The DOI matches its Crossref record; 38 of the 38 references it cites were found in a registry or an index.
Nonrandom utilization of codon pairs in Escherichia coli.
Open accessAbstract
We have analyzed protein-coding sequences of Escherichia coli and find that codon-pair utilization is highly biased, reflecting overrepresentation or underrepresentation of many pairs compared with their random expectations. This effect is over and above that contributed by nonrandomness in the use of amino acid pairs, which itself is highly evident; it is much weaker when nonadjacent codon pairs are examined and virtually disappears when pairs separated by two or three intervening codons are evaluated. There appears to be a high degree of directionality in this bias: any codon that participates in many nonrandom pairs tends to make both over- and underrepresented pairs, but preferentially as a left- or right-hand member. We show a relationship between codon-pair utilization patterns and levels of gene expression: genes encoding proteins expressed at high levels tend to contain more abundant, but more highly underrepresented, codon pairs, relative to genes expressed at low levels. The nonrandom utilization of codon pairs may be a consequence of their effects on translational efficiency, which in turn may be related to the compatibility of adjacent aminoacyl-tRNA isoacceptors at the A and P sites of a translating ribosome.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The text we found for this paper looks like another document, so the self-check wasn’t run.
Citations
Cites
Codon usage in bacteria: correlation with gene expressivity.
Gouy, M., & Gautier, C. (1982) · Nucleic Acids Research · doi:10.1093/nar/10.22.7055 · Cited by 1,182
Codon catalog usage is a genome strategy modulated for gene expressivity
Grantham, R. L., Gautier, C., Gouy, M., Jacobzone, M., & Mercier, R. (1981) · Nucleic Acids Research · doi:10.1093/nar/9.1.213-b · Cited by 939
Recognition of protein coding regions in DNA sequences
Fickett, J. W. (1982) · Nucleic Acids Research · doi:10.1093/nar/10.17.5303 · Cited by 897
Ikemura, T. (1981) · Journal of Molecular Biology · doi:10.1016/0022-2836(81)90363-6 · Cited by 875
Grosjean, H., & Fiers, W. C. (1982) · Gene · doi:10.1016/0378-1119(82)90157-3 · Cited by 855
Prediction of Protein Structure and the Principles of Protein Conformation
Fasman, G. D. (1989) · Springer eBooks · doi:10.1007/978-1-4613-1571-1 · Cited by 817
Gribskov, M., Devereux, J., & Burgess, R. R. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.1part2.539 · Cited by 382
Codon usage can affect efficiency of translation of genes inEscherichia coli
Robinson, M. K., Lilley, R. J., Little, S., Emtage, J. S., Yarranton, G. T., Stephens, P., Millican, A. T., Eaton, M. A. W., & Humphreys, G. O. (1984) · Nucleic Acids Research · doi:10.1093/nar/12.17.6663 · Cited by 297
Effects of surrounding sequence on the suppression of nonsense codons
Miller, J. H., & Albertini, A. M. (1983) · Journal of Molecular Biology · doi:10.1016/0022-2836(83)90087-6 · Cited by 292
The influence of codon context on genetic code translation
Bossi, L., & Roth, J. R. (1980) · Nature · doi:10.1038/286123a0 · Cited by 284
Cited by
Sorted by citations
Synonymous but not the same: the causes and consequences of codon bias
Plotkin, J. B., & Kudla, G. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2899 · Cited by 1,733
Strategies for achieving high-level expression of genes in Escherichia coli
Makrides, S. C. (1996) · Microbiological Reviews · doi:10.1128/mr.60.3.512-538.1996 · Cited by 1,287
Codon Bias as a Means to Fine-Tune Gene Expression
Quax, T. E. F., Claassens, N. J., Söll, D. G., & John van der, O. O. S. T. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.05.035 · Cited by 791
Virus attenuation by genome-scale changes in codon pair bias
