1982; 18(3):335-41. DOI: 10.1016/0378-1119(82)90172-x. View

19.

Weiss R, Gallant J . Mechanism of ribosome frameshifting during translation of the genetic code. Nature. 1983; 302(5907):389-93. DOI: 10.1038/302389a0. View

20.

Bossi L . The hisR locus of Salmonella: nucleotide sequence and expression. Mol Gen Genet. 1983; 192(1-2):163-70. DOI: 10.1007/BF00327662. View