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Codon Optimality Is a Major Determinant of mRNA Stability
Open accessAbstract
mRNA degradation represents a critical regulated step in gene expression. Although the major pathways in turnover have been identified, accounting for disparate half-lives has been elusive. We show that codon optimality is one feature that contributes greatly to mRNA stability. Genome-wide RNA decay analysis revealed that stable mRNAs are enriched in codons designated optimal, whereas unstable mRNAs contain predominately non-optimal codons. Substitution of optimal codons with synonymous, non-optimal codons results in dramatic mRNA destabilization, whereas the converse substitution significantly increases stability. Further, we demonstrate that codon optimality impacts ribosome translocation, connecting the processes of translation elongation and decay through codon optimality. Finally, we show that optimal codon content accounts for the similar stabilities observed in mRNAs encoding proteins with coordinated physiological function. This work demonstrates that codon optimization exists as a mechanism to finely tune levels of mRNAs and, ultimately, proteins.
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“These strategies have yielded modest improvements in RNA stability10, 13–16, and thus alternative approaches to RNA stabilization, such as circularization, are desirable.”
From Engineering circular RNA for potent and stable translation in eukaryotic cells (2018) · cites this paper as [15]
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“Furthermore, the rate of codon-dependent translation elongation has been a primary factor of mRNA stability, codon modification is critical for mRNA stability (Presnyak et al. 2015).”
From Modifications of mRNA vaccine structural elements for improving mRNA stability and translation efficiency (2022) · cites this paper as Presnyak et al. 2015
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“Furthermore, the rate of codon-dependent translation elongation has been a primary factor of mRNA stability, codon modification is critical for mRNA stability (Presnyak et al. 2015).”
From Modifications of mRNA vaccine structural elements for improving mRNA stability and translation efficiency (2022) · cites this paper as Presnyak et al. 2015
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“To improve the safety, efficacy, and stability of mRNA vaccines, researchers usually performed codon optimization172,239–243 on the antigen-coding sequence to enhance translation efficiency.”
From Advances in COVID-19 mRNA vaccine development (2022) · cites this paper as [240]
In the citing paper
“Codon optimization in the mRNA sequence to e.g., match host transfer (t)RNA abundances, or as a determinant of introducing secondary structures, can drastically impact the protein synthesis rate and ribosome dwell time (i.e. mRNA functional half-life) [33,34]”
From The dawn of mRNA vaccines: the COVID-19 case (2021) · cites this paper as [33]
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Citations
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Integration of ENCODE RNAseq and eCLIP Data Sets
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FMRP Links Optimal Codons to mRNA stability in NeuronsPreprint
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Hypoxia-mediated regulation of mRNA metabolism: from transcription to stability
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Dilrangi, K. H., Aretakis, J. R., Vaidya, K., Al-Husini, N., Muthunayake, N. S., Kim, S., & Schrader, J. M. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.116691 · Cited by 3
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BackgroundD-stem mutation in an essential tRNA increases translation speed at the cost of fidelity
Schrock, M. N., Parsawar, K., Hughes, K. T., & Chevance, F. F. V. (2025) · PLoS Genetics · doi:10.1371/journal.pgen.1011569 · Cited by 3
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BackgroundRETRACTED: A 5′ fragment of Xist can sequester RNA produced from adjacent genes on chromatin
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Reading Frame Retrieval of Genes: A New Parameter of Codon Usage Based on the Circular Code Theory
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“…production (Grantham et al. 1981) and codon choice has effects at many biological stages, including transcription (Zhou et al. 2016), translation efficiency (Qian et al. 2012), mRNA stability (Presnyak et al. 2015), protein folding (Buhr et al. 2016) and protein function (Bali and Bebok 2015).”
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BackgroundNew SHH and Known SIX3 Variants in a Series of Latin American Patients with Holoprosencephaly
de Castro, V. F., Mattos, D., de Carvalho, F. M., Cavalcanti, D. P., Dueñas, M., Llerena, J. C., Cosentino, V., Honjo, R. S., Leite, J. C. L., Sanseverino, M. T. V., et al. (2021) · Molecular Syndromology · doi:10.1159/000515044 · Cited by 2
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“Unstable mRNAs possess non-optimal codons, which cause destabilized protein expression, whereas optimal codons are great contributors to mRNA stability (Presnyak et al. 2015).”
