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Domain 4:

Synthesis and Processing of Macromolecules

Modification of the Ribosome and the Translational Machinery during Reduced Growth Due to Environmental Stress

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  • Author: Antón Vila-Sanjurjo1
  • Editor: Susan T. Lovett2
  • VIEW AFFILIATIONS HIDE AFFILIATIONS
    Affiliations: 1: Berkeley Center for Synthetic Biology, University of California, Berkeley, Berkeley, CA 94720-3224; 2: Brandeis University, Waltham, MA
  • Received 17 December 2007 Accepted 19 February 2008 Published 25 July 2008
  • Address correspondence to Antón Vila-Sanjurjo avila@lbl.gov.
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  • Abstract:

    strains normally used under laboratory conditions have been selected for maximum growth rates and require maximum translation efficiency. Recent studies have shed light on the structural and functional changes undergone by the translational machinery in during heat and cold shock and upon entry into stationary phase. In these situations both the composition and the partitioning of this machinery into the different pools of cellular ribosomes are modified. As a result, the translational capacity of the cell is dramatically altered. This review provides a comprehensive account of these modifications, regardless of whether or not their underlying mechanisms and their effects on cellular physiology are known. Not only is the composition of the ribosome modified upon entry into stationary phase, but the modification of other components of the translational machinery, such as elongation factor Tu (EFTu) and tRNAs, has also been observed. Hibernation-promoting factor (HPF), paralog protein Y (PY), and ribosome modulation factor (RMF) may also be related to the general protection against environmental stress observed in stationary-phase cells, a role that would not be revealed necessarily by the viability assays. Even for the best-characterized ribosome-associated factors induced under stress (RMF, PY, and initiation factors), we are far from a complete understanding of their modes of action.

  • Citation: Vila-Sanjurjo A. 2008. Modification of the Ribosome and the Translational Machinery during Reduced Growth Due to Environmental Stress, EcoSal Plus 2008; doi:10.1128/ecosalplus.2.5.6

Key Concept Ranking

Elongation Factor Tu
0.45172527
Stationary Phase
0.42171493
Cold Shock Response
0.3742443
Heat Shock Response
0.37032548
RNA Polymerase
0.34057972
0.45172527

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/content/journal/ecosalplus/10.1128/ecosalplus.2.5.6
2008-07-25
2017-09-25

Abstract:

strains normally used under laboratory conditions have been selected for maximum growth rates and require maximum translation efficiency. Recent studies have shed light on the structural and functional changes undergone by the translational machinery in during heat and cold shock and upon entry into stationary phase. In these situations both the composition and the partitioning of this machinery into the different pools of cellular ribosomes are modified. As a result, the translational capacity of the cell is dramatically altered. This review provides a comprehensive account of these modifications, regardless of whether or not their underlying mechanisms and their effects on cellular physiology are known. Not only is the composition of the ribosome modified upon entry into stationary phase, but the modification of other components of the translational machinery, such as elongation factor Tu (EFTu) and tRNAs, has also been observed. Hibernation-promoting factor (HPF), paralog protein Y (PY), and ribosome modulation factor (RMF) may also be related to the general protection against environmental stress observed in stationary-phase cells, a role that would not be revealed necessarily by the viability assays. Even for the best-characterized ribosome-associated factors induced under stress (RMF, PY, and initiation factors), we are far from a complete understanding of their modes of action.

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Figures

Image of Figure 1
Figure 1

(B) Structure of the 70S ribosome in complex with PY (Protein Data Bank accession no. 1VOQ and 1VOR) A surface model of PY (red) bound in the intersubunit space of a 70S ribosome (30S subunit in yellow, 50S subunit in blue) is shown (C and D) Overlap of the binding sites for PY and A- and P-site tRNAs in the 30S subunit. The structures of the A (cyan)-, P (green)-, and E (grey)-site tRNAs were docked onto the structure of the 30S subunit (yellow) bound to PY (red; Protein Data Bank accession no. 1VOQ). Shown are two different views of the intersubunit face of the 30S subunit, with the landmark features, direction, and magnitude of rotation indicated. (E) Structure of Hsp15 (Protein Data Bank accession no. 1DM9). (F) Structure of CspA (Protein Data Bank accession no. 1MJC). (G) Structure of IF1 (Protein Data Bank accession no. 1AH9). (H) Structure of RbfA (Protein Data Bank accession no. 1KKG).

