YhgC protects Bacillus anthracis from oxidative stress

International Journal of Artificial Organs

Volumn 33, Issue 9, 2010, Pages 590-607

  Kiran, Madanahally D ^a,d   Bala, Shashi ^b   Hirshberg, Miriam ^c   Balaban, Naomi ^a,e  

^a TUFTS UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c WELLCOME TRUST SANGER INSTITUTE   (United Kingdom)

^d IQUUM Inc   (United States)

^e Yale University   (United States)

Author keywords

Bacteria; Stress; YhgC

Indexed keywords

BACTERIOLOGY; CELL MEMBRANES; CYTOLOGY; ENCODING (SYMBOLS); GENE ENCODING; GENE EXPRESSION; MOLECULAR BIOLOGY; OXIDATIVE STRESS; PROTEINS; SIGNAL ENCODING;

B.ANTHRACIS; BACILLUS ANTHRACIS; BIOWEAPONS; ENVIRONMENTAL STRESS; GENES ENCODING; MUTANT STRAIN; PARENT STRAIN; STRESS CONDITION; STRESSES RESPONSE; YHGC;

BACTERIA;

BACTERIAL PROTEIN; CAMELYSIN; CLPP 2 PROTEIN; UNCLASSIFIED DRUG; YHGC PROTEIN;

ARTICLE; BACILLUS ANTHRACIS; BACTERIAL STRAIN; BACTERIAL SURVIVAL; CELL SURFACE; CYTOPLASM; DELETION MUTANT; FUNCTIONAL PROTEOMICS; GENE DELETION; GENE EXPRESSION REGULATION; IMMUNOLOCALIZATION; MACROPHAGE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TRANSCRIPTOMICS;

EID: 78049484934     PISSN: 03913988     EISSN: None     Source Type: Journal    
DOI: 10.1177/039139881003300905     Document Type: Article

References (51)

