Burkholderia cenocepacia C5424 produces a pigment with antioxidant properties using a homogentisate intermediate

Journal of Bacteriology

Volumn 189, Issue 24, 2007, Pages 9057-9065

  Keith, Karen E ^a   Killip, Lauren ^a   He, Panqing ^b   Moran, Graham R ^b   Valvano, Miguel A ^a  

^a UNIVERSITY OF WESTERN ONTARIO   (Canada)

^b UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 HYDROXYPHENYLPYRUVATE DIOXYGENASE; AMINOGUANIDINE; DEXTRAN; DIPHENYLIODONIUM SALT; HOMOGENTISIC ACID; HYDROGEN PEROXIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANTIOXIDANT ACTIVITY; ARTICLE; BACTERIAL STRAIN; BURKHOLDERIA CENOCEPACIA; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DISRUPTION; MACROPHAGE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PIGMENTATION; PRIORITY JOURNAL;

4-HYDROXYPHENYLPYRUVATE DIOXYGENASE; ANIMALS; ANTI-BACTERIAL AGENTS; ANTIOXIDANTS; BURKHOLDERIA CEPACIA COMPLEX; CELL LINE; DRUG RESISTANCE, BACTERIAL; GENE DELETION; GENES, BACTERIAL; GENETIC COMPLEMENTATION TEST; HOMOGENTISIC ACID; HYDROGEN PEROXIDE; LYSOSOMES; MACROPHAGES; MELANINS; MICE; MUTAGENESIS, INSERTIONAL; OXIDANTS; PARAQUAT; SUPEROXIDES;

BURKHOLDERIA CENOCEPACIA; BURKHOLDERIA CEPACIA COMPLEX; MURINAE; NEGIBACTERIA;

EID: 37449013335     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.00436-07     Document Type: Article

References (64)