Coleman, J. R., Papamichail, D., Skiena, S., Futcher, B., Wimmer, E., & Mueller, S. (2008) · Science · doi:10.1126/science.1155761 · Cited by 715
The anti-Shine–Dalgarno sequence drives translational pausing and codon choice in bacteria
Li, G., Oh, E., & Weissman, J. S. (2012) · Nature · doi:10.1038/nature10965 · Cited by 644
Precise Manipulation of Chromosomes in Vivo Enables Genome-Wide Codon Replacement
Isaacs, F. J., Carr, P. A., Wang, H. H., Lajoie, M. J., Sterling, B., Kraal, L., Tolonen, A. C., Gianoulis, T. A., Goodman, D. B., Reppas, N. B., et al. (2011) · Science · doi:10.1126/science.1205822 · Cited by 557
Genome sequence of the recombinant protein production host Pichia pastoris
Schutter, K. D., Lin, Y., Tiels, P., Hecke, A. V., Glinka, S., Weber-Lehmann, J., Rouzé, P., de Peer, Y. V., & Callewaert, N. (2009) · Nature Biotechnology · doi:10.1038/nbt.1544 · Cited by 538
“Some synonymous codon pairs are also more or less frequently used than expected (the codon pair bias”
Organization of the bacterial chromosome
Krawiec, S., & Riley, M. (1990) · Microbiological reviews · doi:10.1128/mr.54.4.502-539.1990 · Cited by 364
Gene Designer: a synthetic biology tool for constructing artificial DNA segments
Villalobos, A., Ness, J. E., Gustafsson, C., Minshull, J., & Govindarajan, S. (2006) · BMC Bioinformatics · doi:10.1186/1471-2105-7-285 · Cited by 379
“Aside from the experimentally validated cases of codon context effect on protein expression levels, there are several publications where in which codon context effects have been proposed based on in silico analysis of genomes [41-43].”
BackgroundDesign Parameters to Control Synthetic Gene Expression in Escherichia coli
Welch, M., Govindarajan, S., Ness, J. E., Villalobos, A., Gurney, A. L., Minshull, J., & Gustafsson, C. (2009) · PLoS ONE · doi:10.1371/journal.pone.0007002 · Cited by 354
Link, A. J., Robison, K. E., & Church, G. M. (1997) · Electrophoresis · doi:10.1002/elps.1150180807 · Cited by 342
Weissman, J., Hou, S., & Fuhrman, J. A. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2016810118 · Cited by 296
“The third (3) measure, codon pair bias, captures associations be- 56 tween neighboring codons, which have been suggested to impact translation [22, 6, 10].”
BackgroundLive attenuated influenza virus vaccines by computer-aided rational design
Mueller, S., Coleman, J. R., Papamichail, D., Ward, C. B., Nimnual, A., Futcher, B., Skiena, S., & Wimmer, E. (2010) · Nature Biotechnology · doi:10.1038/nbt.1636 · Cited by 275
“For reasons that are not understood, some pairs of codons occur more frequently while others occur less frequently than expected (codon pair bias) 14 .”
BackgroundAbsolute in vivo translation rates of individual codons in Escherichia coli
Sørensen, M. A., & Pedersen, S. B. (1991) · Journal of Molecular Biology · doi:10.1016/0022-2836(91)90211-n · Cited by 270
Synonymous but Not Silent: The Codon Usage Code for Gene Expression and Protein Folding
Liu, Y., Yang, Q., & Zhao, F. (2021) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-071320-112701 · Cited by 254
Ribosome‐mediated translational pause and protein domain organization
Thanaraj, T. A., & Argos, P. (1996) · Protein Science · doi:10.1002/pro.5560050814 · Cited by 239
Synonymous Codons: Choose Wisely for Expression
Brule, C. E., & Grayhack, E. J. (2017) · Trends in Genetics · doi:10.1016/j.tig.2017.02.001 · Cited by 241
“coli is biased and correlates with expression levels [72].”
BackgroundAdjacent Codons Act in Concert to Modulate Translation Efficiency in Yeast
Gamble, C. E., Brule, C. E., Dean, K., Fields, S., & Grayhack, E. J. (2016) · Cell · doi:10.1016/j.cell.2016.05.070 · Cited by 229
“Interactions between adjacent codons were first implicated in translation efficiency by the biased use of codon context and codon pairs in organisms in all three kingdoms (Fedorov et al., 2002; Gutman and Hatfield, 1989).”
