The lon gene, encoding an ATP-dependent protease, is a novel member of the HAIR/HspR stress-response regulon in actinomycetes

Sobczyk, André; Bellier, Audrey; Viala, Julie; Mazodier, Philippe

doi:10.1099/00221287-148-6-1931

Cited by 20 publications

(21 citation statements)

References 33 publications

(28 reference statements)

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“…Therefore, the levels of ATP-dependent proteases in the cell seem to require fine tuning, combining transcriptional and post-translational regulation. This is in agreement with the control of lon expression by both ClgR and HspR (Sobczyk et al, 2002), probably allowing a flexible response to a variety of signals.…”

Section: Discussionsupporting

confidence: 69%

Post-translational control of the Streptomyces lividans ClgR regulon by ClpP

2006

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It has been shown previously that expression of the Streptomyces lividans clpP1P2 operon, encoding proteolytic subunits of the Clp complex, the clpC1 gene, encoding the ATPase subunit, and the lon gene, encoding another ATP-dependent protease, are all activated by ClgR. The ClgR regulon also includes the clgR gene itself. It is shown here that the degradation of ClgR and Lon is ClpP1/P2-dependent and that the two C-terminal alanines of these new substrates are involved in their stability. The ClpC1 protein, which does not end with two alanines, is also accumulated in a clpP1P2 mutant. The results presented here support the idea that ClpP1/P2 ensure post-translational control of ClgR regulon members, including ClgR itself.

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Section: Discussionsupporting

confidence: 69%

Post-translational control of the Streptomyces lividans ClgR regulon by ClpP

2006

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“…These conserved structural motifs are probably recognized by the HspR repressor also present in the T. whipplei dnaK regulon. While a few examples of the HspR repressor-HAIR operator system have been described for gram-positive bacteria, such a regulation mechanism is widespread in actinomycetes (18,52) and has also been found recently in Deinococcus radiodurans (49) and C. jejuni (1). Of note is the fact that HSP themselves can participate in the regulation process.…”

Section: Vol 188 2006mentioning

confidence: 99%

“…Another DNA sequence, the HspRassociated inverted repeat (HAIR motif), was described as a regulon under the control of HspR (50). This regulon has been found mainly in high-GϩC-content gram-positive bacteria, particularly actinomycetes (52). HSP are classified according to their regulation characteristics, which differ for each bacterial species.…”

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Global Transcriptome Analysis ofTropheryma whippleiin Response to Temperature Stresses

et al. 2006

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Tropheryma whipplei, the agent responsible for Whipple disease, is a poorly known pathogen suspected to have an environmental origin. The availability of the sequence of the 0.92-Mb genome of this organism made a global gene expression analysis in response to thermal stresses feasible, which resulted in unique transcription profiles. A few genes were differentially transcribed after 15 min of exposure at 43°C. The effects observed included up-regulation of the dnaK regulon, which is composed of six genes and is likely to be under control of two HspR-associated inverted repeats (HAIR motifs) found in the 5 region. Putative virulence factors, like the RibC and IspDF proteins, were also overexpressed. While it was not affected much by heat shock, the T. whipplei transcriptome was strongly modified following cold shock at 4°C. For the 149 genes that were differentially transcribed, eight regulons were identified, and one of them was composed of five genes exhibiting similarity with genes encoding ABC transporters. Up-regulation of these genes suggested that there was an increase in nutrient uptake when the bacterium was exposed to cold stress. As observed for other bacterial species, the major classes of differentially transcribed genes encode membrane proteins and enzymes involved in fatty acid biosynthesis, indicating that membrane modifications are critical. Paradoxically, the heat shock proteins GroEL2 and ClpP1 were up-regulated. Altogether, the data show that despite the lack of classical regulation pathways, T. whipplei exhibits an adaptive response to thermal stresses which is consistent with its specific environmental origin and could allow survival under cold conditions.

