Glutathione-dependent alcohol dehydrogenase AdhC is required for defense against nitrosative stress in Haemophilus influenzae

Infection and Immunity

Volumn 75, Issue 9, 2007, Pages 4506-4513

  Kidd, Stephen P ^a   Jiang, Donald ^a   Jennings, Michael P ^a   McEwan, Alastair G ^a  

^a UNIVERSITY OF QUEENSLAND   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALCOHOL DEHYDROGENASE; ESTERASE; GLUTATHIONE; GLUTATHIONE REDUCTASE; MERR PROTEIN; NITROGEN; REGULATOR PROTEIN; S NITROSOGLUTATHIONE;

ADHC GENE; ARTICLE; BACTERIAL GENE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BACTERIUM ISOLATE; ENZYME ACTIVITY; ESTD GENE; GENE SEQUENCE; GENETIC POLYMORPHISM; GENETIC VARIABILITY; HAEMOPHILUS INFLUENZAE; HOST RESISTANCE; NITROSATIVE STRESS; NMLR GENE; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PRIORITY JOURNAL; PROMOTER REGION;

ALDEHYDE OXIDOREDUCTASES; BASE SEQUENCE; GENE EXPRESSION REGULATION, BACTERIAL; HAEMOPHILUS INFLUENZAE; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; S-NITROSOGLUTATHIONE; TRANSCRIPTION FACTORS;

EID: 34548515549     PISSN: 00199567     EISSN: None     Source Type: Journal    
DOI: 10.1128/IAI.00487-07     Document Type: Article

References (42)

