Saturation mutagenesis of a +1 programmed frameshift-inducing mRNA sequence derived from a yeast retrotransposon

Carla Guarraia; Laura Norris; Ana Raman; Philip J. Farabaugh

doi:10.1261/rna.735107

journal article Sep 19, 2007

Saturation mutagenesis of a +1 programmed frameshift-inducing mRNA sequence derived from a yeast retrotransposon

Carla Guarraia Laura Norris Ana Raman Philip J. Farabaugh

RNA Vol. 13 No. 11 pp. 1940-1947 · Cold Spring Harbor Laboratory

View at Publisher Save 10.1261/rna.735107

Abstract

Errors during the process of translating mRNA information into protein products occur infrequently. Frameshift errors occur less frequently than other types of errors, suggesting that the translational machinery has more robust mechanisms for precluding that kind of error. Despite these mechanisms, mRNA sequences have evolved that increase the frequency up to 10,000-fold. These sequences, termed programmed frameshift sites, usually consist of a heptameric nucleotide sequence, at which the change in frames occurs along with additional sequences that stimulate the efficiency of frameshifting. One such stimulatory site derived from the Ty3 retrotransposon of the yeast Saccharomyces cerevisiae (the Ty3 stimulator) comprises a 14 nucleotide sequence with partial complementarity to a Helix 18 of the 18S rRNA, a component of the ribosome's accuracy center. A model for the function of the Ty3 stimulator predicts that it base pairs with Helix 18, reducing the efficiency with which the ribosome rejects erroneous out of frame decoding. We have tested this model by making a saturating set of single-base mutations of the Ty3 stimulator. The phenotypes of these mutations are inconsistent with the Helix 18 base-pairing model. We discuss the phenotypes of these mutations in light of structural data on the path of the mRNA on the ribosome, suggesting that the true target of the Ty3 stimulator may be rRNA and ribosomal protein elements of the ribosomal entry tunnel, as well as unknown constituents of the solvent face of the 40S subunit.

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References

71

[1]

10.1007/bf00425749

[2]

10.1016/0092-8674(90)90371-k

[3]

10.1007/bf00267704

[4]

10.1016/0022-2836(88)90092-7

[5]

10.1007/bf00267699

[6]

Three widely separated positions in the 16S RNA lie in or close to the ribosomal decoding region; a site-directed cross-linking study with mRNA analogues.

O. Dontsova, S. Dokudovskaya, A. Kopylov et al.

The EMBO Journal 1992 10.1002/j.1460-2075.1992.tb05383.x

[7]

10.1038/369371a0

[8]

Farabaugh, "Enhancer and silencerlike sites within the transcribed portion of a Ty2 transposable element of Saccharomyces cerevisiae" Mol. Cell. Biol. (1989)

[9]

Programmed translational frameshifting

P J Farabaugh

Microbiological Reviews 1996 10.1128/mr.60.1.103-134.1996

[10]

10.1016/0092-8674(93)90297-4

[11]

10.1093/nar/25.8.1559

[12]

10.1126/science.1529352

[13]

Three-dimensional cryo-electron microscopy localization of EF2 in the Saccharomyces cerevisiae 80S ribosome at 17.5 A resolution

M. G. Gomez-Lorenzo

The EMBO Journal 10.1093/emboj/19.11.2710

[14]

10.1073/pnas.88.15.6603

[15]

Gorini, L. (1974) in Ribosomes, Streptomycin and misreading of the genetic code, ed Nomura M. (Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y), pp 791–803.

[16]

RIBOSOMES AND TRANSLATION

Rachel Green, Harry F. Noller

Annual Review of Biochemistry 10.1146/annurev.biochem.66.1.679

[17]

10.1016/s1097-2765(04)00005-x

[18]

Gutell, R.R. (1996) in Structure, evolution, processing and function in protein biosynthesis, Comparative sequence analysis and the structure of 16S and 23S rRNA, eds Dahlberg A.E. Zimmermann R.A. (Ribosomal RNA, CRC Press, Boca Raton, FL), pp 111–128.