1. Henderson I, Yu D, Turnbull PC. Differentiation of Bacillus anthracis and other 'Bacillus cereus group' bacteria using IS231-derived sequences. FEMS Microbiol Lett 1995; 128: 113-8.
2. Koehler TM. Bacillus anthracis genetics and virulence gene regulation. Curr Top Microbiol Immunol 2002; 271: 143-64.
3. Passalacqua KD, Bergman NH, Lee JY, Sherman DH, Hanna PC. The global transcriptional responses of Bacillus anthracis Sterne (34F2) and a Delta sodA1 mutant to paraquat reveal metal ion homeostasis imbalances during endogenous superoxide stress. J Bacteriol 2007; 189: 3996-4013.
4. Scandalios JG. Oxidative stress responses - what have genome-scale studies taught us? Genome Biol 2002; 3: REVIEWS1019.
5. Schumann W. The Bacillus subtilis heat shock stimulon. Cell Stress Chaperones 2003; 8: 207-17.
6. Mogk A, Homuth G, Scholz C, Kim L, Schmid FX, Schumann W. The GroE chaperonin machine is a major modulator of the CIRCE heat shock regulon of Bacillus subtilis. Embo J 1997; 16: 4579-90.
7. Zuber U, Schumann W. CIRCE, a novel heat shock element involved in regulation of heat shock operon dnaK of Bacillus subtilis. J Bacteriol 1994; 176: 1359-63.
8. Petersohn A, Brigulla M, Haas S, Hoheisel JD, Volker U, Hecker M. Global analysis of the general stress response of Bacillus subtilis. J Bacteriol 2001; 183: 5617-31.
9. Benson AK, Haldenwang WG. The sigma B-dependent promoter of the Bacillus subtilis sigB operon is induced by heat shock. J Bacteriol 175: 1993; 1929-35.
10. D erre I, Rapoport G, Msadek T. CtsR, a novel regulator of stress and heat shock response, controls clp and molecular chaperone gene expression in gram-positive bacteria. Mol Microbiol 1999; 31: 117-31.
11. Kruger E, Volker U, Hecker M. Stress induction of clpC in Bacillus subtilis and its involvement in stress tolerance. J Bacteriol 1994; 176: 3360-7.
12. Msadek T, Kunst F, Rapoport G. MecB of Bacillus subtilis, a member of the ClpC ATPase family, is a pleiotropic regulator controlling competence gene expression and growth at high temperature. Proc Natl Acad Sci U S A 1994; 91: 5788-92.
13. Gerth U, Kruger E, Derre I, Msadek T, Hecker M. Stress induction of the Bacillus subtilis clpP gene encoding a homologue of the proteolytic component of the Clp protease and the involvement of ClpP and ClpX in stress tolerance. Mol Microbiol 1998; 28: 787-802.
14. Msadek T, Dartois V, Kunst F, Herbaud ML, Denizot F, Rapoport G. ClpP of Bacillus subtilis is required for competence development, motility, degradative enzyme synthesis, growth at high temperature and sporulation. Mol Microbiol 1998; 27: 899-914.
15. Gerth U, Wipat A, Harwood CR, Carter N, Emmerson PT, Hecker M. Sequence and transcriptional analysis of clpX, a class-III heat-shock gene of Bacillus subtilis. Gene 1996; 181: 77-83.
16. D euerling E, Mogk A, Richter C, Purucker M, Schumann W. The ftsH gene of Bacillus subtilis is involved in major cellular processes such as sporulation, stress adaptation and secretion. Mol Microbiol 1997; 23: 921-33.
17. R iethdorf S, Volker U, Gerth, U, Winkler A, Engelmann S, Hecker M. Cloning, nucleotide sequence, and expression of the Bacillus subtilis lon gene. J Bacteriol 1994; 176: 6518-27.
18. Schulz A, Schwab S, Homuth G, Versteeg S, Schumann W. The htpG gene of Bacillus subtilis belongs to class III heat shock genes and is under negative control. J Bacteriol 1997; 179: 3103-9.
19. Antelmann H, Engelmann S, Schmid R, Hecker, M. General and oxidative stress responses in Bacillus subtilis: cloning, expression, and mutation of the alkyl hydroperoxide reductase operon. J Bacteriol 1996; 178: 6571-78.
20. Bsat N, Chen L, Helmann JD. Mutation of the Bacillus subtilis alkyl hydroperoxide reductase (ahpCF) operon reveals compensatory interactions among hydrogen peroxide stress genes. J Bacteriol 1996; 178: 6579-86.
21. Scharf C, Riethdorf S, Ernst H, Engelmann S, Volker U, Hecker M. Thioredoxin is an essential protein induced by multiple stresses in Bacillus subtilis. J Bacteriol 1998; 180: 869-77.
22. Fedhila S, Msadek T, Nel P, Lereclus D. Distinct clpP genes control specific adaptive responses in Bacillus thuringiensis. J Bacteriol 2002; 184: 5554-62.
23. C ybulski RJ Jr, Sanz P, Alem F, Stibitz S, Bull RL, O'Brien AD. Four superoxide dismutases contribute to Bacillus anthracis virulence and provide spores with redundant protection from oxidative stress. Infect Immun 2009; 77: 274-85.
24. Kumar S, Tamura K, Nei M. MEGA3: Integrated software for Molecular Evolutionary Genetics Analysis and sequence alignment. Brief Bioinform 2004; 5: 150-63.