1. Bang, I.-S., L. Liu, A. Vazquez-Torres, M.-L. Crouch, J. S. Stamler, and F. C. Fang. 2006. Maintenance of nitric oxide and redox homeostasis by the Salmonella flavohemoglobin Hmp. J. Biol. Chem. 281:28039-28047.
2. Barber, R. D., and T. J. Donohue. 1998. Function of a glutathione-dependent formaldehyde dehydrogenase in Rhodobacter sphaeroides formaldehyde oxidation and assimilation. Biochemistry 37:530-537.
3. Bolduc, G. R., V. Bouchet, R.-Z. Jiang, J. Geisselsoder, Q. C. Truong-Bolduc, P. A. Rice, S. I. Pelton, and R. Goldstein. 2000. Variability of outer membrane protein P1 and its evaluation as a vaccine candidate against experimental otitis media due to nontypeable Haemophilus influenzae: an unambiguous, multifaceted approach. Infect. Immun. 68:4505-4517.
4. Brown, N. L., J. V. Stoyanov, S. P. Kidd, and J. L. Hobman. 2003. The MerR family of transcriptional regulators. FEMS Microbiol. Rev. 27:145-163.
5. Buster, B. L., A. C. Weintrob, G. C. Townsend, and W. M. Scheld. 1995. Potential role of nitric oxide in the pathophysiology of experimental bacterial meningitis in rats. Infect. Immun. 63:3835-3839.
6. Cody, A. J., D. Field, E. J. Feil, S. Stringer, M. E. Deadman, A. G. Tsolaki, B. Gratz, V. Bouchet, R. Goldstein, D. W. Hood, and E. R. Moxon. 2003. High rates of recombination in otitis media isolates of non-typeable Haemophilus influenzae. Infect. Gen. Evol. 3:57-66.
7. Coleman, H. N., D. A. Daines, J. Jarisch, and A. L. Smith. 2003. Chemically defined media for growth of Haemophilus influenzae strains. J. Clin. Microbiol. 41:4408-4410.
8. Craig, J. E., A. Cliffe, K. Garnett, and N. J. High. 2001. Survival of non-typeable Haemophilus influenzae in macrophages. FEMS Microbiol. Lett. 203:55-61.
9. Erwin, A. L., K. L. Nelson, T. Mhlanga-Mutangadura, P. J. Bonthuis, J. L. Geelhood, G. Morlin, W. C. T. Unrath, J. Campos, D. W. Crook, M. M. Farley, F. W. Henderson, R. F. Jacobs, K. Muhlemann, S. W. Satola, L. van Alphen, M. Golomb, and A. L. Smith. 2005. Characterization of genetic and phenotypic diversity of invasive nontypeable Haemophilus influenzae. Infect. Immun. 73:5853-5863.
10. Fang, F. C. 2004. Antimicrobial reactive oxygen and nitrogen species: concepts and controversies. Nat. Rev. Microbiol. 2:820-832.
11. Fleischmann, R. D., M. D. Adams, O. White, R. A. Clayton, E. F. Kirkness, A. R. Kerlavage, C. J. Bult, J. F. Tomb, B. A. Dougherty, J. M. Merrick, K. McKenney, G. Sutton, W. Fitzhugh, C. Fields, J. D. Gocayne, J. Scott, R. Shirley, L. I. Liu, A. Glodek, J. M. Kelley, J. F. Weidman, C. A. Phillips, T. Spriggs, E. Hedblom, M. D. Cotton, T. R. Utterback, M. C. Hanna, D. T. Nguyen, D. M. Saudek, R. C. Brandon, L. D. Fine, J. L. Fritchman, J. L. Fuhrmann, N. S. M. Geoghagen, C. L. Gnehm, L. A. McDonald, K. V. Small, C. M. Fraser, H. O. Smith, and J. C. Venter. 1995. Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496-512.
12. Gantt, K. R., T. L. Goldman, M. L. McCormick, M. A. Miller, S. M. B. Jeronimo, E. T. Nascimento, B. E. Britigan, and M. E. Wilson. 2001. Oxidative responses of human and murine macrophages during phagocytosis of Leishmania chagasi. J. Immunol. 167:893-901.
13. Herring, C. D., and F. R. Blattner. 2004. Global transcriptional effects of a suppressor tRNA and the inactivation of the regulator frmR. J. Bacteriol. 186:6714-6720.
14. Herriott, R. M., E. M. Meyer, and M. Vogt. 1970. Defined nongrowth media for stage II development of competence in Haemophilus influenzae. J. Bacteriol. 101:517-524.
15. Hickman, J. W., V. C. Witthuhn, Jr., M. Dominguez, and T. J. Donohue. 2004. Positive and negative transcriptional regulators of glutathione-dependent formaldehyde metabolism. J. Bacteriol. 186:7914-7925.
16. Hood, D. W., K. Makepeace, M. E. Deadman, R. F. Rest, P. Thibault, A. Martin, J. C. Richards, and E. R. Moxon. 1999. Sialic acid in the lipopolysaccharide of Haemophilus influenzae: strain distribution, influence on serum resistance and structural characterization. Mol. Microbiol. 33:679-692.
17. Jensen, D. E., G. K. Belka, and G. C. Du Bois. 1998. S-Nitrosoglutathione is a substrate for rat alcohol dehydrogenase class III isoenzyme. Biochem. J. 331:659-668.
18. Kidd, S. P., A. J. Potter, M. A. Apicella, M. P. Jennings, and A G. McEwan. 2005. NmlR of Neisseria gonorrhoeae: a novel redox responsive transcription factor from the MerR family. Mol. Microbiol. 57:1676-1689.
19. Layne, E. 1957. Spectrophotometric and turbidimetric methods for measuring proteins, vol. 3, p. 447-454. Academic Press, New York, NY.
20. Lee, H., A. Andalibi, P. Webster, S.-K. Moon, K. Teufert, S.-H. Kang, J.-D. Li, M. Nagura, T. Ganz, and D. J. Lim. 2004. Antimicrobial activity of innate immune molecules against Streptococcus pneumoniae, Moraxella catarrhalis and nontypeable Haemophilus influenzae. BMC Infect. Dis. 4:12.