1. Agodi, A., S. Stefani, C. Corsaro, F. Campanile, S. Gribaldo, and G. Sichel. 1996. Study of a melanic pigment of Proteus mirabilis. Res. Microbiol. 147:167-174.
2. Arias-Barrau, E., E. R. Olivera, J. M. Luengo, C. Fernandez, B. Galan, J. L. Garcia, E. Diaz, and B. Minambres. 2004. The homogentisate pathway a central catabolic pathway involved in the degradation of L- phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J. Bacteriol. 186:5062-5077.
3. Aurstad, K., and H. K. Dahle. 1972. The production and some properties of the brown pigment of Aeromonas liquefaciens. Acta Vet. Scand. 13:251-259.
4. Awata, H., F. Endo, and I. Matsuda. 1994. Structure of the human 4-hydroxyphenylpyruvic acid dioxygenase gene (HPD). Genomics 23:534-539.
5. Brownlee, J. M., K. Johnson-Winters, D. H. Harrison, and G. R. Moran. 2004. Structure of the ferrous form of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis in complex with the therapeutic herbicide, NTBC. Biochemistry 43:6370-6377.
6. Byng, G. S., D. C. Eustice, and R. A. Jensen. 1979. Biosynthesis of phenazine pigments in mutant and wild-type cultures of Pseudomonas aeruginosa. J. Bacteriol. 138:846-852.
7. Craig, F. F., J. G. Coote, R. Parton, J. H. Freer, and N. J. Gilmour. 1989. A plasmid which can be transferred between Escherichia coli and Pasteurella haemolytica by electroporation and conjugation. J. Gen. Microbiol. 135:2885-2890.
8. Denoya, C. D., D. D. Skinner, and M. R. Morgenstern. 1994. A Streptomyces avermitilis gene encoding a 4-hydroxyphenylpyruvic acid dioxygenase-like protein that directs the production of homogentisic acid and an ochronotic pigment in Escherichia coli. J. Bacteriol. 176:5312-5319.
9. Endo, F., H. Awata, H. Katoh, and I. Matsuda. 1995. A nonsense mutation in the 4-hydroxyphenylpyruvic acid dioxygenase gene (Hpd) causes skipping of the constitutive exon and hypertyrosinemia in mouse strain III. Genomics 25:164-169.
10. Endo, F., H. Awata, A. Tanoue, M. Ishiguro, Y. Eda, K. Titani, and I. Matsuda. 1992. Primary structure deduced from complementary DNA sequence and expression in cultured cells of mammalian 4-hydroxyphenylpyruvic acid dioxygenase. Evidence that the enzyme is a homodimer of identical subunits homologous to rat liver-specific alloantigen F. J. Biol. Chem. 267:24235-24240.
11. Figurski, D. H., and D. R. Helinski. 1979. Replication of an origin-containing derivative of plasmid RK2 dependent on a plasmid function provided in trans. Proc. Natl. Acad. Sci. USA 76:1648-1652.
12. Flannagan, R. S., D. Aubert, C. Kooi, P. A. Sokol, and M. A. Valvano. 2007. Burkholderia cenocepacia requires a periplasmic HtrA protease for grown under thermal and osmotic stress and for survival in vivo. Infect. Immun. 75:1679-1689.
13. Frases, S., A. Salazar, E. Dadachova, and A. Casadevall. 2007. Cryptococcus neoformans can utilize the bacterial melanin precursor homogentisic acid for fungal melanogenesis. Appl. Environ Microbiol. 73:615-621.
14. Fritze, I. M., L. Linden, J. Freigang, G. Auerbach, R. Huber, and S. Steinbacher. 2004. The crystal structures of Zea mays and Arabidopsis 4-hydroxyphenylpyruvate dioxygenase. Plant Physiol. 134:1388-1400.
15. Garcia, I., D. Job, and M. Matringe. 2000. Inhibition of p-hydroxyphenylpyruvate dioxygenase by the diketonitrile of isoxaflutolc: a case of half-site reactivity. Biochemistry 39:7501-7507.
16. Garcia, I., M. Rodgers, C. Lenne, A. Rolland, A. Sailland, and M. Matringe. 1997. Subcellular localization and purification of a p-hydroxyphenylpyruvate dioxygenase from cultured carrot cells and characterization of the corresponding cDNA. Biochem. J. 325:761-769.
17. Govan, J. R. W., and V. Deretic. 1996. Microbial pathogenesis in cystic fibrosis: mucoid Pseudomonas aeruginosa and Burkholderia cepacia. Microbiol. Rev. 60:539-574.
18. Hanley, W. B. 2004. Adult phenylketonuria. Am. J. Med. 117:590-595.
19. 70. J. Mol Biol. 366:1374-1386.
20. Ikeda, K., T. Masujima, K. Suzuki, and M. Sugiyama. 1996. Cloning and sequence analysis of the highly expressed melanin-synthesizing gene operon from Streptomyces castaneoglobisporus. Appl. Microbiol. Biotechnol. 45:80-85.
21. Isles, A., I. Maclusky, M. Corey, R. Gold, C. Prober, P. Fleming, and H. Levison. 1984. Pseudomonas cepacia infection in cystic fibrosis: an emerging problem. J. Pediatr. 104:206-210.
22. Johnson-Winters, K., V. M. Purpero, M. Kavana, and G. R. Moran. 2005. Accumulation of multiple intermediates in the catalytic cycle of (4-hydroxyphenyl)pyruvate dioxygenase from Streptomyces avermitilis. Biochemistry 44:7189-7199.