BackgroundRaab, D., Graf, M., Notka, F., Schödl, T., & Wagner, R. (2010) · Systems and Synthetic Biology · doi:10.1007/s11693-010-9062-3 · Cited by 209
“…have shown how a number of important sequence properties can be accounted for in the quality function, it is obvious that further optimization parameters, for example the consideration of codon pairings (Gutman and Hatfield 1989), can easily be included in the calculation of the total quality score.”
BackgroundProkaryotic expression of antibodies
Arbabi‐Ghahroudi, M., Tanha, J., & MacKenzie, R. (2005) · Cancer and Metastasis Reviews · doi:10.1007/s10555-005-6193-1 · Cited by 191
“In another approach codon pair usage are optimized by mutating “slow pair” codons to “fast pair” codons [111,112].”
MethodLow-usage codons in Escherichia coli, yeast, fruit fly and primates
Zhang, S., Zubay, G., & Goldman, E. (1991) · Gene · doi:10.1016/0378-1119(91)90514-c · Cited by 188
Peden, J. F. (2010) · Europe PMC (PubMed Central) · Cited by 183
Tulloch, F., Atkinson, N. J., Evans, D. J., Ryan, M. D., & Simmonds, P. (2014) · eLife · doi:10.7554/elife.04531 · Cited by 178
The Yin and Yang of codon usage
Komar, A. A. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw207 · Cited by 176
Bifunctional enhancement of a β-glucanase-xylanase fusion enzyme by optimization of peptide linkers
Lü, P., & Feng, M. (2008) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-008-1468-4 · Cited by 173
Codon Pair Utilization Biases Influence Translational Elongation Step Times
Irwin, B., Heck, J. D., & Hatfield, G. W. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.39.22801 · Cited by 166
“Since our previous statistical analyses (Gutman and Hatfield, 1989; Hatfield and Gutman, 1992) showed that there is no correlation between the directionality of a codon pair and its bias, i.e. codon pair A-B versus B-A, we also wished to determine if there is a lack of correlation between the…”
BackgroundMethodResultInfluentialSelf-citationCodon Pair Bias Is a Direct Consequence of Dinucleotide Bias
Kunec, D., & Osterrieder, N. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.011 · Cited by 159
“Similarly, but independently of codon bias, juxtaposition of codons in open reading frames (ORFs) appears to be not random either (Gutman and Hatfield, 1989).”
BackgroundSynthetic viruses: a new opportunity to understand and prevent viral disease
Wimmer, E., Mueller, S., Tumpey, T. M., & Taubenberger, J. K. (2009) · Nature Biotechnology · doi:10.1038/nbt.1593 · Cited by 155
“This phenomenon, called 'codon pair bias', was discovered in prokaryotic cell”
BackgroundSpecific correlations between relative synonymous codon usage and protein secondary structure
Orešič, M., & Shalloway, D. I. (1998) · Journal of Molecular Biology · doi:10.1006/jmbi.1998.1921 · Cited by 144
Rodnina, M. V., Fricke, R., & Wintermeyer, W. (1994) · Biochemistry · doi:10.1021/bi00206a033 · Cited by 144
Czar, M. J., Anderson, J. C., Bader, J. S., & Peccoud, J. (2008) · Trends in biotechnology · doi:10.1016/j.tibtech.2008.10.007 · Cited by 148
Encell, L. P. (2012) · Current Chemical Genomics · doi:10.2174/1875397301206010055 · Cited by 139
Scalable live-attenuated SARS-CoV-2 vaccine candidate demonstrates preclinical safety and efficacy
Wang, Y., Yang, C., Song, Y., Coleman, J. R., Stawowczyk, M., Tafrova, J., Tasker, S. A., Boltz, D. A., Baker, R., Garcia, L., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2102775118 · Cited by 138
“SAVE takes advantage of naturally occurring codon pair bias in human cells and “deoptimized” viral sequences (7, 8).”
