Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources

Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae, we evaluate for the first time the expecte...

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Published inPLoS computational biology Vol. 14; no. 4; p. e1006055
Main Authors Zarai, Yoram, Tuller, Tamir
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 01.04.2018
Public Library of Science (PLoS)
Subjects
Amino Acid Substitution
Biological evolution
Biology and life sciences
Circuit design
Codon - genetics
Computational Biology
Computer Simulation
Engineering and Technology
Evolution, Molecular
Gene Expression
Genes
Genes, Synthetic
Genome, Fungal
Green Fluorescent Proteins - biosynthesis
Green Fluorescent Proteins - genetics
Kinetics
Level (quantity)
Messenger RNA
Models, Genetic
Monte Carlo Method
Mutation
Observations
Occupancy
Physiological aspects
Protein Biosynthesis
Recombinant Proteins - biosynthesis
Recombinant Proteins - genetics
Research and Analysis Methods
Ribosomes - metabolism
RNA, Fungal - genetics
RNA, Fungal - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - metabolism
Traffic congestion
Traffic jams
Translation (Genetics)
Variations
Israel
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Abstract Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae, we evaluate for the first time the expected effect of mRNA levels fluctuations on translation due to the finite pool of ribosomes. We show that fluctuations of a single gene or a group of genes mRNA levels induce periodic behavior in all S. cerevisiae translation factors and aspects: the ribosomal densities and the translation rates of all S. cerevisiae mRNAs oscillate. We numerically measure the oscillation amplitudes demonstrating that fluctuations of endogenous and heterologous genes can cause a significant fluctuation of up to 50% in the steady-state translation rates of the rest of the genes. Furthermore, we demonstrate by synonymous mutations that oscillating the levels of mRNAs that experience high ribosomal occupancy (e.g. ribosomal "traffic jam") induces the largest impact on the translation of the S. cerevisiae genome. The results reported here should provide novel insights and principles related to the design of synthetic gene expression circuits and related to the evolutionary constraints shaping gene expression of endogenous genes.
AbstractList Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae, we evaluate for the first time the expected effect of mRNA levels fluctuations on translation due to the finite pool of ribosomes. We show that fluctuations of a single gene or a group of genes mRNA levels induce periodic behavior in all S. cerevisiae translation factors and aspects: the ribosomal densities and the translation rates of all S. cerevisiae mRNAs oscillate. We numerically measure the oscillation amplitudes demonstrating that fluctuations of endogenous and heterologous genes can cause a significant fluctuation of up to 50% in the steady-state translation rates of the rest of the genes. Furthermore, we demonstrate by synonymous mutations that oscillating the levels of mRNAs that experience high ribosomal occupancy (e.g. ribosomal "traffic jam") induces the largest impact on the translation of the S. cerevisiae genome. The results reported here should provide novel insights and principles related to the design of synthetic gene expression circuits and related to the evolutionary constraints shaping gene expression of endogenous genes.
Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae, we evaluate for the first time the expected effect of mRNA levels fluctuations on translation due to the finite pool of ribosomes. We show that fluctuations of a single gene or a group of genes mRNA levels induce periodic behavior in all S. cerevisiae translation factors and aspects: the ribosomal densities and the translation rates of all S. cerevisiae mRNAs oscillate. We numerically measure the oscillation amplitudes demonstrating that fluctuations of endogenous and heterologous genes can cause a significant fluctuation of up to 50% in the steady-state translation rates of the rest of the genes. Furthermore, we demonstrate by synonymous mutations that oscillating the levels of mRNAs that experience high ribosomal occupancy (e.g. ribosomal "traffic jam") induces the largest impact on the translation of the S. cerevisiae genome.
Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae, we evaluate for the first time the expected effect of mRNA levels fluctuations on translation due to the finite pool of ribosomes. We show that fluctuations of a single gene or a group of genes mRNA levels induce periodic behavior in all S. cerevisiae translation factors and aspects: the ribosomal densities and the translation rates of all S. cerevisiae mRNAs oscillate. We numerically measure the oscillation amplitudes demonstrating that fluctuations of endogenous and heterologous genes can cause a significant fluctuation of up to 50% in the steady-state translation rates of the rest of the genes. Furthermore, we demonstrate by synonymous mutations that oscillating the levels of mRNAs that experience high ribosomal occupancy (e.g. ribosomal “traffic jam”) induces the largest impact on the translation of the S. cerevisiae genome. The results reported here should provide novel insights and principles related to the design of synthetic gene expression circuits and related to the evolutionary constraints shaping gene expression of endogenous genes.
Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene expression aspects. In this study, based on a whole-cell model simulation of translation in S. cerevisiae , we evaluate for the first time the expected effect of mRNA levels fluctuations on translation due to the finite pool of ribosomes. We show that fluctuations of a single gene or a group of genes mRNA levels induce periodic behavior in all S. cerevisiae translation factors and aspects: the ribosomal densities and the translation rates of all S. cerevisiae mRNAs oscillate. We numerically measure the oscillation amplitudes demonstrating that fluctuations of endogenous and heterologous genes can cause a significant fluctuation of up to 50% in the steady-state translation rates of the rest of the genes. Furthermore, we demonstrate by synonymous mutations that oscillating the levels of mRNAs that experience high ribosomal occupancy (e.g. ribosomal “traffic jam”) induces the largest impact on the translation of the S. cerevisiae genome. The results reported here should provide novel insights and principles related to the design of synthetic gene expression circuits and related to the evolutionary constraints shaping gene expression of endogenous genes. Each cell contains a limited number of macromolecules and factors that participate in the gene expression process. These expression resources are shared between the different molecules that encode the genetic code, resulting in non-trivial couplings and competitions between the different gene expression stages. Such competitions should be considered when analyzing the cellular economy of the cell, the genome evolution, and the design of synthetic expression circuits. Here we study the effect of couplings and competitions for ribosomes by performing a whole-cell simulation of translation of S. cerevisiae , with parameters estimated from experimental data. We demonstrate that by periodically changing the mRNA levels of a single gene (endogenous or heterologous) or a set of genes, the translation of all S. cerevisiae genes are affected in a periodic manner. We numerically estimate the exact impact of the mRNA levels periodicity on the translation process dynamics, as well as on the dynamics of the free ribosomal pool and the way it is affected by parameters such as the codon composition of the oscillating gene, its initiation rate and mRNA levels. Furthermore, we show that the codon compositions of synthetically highly expressed heterologous genes that are expected to oscillate must be carefully considered. For example, synonymous mutations resulting in “traffic jams” of ribosomes along the fluctuated mRNAs may cause significant fluctuations of up to 50% in the steady-state translation rates of all genes.
Audience Academic
Author Zarai, Yoram
Tuller, Tamir
AuthorAffiliation 2 Department of Biomedical Engineering and the Sagol School of Neuroscience, Tel-Aviv University, Tel-Aviv, Israel
1 Department of Biomedical Engineering, Tel-Aviv University, Tel-Aviv, Israel
Rutgers University, UNITED STATES
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/29614119$$D View this record in MEDLINE/PubMed
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ContentType Journal Article
Copyright COPYRIGHT 2018 Public Library of Science
2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zarai Y, Tuller T (2018) Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources. PLoS Comput Biol 14(4): e1006055. https://doi.org/10.1371/journal.pcbi.1006055
2018 Zarai, Tuller 2018 Zarai, Tuller
2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zarai Y, Tuller T (2018) Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources. PLoS Comput Biol 14(4): e1006055. https://doi.org/10.1371/journal.pcbi.1006055
Copyright_xml – notice: COPYRIGHT 2018 Public Library of Science
– notice: 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zarai Y, Tuller T (2018) Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources. PLoS Comput Biol 14(4): e1006055. https://doi.org/10.1371/journal.pcbi.1006055
– notice: 2018 Zarai, Tuller 2018 Zarai, Tuller
– notice: 2018 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Zarai Y, Tuller T (2018) Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources. PLoS Comput Biol 14(4): e1006055. https://doi.org/10.1371/journal.pcbi.1006055
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Current address: Department of Biomedical Engineering, Tel-Aviv University, Tel-Aviv, Israel
The authors have declared that no competing interests exist.
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    fullname: T Gedeon
– volume: 343
  start-page: 536
  issue: 6258
  year: 1990
  ident: ref24
  article-title: Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels
  publication-title: Nature
  doi: 10.1038/343536a0
  contributor:
    fullname: PE Hardin
SSID ssj0035896
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Snippet Recent studies have demonstrated how the competition for the finite pool of available gene expression factors has important effect on fundamental gene...
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SubjectTerms Amino Acid Substitution
Biological evolution
Biology and life sciences
Circuit design
Codon - genetics
Computational Biology
Computer Simulation
Engineering and Technology
Evolution, Molecular
Gene Expression
Genes
Genes, Synthetic
Genome, Fungal
Green Fluorescent Proteins - biosynthesis
Green Fluorescent Proteins - genetics
Kinetics
Level (quantity)
Messenger RNA
Models, Genetic
Monte Carlo Method
Mutation
Observations
Occupancy
Physiological aspects
Protein Biosynthesis
Recombinant Proteins - biosynthesis
Recombinant Proteins - genetics
Research and Analysis Methods
Ribosomes - metabolism
RNA, Fungal - genetics
RNA, Fungal - metabolism
RNA, Messenger - genetics
RNA, Messenger - metabolism
Saccharomyces cerevisiae
Saccharomyces cerevisiae - genetics
Saccharomyces cerevisiae - metabolism
Traffic congestion
Traffic jams
Translation (Genetics)
Variations
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Title Computational analysis of the oscillatory behavior at the translation level induced by mRNA levels oscillations due to finite intracellular resources
URI https://www.ncbi.nlm.nih.gov/pubmed/29614119
https://www.proquest.com/docview/2039765869
https://search.proquest.com/docview/2021730841
https://pubmed.ncbi.nlm.nih.gov/PMC5898785
https://doaj.org/article/58e1146917a7483eb2f3cc8131d2691d
http://dx.doi.org/10.1371/journal.pcbi.1006055
Volume 14
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