DOI: 10.1261/rna.5210803. Transfer RNA modifications that alter +1 frameshifting in general fail to affect −1 frameshifting

Transfer RNA modifications that alter +1 frameshifting in general fail to affect −1 frameshifting

10.1261/rna.5210803

Crossref journal-article

Cold Spring Harbor Laboratory

RNA (246)

Abstract

Using mutants (tgt, mnmA(asuE, trmU), mnmE(trmE), miaA, miaB, miaE, truA(hisT), truB) of either Escherichia coli or Salmonella enterica serovar Typhimurium and the trm5 mutant of Saccharomyces cerevisiae, we have analyzed the influence by the modified nucleosides Q34, mnm5s2U34, ms2io6A37, Ψ39, Ψ55, m1G37, and yW37 on −1 frameshifts errors at various heptameric sequences, at which at least one codon is decoded by tRNAs having these modified nucleosides. The frequency of −1 frameshifting was the same in congenic strains only differing in the allelic state of the various tRNA modification genes. In fact, in one case (deficiency of mnm5s2U34), we observed a reduced ability of the undermodified tRNA to make a −1 frameshift error. These results are in sharp contrast to earlier observations that tRNA modification prevents +1 frameshifting suggesting that the mechanisms by which −1 and +1 frameshift errors occur are different. Possible mechanisms explaining these results are discussed.

Bibliography

URBONAVICÌIUS, J., STAHL, G., DURAND, J. M. B., BEN SALEM, S. N., QIAN, Q., FARABAUGH, P. J., & BJÃRK, G. R. (2003). Transfer RNA modifications that alter +1 frameshifting in general fail to affect â1 frameshifting. RNA, 9(6), 760â768.

Authors 7

JAUNIUS URBONAVIC̆IUS (first)
GUILLAUME STAHL (additional)
JÉRÔME M.B. DURAND (additional)
SAMIA N. BEN SALEM (additional)
QIANG QIAN (additional)
PHILIP J. FARABAUGH (additional)
GLENN R. BJÖRK (additional)

References 41 Referenced 86

Adams, A., Gottschling, D.E., Kaiser, C.A., and Stearns, T. 1997. Methods in yeast genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York.
10.1006/jmbi.1996.0117
10.1016/0092-8674(90)90371-K
10.1128/jb.62.3.293-300.1951 / J. Bacteriol. (1951)
10.1017/S1355838200000443
10.1126/science.2471265
10.1093/emboj/20.1.231
10.1006/jmbi.1997.1134
10.1006/viro.1998.9569
10.1006/viro.2000.0692
Davis, W., Botstein, D., and Roth, J.R. 1980. A manual for genetic engineering: Advanced bacterial genetics. Cold Spring Harbor Laboratory, Cold Spring Harbor, New York.
10.1073/pnas.88.1.174
10.1002/j.1460-2075.1987.tb04778.x / EMBO J. (1987)
10.1128/jb.166.3.1013-1021.1986 / J. Bacteriol. (1986)
10.1128/jb.177.8.1967-1975.1995 / J. Bacteriol. (1995)
10.1016/S0079-6603(00)64004-7 / Prog. Nucleic Acid Res. Mol. Biol. (2000)
10.1016/0092-8674(93)90297-4
10.1007/BF00280474 / Mol. Gen. Genet. (1994)
10.1093/nar/13.15.5697
10.1006/jmbi.1993.1429
10.1093/nar/23.9.1487
10.1016/0092-8674(88)90031-1
Kurland, C.G., Hughes, D., and Ehrenberg, M. 1996. Limitations of translational accuracy. In Escherichia coli and Salmonella: Cellular and molecular biology (eds. F.C. Neidhardt et al.), pp. 979â1004. ASM Press, Washington, DC.
10.1006/jmbi.1997.1176
10.1006/jmbi.1999.3361
10.1007/s00438-002-0725-y
10.1128/jb.175.24.7776-7785.1993 / J. Bacteriol. (1993)
Qian, Q. 1997. Transfer RNA modification and translational frameshifting. SolfjÃ¤dern Offset AB, UmeÃ¥, Sweden.
10.1006/jmbi.1997.1363
10.1016/S0092-8674(02)00619-0
10.1093/nar/27.1.196
10.1093/nar/23.9.1557
10.1016/S0968-0004(02)02064-9
10.1093/emboj/20.17.4863
10.1128/JB.184.19.5348-5357.2002
10.1038/302389a0
10.1093/genetics/112.4.727 / Genetics (1986)
10.1101/SQB.1987.052.01.078
{'key': '2021112105333126000_9.6.760.39', 'first-page': '159', 'volume': '1', 'year': '1989', 'journal-title': 'New Biol.'} / New Biol. (1989)
10.1016/S0079-6603(08)60626-1 / Progr. Nucl. Acid Res. Mol. Biol. (1990)
10.1111/j.1365-2958.1994.tb00310.x

Dates

Type	When
Created	22 years, 3 months ago (May 19, 2003, 6:21 p.m.)
Deposited	3 years, 9 months ago (Nov. 21, 2021, 8:35 a.m.)
Indexed	1 month, 4 weeks ago (July 2, 2025, 2:31 p.m.)
Issued	22 years, 3 months ago (June 1, 2003)
Published	22 years, 3 months ago (June 1, 2003)
Published Online	22 years, 3 months ago (June 1, 2003)
Published Print	22 years, 3 months ago (June 1, 2003)

Funders 0

None

BibTeX

@article{URBONAVIC_IUS_2003, title={Transfer RNA modifications that alter +1 frameshifting in general fail to affect −1 frameshifting}, volume={9}, ISSN={1469-9001}, url={http://dx.doi.org/10.1261/rna.5210803}, DOI={10.1261/rna.5210803}, number={6}, journal={RNA}, publisher={Cold Spring Harbor Laboratory}, author={URBONAVIC̆IUS, JAUNIUS and STAHL, GUILLAUME and DURAND, JÉRÔME M.B. and BEN SALEM, SAMIA N. and QIAN, QIANG and FARABAUGH, PHILIP J. and BJÖRK, GLENN R.}, year={2003}, month=jun, pages={760–768} }

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