New insights into staphylococcus aureus stress tolerance and virulence regulation from an analysis of the role of the ClpP protease in the strains Newman, COL, and SA564

Journal of Proteome Research

Volumn 11, Issue 1, 2012, Pages 95-108

  Frees, Dorte ^a   Andersen, Julie Hove ^a   Hemmingsen, Lene ^a,b   Koskenniemi, Kerttu ^b   Bæk, Kristoffer T ^a   Muhammed, Musemma Kedir ^a   Gudeta, Dereje Dadi ^a   Nyman, Tuula A ^c   Sukura, Antti ^b   Varmanen, Pekka ^b   Savijoki, Kirsi ^b,c  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

2 D DIGE; ClpP; prophages; proteolysis; regulation of virulence; Staphylococcus aureus

Indexed keywords

ENDOPEPTIDASE CLP;

ARTICLE; BACTERIAL GENETICS; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM MUTANT; GENE CONTROL; GENE DELETION; GENE EXPRESSION; NONHUMAN; POPULATION ABUNDANCE; PRIORITY JOURNAL; PROPHAGE; STAPHYLOCOCCUS AUREUS; STRAIN IDENTIFICATION; STRESS; UPREGULATION;

BACTERIAL PROTEINS; CARRIER PROTEINS; DNA-BINDING PROTEINS; ENDOPEPTIDASE CLP; GENE EXPRESSION; GENE EXPRESSION REGULATION, BACTERIAL; GENE KNOCKOUT TECHNIQUES; PHENOTYPE; PROPHAGES; PROTEOME; STAPHYLOCOCCUS AUREUS; STRESS, PHYSIOLOGICAL; TRANS-ACTIVATORS; TWO-DIMENSIONAL DIFFERENCE GEL ELECTROPHORESIS; UREASE; VIRULENCE; VIRULENCE FACTORS;

STAPHYLOCOCCUS AUREUS;

EID: 84855564138     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr200956s     Document Type: Article

References (66)

