Sequences that direct significant levels of frameshifting are frequent in coding regions of Escherichia coli
Open accessAbstract
It is generally believed that significant ribosomal frameshifting during translation does not occur without a functional purpose. The distribution of two frameshift-prone sequences, A_AAA_AAG and CCC_TGA, in coding regions of Escherichia coli has been analyzed. Although a moderate level of selection against the first sequence is evident, 68 genes contain A_AAA_AAG and 19 contain CCC_TGA. The majority of those tested in their genomic context showed >1% frameshifting. Comparative sequence analysis was employed to assess a potential biological role for frameshifting in decoding these genes. Two new candidates, in pheL and ydaY, for utilized frameshifting have been identified in addition to those previously known in dnaX and nine insertion sequence elements. For the majority of the shift-prone sequences no functional role can be attributed to them, and the frameshifting is likely erroneous. However, none of frameshift sequences is in the 306 most highly expressed genes. The unexpected conclusion is that moderate frameshifting during expression of at least some other genes is not sufficiently harmful for cells to trigger strong negative evolutionary pressure.
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Mononucleotide repeats, especially poly(A) and poly(U) tracts, cause transcriptional and translational frameshifting.
“Mononucleotide repeats, especially poly(A) and poly(U) tracts, are also known to cause transcriptional and translational frameshifting [8-10].”
From Preferred and avoided codon pairs in three domains of life (2008) · cites this paper as [10]
The A_AAA_AAG section reports ribosomal frameshifting at an A-rich sequence, and the CCC_UGA section reports frameshifting during translation at UUU_U/C. These support the translational part of the claim, but the paper does not establish that mononucleotide repeats cause transcriptional frameshifting. (LLM, conf=0.86)
Experimental — accuracy not yet measuredCodons in combination with surrounding nucleotides can form mononucleotide repeats, which may cause transcriptional or translational slippage.
“In addition, codons in combination with surrounding nucleotides can form mononucleotide repeats, which may cause transcriptional [8,9] or translational [10] slippage.”
From Preferred and avoided codon pairs in three domains of life (2008) · cites this paper as [10]
Certain heptanucleotides that are prone to frameshifts are under-represented in the coding sequences of Saccharomyces cerevisiae and Escherichia coli.
“For example, it has been shown that certain heptanucleotides that are prone to frameshifts are under-represented in the coding sequences of Saccharomyces cerevisiae [15] and Escherichia coli [10].”
From Preferred and avoided codon pairs in three domains of life (2008) · cites this paper as [10]
Codon pair preferences can be shaped by decrease of frameshifting errors through avoidance of mononucleotide repeats.
“One is the possible decrease of frameshifting errors through avoidance of mononucleotide repeats [8-10].”
From Preferred and avoided codon pairs in three domains of life (2008) · cites this paper as [10]
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References 55 · Cited by 87
Research works printed but not linked: 9
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- Authors
- Gurvich, O. L., Baranov, P. V., Zhou, J., Hammer, A. W., Gesteland, R. F., & Atkins, J. F.
- Affiliations
- University of Utah (US)
- Nitto (United States) (US)
- Corresponding author
- Atkins, John F.
- Venue
- The EMBO Journal
- Published
- 2003-11-03
- Volume
- 22
- Issue
- 21
- Pages
- 5941-5950
- ISSN
- 0261-4189 (ISSN-L)
- 1460-2075
- PMC
- PMC275418
- OpenAlex
- W2066306545
- Cited by
- 87
- References
- 55
- Citations by year
- 2025: 1 · 2024: 3 · 2023: 3 · 2022: 7 · 2021: 5 · 2020: 1 · 2019: 3 · 2018: 3 · 2017: 1 · 2016: 2 · 2015: 4 · 2014: 3 · 2013: 4 · 2012: 5
- FWCI
- 2.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- The EMBO Journal (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- U.S. Department of Energy (FG0301ER63132)
- National Institutes of Health
- National Institute of General Medical Sciences (R01GM048152, GM48152)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Evolution and Genetic Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- ribosomal frameshifting, Escherichia coli, insertion sequences, selection pressure, translation (biology), coding sequences
- MeSH terms
- Base Sequence, Codon, DNA, Bacterial, Escherichia coli, Genes, Bacterial, Recombinant Fusion Proteins, Ribosomes, Frameshifting, Ribosomal, Escherichia coli Proteins
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