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Guo, Q., Liu, B., Guo, X., Yan, P., Cao, B., Liu, R., & Liu, X. (2024) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2024.110848 · Cited by 2
A Symphony of Roles for Codon Usage in Fungal Genomics
LaBella, A. L. (2024) · The mycota · doi:10.1007/978-3-031-75666-5_6 · Cited by 3
Roy, A., & Chakraborty, S. (2025) · Virus Genes · doi:10.1007/s11262-025-02155-1 · Cited by 2
“According to [35], the MSI is the measure of mRNA stability, and it is computed based on the codon stabilization coefficient (CSC) values.”
Designing a cellular MicroRNA-based approach to silence bat-borne Nipah virus genes
Kar, N., & Chakraborty, S. (2025) · Journal of NeuroVirology · doi:10.1007/s13365-025-01268-5 · Cited by 2
“Transcripts exhibiting higher instabil - ity are generally enriched in non-optimal codons, whereas those with greater stability preferentially utilize optimal codons (Presnyak et al. 2015).”
InfluentialAgeing-related decline of translation as a consequence of transcription dysregulation
Pechmann, S. (2025) · Journal of The Royal Society Interface · doi:10.1098/rsif.2025.0323 · Cited by 2
Codon Composition in Human Oocytes Reveals Age-Associated Defects in mRNA Decay
Brachova, P., Christenson, L. K., & Alvarez, N. S. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26199395 · Cited by 2
Pawlak, K., Błażej, P., Mackiewicz, D., & Mackiewicz, P. (2023) · International Journal of Molecular Sciences · doi:10.3390/ijms24021185 · Cited by 3
“It was also proposed that the codon usage changes the gene expression by the influence on the transcription process [28–30] and mRNA stability [31].”
BackgroundMost synonymous allelic variants in HIV tat are not silent
Giacoletto, C. J., Benjamin, R., Deng, H., Rotter, J. I., & Schiller, M. R. (2023) · Genomics · doi:10.1016/j.ygeno.2023.110603 · Cited by 2
“[5,6] One explanation could be adjacent codon interactions during translation which has been observed and reviewed by Brule [5] Nevertheless, codon usage in WT genes seem to be important as rare codons are conserved across species.”
BackgroundMercer, H., Nair, A. M., Ridgel, A. L., & Piontkivska, H. (2023) · PLoS ONE · doi:10.1371/journal.pone.0287078 · Cited by 2
Khandia, R., Pandey, M. K., Garg, R. K., Khan, A. A., Baklanov, I. S., Alanazi, A. M., Nepali, P., Gurjar, P., & Choudhary, O. P. (2024) · Annals of Medicine and Surgery · doi:10.1097/ms9.0000000000001725 · Cited by 2
Ueno, D., Mikami, M., Yamasaki, S., Kaneko, M., Mukuta, T., Demura, T., & Kato, K. (2020) · Plant and Cell Physiology · doi:10.1093/pcp/pcaa147 · Cited by 3
Revilleza, J. E. C., Sato, M., Irie, K., Suda, Y., Mizuno, T., & Irie, K. (2022) · PLoS ONE · doi:10.1371/journal.pone.0268283 · Cited by 2
“Since it is reported that translation efficiency is coupled with mRNA stability [45], the translation efficiency of CLB mRNAs may be involved in both mRNA and protein levels.”