Citation: Vila-Sanjurjo A. 2008. Modification of the Ribosome and the Translational Machinery during Reduced Growth Due to Environmental Stress, EcoSal Plus 2008; doi:10.1128/ecosalplus.2.5.6
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Figure 2

(1) During exponential growth, most ribosomal particles are involved in protein synthesis and are found in the polysome pool, shown as strings of ribosomes at different stages of translation. P, A, and E sites on polysome ribosomes are indicated; mRNA is shown in red, with the 5′-AUG-3′ start codon indicated; and tRNAs and the nascent polypeptide chain are shown as indicated in the symbol legend on the right. In addition to polysomes, a small pool of free subunits and 70S ribosomes exists in the cell (the sedimentation coefficients are indicated for clarity). (2) In the transition to stationary phase (downward arrow from panel 1 to panel 3), proteins RMF (yellow square), PY (green), and HPF (shown as a red, tailless version of PY) are synthesized. (3) The binding of these proteins to ribosomes decreases the number of ribosomes found as polysomes. RMF-containing 90S particles appear at this stage. (4) The levels of the three proteins increase in stationary phase (downward arrow from panel 3 to panel 5), at which point (5) almost all the existing ribosomes are present as either HPF- and RMF-bound 100S particles or PY-bound 70S ribosomes. After a few days in stationary phase, the ribosomes are gradually degraded (not shown). (6) If optimal growth conditions are restored (upward arrow from panel 3 to panel 1), all three proteins are rapidly ejected from the ribosomes, which then become engaged in protein synthesis; i.e., they are found in polysomes.

Citation: Vila-Sanjurjo A. 2008. Modification of the Ribosome and the Translational Machinery during Reduced Growth Due to Environmental Stress, EcoSal Plus 2008; doi:10.1128/ecosalplus.2.5.6
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Figure 3

(1.1) Normal initiation occurs at 37°C (the normal growth temperature is shown as a yellow background). (1.2) The 30S subunit (with the A-, P-, and E-site tRNA binding sites indicated) binds the mRNA (with the 5′-AUG-3′ start codon indicated); the three initiation factors IF1, IF2-GTP in complex with fMet-tRNA, and IF3; and the 50S subunit to form a 70S initiation complex (the previous formation of a 30S initiation complex is not shown). (1.3) Polysomes form during elongation when several ribosomes translate the same mRNA (the peptide chain is shown as a string of white ovals). (2.1) Cold shock acclimation (the low temperature is indicated by a cyan background). Upon cold shock, the subunit/70S equilibrium shifts towards the formation of 70S ribosomes or monosomes (sedimentation coefficients are indicated for clarity). Shortly after cold shock, during acclimation, initiation factors (2.2) and PY (3.1) are expressed. Increased levels of initiation factors are required to dissociate cold-induced 70S ribosomes into the 30S and 50S subunits (2.3a and b) needed to form 30S initiation complexes both on CSF mRNAs (2.4) and on non-CSF mRNAs (2.7). 30S initiation complexes formed on CSF mRNAs (2.4) will result in productive 70S initiation complexes that can proceed to the elongation phase of translation, thus allowing the formation of polysome structures (2.5). These polysomes synthesize CSFs (2.6). This situation is in contrast to that for 30S initiation complexes formed on non-CSF mRNAs (2.7), which due to the discriminatory ability of IF3 in the cold, give rise to nonproductive 70S initiation complexes unable to proceed to the elongation phase of translation (indicated by a stop sign in panel 2.8). In the PY cycle, cold-induced 70S ribosomes (2.1) and free ribosomal subunits (2.1 and 2.3b) are substrates for the 70S ribosome-stabilizing function of the newly synthesized PY (3.1). As a consequence, PY-bound resting 70S ribosomes start accumulating in the cell (3.2). PY is known to compete in the cold with initiation factors and initiator tRNA for binding to ribosomes. As a result, PY may reduce the accumulation of stalled 70S initiation complexes formed on non-CSF mRNAS (3.3) by displacing initiation factors and initiator tRNAs (3.5). Since, in principle, PY could disrupt the process of initiation complex formation on any mRNA, this possibility is noted in panel 3.4, where red mRNAs represent both CSF and non-CSF transcripts being recruited into initiation complexes. The disruption of initiation complexes by PY in the cold would increase the fraction of PY-bound resting 70S ribosomes (3.2). (4.1) Post-acclimation phase (the end of acclimation is indicated by a broken line).

Upon growth resumption, at the end of acclimation, PY is released from resting 70S ribosomes and the pre-cold shock 70S ribosome-initiation factor balance is restored (not shown). The factor(s) triggering PY release remains unknown (as indicated by red question marks). (4.2) At the same time, the decreased levels of initiation factors allow polysome formation on non-CSF mRNAs, thus permitting cell growth in the cold. Also shown in panel 4.2 is the contribution of some CSFs to the translation of bulk mRNAs by acting as chaperones and/or helicases. (5.1) Return to 37°C during acclimation. Should the normal growth temperature be suddenly restored during acclimation, initiation factors can rapidly eject PY from the PY-bound, resting 70S ribosomes. (5.2) Because the discriminatory activity of IF3 against non-CSF mRNAs is no longer relevant at 37°C, initiation complexes can rapidly form on regular mRNAs, which are now competent to proceed to the elongation phase of translation.

Citation: Vila-Sanjurjo A. 2008. Modification of the Ribosome and the Translational Machinery during Reduced Growth Due to Environmental Stress, EcoSal Plus 2008; doi:10.1128/ecosalplus.2.5.6
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