Staphylococcus aureus ClpC ATPase is a late growth phase effector of metabolism and persistence

Proteomics

Volumn 9, Issue 5, 2009, Pages 1152-1176

  Chatterjee, Indranil ^a   Schmitt, Sigrid ^b   Batzilla, Christoph F ^c   Engelmann, Susanne ^d   Keller, Andreas ^e   Ring, Michael W ^e   Kautenburger, Ralf ^e   Ziebuhr, Wilma ^c   Hecker, Michael ^d   Preissner, Klaus T ^b   Bischoff, Markus ^a   Proctor, Richard A ^f   Beck, Horst P ^e   Lenhof, Hans Peter ^e   Somerville, Greg A ^g   Herrmann, Mathias ^a  

^a SAARLAND UNIVERSITY   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

^c UNIVERSITY OF WÜRZBURG   (Germany)

^d UNIVERSITY OF GREIFSWALD   (Germany)

^e SAARLAND UNIVERSITY   (Germany)

^f UNIVERSITY OF WISCONSIN MADISON   (United States)

^g UNIVERSITY OF NEBRASKA LINCOLN   (United States)

Author keywords

ClpC; Metabolism; Persistence; Staphylococcus aureus; Tricarboxylic acid cycle

Indexed keywords

ABC TRANSPORTER; ACONITATE HYDRATASE; ALANINE DEHYDROGENASE; CARBON; DNA TOPOISOMERASE (ATP HYDROLYSING) B; DNA TOPOISOMERASE IV; FATTY ACID; FERREDOXIN; FERRIC UPTAKE REGULATOR; FERRITIN; FORMATE DEHYDROGENASE; FRUCTOSE BISPHOSPHATASE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLUTATHIONE PEROXIDASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCINE HYDROXYMETHYLTRANSFERASE; HEAT SHOCK PROTEIN 100; HEAT SHOCK PROTEIN 60; MALIC ACID; METAL ION; METHIONINE SULFOXIDE REDUCTASE A; NICOTINAMIDASE; PHOSPHOGLUCONATE DEHYDROGENASE; PROTEIN DNAJ; PYRUVIC ACID; RECF PROTEIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; SUCCINATE DEHYDROGENASE; THIOREDOXIN; UNINDEXED DRUG;

APOPTOSIS; ARTICLE; BACTERIAL GROWTH; BACTERIAL SURVIVAL; CARBON METABOLISM; DNA MICROARRAY; ELECTRON TRANSPORT; ENERGY METABOLISM; FATTY ACID METABOLISM; GENE EXPRESSION; GLUCONEOGENESIS; HOMEOSTASIS; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE METABOLISM; OXIDATIVE STRESS; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN METABOLISM; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; CARBON; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, BACTERIAL; HEAT-SHOCK PROTEINS; METABOLIC NETWORKS AND PATHWAYS; PHENOTYPE; STAPHYLOCOCCUS AUREUS; TIME FACTORS;

STAPHYLOCOCCUS AUREUS;

EID: 63049093299     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200800586     Document Type: Article

References (61)