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“…The role of the Lon and Clp proteases in the Streptomyces lividans differentiation cycle was investigated. The Lon protease does not seem to play a major role in Streptomyces differentiation (33), whereas the first clpP operon (clpP1 clpP2) has been shown to be required for a normal cell cycle, since a clpP1 mutant presents a bald phenotype (8).…”

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“…In the model organisms E. coli and B. subtilis, lon is heat induced (7,29). In S. lividans, lon is also heat induced, since it is repressed under non-heat shock conditions via the regulator HspR, which binds to the HspRassociated inverted repeat (HAIR) operator sequence (33).…”

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ClgR, a Novel Regulator of clp and lon Expression in Streptomyces

Bellier

Mazodier

2004

J Bacteriol

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The clp genes encoding the Clp proteolytic complex are widespread among living organisms. Five clpP genes are present in Streptomyces. Among them, the clpP1 clpP2 operon has been shown to be involved in the Streptomyces growth cycle, as a mutation blocked differentiation at the substrate mycelium step. Four Clp ATPases have been identified in Streptomyces coelicolor (ClpX and three ClpC proteins) which are potential partners of ClpP1 ClpP2. The clpC1 gene appears to be essential, since no mutant has yet been obtained. clpP1 clpP2 and clpC1 are important for Streptomyces growth, and a study of their regulation is reported here. The clpP3 clpP4 operon, which has been studied in Streptomyces lividans, is induced in a clpP1 mutant strain, and regulation of its expression is mediated via PopR, a transcriptional regulator. We report here studies of clgR, a paralogue of popR, in S. lividans. Gel mobility shift assays and DNase I footprinting indicate that ClgR binds not only to the clpP1 and clpC1 promoters, but also to the promoter of the Lon ATP-dependent protease gene and the clgR promoter itself. ClgR recognizes the motif GTTCGC-5N-GCG. In vivo, ClgR acts as an activator of clpC1 gene and clpP1 operon expression. Similarly to PopR, ClgR degradation might be ClpP dependent and could be mediated via recognition of the two carboxy-terminal alanine residues.The temporally coordinated presence of various bacterial regulators has been shown to be essential for coordination of life cycle events (10), and this temporal control is often achieved via specific degradation (19) involving several proteins, including ATP-dependent proteases. Different families of ATP-dependent proteases have been characterized in bacteria: Clp (ClpAP and ClpXP), HslUV (ClpYQ), FtsH, and the Lon family (Lon). These proteases are large multisubunit complexes. The ATPase domains, which confer substrate specificity, denature and translocate substrates into the proteolytic chamber for degradation. The polypeptide chain Lon contains these two different activities on the same polypeptide chain. In contrast, Clp proteases contain two different subunits: the ATPase subunit (ClpX, ClpA, or ClpC) and the proteolytic subunit (ClpP), which contains a consensus serine protease active site (14).clpP genes are generally present as single copies in eubacteria, but some organisms possess a multigenic clpP family. For example, two clpP genes are present in Bacillus thuringiensis (11) and in Mycobacterium tuberculosis, four genes are present in the cyanobacterium Synechococystis (32), and five genes are present in Streptomyces coelicolor. In S. coelicolor, the clpP genes are organized as two bicistronic operons and one monocistronic gene, all located at different sites on the chromosome. In S. coelicolor, there are three monocistronic clpC genes and one clpX gene, which follows the clpP1 operon. Streptomyces is the first genus with a multigenic clpC family that has been reported.Streptomyces, a gram-positive soil bacterium with high GϩC content, is a model of bacte...

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The lon gene, encoding an ATP-dependent protease, is a novel member of the HAIR/HspR stress-response regulon in actinomycetes

Cited by 20 publications

References 33 publications

Post-translational control of the Streptomyces lividans ClgR regulon by ClpP

Post-translational control of the Streptomyces lividans ClgR regulon by ClpP

Global Transcriptome Analysis ofTropheryma whippleiin Response to Temperature Stresses

ClgR, a Novel Regulator of clp and lon Expression in Streptomyces

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