[19]

Studies on transformation of Escherichia coli with plasmids

Douglas Hanahan

Journal of Molecular Biology 10.1016/s0022-2836(83)80284-8

[20]

Hancock, "Evolution of the secondary structures and compensatory mutations of the ribosomal RNAs of Drosophila melanogaster" Mol. Biol. Evol. (1988)

[21]

Hendrick, "Yeast frameshift suppressor mutations in the genes coding for transcription factor Mbf1p and ribosomal protein S3: Evidence for autoregulation of S3 synthesis" Genetics (2001) 10.1093/genetics/157.3.1141

[22]

Kinetic Proofreading: A New Mechanism for Reducing Errors in Biosynthetic Processes Requiring High Specificity

J. J. Hopfield

Proceedings of the National Academy of Sciences 10.1073/pnas.71.10.4135

[23]

VMD: Visual molecular dynamics

William Humphrey, Andrew Dalke, Klaus Schulten

Journal of Molecular Graphics 10.1016/0263-7855(96)00018-5

[24]

Transformation of intact yeast cells treated with alkali cations

H Ito, Y Fukuda, K Murata et al.

Journal of Bacteriology 1983 10.1128/jb.153.1.163-168.1983

[25]

10.1016/0378-1119(95)00134-r

[26]

Kawakami, "A rare tRNA-Arg(CCU) that regulates Ty1 element ribosomal frameshifting is essential for Ty1 retrotransposition in Saccharomyces cerevisiae" Genetics (1993) 10.1093/genetics/135.2.309

[27]

10.1017/s1355838200000595

[28]

Larsen, "Upstream stimulators for recoding" Biochem. Cell Biol. (1995) 10.1139/o95-121

[29]

10.1017/s0033583599003479

[30]

10.1017/s135583820100190x

[31]

10.1006/jmbi.1994.1668

[32]

10.1128/jb.183.11.3499-3505.2001

[33]

10.1016/s1097-2765(04)00031-0

[34]

10.1016/j.sbi.2005.05.004

[35]

10.1016/s0300-9084(75)80139-8

[36]

O'Connor, "Genetic probes of ribosomal RNA function" Biochem. Cell Biol. (1995) 10.1139/o95-093

[37]

10.1093/nar/25.6.1185

[38]

10.1073/pnas.96.16.8973

[39]

10.1016/s0968-0004(03)00066-5

[40]

Olins, "A novel sequence element derived from bacteriophage T7 mRNA acts as an enhancer of translation of the lacZ gene in Escherichia coli" J. Biol. Chem. (1989) 10.1016/s0021-9258(18)71444-0

[41]

Pulling the Ribosome out of Frame by 11 at a Programmed Frameshift Site by Cognate Binding of Aminoacyl-tRNA

Suchira Pande, Arunachalam Vimaladithan, Hong Zhao et al.

Molecular and Cellular Biology 1995 10.1128/mcb.15.1.298

[42]

Parker, "Errors and alternatives in reading the universal genetic code" Microbiol. Rev. (1989) 10.1128/mr.53.3.273-298.1989

[43]

10.1016/0092-8674(87)90564-2

[44]

Dominant lethal mutations in a conserved loop in 16S rRNA.

Ted Powers, H F Noller

Proceedings of the National Academy of Sciences 10.1073/pnas.87.3.1042

[45]

Resch, "Downstream boxanti-downstream box interactions are dispensable for translation initiation of leaderless mRNAs" EMBO J. (1996) 10.1002/j.1460-2075.1996.tb00851.x

[46]

Site-directed cross-linking of mRNA analogues to 16S ribosomal RNA; a complete scan of cross-links from all positions between ‘+ 1’ and ‘+ 16’ on the mRNA, downstream from the decoding site

Jutta Rinke-Appel, Nicole Jünke, Richard Brimacombe et al.

Nucleic Acids Research 10.1093/nar/21.12.2853

[47]

10.1016/j.febslet.2004.11.048

[48]

Santer, "The 530 loop of 16S ribosomal RNA: Each base change confers its own phenotype" Mol. Biol. Cell (1993)

[49]

Compensatory mutations suggest that base-pairing with a small nuclear RNA is required to form the 3′ end of H3 messenger RNA

Fred Schaufele, Gregory M. Gilmartin, Willi Bannwarth et al.

Nature 10.1038/323777a0

[50]

Structures of the Bacterial Ribosome at 3.5 Å Resolution

Barbara S. Schuwirth, Maria A. Borovinskaya, Cathy W. Hau et al.

Science 10.1126/science.1117230

Showing 50 of 71 references

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Details

Published: Sep 19, 2007
Vol/Issue: 13(11)
Pages: 1940-1947

Authors

Department of Biological Sciences, University of Maryland

Cite This Article

Carla Guarraia, Laura Norris, Ana Raman, et al. (2007). Saturation mutagenesis of a +1 programmed frameshift-inducing mRNA sequence derived from a yeast retrotransposon. RNA, 13(11), 1940-1947. https://doi.org/10.1261/rna.735107

Saturation mutagenesis of a +1 programmed frameshift-inducing mRNA sequence derived from a yeast retrotransposon

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