25. R ost B. PHD: predicting one-dimensional protein structure by profile-based neural networks. Methods Enzymol 1996; 266: 525-39.
26. Saile E, Koehler TM. Control of anthrax toxin gene expression by the transition state regulator abrB. J Bacteriol 2002; 184: 370-80.
27. C hen Y, Tenover FC, Koehler TM. Beta-lactamase gene expression in a penicillin-resistant Bacillus anthracis strain. Antimicrob Agents Chemother 2004; 48: 4873-7.
28. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-8.
29. C hand HS, Drysdale M, Lovchik J, Koehler TM, Lipscomb MF, Lyons CR. Discriminating virulence mechanisms among Bacillus anthracis strains by using a murine subcutaneous infection model. Infect Immun 2009; 77: 429-35.
30. Ivanova N, Sorokin A, Anderson I, et al. Genome sequence of Bacillus cereus and comparative analysis with Bacillus anthracis. Nature 2003; 423: 87-91.
31. Gov Y, Borovok I, Korem M, et al. Quorum sensing in Staphylococci is regulated via phosphorylation of three conserved histidine residues. J Biol Chem 2004; 279: 14665-72.
32. Antelmann H, Williams RC, Miethke M, et al. The extracellular and cytoplasmic proteomes of the non-virulent Bacillus anthracis strain UM23C1-2. Proteomics 2005; 5: 3684-95.
33. Francis AW, Ruggiero CE, Koppisch AT, et al. Proteomic analysis of Bacillus anthracis Sterne vegetative cells. Biochim Biophys Acta 2005; 1748: 191-200.
34. Frees D, Qazi SN, Hill PJ and Ingmer H. Alternative roles of ClpX and ClpP in Staphylococcus aureus stress tolerance and virulence. Mol Microbiol 2003; 48: 1565-78.
35. Michel A, Agerer F, Hauck CR, 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: 5783-96.
36. Shatalin K, Gusarov I, Avetissova E, et al. Bacillus anthracis-derived nitric oxide is essential for pathogen virulence and survival in macrophages. Proc Natl Acad Sci U S A 2008; 105: 1009-13.
37. Sapra R, Gaucher SP, Lachmann JS, et al. Proteomic analyses of murine macrophages treated with Bacillus anthracis lethal toxin. Microb Pathog 2006; 41: 157-67.
38. Perez-Casal J, Caparon MG, Scott JR. Mry, a trans-acting positive regulator of the M protein gene of Streptococcus pyogenes with similarity to the receptor proteins of two-component regulatory systems. J Bacteriol 1991; 173: 2617-24.
39. O'Toole GA, Kolter R. Initiation of biofilm formation in Pseudomonas fluorescens WCS365 proceeds via multiple, convergent signalling pathways: a genetic analysis. Mol Microbiol 1998; 28: 449-61.
40. Hung DY, Shapiro L. A signal transduction protein cues proteolytic events critical to Caulobacter cell cycle progression. Proc Natl Acad Sci U S A 2002; 99: 13160-5.
41. de Crecy-Lagard V, Servant-Moisson P, Viala J, Grandvalet C, Mazodier P. Alteration of the synthesis of the Clp ATP-dependent protease affects morphological and physiological differentiation in Streptomyces. Mol Microbiol 1999; 32: 505-17.
42. VanBogelen RA, Neidhard FC. (1990) Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A 87: 5589-93.
43. Grass G, Schierhorn A, Sorkau E, et al. Camelysin is a novel surface metalloproteinase from Bacillus cereus. Infect Immun 2004; 72: 219-28.
44. Fricke B, Drossler K, Willhardt I, Schierhorn A, Menge S, Rucknagel P. The cell envelope-bound metalloprotease (camelysin) from Bacillus cereus is a possible pathogenic factor. Biochim Biophys Acta 2001; 1537: 132-46.
45. Kruger E, Witt E, Ohlmeier S, Hanschke R, Hecker M. The clp proteases of Bacillus subtilis are directly involved in degradation of misfolded proteins. J Bacteriol 2000; 182: 3259-65.
46. Kiran MD, Balaban, N. TR AP plays a role in stress response in Staphylococcus aureus. Int J Artif Organs 2009; 32: 592-9.
47. Kiran MD, Akiyoshi DE, Giacometti A, Cirioni O, Scalise G, Balaban N. OpuC - an ABC transporter that is associated with Staphylococcus aureus pathogenesis. Int J Artif Organs 2009; 32: 600-10.
48. Gold JA, Hoshino Y, Hoshino S, Jones MB, Nolan A, Weiden MD. Exogenous gamma and alpha/beta interferon rescues human macrophages from cell death induced by Bacillus anthracis. Infect Immun 2004; 72: 1291-7.
49. Ireland JA, Hanna PC. Macrophage-enhanced germination of Bacillus anthracis endospores requires gerS. Infect Immun 2002; 70: 5870-2.
50. C endrowski S, MacArthur W and Hanna P. Bacillus anthracis requires siderophore biosynthesis for growth in macrophages and mouse virulence. Mol Microbiol 2004; 51: 407-17.
51. Athamna A, Massalha M, Athamna M, et al. In vitro susceptibility of Bacillus anthracis to various antibacterial agents and their time-kill activity. J Antimicrob Chemother 2004; 53: 247-51.