Cited by 463RNA and protein synthesis mechanismsRNA Research and SplicingGenomics and Chromatin Dynamics

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Rate-Limiting Steps in Yeast Protein Translation

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Shah, Premal, Ding, Yang, Niemczyk, Malwina, Kudla, Grzegorz, Plotkin, Joshua B.·2013·Cell

DOI 10.1016/j.cell.2013.05.049PMC PMC3694300

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Abstract

Deep sequencing now provides detailed snapshots of ribosome occupancy on mRNAs. We leverage these data to parameterize a computational model of translation, keeping track of every ribosome, tRNA, and mRNA molecule in a yeast cell. We determine the parameter regimes in which fast initiation or high codon bias in a transgene increases protein yield and infer the initiation rates of endogenous Saccharomyces cerevisiae genes, which vary by several orders of magnitude and correlate with 5' mRNA folding energies. Our model recapitulates the previously reported 5'-to-3' ramp of decreasing ribosome densities, although our analysis shows that this ramp is caused by rapid initiation of short genes rather than slow codons at the start of transcripts. We conclude that protein production in healthy yeast cells is typically limited by the availability of free ribosomes, whereas protein production under periods of stress can sometimes be rescued by reducing initiation or elongation rates.

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“…approaches and at different levels of granularity (Choi and Covert 2023; Cope and Shah 2025; Dykeman 2024; Katz et al. 2022; Levin and Tuller 2020; Raveh et al. 2016; Reuveni et al. 2011; Seeger et al. 2023; Shah and Gilchrist 2011; Shah et al. 2013; Subramaniam et al. 2014; Zarai et al. 2016).”
METTL16 enhances proteasome inhibitor resistance in multiple myeloma by inhibiting eIF2α-PERK interaction and promoting PSMB5 translation
Wang, G., Gao, X., Zhang, H., Hu, K., Feng, Q., Liu, Y., Hu, C., Guo, S., Yu, D., Chang, S., et al. (2026) · Oncogene · doi:10.1038/s41388-026-03706-y · Cited by 1
Mechanistic modeling of recessive disease through allelic integration of variant effects
Çubuk, H., Plech, M., Aslanzadeh, V., Zikánová, M., Škopová, V., Kmoch, S., Shen, Y., Marsh, J. A., & Kudla, G. (2026) · Cell Systems · doi:10.1016/j.cels.2026.101595 · Cited by 2
Self-citation
Paused in Translation: A Model for the Transcript Length-Dependent Impact of Ribosome-Targeting Antibiotics on Degrading mRNAs
Keisers, J., Kern, N., & Ciandrini, L. (2026) · PRX Life · doi:10.1103/vrqp-4y74 · Cited by 1
Precursor supply and translational machinery engineering of Saccharomyces cerevisiae for improving cellular protein content and biomass-based microbial protein bioproduction
Liu, Y., Jin, C., Shen, W., Wu, Y., Lv, X., Li, J. H., Liu, L. T., Du, G., Chen, J. X., & Liu, Y. (2026) · Bioresource Technology · doi:10.1016/j.biortech.2026.135462 · Cited by 1
Characterization of overexpression of the alternatively spliced isoform of the protein phosphatase 2A catalytic subunit in cells
Tang, S., Liu, Y., Wang, X., Liang, Z., Cai, H., Mo, L., Xiao, D., Guo, S., Ouyang, Y., Sun, B., et al. (2017) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2017.10.093 · Cited by 1
“The cause may be related to ribosomes because the availability of free ribosomes is the rate-limiting step of protein translation [21].”
Background
Bioinformatic Analysis Reveals the Role of Translation Elongation Efficiency Optimisation in the Evolution of Ralstonia Genus
Korenskaia, A. E., Matushkin, Y. G., Мустафин, З. С., Lashin, S. A., & Klimenko, A. I. (2023) · Biology · doi:10.3390/biology12101338 · Cited by 1
“Secondary structures in mRNA increase pause duration, which leads to a decrease in the elongation translation rate [25–27].”
Background
Synergistic Methods to Investigate Eukaryotic Translation and Its Quality Control
Emmi, A. J., McFarland, A. S., Grimes, M. M., Cole, I. J., & Lawson, M. R. (2025) · Journal of Molecular Biology · doi:10.1016/j.jmb.2025.169355 · Cited by 1
Establishment of 5′–3′ interactions in mRNA independent of a continuous ribose-phosphate backbone
Kluge, F., Götze, M., & Wahle, E. (2020) · RNA · doi:10.1261/rna.073759.119 · Cited by 1
“2013; Thompson and Gilbert 2017), and modeling has suggested that this is due to higher frequencies of initiation (Arava et al. 2005; Shah et al. 2013).”
BackgroundInfluential
Genetic influences on translation in yeastPreprint
Albert, F. W., Muzzey, D., Weissman, J. S., & Kruglyak, L. (2014) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/003319 · Cited by 1
Quantitative Principles of cis -translational control by general mRNA sequence features in eukaryotes
Li, J. J., Chew, G.-L., & Biggin, M. D. (2019) · doi:10.1101/587584 · Cited by 1
A Simulation Study of mRNA Diffusion and Mitochondrial LocalizationPreprint
Horton, P. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/614883 · Cited by 1
“Specifically, we included genes which had a measured value for each of the following features: Average Translation Initiation Time [2] Average Number of Ribosomes per mRNA molecule [3] Om45 ribosome proximity profiling based mRNA mitochondrial localization measurement [5] which resulted in the 497 genes.”