1. Frees, D., Sorensen, K., Ingmer, H., Global virulence regulation in Staphylococcus aureus: Pinpointing the roles of ClpP and ClpX in the sar/agr regulatory network. Infect. Immun. 2005, 73, 8100-8108.
2. Frees, D., Chastanet, A., Qazi, S., Sorensen, K. et al., Clp ATPases are required for stress tolerance, intracellular replication and biofilm formation in Staphylococcus aureus. Mol. Microbiol. 2004, 54, 1445-1462.
3. Michel, A., Agerer, F., Hauck, C. R., Herrmann, M. et al., Global regulatory impact of ClpP protease of Staphylococcus aureus on regulons involved in virulence, oxidative stress response, autolysis, and DNA repair. J. Bacteriol. 2006, 188, 5783-5796.
4. Bore, E., Langsrud, S., Langsrud, O., Rode, T. M. et al., Acid-shock responses in Staphylococcus aureus investigated by global gene expression analysis. Microbiology 2007, 153, 2289-2303.
5. Mascio, C. T., Alder, J. D., Silverman, J. A., Bactericidal action of daptomycin against stationary-phase and non-dividing Staphylococcus aureus cells. Antimicrob. Agents Chemother. 2007, 51, 4255-4260.
6. Manteca, A., Mader, U., Connolly, B. A., Sanchez, J., A proteomic analysis of Streptomyces coelicolor programmed cell death. Proteomics 2006, 6, 6008-6022.
7. Goff, S. A., Goldberg, A. L., Production of abnormal proteins in E. coli stimulates transcription of lon and other heat shock genes. Cell 1985, 41, 587-595.
8. Gerth, U., Kock, H., Kusters, I., Michalik, S. et al., Clp-dependent proteolysis down-regulates central metabolic pathways in glucose-starved Bacillus subtilis. J. Bacteriol. 2008, 190, 321-331.
9. Chatterjee, I., Becker, P., Grundmeier, M., Bischoff, M. et al., Staphylococcus aureus ClpC is required for stress resistance, aconitase activity, growth recovery, and death. J. Bacteriol. 2005, 187, 4488-4496.
10. Chatterjee, I., Herrmann, M., Proctor, R. A., Peters, G. et al., Enhanced post-stationary-phase survival of a clinical thymidine-dependent small-colony variant of Staphylococcus aureus results from lack of a functional tricarboxylic acid cycle. J. Bacteriol. 2007, 189, 2936-2940.
11. Chatterjee, I., Kriegeskorte, A., Fischer, A., Deiwick, S. et al., In vivo mutations of thymidylate synthase (encoded by thyA) are responsible for thymidine dependency in clinical small-colony variants of Staphylococcus aureus. J. Bacteriol. 2008, 190, 834-842.
12. Gorg, A., Obermaier, C., Boguth, G., Harder, A. et al., The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 2000, 21, 1037-1053.
13. Stensballe, A., Jensen, O. N., Phosphoric acid enhances the performance of Fe(III) affinity chromatography and matrix-assisted laser desorption/ionization tandem mass spectrometry for recovery, detection and sequencing of phosphopeptides. Rapid Commun. Mass Spectrom. 2004, 18, 1721-1730.
14. Somerville, G. A., Cockayne, A., Dürr, M., Peschel, A. et al., Synthesis and deformylation of Staphylococcus aureus δ-toxin are linked to tricarboxylic acid cycle activity. J. Bacteriol. 2003, 185, 6686-6694.
15. Bode, H. B., Ring, M. W., Schwar, G., Kroppenstedt, R. M. et al., 3-Hydroxy-3-methylglutaryl-coenzyme A (CoA) synthase is involved in biosynthesis of isovaleryl-CoA in the myxobacterium Myxococcus xanthus during fruiting body formation. J. Bacteriol. 2006, 188, 6524-6528.
16. Backes, C., Keller, A., Kuentzer, J., Kneissl, B. et al., Genetrail-advanced gene set enrichment analysis. Nucleic Acids Res. 2007, 35, W186-W192.
17. Goto, S., Bono, H., Ogata, H., Fujibuchi, W. et al., Organizing and computing metabolic pathway data in terms of binary relations. Pac. Symp. Biocomput. 1997, 175-186.
18. Ogata, H., Goto, S., Sato, K., Fujibuchi, W. et al., KEGG: Kyoto encyclopedia of genes and genomes. Nucleic Acids Res. 1999, 27, 29-34.
19. Keller, A., Backes, C., Lenhof, H. P., Computation of significance scores of unweighted gene set enrichment analyses. BMC Bioinformatics 2007, 8, 290.
20. Kunst, F., Ogasawara, N., Moszer, I., Albertini, A. M. et al., The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 1997, 390, 249-256.