BackgroundElucidation of Codon Usage Signatures across the Domains of LifePreprint
Novoa, E. M., Jaillon, O., Jungreis, I., & Kellis, M. (2018) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/421487 · Cited by 2
The development of gene drives for genetic control of the malaria mosquito
Hammond, A. (2016) · Spiral (Imperial College London) · doi:10.25560/53131 · Cited by 2
Mercier, B. C., Labaronne, E., Cluet, D., Bicknell, A. A., Corbin, A., Guiguettaz, L., Aubé, F., Modolo, L., Auboeuf, D., Moore, M. J., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.10.16.341222 · Cited by 2
Codon Bias Confers Stability to mRNAs via ILF2 in HumansPreprint
Hia, F., Yang, S. F., Shichino, Y., Yoshinaga, M., Murakawa, Y., Vandenbon, A., Fukao, A., Fujiwara, T., Landthaler, M., Natsume, T., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/585992 · Cited by 2
“However, we could not exclude the possibility that these factors induced the degradation of AU-rich transcripts independent of the model proposed by Presnyak and Radhakrishnan (12, 13) as our RBP identification method was not reflective of the active translational status required for co-translational degradation of mR…”
BackgroundResultInfluentialCodon composition in human oocytes reveals age-associated defects in mRNA decayPreprint
Alvarez, N. S., Brachova, P., & Christenson, L. K. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.01.05.425501 · Cited by 2
Extensive in vitro and in vivo protein translation via in situ circularized RNAsPreprint
Kumar, A., Palmer, N. D., Miyasaki, K. F., Finburgh, E. N., Xiang, Y., Portell, A. J., Dailamy, A., Suhardjo, A., Chew, W. L., Kwon, E. J., et al. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.02.11.480072 · Cited by 1
Manipulating the 3D Organization of the Largest Synthetic Yeast ChromosomePreprint
Zhang, W., Lazar‐Stefanita, L., Yamashita, H., Shen, M. J., MITCHELL, L. A., Kurasawa, H., Haase, M. A. B., Sun, X., Jiang, Q., Lauer, S. L., et al. (2022) · SSRN Electronic Journal · doi:10.2139/ssrn.4138701 · Cited by 2
Snyman, M., & Xu, S. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.28.530525 · Cited by 2
Isoform-specific translational control is evolutionarily conserved in primatesPreprint
Draper, J. M., Philipp, J., Neeb, Z., Thomas, R. C., Katzman, S. J., Salama, S. R., Haussler, D. H., & Sanford, J. R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.04.21.537863 · Cited by 3
“Likewise, codon optimality influences translation elongation and RNA stability in a variety of species (Gu et al. 2010; Tuller et al. 2010; Presnyak et al. 2015).”
BackgroundNo Ramp Needed: Spandrels, Statistics, and a Slippery SlopePreprint
Sejour, R., Leatherwood, J., Yurovsky, A., & Futcher, B. (2023) · eLife · doi:10.7554/elife.89656.1 · Cited by 2
Post-transcriptional control contributes to hypoxia-induced tumorigenic phenotypes in macrophagesPreprint
Courvan, E. M. C., & Parker, R. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.10.09.561558 · Cited by 2
tRNA modifications tune decoding of codon pairs to prevent cellular quality control responsesPreprint
Wu, J., Eggers, C., Sin, O., Koziej, L., Mancilla, H., Mollet, F., Schöler, H. R., Drexler, H. C. A., Ranff, T., Fufezan, C., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.27.582385 · Cited by 2
“Codon-specific translation rates, and therefore codon optimality, are generally determined by averaging ribosome occupancy of all instances of a codon across the transcriptome 8,9,71–74 .”
BackgroundKulkarni, S. D., Morrissey, A., Sebastian, A., Giardine, B. M., Smith, C., Akinniyi, O. T., Keller, C. A., Arnaoutov, A., Albert, I. U., Mahony, S., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.09.10.612038 · Cited by 2
“We observed a strong and highly significant correlation between codon optimality content and transcript half-lives, suggesting that our measurements indeed supported the previously known relationship between codon content and mRNA half-lives (Forrest et al. 2020; Presnyak et al. 2015).”
BackgroundResultKumar, R., Zhang, F., Niphadkar, S., Onu, C., Vijjamarri, A. K., Greenberg, M. L., Laxman, S., & Hinnebusch, A. G. (2024) · eLife · doi:10.7554/elife.102287 · Cited by 2
“Sheet ‘Codon Opt Scores nonESR mRNAs’ lists the tRNA adaptation index (tAI), species-specific tRNA adaptation index (stAI), and the average codon stabilization coefficient (AvgCSC) for all non-ESR yeast genes ( Presnyak et al., 2015 ; Radhakrishnan et al., 2016 ).”