BackgroundInfluential
Deconstructing the individual steps of vertebrate translation initiationPreprint
Giess, A. P., Cleuren, Y. N. T., Tjeldnes, H., Krause, M., Bizuayehu, T. T., Hiensch, S., Okon, A. M., Wagner, C. R., & Valen, E. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/811810 · Cited by 1
A specific eIF4A paralog facilitates LARP1-mediated translation repression during mTORC1 inhibitionPreprint
Shichino, Y., Mito, M., Kashiwagi, K., Takahashi, M., Ito, T., Ingolia, N. T., & Iwasaki, S. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.09.18.460932 · Cited by 1
“Introduction Translation initiation — a rate-limiting step of protein synthesis (Shah et al., 2013; Yan et al., 2016) — is precisely controlled to regulate cellular homeostasis and stress responses.”
Background
Human cellular homeostasis buffers trans -acting translational effects of heterologous gene expression with very different codon usage biasPreprint
Jallet, A., Demange, A., Leblay, F., Decourcelle, M., Koulali, K. E., Picard, M., & Bravo, I. G. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.12.09.471957 · Cited by 1
“This may be especially the case if highly abundant mRNA species are not efficiently translated (Shah et al, 2013) – for example due to a poor CUBias.”
BackgroundInfluential
Adaptive Partitioning of the tRNA Interaction Interface by Aminoacyl-tRNA-SynthetasesPreprint
Collins-Hed, A., & Ardell, D. H. (2018) · bioRxiv · doi:10.1101/312462 · Cited by 1
Proteomic analyses of the Arabidopsis cap-binding complex define core set and TOR-dependent protein componentsPreprint
Matthes, A., Ouibrahim, L., Lecampion, C., Caranta, C., Davanture, M., Lebrun, R., Couté, Y., Baudet, M., Meyer, C., & Robaglia, C. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.02.16.528822 · Cited by 1
Dysregulation of amino acid metabolism upon rapid depletion of cap-binding protein eIF4EPreprint
Diamond, P. D., McGlincy, N. J., & Ingolia, N. T. (2023) · bioRxiv · doi:10.1101/2023.05.11.540079 · Cited by 1
“Often, this regulation affects translation initiation, a rate-limiting step and a point of commitment to protein synthesis (Shah et al., 2013).”
The one-message-per-cell-cycle rule: A conserved minimum transcription level for essential genesPreprint
Lo, T. W., Choi, H. J., Huang, D., & Wiggins, P. A. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.06.548020 · Cited by 1
“Note that the objective here is only to estimate µ m from µ p , not to model the process mechanistically ( e.g. [23].)”
Single-molecule RNA-FISH analysis reveals stochasticity in reactivation of latent HIV-1 regulated by Nuclear Orphan Receptors NR4A and cMYCPreprint
Porte, A. L., Pathak, R., Eliscovich, C., Martins, L. J., Nell, R., Spivak, A. M., Suzuki, M., Planelles, V., Singer, R. H., & Kalpana, G. V. (2024) · Research Square · doi:10.21203/rs.3.rs-4166090/v1 · Cited by 1
“The eukaryotic transcription is characterized as “bursty” or “stochastic” as opposed to “Poissonian” 9–13 .”
Synchronization between chloroplastic and cytosolic protein synthesis for photosynthesis complex assemblyPreprint
Wakigawa, T., Fujita, T., Kawamoto, N., Kurihara, Y., Hirose, Y., Hirayama, T., Toh, H., Kuriyama, T., Hashimoto, A., Matsuura-Suzuki, E., et al. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.05.03.592458 · Cited by 1
Evolutionary principles underpinning codon usage bias: patterns, functions, and mechanismsPreprint
Cope, A., Shah, P., Shah, P., & Wallace, E. W. J. (2024) · doi:10.32942/x2802v · Cited by 1
Self-citation
Disentangling the fitness cost of gene expressionPreprint
Yan, Y., & Lin, J. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.02.656972 · Cited by 1
“Interestingly, the predicted ribosome cost is very close to the measured translation cost (Table I), meaning that ri-221 bosome competition is the dominant source of translation cost, consistent with previous findings [19, 42, 43].”
Mechanistic Modelling of Recessive Disease through Allelic Integration of Variant EffectsPreprint
Çubuk, H., Plech, M., Aslanzadeh, V., Zikánová, M., Škopová, V., Kmoch, S., Shen, Y., Marsh, J. A., & Kudla, G. R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.08.15.670494 · Cited by 1
Self-citation
TOM: Transformer Neural Network Optimization of mRNA initiator regionPreprint
Gupta, R. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.10.30.685412 · Cited by 1
“Translation initiation has been accepted as the rate limiting step for gene expression [18].”
A ribosomal kinetic checkpoint governs selective mRNA recruitmentPreprint
Sokabe, M., Alvarado, C., Lapointe, C. P., Villa, N., Puglisi, J. D., & Fraser, C. S. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.06.12.731988 · Cited by 1
“≥ ⁻ Its characteristic rate ( 0.1 s ¹) aligns well with the fastest estimates of initiation kinetics (~4 s total) 20 , supporting the view that accommodation constitutes a key rate-limiting and regulatory step in the transition toward scanning.”
Influential
Homeostasis in the Central Dogma of Molecular Biology: the importance of mRNA instability
Pérez-Ortín, J. E., Tordera, V., & Chávez, S. (2019) · doi:10.1101/599050 · Cited by 1

