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Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins

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  • Clement T.Y. Chan

    (Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, USA.
    Massachusetts Institute of Technology
    Present address: Department of Biomedical Engineering, Boston University, 44 Cummington Street , MA 02215 , USA)

  • Yan Ling Joy Pang

    (Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, USA.)

  • Wenjun Deng

    (Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, USA.)

  • I. Ramesh Babu

    (Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, USA.)

  • Madhu Dyavaiah

    (College of Nanoscale Science and Engineering, University at Albany, SUNY)

  • Thomas J. Begley

    (College of Nanoscale Science and Engineering, University at Albany, SUNY)

  • Peter C. Dedon

    (Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, 02139, USA.
    Center for Environmental Health Sciences, Massachusetts Institute of Technology)

Abstract

Selective translation of survival proteins is an important facet of the cellular stress response. We recently demonstrated that this translational control involves a stress-specific reprogramming of modified ribonucleosides in tRNA. Here we report the discovery of a step-wise translational control mechanism responsible for survival following oxidative stress. In yeast exposed to hydrogen peroxide, there is a Trm4 methyltransferase-dependent increase in the proportion of tRNALeu(CAA) containing m5C at the wobble position, which causes selective translation of mRNA from genes enriched in the TTG codon. Of these genes, oxidative stress increases protein expression from the TTG-enriched ribosomal protein gene RPL22A, but not its unenriched paralogue. Loss of either TRM4 or RPL22A confers hypersensitivity to oxidative stress. Proteomic analysis reveals that oxidative stress causes a significant translational bias towards proteins coded by TTG-enriched genes. These results point to stress-induced reprogramming of tRNA modifications and consequential reprogramming of ribosomes in translational control of cell survival.

Suggested Citation

  • Clement T.Y. Chan & Yan Ling Joy Pang & Wenjun Deng & I. Ramesh Babu & Madhu Dyavaiah & Thomas J. Begley & Peter C. Dedon, 2012. "Reprogramming of tRNA modifications controls the oxidative stress response by codon-biased translation of proteins," Nature Communications, Nature, vol. 3(1), pages 1-9, January.
    • Handle: RePEc:nat:natcom:v:3:y:2012:i:1:d:10.1038_ncomms1938
    DOI: 10.1038/ncomms1938
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