An evolutionarily conserved mechanism for controlling the efficiency of protein translation

Tamir Tuller; Asaf Carmi; Kalin Vestsigian; Sivan Navon; Yuval Dorfan; John Zaborske; Tao Pan; Orna Dahan; Itay Furman; Yitzhak Pilpel

doi:10.1016/j.cell.2010.03.031

An evolutionarily conserved mechanism for controlling the efficiency of protein translation

Tamir Tuller, Asaf Carmi, Kalin Vestsigian, Sivan Navon, Yuval Dorfan, John Zaborske, Tao Pan, Orna Dahan, Itay Furman, Yitzhak Pilpel

Research output: Contribution to journal › Article › peer-review

656 Scopus citations

Abstract

Recent years have seen intensive progress in measuring protein translation. However, the contributions of coding sequences to the efficiency of the process remain unclear. Here, we identify a universally conserved profile of translation efficiency along mRNAs computed based on adaptation between coding sequences and the tRNA pool. In this profile, the first ∼30-50 codons are, on average, translated with a low efficiency. Additionally, in eukaryotes, the last ∼50 codons show the highest efficiency over the full coding sequence. The profile accurately predicts position-dependent ribosomal density along yeast genes. These data suggest that translation speed and, as a consequence, ribosomal density are encoded by coding sequences and the tRNA pool. We suggest that the slow " ramp" at the beginning of mRNAs serves as a late stage of translation initiation, forming an optimal and robust means to reduce ribosomal traffic jams, thus minimizing the cost of protein expression.

Original language	English
Pages (from-to)	344-354
Number of pages	11
Journal	Cell
Volume	141
Issue number	2
DOIs	https://doi.org/10.1016/j.cell.2010.03.031
State	Published - 16 Apr 2010
Externally published	Yes

Bibliographical note

Funding Information:
We thank the Pilpel lab and Chaim Kahana, Ran Kafri, Ron Milo, Uri Alon, Michael Springer, Jeremy Gunawardena, Eytan Ruppin, and Martin Kupiec for stimulating discussions and Orna Man for critically reading the manuscript. We thank the “Ideas” program of the European Research Council, EMBRACE Network of Excellence grant of the European Commission within its FP6 Programme, and the Ben May Charitable Trust for grant support. T.T. is a Koshland Scholar at the Weizmann Institute of Science.

Funding

We thank the Pilpel lab and Chaim Kahana, Ran Kafri, Ron Milo, Uri Alon, Michael Springer, Jeremy Gunawardena, Eytan Ruppin, and Martin Kupiec for stimulating discussions and Orna Man for critically reading the manuscript. We thank the “Ideas” program of the European Research Council, EMBRACE Network of Excellence grant of the European Commission within its FP6 Programme, and the Ben May Charitable Trust for grant support. T.T. is a Koshland Scholar at the Weizmann Institute of Science.

Funders	Funder number
FP6 Programme
National Institute of General Medical Sciences	T32GM007183
Ben May Charitable Trust
European Commission
European Commission

Keywords

Proteins

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10.1016/j.cell.2010.03.031

Cite this

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abstract = "Recent years have seen intensive progress in measuring protein translation. However, the contributions of coding sequences to the efficiency of the process remain unclear. Here, we identify a universally conserved profile of translation efficiency along mRNAs computed based on adaptation between coding sequences and the tRNA pool. In this profile, the first ∼30-50 codons are, on average, translated with a low efficiency. Additionally, in eukaryotes, the last ∼50 codons show the highest efficiency over the full coding sequence. The profile accurately predicts position-dependent ribosomal density along yeast genes. These data suggest that translation speed and, as a consequence, ribosomal density are encoded by coding sequences and the tRNA pool. We suggest that the slow {"} ramp{"} at the beginning of mRNAs serves as a late stage of translation initiation, forming an optimal and robust means to reduce ribosomal traffic jams, thus minimizing the cost of protein expression.",

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An evolutionarily conserved mechanism for controlling the efficiency of protein translation

Abstract

Bibliographical note

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Keywords

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