Authors: Shah, P., Ding, Y., Niemczyk, M., Kudla, G., & Plotkin, J. B.
Affiliations: University of Pennsylvania (US)
Wellcome Centre for Cell Biology (GB)
Corresponding author: Plotkin, Joshua B.
ORCID: Shah, Premal
Ding, Yang
Kudla, Grzegorz
Plotkin, Joshua B.
Venue: Cell
Publisher: Elsevier BV
Published: 2013-06
Volume: 153
Issue: 7
Pages: 1589-1601
ISSN: 0092-8674 (ISSN-L)
DOI: 10.1016/j.cell.2013.05.049
PMC: PMC3694300
OpenAlex: W2011503994
Cited by: 463
References: 72
Citations by year: 2026: 15 · 2025: 24 · 2024: 31 · 2023: 33 · 2022: 37 · 2021: 27 · 2020: 40 · 2019: 37 · 2018: 42 · 2017: 50 · 2016: 48 · 2015: 26 · 2014: 44 · 2013: 9
FWCI: 18.98
Type: journal article
Language: en
Open access: hybrid
doi.org
Licence: cc-by
www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/legal/tdmrep-license (tdm)
creativecommons.org/licenses/by/3.0/ (vor, 45 d)
Locations: Cell (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
Edinburgh Research Explorer (University of Edinburgh) (submittedVersion, cc-by)
Funders: Burroughs Wellcome Fund
Army Research Office (D12AP00025, W911NF-12-1-0552)
James S. McDonnell Foundation
David and Lucile Packard Foundation
U.S. Department of the Interior
Wellcome Trust (077248)
Alfred P. Sloan Foundation (RFP-12-16)
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 › Genomics and Chromatin Dynamics
Keywords: mRNA translation, ribosome occupancy, translation initiation rate, codon usage bias, free ribosomes, protein production, Saccharomyces cerevisiae, tRNA availability, stress response
MeSH terms: Codon, Markov Chains, Models, Genetic, Ribosomes, RNA, Messenger, RNA, Transfer, Saccharomyces cerevisiae, Protein Biosynthesis

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Rate-Limiting Steps in Yeast Protein Translation

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