Haemophilus influenzae OxyR: Characterization of Its Regulation, Regulon and Role in Fitness

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Whitby, Paul W ^a   Morton, Daniel J ^a   VanWagoner, Timothy M ^a,b   Seale, Thomas W ^a   Cole, Brett K ^a   Mussa, Huda J ^a   McGhee, Phillip A ^a   Bauer, Chee Yoon S ^a   Springer, Jennifer M ^a   Stull, Terrence L ^a  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b OKLAHOMA CHRISTIAN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CATALASE; GLUTAREDOXIN; OXYR PROTEIN; PEROXIREDOXIN; REACTIVE OXYGEN METABOLITE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; CHINCHILLA; COLONY FORMING UNIT; CONTROLLED STUDY; DPS GENE; ENZYME REGULATION; FITNESS; GENE DELETION; GENE MUTATION; GENETIC TRANSCRIPTION; HAEMOPHILUS INFLUENZAE; HKTE GENE; MIDDLE EAR EFFUSION; NONHUMAN; OPERON; OTITIS MEDIA; OXIDATIVE STRESS; PGDX GENE; POLYMERASE CHAIN REACTION; QUANTITATIVE ANALYSIS; RAT; REGULON; UPREGULATION; YFEB GENE;

ANIMALS; BACTEREMIA; BACTERIAL PROTEINS; CATALASE; FEMALE; GENE EXPRESSION REGULATION, BACTERIAL; HAEMOPHILUS INFLUENZAE; HEME; INTRACELLULAR SPACE; IRON; KINETICS; MUTATION; OTITIS MEDIA; OXIDATIVE STRESS; PEROXIREDOXINS; PREGNANCY; RATS; REGULON; SPECIES SPECIFICITY; TRANSCRIPTION, GENETIC;

ANIMALIA; BACTERIA (MICROORGANISMS); HAEMOPHILUS INFLUENZAE; RATTUS;

EID: 84870591134     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050588     Document Type: Article

References (56)