BackgroundWang, Y., Halls, C. E., Zhang, J., Matsuno, M., Zhang, Y., & Yu, O. S. (2011) · Metabolic Engineering · doi:10.1016/j.ymben.2011.04.005 · Cited by 135
Attenuation of human respiratory syncytial virus by genome-scale codon-pair deoptimization
Nouën, C. L., Brock, L. G., Luongo, C., McCarty, T. C., Yang, L., Mehedi, M., Wimmer, E., Mueller, S., Collins, P. L., Buchholz, U. J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411290111 · Cited by 123
You're one in a googol: optimizing genes for protein expression
Welch, M., Villalobos, A., Gustafsson, C., & Minshull, J. (2009) · Journal of The Royal Society Interface · doi:10.1098/rsif.2008.0520.focus · Cited by 120
The signal for the termination of protein synthesis in procaryotes
Brown, C. M., Stockwell, P. A., Trotman, C. N. A., & Tate, W. P. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.8.2079 · Cited by 120
Grothuesi, D., & Tümmler, B. (1991) · Molecular Microbiology · doi:10.1111/j.1365-2958.1991.tb01985.x · Cited by 118
Trinh, R. K., Gurbaxani, B. M., Morrison, S. L., et al. (2003) · Molecular Immunology · doi:10.1016/j.molimm.2003.08.006 · Cited by 116
Preferred and avoided codon pairs in three domains of life
Tats, A., Tenson, T., & Remm, M. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-463 · Cited by 112
“There have been many studies analyzing codon pair biases in a limited number of species [16-21].”
BackgroundMethodtRNA properties help shape codon pair preferences in open reading frames
Buchan, J. R. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkj488 · Cited by 108
“coli and yeast, confirming that codon pair frequencies are indeed highly biased (25,26), and that there are detectable differences in codon pair bias between high and low codonbiased gene sets (23,25).”
BackgroundInfluentialGaunt, E., Wise, H. M., Zhang, H., Lee, L. N., Atkinson, N. J., Nicol, M. Q., Highton, A. J., Klenerman, P., Beard, P. M., Dutia, B. M., et al. (2016) · eLife · doi:10.7554/elife.12735 · Cited by 107
“Production of synthetic coding sequences with increasing 72 frequencies of codon pairs that are naturally under-represented in vertebrate and viral genomes 73 have been similarly proposed to reduce translation efficiency (8-15).”
BackgroundMoura, G., Pinheiro, M., Arrais, J., Gomes, A. C., Carreto, L., Freitas, A., Oliveira, J. L., & Santos, M. A. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000847 · Cited by 107
“The few studies carried out to date on codon-pair context were unable to distinguish those two types of biases [12,36–38].”
BackgroundYang, C., Skiena, S., Futcher, B., Mueller, S., & Wimmer, E. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1307473110 · Cited by 103
“Proc Natl Acad Sci USA 86(10):3699–3703.”
Zhou, Z., Schnake, P., Xiao, L., & Lal, A. A. (2004) · Protein Expression and Purification · doi:10.1016/j.pep.2003.11.006 · Cited by 100
Large-scale recoding of an arbovirus genome to rebalance its insect versus mammalian preference
Shen, S. H., Stauft, C. B., Gorbatsevych, O., Song, Y., Ward, C. B., Yurovsky, A., Mueller, S., Futcher, B., & Wimmer, E. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1502864112 · Cited by 99
“Codon pair preference, or codon pair bias (CPB), is a phenomenon in which certain pairs of adjacent codons are used more frequently or less frequently than expected after accounting for use of individual codons (14 – 16).”
BackgroundMirzaei, H., McBee, J. K., Watts, J. D., & Aebersold, R. H. (2007) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m700495-mcp200 · Cited by 97
“DNA sequences encoding the designed QconCAT sequences were optimized by removal of translational “pause” sites, thus improving translation efficiencies (17, 18).”
MethodComputational Tools and Algorithms for Designing Customized Synthetic Genes
Gould, N., Hendy, O., & Papamichail, D. (2014) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2014.00041 · Cited by 98
The Effects of Selection Against Spurious Transcription Factor Binding Sites
Hahn, M. W. (2003) · Molecular Biology and Evolution · doi:10.1093/molbev/msg096 · Cited by 95
“Unfortunately, this method does not take into account any effects of di-codon bias: the nonrandom distribution of neighboring codon pairs (Gut-man and Hatfield 1989).”