Snell, P. H., Naeli, P., Garzia, A., Waldron, J. A., Chatterjee, S., McGirr, T., Ladak, R. J., Choi, J., Luo, J., Leino, S. A., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.21.649502 · Cited by 2
“The presence of non-optimal codons generally leads to slower mRNA translation and enhanced rate of decay, through a loosely defined process named codon optimality-mediated mRNA degradation [8, 9].”
Discovery of a tRNA-regulatory transcription factor that suppresses breast cancer metastasisPreprint
Chen, S., Markett, D., Karimzadeh, M., Luo, Y., Khoroshkin, M., Boyraz, B., Lee, S. B., Carpenter, C., Nguyen, P. T., Garcia, K., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.04.26.650725 · Cited by 2
Akiyama, M., Tashiro, M., Huang, Y., Uehara, M., Kanzaki, T., Itaya, M., Kataoka, M., Miyamoto, K., & Sakakibara, Y. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.08.652991 · Cited by 2
“As a result, a sequence optimized purely on codon usage frequencies may still perform suboptimally in the host, and in some instances over-optimization can even reduce protein yield 7,10 .”
A Unified Framework for Model-Informed and Agentic RNA DesignPreprint
Riley, A. T., Vlasity, M., Becicka, W. M., Huang, J., Pang, S., Wong, W. W., Grinstaff, M. W., & Green, A. A. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.17.659751 · Cited by 3
A code within a code: how codons influence mRNA stability
Martı̂nez, J., & Žagrović, B. (2016) · The EMBO Journal · doi:10.15252/embj.201695283 · Cited by 1
“…by Bazzini et al (2016) complements and extends an exciting line of recent research showing similar effects in bacteria (Boel et al , 2016), yeast (Presnyak et al , 2015), and zebrafish (Mishima & Tomari, 2016), suggesting that the involved mechanisms may be a fundamental property of living…”
Elucidating the roles of naturally occurring silent mutations in Polycystic Ovary Syndrome (PCOS)
Gümüşgül, M. D., Şahin, Ş., Turan, H., Karaca, B. T., & Kutlu, A. (2020) · Meta Gene · doi:10.1016/j.mgene.2020.100707 · Cited by 1
Brümmer, A., Dreos, R., Marques, A. C., & Bergmann, S. (2021) · Molecular Biology and Evolution · doi:10.1093/molbev/msab356 · Cited by 1
“Furthermore, it may hinder a potential regulatory function of lincRNAs, and, given the association between mRNA translation and transcript stability (Presnyak et al. 2015; Tuck et al. 2020), translation of lincRNAs might impact their cytoplasmic expression levels, with potentially disadvantageous…”
Background
Metadata
- Authors
- Presnyak, V., Alhusaini, N., Chen, Y.-H., Martin, S., Morris, N., Kline, N., Olson, S., Weinberg, D., Baker, K. E., Graveley, B. R., & Coller, J.
- Affiliations
- Case Western Reserve University (US)
- UConn Health (US)
- University of California, San Francisco (US)
- Corresponding author
- Coller, Jeff
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-03
- Volume
- 160
- Issue
- 6
- Pages
- 1111-1124
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4359748
- OpenAlex
- W2013321787
- Cited by
- 1,078
- References
- 43
- Citations by year
- 2026: 94 · 2025: 139 · 2024: 122 · 2023: 115 · 2022: 77 · 2021: 127 · 2020: 93 · 2019: 70 · 2018: 96 · 2017: 68 · 2016: 57 · 2015: 20
- FWCI
- 34.90
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Funders
- National Institutes of Health (GM080465, GM095621)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA modifications and cancer
- Keywords
- codon optimality, mRNA stability, mRNA degradation, codon usage bias, synonymous codons, ribosome translocation, translation elongation, gene expression regulation, mRNA half-life
- MeSH terms
- Codon, RNA, Fungal, RNA, Messenger, Saccharomyces cerevisiae, Protein Biosynthesis, RNA Stability
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