Preferential translation of cold-shock mRNAs during cold adaptation
Open Access
- 16 January 2004
- journal article
- research article
- Published by Cold Spring Harbor Laboratory in RNA
- Vol. 10 (2), 265-276
- https://doi.org/10.1261/rna.5164904
Abstract
Upon temperature downshift below the lower threshold of balanced growth (~20°C), the Escherichia coli translational apparatus undergoes modifications allowing the selective translation of the transcripts of cold shock-induced genes, while bulk protein synthesis is drastically reduced. Here we were able to reproduce this translational bias in E. coli cell-free extracts prepared at various times during cold adaptation which were found to display different capacities to translate different types of mRNAs as a function of temperature. Several causes were found to contribute to the cold-shock translational bias: Cold-shock mRNAs contain cis-elements, making them intrinsically more prone to being translated in the cold, and they are selective targets for trans-acting factors present in increased amounts in the translational apparatus of cold-shocked cells. CspA was found to be among these trans-acting factors. In addition to inducing a higher level of CspA, cold shock was found to cause a strong (two- to threefold) stoichiometric imbalance of the ratio between initiation factors (IF1, IF2, IF3) and ribosomes without altering the stoichiometric ratio between the factors themselves. The most important sources of cold-shock translational bias is IF3, which strongly and selectively favors translation of cold-shock mRNAs in the cold. IF1 and the RNA chaperone CspA, which stimulate translation preferentially in the cold without mRNA selectivity, can also contribute to the translational bias. Finally, in contrast to a previous claim, translation of cold-shock cspA mRNA in the cold was found to be as sensitive as that of a non-cold-shock mRNA to both chloramphenicol and kanamycin inhibition.Keywords
This publication has 21 references indexed in Scilit:
- Selective expression of the β‐subunit of nucleoid‐associated protein HU during cold shock in Escherichia coliMolecular Microbiology, 2002
- Different in vivo localization of theEscherichia coliproteins CspD and CspAFEMS Microbiology Letters, 2001
- Variation in HU composition during growth of Escherichia coli: the heterodimer is required for long term survivalJournal of Molecular Biology, 1997
- CspA, the Major Cold-shock Protein of Escherichia coli, Is an RNA ChaperoneJournal of Biological Chemistry, 1997
- Complete growth inhibition of Escherichia coli by ribosome trapping with truncated cspA mRNA at low temperatureGenes to Cells, 1996
- Post‐transcriptional regulation of CspA expression in Escherichia coliMolecular Microbiology, 1996
- The cold‐shock response — a hot topicMolecular Microbiology, 1994
- Identification of a cold shock transcriptional enhancer of the Escherichia coli gene encoding nucleoid protein H-NS.Proceedings of the National Academy of Sciences of the United States of America, 1991
- Major cold shock protein of Escherichia coli.Proceedings of the National Academy of Sciences, 1990
- Chemical synthesis and in vivo hyperexpression of a modular gene coding for Escherichia coli translational initiation factor IF1Molecular Genetics and Genomics, 1987