1. Lowy, F. D. Staphylococcus aureus infections N. Engl. J. Med. 1998, 339 (8) 520-532
2. DeLeo, F. R.; Chambers, H. F. Reemergence of antibiotic-resistant Staphylococcus aureus in the genomics era J. Clin. Invest. 2009, 119 (9) 2464-2474
3. Novick, R. P. Staphylococcal pathogenesis and pathogenicity factors: genetics and regulation. In Gram-positive Pathogens; Fischetti, V. A.; Novick, R.; Ferretti, J. J.; Portnoy, D. A.; Rood, J. I., Eds.; ASM Press: Washington, D.C., 2006.
4. Dreisbach, A.; Hempel, K.; Buist, G.; Hecker, M.; Becher, D.; van Dijl, J. M. Profiling the surfacome of Staphylococus aureus Proteomics 2010, 10 (17) 3082-3096
5. Ziebandt, A.-K.; Kusch, H.; Degner, M.; Jaglitz, S.; Sibbald, M. J. J. B.; Arends, J. P.; Chlebowicz, M. A.; Albrecht, D.; Pantuček, R.; Doškar, J.; Ziebuhr, W.; Bröker, B. M.; Hecker, M.; van Dijl, J. M.; Engelmann, S. Proteomics uncovers extreme heterogeneity in the Staphylococcus aureus exoproteome due to genomic plasticity and variant gene regulation Proteomics 2010, 10 (8) 1634-1644
6. Lindsay, J. A.; Holden, M. T. G. Staphylococcus aureus: superbug, super genome? Trends Microbiol. 2004, 12 (8) 378-385 (Pubitemid 38987825)
7. Jelsbak, L.; Hemmingsen, L.; Donat, S.; Ohlsen, K.; Boye, K.; Westh, H.; Ingmer, H.; Frees, D. Growth phase-dependent regulation of the global virulence regulator Rot in clinical isolates of Staphylococcus aureus Int. J. Med. Microbiol. 2010, 300 (4) 229-236
8. Li, M.; Diep, B. A.; Villaruz, A. E.; Braughton, K. R.; Jiang, X.; DeLeo, F. R.; Chambers, H. F.; Lu, Y.; Otto, M. Evolution of virulence in epidemic community-associated methicillin-resistant Staphylococcus aureus Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (14) 5883-5888
9. Herbert, S.; Ziebandt, A.-K.; Ohlsen, K.; Schäfer, T.; Hecker, M.; Albrecht, D.; Novick, R.; Götz, F. Repair of global regulators in Staphylococcus aureus 8325 and comparative analysis with other clinical isolates Infect. Immun. 2010, 78 (6) 2877-2889
10. B activity depends on RsbU in Staphylococcus aureus J. Bacteriol. 2001, 183 (6) 1843-1852 (Pubitemid 32225979)
11. B modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4 J. Bacteriol. 2002, 184 (19) 5457-5467 (Pubitemid 35024393)
12. Oscarsson, J.; Kanth, A.; Tegmark-Wisell, K.; Arvidson, S. SarA is a repressor of hla (alpha-hemolysin) transcription in Staphylococcus aureus: its apparent role as an activator of hla in the prototype strain NCTC 8325 depends on reduced expression of sarS J. Bacteriol. 2006, 188 (24) 8526-8533 (Pubitemid 44894054)
13. Mainiero, M.; Goerke, C.; Geiger, T.; Gonser, C.; Herbert, S.; Wolz, C. Differential target gene activation by the Staphylococcus aureus two-component system saeRS J. Bacteriol. 2010, 192 (3) 613-623
14. Maurizi, M. R.; Clark, W. P.; Kim, S.-H.; Gottesman, S. ClpP represents a unique family of serine proteases J. Biol. Chem. 1990, 265 (21) 12546-12552
15. Kessel, M.; Maurizi, M. R.; Kim, B.; Kocsis, E.; Trus, B. L.; Singh, S. K.; Steven, A. C. Homology in structural organization between E. coli ClpAP protease and the eukaryotic 26 S proteasome J. Mol. Biol. 1995, 250 (5) 587-594
16. Frees, D.; Savijoki, K.; Varmanen, P.; Ingmer, H. Clp ATPases and ClpP proteolytic complexes regulate vital biological processes in low GC, Gram-positive bacteria Mol. Microbiol. 2007, 63 (5) 1285-1295