MethodComputational codon optimization of synthetic gene for protein expression
Chung, B. K.-S., & Lee, D. (2012) · BMC Systems Biology · doi:10.1186/1752-0509-6-134 · Cited by 97
“This phenomenon is termed “ codon context ” as it implicates some “ rule ” for organizing neighboring codons as a result of potential tRNA-tRNA steric interaction within the ribosomes [17,18].”
BackgroundComparative context analysis of codon pairs on an ORFeome scale
Moura, G., Pinheiro, M., Silva, R., Miranda, I., Afreixo, V., Dias, G., Freitas, A., Oliveira, J. L., & Santos, M. A. (2005) · Genome Biology · doi:10.1186/gb-2005-6-3-r28 · Cited by 90
Karlin, S., Blaisdell, B. E., & Schachtel, G. A. (1990) · Journal of Virology · doi:10.1128/jvi.64.9.4264-4273.1990 · Cited by 85
Components of Vectors for Gene Transfer and Expression in Mammalian Cells
Makrides, S. C. (1999) · Protein Expression and Purification · doi:10.1006/prep.1999.1137 · Cited by 87
Mechanism of Virus Attenuation by Codon Pair Deoptimization
Groenke, N., Trimpert, J., Merz, S., Conradie, A. M., Wyler, E., Zhang, H., Hazapis, O.-G., Rausch, S., Landthaler, M., Osterrieder, N., et al. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107586 · Cited by 85
“This is an open access article under the CC BY-N be expected based on the overall frequencies of two codons that form a particular codon pair (Coleman et al., 2008; Gutman and Hatfield, 1989; Mueller et al., 2006).”
BackgroundMartrus, G., Nevot, M., Andres, C., Clotet, B., & Martinez, M. A. (2013) · Retrovirology · doi:10.1186/1742-4690-10-78 · Cited by 85
“Although the reasons are still not well understood, some codon pairs occur more frequently, and others less frequently, than expected [12].”
BackgroundFunctionally acceptable substitutions in two α‐helical regions of λ repressor
Reidhaar-Olson, J. F., & Sauer, R. T. (1990) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.340070403 · Cited by 84
Synonymous Virus Genome Recoding as a Tool to Impact Viral Fitness
Martı́nez, M. Á., Jordan-Paiz, A., Franco, S., & Nevot, M. (2015) · Trends in Microbiology · doi:10.1016/j.tim.2015.11.002 · Cited by 83
“coli suggested that the frequency with which codons are juxtaposed is nonrandom [50].”
BackgroundCodon pairs in the genome of Escherichia coli
Boycheva, S., Chkodrov, G., & Ivanov, I. G. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg082 · Cited by 81
“In an early study based on the analysis of 237 E.coli protein coding genes (Gutman and Hatfield, 1989) showed that some codon pairs were overrepresented and others were underrepresented in comparison with the theoretically predicted means.”
BackgroundInfluentialRibosome dynamics and mRNA turnover, a complex relationship under constant cellular scrutiny
Morris, C., Cluet, D., & Ricci, E. P. (2021) · Wiley Interdisciplinary Reviews - RNA · doi:10.1002/wrna.1658 · Cited by 82
“In some bacteria, lower eukaryotes (such as S. cerevisiae, C. elegans, and D. melanogaster) and plants (A. thaliana), codon usage has been shown to be biased towards the most abundant tRNAs (Duret & Mouchiroud, 1999; Grantham et al., 1980; Gutman & Hatfield, 1989; Ikemura, 1985).”