1. Turk DC, (1984) The pathogenicity of Haemophilus influenzae. J Med Microbiol 18: 1-16.
2. Murphy TF, Faden H, Bakaletz LO, Kyd JM, Forsgren A, et al. (2009) Nontypeable Haemophilus influenzae as a pathogen in children. Pediatr Infect Dis J 28: 43-48.
3. Morton DJ, Stull TL (2004) Haemophilus. In: Crosa JH, Mey AR, Payne SM, editors. Iron Transport in Bacteria. Washington, DC: American Society for Microbiology. 273-292.
4. Morton DJ, Smith A, Ren Z, Madore LL, VanWagoner TM, et al. (2004) Identification of a haem-utilization protein (Hup) in Haemophilus influenzae. Microbiology 150: 3923-3933.
5. Morton DJ, Madore LL, Smith A, VanWagoner TM, Seale TW, et al. (2005) The heme-binding lipoprotein (HbpA) of Haemophilus influenzae: role in heme utilization. FEMS Microbiol Lett 253: 193-199.
6. Morton DJ, Seale TW, Madore LL, VanWagoner TM, Whitby PW, et al. (2007) The haem-haemopexin utilization gene cluster (hxuCBA) as a virulence factor of Haemophilus influenzae. Microbiology 153: 215-224.
7. Morton DJ, Smith A, VanWagoner TM, Seale TW, Whitby PW, et al. (2007) Lipoprotein e (P4) of Haemophilus influenzae: Role in heme utilization and pathogenesis. Microbes Infect 9: 932-939.
8. Morton DJ, Whitby PW, Jin H, Ren Z, Stull TL, (1999) Effect of multiple mutations in the hemoglobin- and hemoglobin-haptoglobin-binding proteins, HgpA, HgpB, and HgpC of Haemophilus influenzae type b. Infect Immun 67: 2729-2739.
9. Morton DJ, Seale TW, VanWagoner TM, Whitby PW, Stull TL, (2009) The dppBCDF gene cluster of Haemophilus influenzae: Role in heme utilization. BMC Res Notes 2: 166.
10. Morton DJ, Turman EJ, Hensley PD, VanWagoner TM, Seale TW, et al. (2010) Identification of a siderophore utilization locus in nontypeable Haemophilus influenzae. BMC Microbiol 10: 113.
11. Whitby PW, VanWagoner TM, Seale TW, Morton DJ, Stull TL, (2006) Transcriptional profile of Haemophilus influenzae: Effects of iron and heme. J Bacteriol 188: 5640-5645.
12. Whitby PW, Seale TW, VanWagoner TM, Morton DJ, Stull TL, (2009) The iron/heme regulated genes of Haemophilus influenzae: Comparative transcriptional profiling as a tool to define the species core modulon. BMC Genomics 10: 6.
13. Benjamin JA, Desnoyers G, Morissette A, Salvail H, Masse E, (2010) Dealing with oxidative stress and iron starvation in microorganisms: an overview. Can J Physiol Pharmacol 88: 264-272.
14. Maciver I, Hansen EJ, (1996) Lack of expression of the global regulator OxyR in Haemophilus influenzae has a profound effect on growth phenotype. Infect Immun 64: 4618-4629.
15. Chiang SM, Schellhorn HE (2012) Regulators of oxidative stress response genes in Escherichia coli and their functional conservation in bacteria. Arch Biochem Biophys. S0003-9861(12)00058-6 [pii];10.1016/j.abb.2012.02.007 [doi].
16. Imlay JA, (2008) Cellular defenses against superoxide and hydrogen peroxide. Annu Rev Biochem 77: 755-776.
17. Antelmann H, Helmann JD, (2011) Thiol-based redox switches and gene regulation. Antioxid Redox Signal 14: 1049-1063.
18. Hoopman TC, Liu W, Joslin SN, Pybus C, Brautigam CA, et al. (2011) Identification of gene products involved in the oxidative stress response of Moraxella catarrhalis. Infect Immun 79: 745-755.
19. Tseng HJ, McEwan AG, Apicella MA, Jennings MP, (2003) OxyR acts as a repressor of catalase expression in Neisseria gonorrhoeae. Infect Immun 71: 550-556.
20. Hishinuma S, Yuki M, Fujimura M, Fukumori F, (2006) OxyR regulates the expression of two major catalases, KatA and KatB, along with peroxiredoxin, AhpC in Pseudomonas putida. Environ Microbiol 8: 2115-2124.
21. Knapp GS, Tsai JW, Hu JC, (2009) The oligomerization of OxyR in Escherichia coli. Protein Sci 18: 101-107.
22. Seib KL, Wu HJ, Srikhanta YN, Edwards JL, Falsetta ML, et al. (2007) Characterization of the OxyR regulon of Neisseria gonorrhoeae. Mol Microbiol 63: 54-68.
23. Sund CJ, Rocha ER, Tzianabos AO, Wells WG, Gee JM, et al. (2008) The Bacteroides fragilis transcriptome response to oxygen and H2O2: the role of OxyR and its effect on survival and virulence. Mol Microbiol 67: 129-142.
24. Harrison A, Ray WC, Baker BD, Armbruster DW, Bakaletz LO, et al. (2007) The OxyR regulon in nontypeable Haemophilus influenzae. J Bacteriol 189: 1004-1012.
25. Calhoun LN, Kwon YM, (2011) Structure, function and regulation of the DNA-binding protein Dps and its role in acid and oxidative stress resistance in Escherichia coli: a review. J Appl Microbiol 110: 375-386.
26. Whitby PW, Seale TW, Morton DJ, VanWagoner TM, Stull TL, (2010) Characterization of the Haemophilus influenzae tehB gene and its role in virulence. Microbiology 156: 1188-1200.
27. Morton DJ, Seale TW, Bakaletz LO, Jurcisek JA, Smith A, et al. (2009) The heme-binding protein (HbpA) of Haemophilus influenzae as a virulence determinant. Int J Med Microbiol 299: 479-488.
28. Seale TW, Morton DJ, Whitby PW, Wolf R, Kosanke SD, et al. (2006) Complex role of hemoglobin and hemoglobin-haptoglobin binding proteins in Haemophilus influenzae virulence in the infant rat model of invasive infection. Infect Immun 74: 6213-6225.
29. Bishai WR, Howard NS, Winkelstein JA, Smith HO, (1994) Characterization and virulence analysis of catalase mutants of Haemophilus influenzae. Infect Immun 62: 4855-4860.