17. Becker, G.; Klauck, E.; Hengge-Aronis, R. Regulation of RpoS proteolysis in Escherichia coli: The response regulator RssB is a recognition factor that interacts with the turnover element in RpoS Proc. Natl. Acad. Sci. U.S.A. 1999, 96 (11) 6439-6444 (Pubitemid 29256684)
18. S for degradation by ClpXP Genes Dev. 2001, 15 (5) 627-637 (Pubitemid 32205150)
19. Turgay, K.; Hahn, J.; Burghoorn, J.; Dubnau, D. Competence in Bacillus subtilis is controlled by regulated proteolysis of a transcription factor EMBO J. 1998, 17 (22) 6730-6738 (Pubitemid 28521806)
20. Frees, D.; Qazi, S. N. A.; Hill, P. J.; Ingmer, H. Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence Mol. Microbiol. 2003, 48 (6) 1565-1578 (Pubitemid 36751062)
21. Frees, D.; Sørensen, 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 (12) 8100-8108 (Pubitemid 41740297)
22. Michel, A.; Agerer, F.; Hauck, C. R.; Herrmann, M.; Ullrich, J.; Hacker, J.; Ohlsen, K. 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 (16) 5783-5796 (Pubitemid 44384086)
23. B in Staphylococcus aureus reveals its function as a global regulator of virulence genes J. Bacteriol. 1998, 180 (18) 4814-4820 (Pubitemid 28429367)
24. Hecker, M.; Pané-Farré, J.; Völker, U. SigB-dependent general stress response in Bacillus subtilis and related Gram-positive bacteria Annu. Rev. Microbiol. 2007, 61, 215-236 (Pubitemid 350058207)
25. B Int. J. Food Microbiol. 2009, 135 (3) 274-280
26. B on Staphylococcus aureus resistance to stresses of relevance to food preservation J. Appl. Microbiol. 2009, 107 (1) 187-196
27. Brötz-Oesterhelt, H.; Beyer, D.; Kroll, H.-P.; Endermann, R.; Ladel, C.; Schroeder, W.; Hinzen, B.; Raddatz, S.; Paulsen, H.; Henninger, K.; Bandow, J. E.; Sahl, H.-G.; Labischinski, H. Dysregulation of bacterial proteolytic machinery by a new class of antibiotics Nat. Med. 2005, 11 (10) 1082-1087 (Pubitemid 41486830)
28. Luong, T. T.; Lee, C. Y. Improved single-copy integration vectors for Staphylococcus aureus J. Microbiol. Methods 2007, 70 (1) 186-190 (Pubitemid 46962783)
29. Koskenniemi, K.; Koponen, J.; Kankainen, M.; Savijoki, K.; Tynkkynen, S.; de Vos, W. M.; Kalkkinen, N.; Varmanen, P. Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media J. Proteome Res. 2009, 8 (11) 4993-5007
30. O'Connell, K. L.; Stults, J. T. Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests Electrophoresis 1997, 18 (3-4) 349-359 (Pubitemid 27174419)
31. Koskenniemi, K.; Laakso, K.; Koponen, J.; Kankainen, M.; Greco, D.; Auvinen, P.; Savijoki, K.; Nyman, T. A.; Surakka, A.; Salusjärvi, T.; de Vos, W. M.; Tynkkynen, S.; Kalkkinen, N.; Varmanen, P. Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG Mol. Cell. Proteomics 2011, 10 (2) M110.002741
32. Baba, T.; Bae, T.; Schneewind, O.; Takeuchi, F.; Hiramatsu, K. Genome sequence of Staphylococcus aureus strain Newman and comparative analysis of staphylococcal genomes: polymorphism and evolution of two major pathogenicity islands J. Bacteriol. 2008, 190 (1) 300-310
33. Gillaspy, A. F.; Worrell, V.; Orvis, J.; Roe, B. A.; Dyer, D. W.; Landolo, J. J. The Staphylococcus aureus NCTC 8325 genome. In Gram-positive Pathogens; Fischetti, V. A.; Novick, R. P.; Ferretti, J. J.; Portnoy, D. A.; Rood, J. I., Eds.; ASM Press: Washington, D.C., 2006.
34. Jelsbak, L.; Ingmer, H.; Valihrach, L.; Cohn, M. T.; Christiansen, M. H. G.; Kallipolitis, B. H.; Frees, D. The chaperone ClpX stimulates expression of Staphylococcus aureus protein A by Rot dependent and independent pathways PLoS One 2010, 5 (9) e12752