BackgroundWebster, G. R., Teh, A. Y., & K‐C., J. (2016) · Biotechnology and Bioengineering · doi:10.1002/bit.26183 · Cited by 86
Chen, S., Li, K., Cao, W., Wang, J., Zhao, T., Huan, Q., Yang, Y., Wu, S., & Qian, W. (2017) · Molecular Biology and Evolution · doi:10.1093/molbev/msx229 · Cited by 75
“The variable impact of an individual synonymous mutation is unlikely caused by the interaction between neighboring codons or tRNA recycling It has been proposed that two mechanisms, the interaction between neighboring codons and the reuse of synonymous codons recognized by the same tRNA (tRNA recycling), can regulate…”
BackgroundZika Virus Attenuation by Codon Pair Deoptimization Induces Sterilizing Immunity in Mouse Models
Li, P., Ke, X., Wang, T., Tan, Z., Luo, D., Miao, Y., Sun, J., Zhang, Y., Liu, Y., Hu, Q., et al. (2018) · Journal of Virology · doi:10.1128/jvi.00701-18 · Cited by 74
“88 Codon pair bias is interpreted as the unequal frequency in the usage of synonymous 89 codon pairs in certain species (27-29).”
BackgroundThe translational termination signal database
Brown, C. M., Dalphin, M. E., Stockwell, P. A., & Tate, W. P. (1993) · Nucleic Acids Research · doi:10.1093/nar/21.13.3119 · Cited by 75
Hatfield, G. W., & Roth, D. A. (2007) · Biotechnology annual review · doi:10.1016/s1387-2656(07)13002-7 · Cited by 70
Self-citationZhou, Z., Dang, Y., Zhou, M., Yuan, H., & Liu, Y. (2018) · eLife · doi:10.7554/elife.33569 · Cited by 71
Ni, Y.-Y., Zhao, Z., Opriessnig, T., Subramaniam, S., Zhou, L., Cao, D., Cao, Q. M., Yang, H., & Meng, X. (2014) · Virology · doi:10.1016/j.virol.2013.12.009 · Cited by 68
“It is known that, among the synonymous codon pairs encoding the same amino acid residues, some codon pairs occur more frequently than others in certain species (Fedorov et al., 2002; Gutman and Hatfield, 1989; Moura et al., 2007), which is known as codon-pair bias.”
BackgroundThe effect of context on synonymous codon usage in genes with low codon usage bias
Bulmer, M. G. (1990) · Nucleic Acids Research · doi:10.1093/nar/18.10.2869 · Cited by 66
Cridge, A. G. (2006) · Nucleic Acids Research · doi:10.1093/nar/gkl074 · Cited by 62
Atkinson, J., & Martin, R. H. (1994) · Nucleic Acids Research · doi:10.1093/nar/22.8.1327 · Cited by 61
Wang, B., Chen, Y., Tekes, G., Mueller, S., Paul, A. V., Whelan, S. P. J., & Wimmer, E. (2015) · mBio · doi:10.1128/mbio.00237-15 · Cited by 59
“Here, we report attempts to develop a live attenuated VSV strain, making use of a genetic phenomenon known as codon pair bias (CPB) (15, 16).”
MethodPhysical and genetic map of the Neisseria gonorrhoeae strain MS11‐N198 chromosome
Bihlmater, A., Römling, U., Meyer, T. F., et al. (1991) · Molecular Microbiology · doi:10.1111/j.1365-2958.1991.tb02099.x · Cited by 58
The Ongoing Quest to Crack the Genetic Code for Protein Production
Nieuwkoop, T., Finger‐Bou, M., John van der, O. O. S. T., & Claassens, N. J. (2020) · Molecular Cell · doi:10.1016/j.molcel.2020.09.014 · Cited by 51
Impact of C‐terminal amino acid composition on protein expression in bacteria
Weber, M. L., Burgos, R., Yus, E., Yang, J., Lluch‐Senar, M., & Serrano, L. G. (2020) · Molecular Systems Biology · doi:10.15252/msb.20199208 · Cited by 54
Raymond, A. C., Lovell, S., Lorimer, D. D., Walchli, J., Mixon, M. B., Wallace, E., Thompkins, K. B., Archer, K., Burgin, A. B., & Stewart, L. J. (2009) · BMC Biotechnology · doi:10.1186/1472-6750-9-37 · Cited by 55
“coli [21-23].”
Bicodon bias can determine the role of synonymous SNPs in human diseases
McCarthy, C. B., Carrea, A., & Diambra, L. A. (2017) · BMC Genomics · doi:10.1186/s12864-017-3609-6 · Cited by 53
“In addition, we have also computed the residual score χ2, defined in [42], which indicates when the observed bicodon bias can be explained, or not, by the codon usage bias.”
