Modulation of mRNA Stability Participates in Stationary-Phase-Specific Expression of Ribosome Modulation Factor

Aiso, Toshiko; Yoshida, Hideji; Wada, Akira; Ohki, Reiko

doi:10.1128/jb.187.6.1951-1958.2005

Cited by 51 publications

(63 citation statements)

References 41 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Dimerization of 70S ribosomes requires the ribosome modulation factor (Rmf) and is promoted by the hibernation-promoting factor (Hpf, previously called YhbH), both of which are specifically expressed during the stationary phase (Maki et al, 2000;Ueta et al, 2005). When cells in the stationary phase are transferred to fresh medium, Rmf and Hpf are immediately released from the 100S ribosomes, as a result of which 100S ribosomes dissociate and form active 70S ribosomes (Aiso et al, 2005;Ueta et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis

et al. 2016

View full text Add to dashboard Cite

Ribosome dimers are a translationally inactive form of ribosomes found in Escherichia coli and many other bacterial cells. In this study, we found that the 70S ribosomes of Bacillus subtilis dimerized during the early stationary phase and these dimers remained in the cytoplasm until regrowth was initiated. Ribosome dimerization during the stationary phase required the hpf gene, which encodes a homologue of the E. coli hibernation-promoting factor (Hpf). The expression of hpf was induced at an early stationary phase and its expression was observed throughout the rest of the experimental period, including the entire 6 h of the stationary phase. Ribosome dimerization followed the induction of hpf in WT cells, but the dimerization was impaired in cells harbouring a deletion in the hpf gene. Although the absence of ribosome dimerization in these Hpf-deficient cells did not affect their viability in the stationary phase, their ability to regrow from the stationary phase decreased. Thus, following the transfer of stationary-phase cells to fresh LB medium, Dhpf mutant cells grew slower than WT cells. This observed lag in growth of Dhpf cells was probably due to a delay in restoring their translational activity. During regrowth, the abundance of ribosome dimers in WT cells decreased with a concomitant increase in the abundance of 70S ribosomes and growth rate. These results suggest that the ribosome dimers, by providing 70S ribosomes to the cells, play an important role in facilitating rapid and efficient regrowth of cells under nutrient-rich conditions.

show abstract

Section: Introductionmentioning

confidence: 99%

Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis

et al. 2016

View full text Add to dashboard Cite

show abstract

“…E. coli also possesses an HPF paralog (referred to as YfiA or pY or RaiA) that silences the 70S ribosome (27-29) and antagonizes the formation of the 100S complex (21, 23). YfiA is absent from Firmicutes and the majority of bacteria but is functionally homologous to PSRP1 in plant chloroplasts (30,31).The two 70S monomers in the 100S complex are not irreversibly interlocked; instead, the disassembly of the E. coli 100S ribosome can occur within 1 min after transferring the aged culture into fresh medium (16,32). The 100S ribosomes connected by the long-form HPFs in Firmicutes are more stable by one order of magnitude than the ones generated by the short-form HPF and RMF (2, 14).…”

mentioning

confidence: 99%

“…The two 70S monomers in the 100S complex are not irreversibly interlocked; instead, the disassembly of the E. coli 100S ribosome can occur within 1 min after transferring the aged culture into fresh medium (16,32). The 100S ribosomes connected by the long-form HPFs in Firmicutes are more stable by one order of magnitude than the ones generated by the short-form HPF and RMF (2, 14).…”

mentioning

confidence: 99%

Disassembly of theStaphylococcus aureushibernating 100S ribosome by an evolutionarily conserved GTPase

Basu

Yap

2017

Proc. Natl. Acad. Sci. U.S.A.

View full text Add to dashboard Cite

The bacterial hibernating 100S ribosome is a poorly understood form of the dimeric 70S particle that has been linked to pathogenesis, translational repression, starvation responses, and ribosome turnover. In the opportunistic pathogen Staphylococcus aureus and most other bacteria, hibernation-promoting factor (HPF) homodimerizes the 70S ribosomes to form a translationally silent 100S complex. Conversely, the 100S ribosomes dissociate into subunits and are presumably recycled for new rounds of translation. The regulation and disassembly of the 100S ribosome are largely unknown because the temporal abundance of the 100S ribosome varies considerably among different bacterial phyla. Here, we identify a universally conserved GTPase (HflX) as a bona fide dissociation factor of the S. aureus 100S ribosome. The expression levels hpf and hflX are coregulated by general stress and stringent responses in a temperature-dependent manner. While all tested guanosine analogs stimulate the splitting activity of HflX on the 70S ribosome, only GTP can completely dissociate the 100S ribosome. Our results reveal the antagonistic relationship of HPF and HflX and uncover the key regulators of 70S and 100S ribosome homeostasis that are intimately associated with bacterial survival.T he biogenesis and function of bacterial 30S and 50S ribosomal subunits and the 70S complex have been studied extensively, but the significance of the 100S ribosome (homodimeric 70S) has only begun to emerge in recent years (1). The 100S ribosome is ubiquitously found in all bacterial phyla and is important for bacterial survival during nutrient limitation (2-6), antibiotic stress (7), host colonization (8), dark adaptation (9), and biofilm formation (10, 11). A common feature of these biological processes is that cells generally conserve energy by undergoing metabolic and translational dormancy because protein synthesis accounts for >50% of energy costs (12, 13). The dimerization of 70S ribosomes has been shown to down-regulate translational efficiency in vivo (3) and in vitro (3,14), and bacteria lacking 100S ribosomes are prone to early cell death concomitant with rapid ribosome degradation (3,10,15,16). These studies lead to a model whereby the formation of the 100S complex sequesters the ribosome pool away from active translation, and 70S self-dimerization prevents ribosome degradation by an unknown pathway (3,17). During the stationary phase, the 100S ribosomes are presumably dissociated and reused for new cycles of translation, thereby maintaining cell viability (1,3,16,18). The process and dissociation factors involved in the reversible transition of silent 100S to a translationally competent 70S ribosome remain poorly understood.By contrast, the 70S dimerizing factor has been characterized in many bacterial species (1,2,4,14). In Firmicutes (such as Staphylococcus aureus and Bacillus subtilis), a single long form of hibernation-promoting factor (HPF) provides the binding platform to conjoin the 30S subunits of the two 70S monomers via a direct inter...