35. Lee, B.-G.; Park, E. Y.; Lee, K.-E.; Jeon, H.; Sung, K. H.; Paulsen, H.; Rübsamen-Schaeff, H.; Brötz-Oesterhelt, H.; Song, H. K. Structures of ClpP in complex with acyldepsipeptide antibiotics reveal its activation mechanism Nat. Struct. Mol. Biol. 2010, 17 (4) 471-478
36. Novick, R. P. Properties of a cryptic high-frequency transducing phage in Staphylococcus aureus Virology 1967, 33 (1) 155-166
37. B regulon in Staphylococcus aureus and its regulation Int. J. Med. Microbiol. 2006, 296 (4-5) 237-258 (Pubitemid 44016170)
38. Viswanathan, S.; Ünlü, M.; Minden, J. S. Two-dimensional difference gel electrophoresis Nat. Protoc. 2006, 1 (3) 1351-1358
39. Bae, T.; Baba, T.; Hiramatsu, K.; Schneewind, O. Prophages of Staphylococcus aureus Newman and their contribution to virulence Mol. Microbiol. 2006, 62 (4) 1035-1047 (Pubitemid 44655316)
40. Owens, R. M.; Pritchard, G.; Skipp, P.; Hodey, M.; Connell, S. R.; Nierhaus, K. H.; O'Connor, C. D. A dedicated translation factor controls the synthesis of the global regulator Fis EMBO J. 2004, 23 (16) 3375-3385 (Pubitemid 39209161)
41. Zybailov, B.; Friso, G.; Kim, J.; Rudella, A.; Rodríguez, V. R.; Asakura, Y.; Sun, Q.; van Wijk, K. J. Large scale comparative proteomics of a chloroplast Clp protease mutant reveals folding stress, altered protein homeostasis, and feedback regulation of metabolism Mol. Cell. Proteomics 2009, 8 (8) 1789-1810
42. Bingel-Erlenmeyer, R.; Kohler, R.; Kramer, G.; Sandikci, A.; Antolić, S.; Maier, T.; Schaffitzel, C.; Wiedmann, B.; Bukau, B.; Ban, N. A peptide deformylase-ribosome complex reveals mechanism of nascent chain processing Nature 2008, 452 (7183) 108-111 (Pubitemid 351355096)
43. Glanzmann, P.; Gustafson, J.; Komatsuzawa, H.; Ohta, K.; Berger-Bächi, B. glmM operon and methicillin-resistant glmM suppressor mutants in Staphylococcus aureus Antimicrob. Agents Chemother. 1999, 43 (2) 240-245 (Pubitemid 29079152)
44. Kirstein, J.; Dougan, D. A.; Gerth, U.; Hecker, M.; Turgay, K. The tyrosine kinase McsB is a regulated adaptor protein for ClpCP EMBO J. 2007, 26 (8) 2061-2070 (Pubitemid 46625790)
45. 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 (4) 840-857 (Pubitemid 350050417)
46. Kock, H.; Gerth, U.; Hecker, M. The ClpP peptidase is the major determinant of bulk protein turnover in Bacillus subtilis J. Bacteriol. 2004, 186 (17) 5856-5864 (Pubitemid 39128659)
47. Pamp, S. J.; Frees, D.; Engelmann, S.; Hecker, M.; Ingmer, H. Spx is a global effector impacting stress tolerance and biofilm formation in Staphylococcus aureus J. Bacteriol. 2006, 188 (13) 4861-4870 (Pubitemid 43956084)
48. Nakano, S.; Küster-Schöck, E.; Grossman, A. D.; Zuber, P. Spx-dependent global transcriptional control is induced by thiol-specific oxidative stress in Bacillus subtilis Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (23) 13603-13608 (Pubitemid 37444787)
49. Staphylococci in Human Disease; Crossley, K. B.; Jefferson, K. K.; Archer, G. L.; Fowler, V. G., Jr., Eds.; Blackwell Publishing Ltd: West Sussex, U.K., 2009.
50. Luong, T. T.; Dunman, P. M.; Murphy, E.; Projan, S. J.; Lee, C. Y. Transcription profiling of the mgrA regulon in Staphylococcus aureus J. Bacteriol. 2006, 188 (5) 1899-1910 (Pubitemid 43346869)