Illingworth, C. J. R., Parkes, K. E. B., Snell, C. R., et al. (2007) · Biophysical Chemistry · doi:10.1016/j.bpc.2007.11.004 · Cited by 54
Krasheninnikov, I. A., Komar, A. A., & Adzhubei, I. A. (1991) · Journal of Protein Chemistry · doi:10.1007/bf01025472 · Cited by 47
Codon context and protein synthesis: Enhancements of the genetic code
Buckingham, R. H. (1994) · Biochimie · doi:10.1016/0300-9084(94)90108-2 · Cited by 44
RNA stem-loop enhanced expression of previously non-expressible genes
Paulus, M. (2004) · Nucleic Acids Research · doi:10.1093/nar/gnh076 · Cited by 43
Coleman, J. R., Papamichail, D., Yano, M., et al. (2011) · The Journal of Infectious Diseases · doi:10.1093/infdis/jir010 · Cited by 43
“CPB is observed across the kingdoms of life, can be quantified statistically [1, 2], and”
BackgroundIntra-genome variability in the dinucleotide composition of SARS-CoV-2
Digard, P., Lee, H. M., Sharp, C., Grey, F. E., & Gaunt, E. R. (2020) · Virus Evolution · doi:10.1093/ve/veaa057 · Cited by 42
“CPB (Gutman and Hatfield, 1989) scores across the SARS-CoV-2 ORFeome were calculated using the SSE v1.”
MethodGenetic Engineering of Polymeric Materials
Tirrell, D. A., Fournier, M. J., & Mason, T. L. (1991) · MRS Bulletin · doi:10.1557/s0883769400056505 · Cited by 41
Trimpert, J., Adler, J. M., Eschke, K., Abdelgawad, A., Firsching, T. C., Ebert, N., Thao, T. T. N., Gruber, A. D., Thiel, V., Osterrieder, N., et al. (2021) · Science Advances · doi:10.1126/sciadv.abk0172 · Cited by 41
“CPD is based on the observation that some codon pairs occur in protein-coding sequences significantly less or more frequently than would be statistically expected (26).”
BackgroundFriberg, M. T., von Rohr, P., & Gonnet, G. H. (2004) · Yeast · doi:10.1002/yea.1150 · Cited by 40
Gao, L., Wang, L., Huang, C., Yang, L., Guo, X.-K., Yu, Z., Liu, Y., Yang, P., & Feng, W.-H. (2015) · Virology · doi:10.1016/j.virol.2015.07.012 · Cited by 40
“This phenomenon is termed as codon pair bias (CPB) (Gutman and Hatfield, 1989).”
BackgroundHuman body temperature and new approaches to constructing temperature-sensitive bacterial vaccines
White, M. D., Bosio, C. M., Duplantis, B. N., & Nano, F. E. (2011) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-011-0734-2 · Cited by 39
“Also, changes in the nucleotide sequence could affect the efficiency of translation if rare codons [75, 76] or rare codon pairs [77] for the host organism are introduced.”
Species-Specific Codon Context Rules Unveil Non-Neutrality Effects of Synonymous Mutations
Moura, G. R., Pinheiro, M. M., Freitas, A. V., Oliveira, J. L., Frommlet, J. C., Carreto, L. C., Soares, A. R., Bezerra, A. R., & Santos, M. A. S. (2011) · PLoS ONE · doi:10.1371/journal.pone.0026817 · Cited by 39
“independent of codon-usage biases [3,4], indicating that these two”
BackgroundPicataggio, S. K. (2009) · Current Opinion in Biotechnology · doi:10.1016/j.copbio.2009.04.003 · Cited by 39
Codon usage and codon context bias in Xanthophyllomyces dendrorhous
Baeza, M., Alcaı́no, J., Barahona, S., Sepúlveda, D., & Cifuentes, V. (2015) · BMC Genomics · doi:10.1186/s12864-015-1493-5 · Cited by 39
“Codon context bias is likely associated with the accuracy of decoding, indicating the ability of the translational machinery to detect codon pairs present at ribosomal decoding sites [30-33].”