30. Vergauwen B, Pauwels F, Van Beeumen JJ, (2003) Glutathione and catalase provide overlapping defenses for protection against respiration-generated hydrogen peroxide in Haemophilus influenzae. J Bacteriol 185: 5555-5562.
31. Vergauwen B, Herbert M, Van Beeumen JJ, (2006) Hydrogen peroxide scavenging is not a virulence determinant in the pathogenesis of Haemophilus influenzae type b strain Eagan. BMC Microbiol 6: 3.
32. Wong SM, Alugupalli KR, Ram S, Akerley BJ, (2007) The ArcA regulon and oxidative stress resistance in Haemophilus influenzae. Mol Microbiol 64: 1375-1390.
33. Aslund F, Zheng M, Beckwith J, Storz G, (1999) Regulation of the OxyR transcription factor by hydrogen peroxide and the cellular thiol-disulfide status. Proc Natl Acad Sci USA 96: 6161-6165.
34. Anjem A, Varghese S, Imlay JA, (2009) Manganese import is a key element of the OxyR response to hydrogen peroxide in Escherichia coli. Mol Microbiol 72: 844-858.
35. Runyen-Janecky L, Dazenski E, Hawkins S, Warner L, (2006) Role and regulation of the Shigella flexneri Sit and MntH systems. Infect Immun 74: 4666-4672.
36. Seaver LC, Imlay JA, (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183: 7173-7181.
37. Pauwels F, Vergauwen B, Van Beeumen JJ, (2004) Physiological characterization of Haemophilus influenzae Rd deficient in its glutathione-dependent peroxidase PGdx. J Biol Chem 279: 12163-12170.
38. Lushchak VI, (2011) Adaptive response to oxidative stress: Bacteria, fungi, plants and animals. Comp Biochem Physiol C Toxicol Pharmacol 153: 175-190.
39. Zheng M, Aslund F, Storz G, (1998) Activation of the OxyR transcription factor by reversible disulfide bond formation. Science 279: 1718-1721.
40. Gawronski JD, Wong SM, Giannoukos G, Ward DV, Akerley BJ, (2009) Tracking insertion mutants within libraries by deep sequencing and a genome-wide screen for Haemophilus genes required in the lung. Proc Natl Acad Sci USA 106: 16422-16427.
41. Qu J, Lesse AJ, Brauer AL, Cao J, Gill SR, et al. (2010) Proteomic expression profiling of Haemophilus influenzae grown in pooled human sputum from adults with chronic obstructive pulmonary disease reveal antioxidant and stress responses. BMC Microbiol 10: 162.
42. Suzuki K, Bakaletz LO, (1994) Synergistic effect of adenovirus type 1 and nontypeable Haemophilus influenzae in a chinchilla model of experimental otitis media. Infect Immun 62: 1710-1718.
43. Morton DJ, Bakaletz LO, Jurcisek JA, VanWagoner TM, Seale TW, et al. (2004) Reduced severity of middle ear infection caused by nontypeable Haemophilus influenzae lacking the hemoglobin/hemoglobin-haptoglobin binding proteins (Hgp) in a chinchilla model of otitis media. Microb Pathog 36: 25-33.
44. Bakaletz LO, Kennedy B-J, Novotnoy LA, Duquesne G, Cohen J, et al. (1999) Protection against development of otitis media induced by nontypeable Haemophilus influenzae by both active and passive immunization in a chinchilla model of virus-bacterium superinfection. Infect Immun 67: 2746-2762.
45. Harrison A, Dyer DW, Gillaspy A, Ray WC, Mungur R, et al. (2005) Genomic sequence of an otitis media isolate of nontypeable Haemophilus influenzae: comparative study with H. influenzae serotype d, strain KW20. J Bacteriol 187: 4627-4636.
46. Fleischmann RD, Adams MD, White O, Clayton RA, Kirkness EF, et al. (1995) Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269: 496-512.
47. Whitby PW, Morton DJ, Stull TL, (1998) Construction of antibiotic resistance cassettes with multiple paired restriction sites for insertional mutagenesis of Haemophilus influenzae. FEMS Microbiol Lett 158: 57-60.
48. Saeed-Kothe A, Yang W, Mills SD, (2004) Use of the riboflavin synthase gene (ribC) as a model for development of an essential gene disruption and complementation system for Haemophilus influenzae. Appl Environ Microbiol 70: 4136-4143.
49. Poje G, Redfield RJ, (2003) Transformation of Haemophilus influenzae. Methods Mol Med 71: 57-70.
50. Morton DJ, VanWagoner TM, Seale TW, Whitby PW, Stull TL, (2006) Differential utilization by Haemophilus influenzae of hemoglobin complexed to the three human haptoglobin phenotypes. FEMS Immunol Med Microbiol 46: 426-432.
51. VanWagoner TM, Whitby PW, Morton DJ, Seale TW, Stull TL, (2004) Characterization of three new competence-regulated operons in Haemophilus influenzae. J Bacteriol 186: 6409-6421.
52. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCt method. Methods 25: 402-408.
53. Jett BD, Hatter KL, Huycke MM, Gilmore MS, (1997) Simplified agar plate method for quantifying viable bacteria. Biotechniques 23: 648-650.
54. Morton DJ, Hempel RJ, Seale TW, Whitby PW, Stull TL, (2012) A functional tonB gene is required for both virulence and competetive fitness in a chinchilla model of Haemophilus influenzae otitis media. BMC Res Notes 5: 327.
55. Bakaletz LO, Leake ER, Billy JM, Kaumaya PTP, (1997) Relative immunogenicity and efficacy of two synthetic chimeric peptides of fimbrin as vaccinogens against nasopharyngeal colonization by nontypeable Haemophilus influenzae in the chinchilla. Vaccine 15: 955-961.
56. Gitiban N, Jurcisek JA, Harris RH, Mertz SE, Durbin RK, et al. (2005) Chinchilla and murine models of upper respiratory tract infections with respiratory syncytial virus. J Virol 79: 6035-6042.