21. Beenken, K. E., Dunman, P. M., McAleese, F., Macapagal, D. et al., Global gene expression in Staphylococcus aureus biofilms. J. Bacteriol. 2004, 186, 4665-4684.
22. Vuong, C., Kidder, J. B., Jacobson, E. R., Otto, M. et al., Staphylococcus epidermidis polysaccharide intercellular adhesin production significantly increases during tricarboxylic acid cycle stress. J. Bacteriol. 2005, 187, 2967-2973.
23. Nelson, J. L., Rice, K. C., Slater, S. R., Fox, P. M. et al., Vancomycin-intermediate Staphylococcus aureus strains have impaired acetate catabolism: Implications for polysaccharide intercellular adhesin synthesis and autolysis. Antimicrob. Agents Chemother. 2007, 51, 616-622.
24. Eymann, C., Homuth, G., Scharf, C., Hecker, M., Bacillus subtilis functional genomics: Global characterization of the stringent response by proteome and transcriptome analysis. J. Bacteriol. 2002, 184, 2500-2520.
25. Baracchini, E., Bremer, H., Stringent and growth control of rRNA synthesis in Escherichia coli are both mediated by ppGpp. J. Biol. Chem. 1988, 263, 2597-2602.
26. Kazakov, A. E., Vassieva, O., Gelfand, M. S., Osterman, A. et al., Bioinformatics classification and functional analysis of PhoH homologs. In Silico Biol. 2003, 3, 3-15.
27. Cashel, M., Gentry, D. R., Hernandez, V. J., Vinella, D., Escherichia Coli and Salmonella: Cellular and Molecular Biology, ASM Press, Washington DC 1996.
28. Magnusson, L. U., Nystrom, T., Farewell, A., Underproduction of sigma 70 mimics a stringent response. A proteome approach. J. Biol. Chem. 2003, 278, 968-973.
29. Nystrom, T., Neidhardt, F. C., Cloning, mapping and nucleotide sequencing of a gene encoding a universal stress protein in Escherichia coli. Mol. Microbiol. 1992, 6, 3187-3198.
30. Kvint, K., Hosbond, C., Farewell, A., Nybroe, O. et al., Emergency derepression: Stringency allows RNA polymerase to override negative control by an active repressor. Mol. Microbiol. 2000, 35, 435-443.
31. Nachin, L., Nannmark, U., Nystrom, T., Differential roles of the universal stress proteins of Escherichia coli in oxidative stress resistance, adhesion, and motility. J. Bacteriol. 2005, 187, 6265-6272.
32. Gross, M., Marianovsky, I., Glaser, G., MazG - a regulator of programmed cell death in Escherichia coli. Mol. Microbiol. 2006, 59, 590-601.
33. Chang, D. E., Smalley, D. J., Conway, T., Gene expression profiling of Escherichia coli growth transitions: An expanded stringent response model. Mol. Microbiol. 2002, 45, 289-306.
34. Suutari, M., Laakso, S., Microbial fatty acids and thermal adaptation. Crit. Rev. Microbiol. 1994, 20, 285-328.
35. Suutari, M., Laakso, S., Unsaturated and branched chain-fatty acids in temperature adaptation of Bacillus subtilis and Bacillus megaterium. Biochim. Biophys. Acta 1992, 1126, 119-124.
36. Suutari, M., Laakso, S., Changes in fatty acid branching and unsaturation of Streptomyces griseus and Brevibacterium fermentans as a response to growth temperature. Appl. Environ. Microbiol. 1992, 58, 2338-2340.
37. Choi, K. H., Heath, R. J., Rock, C. O., beta-ketoacyl-acyl carrier protein synthase III (FabH) is a determining factor in branched-chain fatty acid biosynthesis. J. Bacteriol. 2000, 182, 365-370.
38. Paoletti, L., Lu, Y. J., Schujman, G. E., de Mendoza, D. et al., Coupling of fatty acid and phospholipid synthesis in Bacillus subtilis. J. Bacteriol. 2007, 189, 5816-5824.
39. Massey, L. K., Sokatch, J. R., Conrad, R. S., Branched-chain amino acid catabolism in bacteria. Bacteriol. Rev. 1976, 40, 42-54.
40. Beck, H. C., Hansen, A. M., Lauritsen, F. R., Catabolism of leucine to branched-chain fatty acids in Staphylococcus xylosus. J. Appl. Microbiol. 2004, 96, 1185-1193.
41. Beck, H. C., Branched-chain fatty acid biosynthesis in a branched-chain amino acid aminotransferase mutant of Staphylococcus carnosus. FEMS Microbiol. Lett. 2005, 243, 37-44.
42. Annous, B. A., Kozempel, M. F., Kurantz, M. J., Changes in membrane fatty acid composition of Pediococcus sp. strain NRRL B-2354 in response to growth conditions and its effect on thermal resistance. Appl. Environ. Microbiol. 1999, 65, 2857-2862.