BackgroundFages‐Lartaud, M., Hundvin, K., & Hohmann‐Marriott, M. F. (2022) · The Plant Journal · doi:10.1111/tpj.15970 · Cited by 41
“The expected codon pair frequency ( e ij ) was corrected for the dipeptide bias as previously described (Buchan et al., 2006; Gutman & Hatfield, 1989).”
InfluentialIn silico methods for predicting functional synonymous variants
Lin, B. C., Katneni, U., Jankowska, K. I., Meyer, D., & Kimchi‐Sarfaty, C. (2023) · Genome biology · doi:10.1186/s13059-023-02966-1 · Cited by 41
Shao, Z., Zhang, Y., Feng, X.-Y., Wang, B., & Chen, J. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033547 · Cited by 38
“It has been found that adjacent codon pairs, which encode either the same or different amino acids, have biased occurrence frequencies within a genome [24,25].”
BackgroundDifferential bicodon usage in lowly and highly abundant proteins
Diambra, L. A. (2017) · PeerJ · doi:10.7717/peerj.3081 · Cited by 37
“has been previously established in (Gutman and Hatfield, 1989; Buchan et al., 2006).”
BackgroundMethodResultInfluentialBuckingham, R. H. (1990) · Cellular and Molecular Life Sciences · doi:10.1007/bf01936922 · Cited by 39
TISIGNER.com: web services for improving recombinant protein production
Bhandari, B. K., Lim, C. S., & Gardner, P. P. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab175 · Cited by 38
Attenuation of Human Respiratory Viruses by Synonymous Genome Recoding
Nouën, C. L., Collins, P. L., & Buchholz, U. J. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.01250 · Cited by 39
“These Leu and Ser mutations did not affect the CB, CPB, CpG content or dinucleotide frequency ( Figure 1D ) (15).”
BackgroundMethodInfluentialUnderstanding the Genetic Code
Saier, M. H. (2019) · Journal of Bacteriology · doi:10.1128/jb.00091-19 · Cited by 44
Can simple codon pair usage predict protein–protein interaction?
Zhou, Y., Zhou, Y., He, F., Song, J., & Zhang, Z. (2012) · Molecular BioSystems · doi:10.1039/c2mb05427b · Cited by 38
Codon engineering for improved antibody expression in mammalian cells
Carton, J. M., Sauerwald, T. M., Hawley‐Nelson, P., Morse, B. A., Peffer, N. J., Beck, H., Lu, J., Cotty, A., Amegadzie, B. Y., & Sweet, R. (2007) · Protein Expression and Purification · doi:10.1016/j.pep.2007.05.017 · Cited by 34
Spatial Patterns of Gene Expression in Bacterial Genomes
Lato, D. F., & Golding, G. B. (2020) · Journal of Molecular Evolution · doi:10.1007/s00239-020-09951-3 · Cited by 31
Metadata
- Authors
- Gutman, G. A., & Hatfield, G. W.
- Affiliations
- University of California, Irvine (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 1989-05
- Volume
- 86
- Issue
- 10
- Pages
- 3699-3703
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC287207
- OpenAlex
- W2063504601
- Semantic Scholar
- 2e078282edbdc0cc228e53846cc1e546a9101d97
- Cited by
- 261
- References
- 38
- Citations by year
- 2026: 4 · 2025: 1 · 2024: 6 · 2023: 6 · 2022: 9 · 2021: 16 · 2020: 14 · 2019: 16 · 2018: 8 · 2017: 17 · 2016: 11 · 2015: 14 · 2014: 11 · 2013: 7 · 2012: 12
- FWCI
- 2.73
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (submittedVersion)
- Funders
- University of Southern California
- U.S. Public Health Service
- University of California, San Diego
- National Institute of General Medical Sciences (GM24330)
- National Institute of Allergy and Infectious Diseases (AI-21366)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- codon pair bias, Escherichia coli, gene expression levels, translation efficiency, protein-coding sequences, codon usage
- MeSH terms
- Bacterial Proteins, Codon, DNA, Bacterial, Escherichia coli, Gene Expression Regulation, Genes, Bacterial, Peptide Chain Termination, Translational, Probability, RNA, Messenger
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review