51. Smith, E. J.; Visai, L.; Kerrigan, S. W.; Speziale, P.; Foster, T. J. The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus Infect. Immun. 2011, 79 (9) 3801-3809
52. W stress response Mol. Microbiol. 2006, 61 (6) 1569-1582 (Pubitemid 44359384)
53. Geisinger, E.; Adhikari, R. P.; Jin, R.; Ross, H. F.; Novick, R. P. Inhibition of rot translation by RNAIII, a key feature of agr function Mol. Microbiol. 2006, 61 (4) 1038-1048 (Pubitemid 44134179)
54. Boisset, S.; Geissmann, T.; Huntzinger, E.; Fechter, P.; Bendridi, N.; Possedko, M.; Chevalier, C.; Helfer, A. C.; Benito, Y.; Jacquier, A.; Gaspin, C.; Vandenesch, F.; Romby, P. Staphylococcus aureus RNAIII coordinately represses the synthesis of virulence factors and the transcription regulator Rot by an antisense mechanism Genes Dev. 2007, 21 (11) 1353-1366 (Pubitemid 46871039)
55. Chen, P. R.; Nishida, S.; Poor, C. B.; Cheng, A.; Bae, T.; Kuechenmeister, L.; Dunman, P. M.; Missiakas, D.; He, C. A new oxidative sensing and regulation pathway mediated by the MgrA homologue SarZ in Staphylococcus aureus Mol. Microbiol. 2009, 71 (1) 198-211
56. Chen, P. R.; Bae, T.; Williams, W. A.; Duguid, E. M.; Rice, P. A.; Schneewind, O.; He, C. An oxidation-sensing mechanism is used by the global regulator MgrA in Staphylococcus aureus Nat. Chem. Biol. 2006, 2 (11) 591-595 (Pubitemid 44610343)
57. Tegmark, K.; Karlsson, A.; Arvidson, S. Identification and characterization of SarH1, a new global regulator of virulence gene expression in Staphylococcus aureus Mol. Microbiol. 2000, 37 (2) 398-409 (Pubitemid 30481022)
58. Ingavale, S.; van Wamel, W.; Luong, T. T.; Lee, C. Y.; Cheung, A. L. Rat/MgrA, a regulator of autolysis, is a regulator of virulence genes in Staphylococcus aureus Infect. Immun. 2005, 73 (3) 1423-1431 (Pubitemid 40470728)
59. Geuskens, V.; Mhammedi-Alaoue, A.; Desmet, L.; Toussanint, A. Virulence in bacteriphage Mu: a case of trans -dominant proteolysis by the Escherichia coli Clp serine protease EMBO J. 1992, 11 (13) 5121-5127 (Pubitemid 23023456)
60. Wojtkowiak, D.; Georgopoulos, C.; Zylicz, M. Isolation and characterization of ClpX, a new ATP-dependent specificity component of the Clp protease of Escherichia coli J. Biol. Chem. 1993, 268 (30) 22609-22617 (Pubitemid 23318316)
61. Lehnherr, H.; Yarmolinsky, M. B. Addiction protein Phd of plasmid prophage P1 is a substrate of the ClpXP serine protease of Escherichia coli Proc. Natl. Acad. Sci. U.S.A. 1995, 92 (8) 3274-3277
62. Somerville, G. A.; Proctor, R. A. At the crossroads of bacterial metabolism and virulence factor synthesis in staphylococci Microbiol. Mol. Biol. Rev. 2009, 73 (2) 233-248
63. Dyke, K. G. H.; Jevons, M. P.; Parker, M. T. Penicillinase production and intrinsic resistance to penicillins in Staphylococcus aureus Lancet 1966, 1 (7442) 835-838
64. Duthie, E. S.; Lorenz, L. L. Staphylococcal coagulase: mode of action and antigenicity J. Gen. Microbiol. 1952, 6 (1-2) 95-107
65. Somerville, G. A.; Beres, S. B.; Fitzgerald, J. R.; DeLeo, F. R.; Cole, R. L.; Hoff, J. S.; Musser, J. M. In vitro serial passage of Staphylococcus aureus: changes in physiology, virulence factor production, and agr nucleotide sequence J. Bacteriol. 2002, 184 (5) 1430-1437 (Pubitemid 34157567)
66. Christensen, W. B. Urea decomposition as a means of differentiating Proteus and paracolon cultures from each other and from Salmonella and Shigella types J. Bacteriol. 1946, 52 (4) 461-466