DOI: 10.1038/embor.2009.255. Transfer–messenger RNA controls the translation of cell‐cycle and stress proteins in <i>Streptomyces</i>

Transfer–messenger RNA controls the translation of cell‐cycle and stress proteins in Streptomyces

10.1038/embor.2009.255

Crossref journal-article

Springer Science and Business Media LLC

EMBO reports (297)

Abstract

The transfer–messenger RNA (tmRNA)‐mediated trans‐translation mechanism is highly conserved in bacteria and functions primarily as a system for the rescue of stalled ribosomes and the removal of aberrantly produced proteins. Here, we show that in the antibiotic‐producing soil bacterium Streptomyces coelicolor, trans‐translation has a specialized role in stress management. Analysis of proteins that were carboxy‐terminally His8‐tagged by a recombinant tmRNA identified only 10 targets, including the stress proteins: DnaK heat‐shock protein 70, thiostrepton‐induced protein A, universal stress protein A, elongation factor Tu3, and the cell‐cycle control proteins DasR, SsgA, SsgF and SsgR. Although tmRNA‐tagged proteins are degraded swiftly, the translation of dnaK and dasR messenger RNAs (mRNAs) depends fully on tmRNA, whereas transcription is unaffected. The data unveil a surprisingly dedicated functionality for tmRNA, promoting the translation of the same mRNA it targets, at the expense of sacrificing the first nascent protein. In streptomycetes, tmRNA has evolved into a dedicated task force that ensures the instantaneous response to the exposure to stress.

Bibliography

Barends, S., Zehl, M., Bialek, S., de Waal, E., Traag, B. A., Willemse, J., Jensen, O. N., Vijgenboom, E., & van Wezel, G. P. (2009). Transferâmessenger RNA controls the translation of cellâcycle and stress proteins in Streptomyces. EMBO Reports, 11(2), 119â125. Portico.

Authors 9

Sharief Barends (first)
Martin Zehl (additional)
Sylwia Bialek (additional)
Ellen de Waal (additional)
Bjørn A Traag (additional)
Joost Willemse (additional)
Ole Nørregaard Jensen (additional)
Erik Vijgenboom (additional)
Gilles P van Wezel (additional)

References 33 Referenced 20

10.1093/emboj/19.14.3762
10.1074/mcp.M600007-MCP200
10.1007/s00203-005-0051-y
10.1046/j.1365-2958.2003.03696.x
10.1038/nrmicro1968
10.1101/gad.1219204
10.1126/science.276.5311.431
10.1093/emboj/cdg181
10.1038/75843 / Nat Struct Biol / The SsrA–SmpB system for protein tagging, directed degradation and ribosome rescue by Karzai AW (2000)
10.1128/JB.185.6.1825-1830.2003
10.1126/science.271.5251.990
KieserT BibbMJ ButtnerMJ ChaterKF HopwoodDA(2000)Practical Streptomyces Genetics. Norwich UK: John Innes Foundation
10.1261/rna.2212606
10.1146/annurev.biochem.75.103004.142733
10.1111/j.1365-2958.2007.05732.x
10.1111/j.1365-2958.2005.04883.x
10.1111/j.1365-2958.1992.tb01774.x
10.1046/j.1365-2958.2001.02675.x
10.1007/BF02931615
10.1128/JB.01838-06
10.1016/0092-8674(95)90164-7
10.1111/j.1365-2958.2006.05319.x
10.1038/embor.2008.83
10.1074/jbc.M103864200
SambrookJ FritschEF ManiatisT(1989)Molecular Cloning: A Laboratory Manual. Cold Spring Harbor NY USA: Cold Spring Harbor Laboratory Press
10.1074/jbc.M312805200
10.1111/j.1365-2958.2004.04186.x
10.1016/0167-4781(94)90085-X
10.1099/13500872-141-10-2519
10.1128/JB.182.20.5653-5662.2000
10.1159/000096461
10.1038/350165a0
10.1371/journal.pone.0004459

Dates

Type	When
Created	15 years, 8 months ago (Dec. 18, 2009, 6:32 a.m.)
Deposited	1 year, 8 months ago (Dec. 18, 2023, 3:58 p.m.)
Indexed	1 month, 2 weeks ago (July 19, 2025, 11:54 p.m.)
Issued	15 years, 8 months ago (Dec. 18, 2009)
Published	15 years, 8 months ago (Dec. 18, 2009)
Published Online	15 years, 8 months ago (Dec. 18, 2009)
Published Print	15 years, 7 months ago (Feb. 1, 2010)

Funders 0

None

BibTeX

@article{Barends_2009, title={Transfer–messenger RNA controls the translation of cell‐cycle and stress proteins in Streptomyces}, volume={11}, ISSN={1469-3178}, url={http://dx.doi.org/10.1038/embor.2009.255}, DOI={10.1038/embor.2009.255}, number={2}, journal={EMBO reports}, publisher={Springer Science and Business Media LLC}, author={Barends, Sharief and Zehl, Martin and Bialek, Sylwia and de Waal, Ellen and Traag, Bjørn A and Willemse, Joost and Jensen, Ole Nørregaard and Vijgenboom, Erik and van Wezel, Gilles P}, year={2009}, month=dec, pages={119–125} }

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