show abstract

“…Changes in global patterns of gene expression in the stationary growth phase in organisms such as Escherichia coli involve drastic changes in cellular machineries, including changes in nucleoid conformation, transcription apparatus, and translation machinery (5, 9). From the variety of changes in the bacterial cell, we focused our attention on ribosomal changes in E. coli cells during transition from the exponential to the stationary phase (1,14). Ribosomes are universally conserved ribonucleoproteins and are comprised of two asymmetric subunits.…”

mentioning

confidence: 99%

YqjD Is an Inner Membrane Protein Associated with Stationary-Phase Ribosomes in Escherichia coli

et al. 2012

Self Cite

View full text Add to dashboard Cite

Here, we provide evidence that YqjD, a hypothetical protein of Escherichia coli, is an inner membrane and ribosome binding protein. This protein is expressed during the stationary growth phase, and expression is regulated by stress response sigma factor RpoS. YqjD possesses a transmembrane motif in the C-terminal region and associates with 70S and 100S ribosomes at the N-terminal region. Interestingly, E. coli possesses two paralogous proteins of YqjD, ElaB and YgaM, which are expressed and bind to ribosomes in a similar manner to YqjD. Overexpression of YqjD leads to inhibition of cell growth. It has been suggested that YqjD loses ribosomal activity and localizes ribosomes to the membrane during the stationary phase. In nature, bacteria survive in various environments, usually under stress conditions including nutrient starvation, temperature shock, osmolarity changes, and sudden changes in pH. For prolonged survival under such conditions, ordered expression of many stringent-response genes is required. The expression patterns of a large fraction of genes on the genome are altered by turning off or reducing expression of growth-related genes while switching on a set of genes that are required for adaptation to the specific stress condition. Changes in global patterns of gene expression in the stationary growth phase in organisms such as Escherichia coli involve drastic changes in cellular machineries, including changes in nucleoid conformation, transcription apparatus, and translation machinery (5, 9). From the variety of changes in the bacterial cell, we focused our attention on ribosomal changes in E. coli cells during transition from the exponential to the stationary phase (1,14). Ribosomes are universally conserved ribonucleoproteins and are comprised of two asymmetric subunits. In bacteria, large (50S) and small (30S) subunits associate to form functional 70S ribosomes. Ribosomes can account for as much as 45% of the total mass of bacterial cells in organisms such as E. coli during the exponential phase and actively synthesize all of the cellular proteins required. However, in cells under stress conditions, such as starvation, it has been shown that ribosomal biosynthesis is repressed and that protein synthesis is also suppressed. These systems, which allow translational regulation, are very important for bacteria to survive in harsh environments.In eukaryotes, it is known that phosphorylation of initiation factor 2␣ (eIF2␣) is an adaptive mechanism for downregulating protein synthesis under stress conditions (7). In the Gammaproteobacteria, which includes E. coli, protein synthesis is mainly suppressed by the formation of 100S ribosomes (21). The 100S ribosome is a dimer of 70S ribosomes which is formed by the binding of ribosome modulation factor (RMF) to ribosomes (13). RMF is a small (M r of 6,507), basic (pI 11.3) protein, and its expression increases remarkably during transition from the exponential phase to the stationary phase. Another protein factor expressed during the stationary phase, hibernati...

show abstract

Modulation of mRNA Stability Participates in Stationary-Phase-Specific Expression of Ribosome Modulation Factor

Cited by 51 publications

References 41 publications

Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis

Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis

Disassembly of theStaphylococcus aureushibernating 100S ribosome by an evolutionarily conserved GTPase

YqjD Is an Inner Membrane Protein Associated with Stationary-Phase Ribosomes in Escherichia coli

Contact Info

Product

Resources

About