43. Guerzoni, M. E., Lanciotti, R., Cocconcelli, P. S., Alteration in cellular fatty acid composition as a response to salt, acid, oxidative and thermal stresses in Lactobacillus helveticus. Microbiology 2001, 147, 2255-2264.
44. Di Pasqua, R., Hoskins, N., Betts, G., Mauriello, G., Changes in membrane fatty acids composition of microbial cells induced by addiction of thymol, carvacrol, limonene, cinnamaldehyde, and eugenol in the growing media. J. Agric. Food Chem. 2006, 54, 2745-2749.
45. van Schaik, W., Gahan, C. G., Hill, C., Acid-adapted Listeria monocytogenes displays enhanced tolerance against the lantibiotics nisin and lacticin 3147. J. Food Prot. 1999, 62, 536-539.
46. Bayer, A. S., McNamara, P., Yeaman, M. R., Lucindo, N. et al., Transposon disruption of the complex I NADH oxidoreductase gene (snoD) in Staphylococcus aureus is associated with reduced susceptibility to the microbicidal activity of thrombin-induced platelet microbicidal protein 1. J. Bacteriol. 2006, 188, 211-222.
47. Jones, T., Yeaman, M. R., Sakoulas, G., Yang, S. J. et al., Failures in clinical treatment of Staphylococcus aureus Infection with daptomycin are associated with alterations in surface charge, membrane phospholipid asymmetry, and drug binding. Antimicrob. Agents Chemother. 2008, 52, 269-278.
48. Horsburgh, M. J., in: Lindsay, J. A. (Ed.), The Response of S. aureus to Environmental Stimuli, Caister Academic Press, UK 2008, pp. 185-206.
49. Kitaoka, S., Wada, K., Hasegawa, Y., Minami, Y. et al., Crystal structure of Escherichia coli SufC, an ABC-type ATPase component of the SUF iron-sulfur cluster assembly machinery. FEBS Lett. 2006, 580, 137-143.
50. Ayala-Castro, C., Saini, A., Outten, F. W., Fe-S cluster assembly pathways in bacteria. Microbiol. Mol. Biol. Rev. 2008, 72, 110-125.
51. Flynn, J. M., Neher, S. B., Kim, Y. I., Sauer, R. T. et al., Proteomic discovery of cellular substrates of the ClpXP protease reveals five classes of ClpX-recognition signals. Mol. Cell 2003, 11, 671-683.
52. Genevaux, P., Georgopoulos, C., Kelley, W. L., The Hsp70 chaperone machines of Escherichia coli: A paradigm for the repartition of chaperone functions. Mol. Microbiol. 2007, 66, 840-857.
53. Singh, V. K., Moskovitz, J., Multiple methionine sulfoxide reductase genes in Staphylococcus aureus: Expression of activity and roles in tolerance of oxidative stress. Microbiology 2003, 149, 2739-2747.
54. Resch, A., Rosenstein, R., Nerz, C., Gotz, F., Differential gene expression profiling of Staphylococcus aureus cultivated under biofilm and planktonic conditions. Appl. Environ. Microbiol. 2005, 71, 2663-2676.
55. Anderson, K. L., Roberts, C., Disz, T., Vonstein, V. et al., Characterization of the Staphylococcus aureus heat shock, cold shock, stringent, and SOS responses and their effects on log-phase mRNA turnover. J. Bacteriol. 2006, 188, 6739-6756.
56. Persson, O., Valadi, A., Nystrom, T., Farewell, A., Metabolic control of the Escherichia coli universal stress protein response through fructose-6-phosphate. Mol. Microbiol. 2007, 65, 968-978.
57. Nystrom, T., Neidhardt, F. C., Expression and role of the universal stress protein, UspA, of Escherichia coli during growth arrest. Mol. Microbiol. 1994, 11, 537-544.
58. Nanamiya, H., Kasai, K., Nozawa, A., Yun, C. S. et al., Identification and functional analysis of novel (p)ppGpp synthetase genes in Bacillus subtilis. Mol. Microbiol. 2008, 67, 291-304.
59. Zhang, J., Zhang, Y., Inouye, M., Thermotoga maritima MazG protein has both nucleoside triphosphate pyrophosphohydrolase and pyrophosphatase activities. J. Biol. Chem. 2003, 278, 21408-21414.
60. Kim, S. K., Makino, K., Amemura, M., Shinagawa, H. et al., Molecular analysis of the phoH gene, belonging to the phosphate regulon in Escherichia coli. J. Bacteriol. 1993, 175, 1316-1324.
61. Allenby, N. E., O'Connor, N., Pragai, Z., Ward, A. C. et al., Genome-wide transcriptional analysis of the phosphate starvation stimulon of Bacillus subtilis. J. Bacteriol. 2005, 187, 8063-8080.