Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels

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Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. / Frenkel-Morgenstern, Milana; Danon, Tamar; Christian, Thomas; Igarashi, Takao; Cohen, Lydia; Hou, Ya-Ming; Jensen, Lars Juhl.

In: Molecular Systems Biology, Vol. 8, 2012, p. 572.

Research output: Contribution to journalJournal articleResearchpeer-review

Harvard

Frenkel-Morgenstern, M, Danon, T, Christian, T, Igarashi, T, Cohen, L, Hou, Y-M & Jensen, LJ 2012, 'Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels', Molecular Systems Biology, vol. 8, pp. 572. https://doi.org/10.1038/msb.2012.3

APA

Frenkel-Morgenstern, M., Danon, T., Christian, T., Igarashi, T., Cohen, L., Hou, Y-M., & Jensen, L. J. (2012). Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Molecular Systems Biology, 8, 572. https://doi.org/10.1038/msb.2012.3

Vancouver

Frenkel-Morgenstern M, Danon T, Christian T, Igarashi T, Cohen L, Hou Y-M et al. Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. Molecular Systems Biology. 2012;8:572. https://doi.org/10.1038/msb.2012.3

Author

Frenkel-Morgenstern, Milana ; Danon, Tamar ; Christian, Thomas ; Igarashi, Takao ; Cohen, Lydia ; Hou, Ya-Ming ; Jensen, Lars Juhl. / Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels. In: Molecular Systems Biology. 2012 ; Vol. 8. pp. 572.

Bibtex

@article{eaaeb80499264aa797a79f747e81793a,
title = "Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels",
abstract = "The cell cycle is a temporal program that regulates DNA synthesis and cell division. When we compared the codon usage of cell cycle-regulated genes with that of other genes, we discovered that there is a significant preference for non-optimal codons. Moreover, genes encoding proteins that cycle at the protein level exhibit non-optimal codon preferences. Remarkably, cell cycle-regulated genes expressed in different phases display different codon preferences. Here, we show empirically that transfer RNA (tRNA) expression is indeed highest in the G2 phase of the cell cycle, consistent with the non-optimal codon usage of genes expressed at this time, and lowest toward the end of G1, reflecting the optimal codon usage of G1 genes. Accordingly, protein levels of human glycyl-, threonyl-, and glutamyl-prolyl tRNA synthetases were found to oscillate, peaking in G2/M phase. In light of our findings, we propose that non-optimal (wobbly) matching codons influence protein synthesis during the cell cycle. We describe a new mathematical model that shows how codon usage can give rise to cell-cycle regulation. In summary, our data indicate that cells exploit wobbling to generate cell cycle-dependent dynamics of proteins.",
keywords = "Arabidopsis, Base Sequence, Biological Clocks, Cell Cycle, Cell Cycle Proteins, Codon, Gene Expression Regulation, Genes, Genetic Code, Humans, Models, Biological, Models, Theoretical, Proteins, Saccharomyces cerevisiae, Schizosaccharomyces",
author = "Milana Frenkel-Morgenstern and Tamar Danon and Thomas Christian and Takao Igarashi and Lydia Cohen and Ya-Ming Hou and Jensen, {Lars Juhl}",
year = "2012",
doi = "10.1038/msb.2012.3",
language = "English",
volume = "8",
pages = "572",
journal = "Molecular Systems Biology",
issn = "1744-4292",
publisher = "Wiley-Blackwell",

}

RIS

TY - JOUR

T1 - Genes adopt non-optimal codon usage to generate cell cycle-dependent oscillations in protein levels

AU - Frenkel-Morgenstern, Milana

AU - Danon, Tamar

AU - Christian, Thomas

AU - Igarashi, Takao

AU - Cohen, Lydia

AU - Hou, Ya-Ming

AU - Jensen, Lars Juhl

PY - 2012

Y1 - 2012

N2 - The cell cycle is a temporal program that regulates DNA synthesis and cell division. When we compared the codon usage of cell cycle-regulated genes with that of other genes, we discovered that there is a significant preference for non-optimal codons. Moreover, genes encoding proteins that cycle at the protein level exhibit non-optimal codon preferences. Remarkably, cell cycle-regulated genes expressed in different phases display different codon preferences. Here, we show empirically that transfer RNA (tRNA) expression is indeed highest in the G2 phase of the cell cycle, consistent with the non-optimal codon usage of genes expressed at this time, and lowest toward the end of G1, reflecting the optimal codon usage of G1 genes. Accordingly, protein levels of human glycyl-, threonyl-, and glutamyl-prolyl tRNA synthetases were found to oscillate, peaking in G2/M phase. In light of our findings, we propose that non-optimal (wobbly) matching codons influence protein synthesis during the cell cycle. We describe a new mathematical model that shows how codon usage can give rise to cell-cycle regulation. In summary, our data indicate that cells exploit wobbling to generate cell cycle-dependent dynamics of proteins.

AB - The cell cycle is a temporal program that regulates DNA synthesis and cell division. When we compared the codon usage of cell cycle-regulated genes with that of other genes, we discovered that there is a significant preference for non-optimal codons. Moreover, genes encoding proteins that cycle at the protein level exhibit non-optimal codon preferences. Remarkably, cell cycle-regulated genes expressed in different phases display different codon preferences. Here, we show empirically that transfer RNA (tRNA) expression is indeed highest in the G2 phase of the cell cycle, consistent with the non-optimal codon usage of genes expressed at this time, and lowest toward the end of G1, reflecting the optimal codon usage of G1 genes. Accordingly, protein levels of human glycyl-, threonyl-, and glutamyl-prolyl tRNA synthetases were found to oscillate, peaking in G2/M phase. In light of our findings, we propose that non-optimal (wobbly) matching codons influence protein synthesis during the cell cycle. We describe a new mathematical model that shows how codon usage can give rise to cell-cycle regulation. In summary, our data indicate that cells exploit wobbling to generate cell cycle-dependent dynamics of proteins.

KW - Arabidopsis

KW - Base Sequence

KW - Biological Clocks

KW - Cell Cycle

KW - Cell Cycle Proteins

KW - Codon

KW - Gene Expression Regulation

KW - Genes

KW - Genetic Code

KW - Humans

KW - Models, Biological

KW - Models, Theoretical

KW - Proteins

KW - Saccharomyces cerevisiae

KW - Schizosaccharomyces

U2 - 10.1038/msb.2012.3

DO - 10.1038/msb.2012.3

M3 - Journal article

C2 - 22373820

VL - 8

SP - 572

JO - Molecular Systems Biology

JF - Molecular Systems Biology

SN - 1744-4292

ER -

ID: 40290716