21. Lepoivre, M., F. Fieschi, J. Coves, L. Thelander, and M. Fontecave. 1991. Inactivation of ribonucleotide reductase by nitric oxide. Biochem. Biophys. Res. Commun. 179:442-448.
22. Liu, L., A. Hausladen, M. Zeng, L. Que, J. Heitman, and J. S. Stamler. 2001. A metabolic enzyme for S-nitrosothiol conserved from bacteria to humans. Nature 410:490-494.
23. Long, J. P., H. H. Tong, P. A. Shannon, and T. F. DeMaria. 2003. Differential expression of cytokine genes and inducible nitric oxide synthetase induced by opacity phenotype variants of Streptococcus pneumoniae during acute otitis media in the rat. Infect. Immun. 71:5531-5540.
24. Lushchak, V. I. 2001. Oxidative stress and mechanisms of protection against it in bacteria. Biochemistry 66:476-489.
25. Marrs, C. F., G. P. Krasan, K. W. McCrea, D. L. Clemans, and J. R. Gilsdorf. 2001. Haemophilus influenzae: human specific bacteria. Front. Biosci. 6:e41-e60.
26. Meats, E, E. J. Feil, S. Stringer, A. J. Cody, R. Goldstein, J. S. Kroll, T. Popovic, and B. G. Spratt. 2003. Characterization of encapsulated and non-capsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J. Clin. Microbiol. 41:1623-1636.
27. Melhus, A., and A. F. Ryan. 2000. Expression of cytokine genes during pneumococcal and nontypeable Haemophilus influenzae acute otitis media in the rat. Infect. Immun. 68:4024-4031.
28. Orman, K. L., J. L. Shenep, and B. K. English. 1998. Pneumococci stimulate the production of the inducible nitric oxide synthase and nitric oxide by murine macrophages. J. Infect. Dis. 178:1649-1657.
29. Pacelli, R., D. A. Wink, J. A. Cook, M. C. Krishna, W. DeGraff, N. Friedman, M. Tsokos, A. Samuni, and J. B. Mitchell. 1995. Nitric oxide potentiates hydrogen peroxide-induced killing of Escherichia coli. J. Exp. Med. 182:1469-1479.
30. Paget, M. S. B., and M. J. Buttner. 2003. Thiol-based regulatory switches. Annu. Rev. Genet. 37:91-121.
31. Potter, A. J., S. P. Kidd, M. P. Jennings, and A. G. McEwan. 2007. Evidence for distinctive mechanisms of S-nitrosoglutathione metabolism by AdhC in two closely related species, Neisseria gonorrhoeae and Neisseria meningitidis. Infect. Immun. 75:1534-1536.
32. Rao, V. K., G. P. Krasan, D. R. Hendrixson, S. Dawid, and J. W. St. Geme. 1999. Molecular determinants of the pathogenesis of disease due to non-typeable Haemophilus influenzae. FEMS Microbiol. Rev. 23:99-129.
33. Ras, J., P. Van Ophem, W. Reijnders, R. Van Spanning, J. Duine, A. Stouthamer, and N. Harms. 1995. Isolation, sequencing, and mutagenesis of the gene encoding NAD- and glutathione-dependent formaldehyde dehydrogenase (GD-FALDH) from Paracoccus denitrificans, in which GD-FALDH is essential for methylotrophic growth. J. Bacteriol. 177:247-251.
34. Sato, K., C. L. Liebeler, M. K. Quartey, C. T. Le, and G. S. LGeibink. 1999. Middle ear fluid cytokine and inflammatory cell kinetics in the chinchilla otitis media model. Infect. Immun. 67:1943-1946.
35. Schapiro, J. M., S. J. Libby, and F. C. Fang. 2003. Inhibition of bacterial DNA replication by zinc mobilization during nitrosative stress. Proc. Natl. Acad. Sci. USA 100:8496-8501.
36. Stevanin, T. M., N. Ioannidis, C. E. Mills, S. O. Kim, M. N. Hughes, and R. K. Poole. 2000. Flavohemoglobin Hmp affords inducible protection for Escherichia coli respiration, catalyzed by cytochromes bo′ or bd, from nitric oxide. J. Biol. Chem. 275:35868-35875.
37. St. Geme, J. W. 2002. Molecular and cellular determinants of non-typeable Haemophilus influenzae adherence and invasion. Cell. Microbiol. 4:191-200.
38. Storz, G., and J. A. Imlay. 1999. Oxidative stress. Curr. Opin. Microbiol. 2:188-194.
39. 38a. Stroeher, U. H., S. P. Kidd, S. L. Stafford, M. P. Jennings, J. C. Paton, and A. G. McEwan. A pneumococcal MerR-like regulator and S-nitrosoglutathione reductase are required for systemic virulence. J. Infect. Dis., in press.
40. Tong, H. H., Y. Chen, M. James, J. Van Deusen, D. B. Welling, and T. F. DeMaria. 2001. Expression of cytokine and chemokine genes by human middle ear epithelial cells induced by formalin-killed Haemophilus influenzae or its lipooligosaccharide htrB and rfaD mutants. Infect. Immun. 69:3678-3684.
41. Vergauwen, B., F. Pauwels, and J. J. Van Beeumen. 2003. Glutathione and catalase provide overlapping defenses for protection against respiration-generated hydrogen peroxide in Haemophilus influenzae. J. Bacteriol. 185:5555-5562.
42. Yelboina, S, J. Seshadri, M. S. Kumar, and A. Ranjan. 2004. PredictRegulon: a web server for the prediction of the regulatory protein binding sites and operons in prokaryote genomes. Nucleic Acids Res. 32:W318-W320.