23. Kavana, M., and G. R. Moran. 2003. Interaction of (4-hydroxyphenyl)pyruvate dioxygenase with the specific inhibitor 2-[2-nitro-4-(trifluoromethyl)benzoyl]-1,3-cyclohexanedione. Biochemistry 42:10238-10245.
24. Keith, K. E., and M. A. Valvano. 2007. Characterization of SodC, a periplasmic superoxide dismutase from Burkholderia cenocepacia. Infect. Immun. 75:2451-2460.
25. Keon, J., and J. Hargreaves. 1998. Isolation and heterologous expression of a gene encoding 4-hydroxyphenylpyruvate dioxygenase from the wheat leaf-spot pathogen, Mycosphaerella graminicola. FEMS Microbiol. Lett. 161:337-343.
26. Kotob, S. I., S. L. Coon, E. J. Quintero, and R. M. Weiner. 1995. Homogentisic acid is the primary precursor of melanin synthesis in Vibrio cholerae, a Hyphomonas strain, and Shewanella colwelliana. Appl. Environ. Microbiol. 61:1620-1622.
27. Lamothe, J., K. K. Huynh, S. Grinstein, and M. A. Valvano. 2006. Intracellular survival of Burkholderia cenocepacia in macrophages is associated with a delay in the maturation of bacteria-containing vacuoles. Cell Microbiol. 9:40-53.
28. Lamothe, J., S. Thyssen, and M. A. Valvano. 2004. Burkholderia cepacia complex isolates survive intracellularly without replication within acidic vacuoles of Acanthamoeba polyphaga. Cell Microbiol. 6:1127-1138.
29. Ledson, M. J., M. J. Gallagher, M. Jackson, C. A. Hart, and M. J. Walshaw. 2002. Outcome of Burkholderia cepacia colonisation in an adult cystic fibrosis centre. Thorax 57:142-145.
30. Lefebre, M. D., and M. A. Valvano. 2001. Catalases and superoxide dismutases in strains of the Burkholderia cepacia complex and their roles in resistance to reactive oxygen species. Microbiology 147:97-109.
31. Leinberger, R., W. E. Hull, H. Simon, and J. Retey. 1981. Steric course of the NIH shift in the enzymic formation of homogentisic acid. Eur. J. Biochem. 117:311-318.
32. Liu, G. Y., K. S. Doran, T. Lawrence, N. Turkson, M. Puliti, L. Tissi, and V. Nizet. 2004. Sword and shield: linked group B streptococcal beta-hemolysin/cytolysin and carotenoid pigment function to subvert host phagocyte defense. Proc. Natl. Acad. Sci. USA 101:14491-14496.
33. Mahenthiralingam, E., T. Coenye, J. W. Chung, D. P. Speert, J. R. Govan, P. Taylor, and P. Vandamme. 2000. Diagnostically and experimentally useful panel of strains from the Burkholderia cepacia complex. J. Clin. Microbiol. 38:910-913.
34. Marolda, C. L., B. Hauröder, M. A. John, R. Michel, and M. A. Valvano. 1999. Intracellular survival and saprophytic growth of isolates from the Burkholderia cepacia complex in free-living amoebae. Microbiology 145:1509-1517.
35. McDowell, A., E. Mahenthiralingam, K. E. Dunbar, J. E. Moore, M. Crowe, and J. S. Elborn. 2004. Epidemiology of Burkholderia cepacia complex species recovered from cystic fibrosis patients: issues related to patient segregation. J. Med. Microbiol. 53:663-668.
36. Norris, S. R., X. Shen, and D. DellaPenna. 1998. Complementation of the Arabidopsis pds1 mutation with the gene encoding p-hydroxyphenylpyruvate dioxygenase. Plant Physiol. 117:1317-1323.
37. Nosanchuk, J. D., and A. Casadevall. 2003. The contribution of melanin to microbial pathogenesis. Cell Microbiol. 5:203-223.
38. Nosanchuk, J. D., and A. Casadevall. 2006. Impact of melanin on microbial virulence and clinical resistance to antimicrobial compounds. Antimicrob. Agents Chemother. 50:3519-3528.
39. Pace, C. N., F. Vajdos, L. Fee, G. Grimsley, and T. Gray. 1995. How to measure and predict the molar absorption coefficient of a protein. Protein Sci. 4:2411-2423.
40. Page, W. J., and S. Shivprasad. 1995. Iron binding to Azotobacter salinestris melanin, iron mobilization and uptake mediated by siderophores. Biometals 8:59-64.
41. Purpero, V. M., and G. R. Moran. 2006. Catalytic, noncatalytic, and inhibitory phenomena: kinetic analysis of (4-hydroxyphenyl)pyruvate dioxygenase from Arabidopsis thaliana. Biochemistry 45:6044-6055.
42. Riley, P. A. 1997. Melanin. Int. J. Biochem. Cell. Biol. 29:1235-1239.
43. Romero-Martinez, R., M. Wheeler, A. Guerrero-Plata, G. Rico, and H. Torres-Guerrero. 2000. Biosynthesis and functions of melanin in Sporothrix schenckii. Infect. Immun. 68:3696-3703.
44. Ruetschi, U., A. Dellsen, P. Sahlin, G. Stenman, L. Rymo, and S. Lindstedt. 1993. Human 4-hydroxyphenylpyruvate dioxygenase. Primary structure and chromosomal localization of the gene. Eur. J. Biochem. 213:1081-1089.
45. Ruetschi, U., B. Odelhog, S. Lindstedt, J. Barros-Soderling, B. Persson, and H. Jornvall. 1992. Characterization of 4-hydroxyphenylpyruvate dioxygenase. Primary structure of the Pseudomonas enzyme. Eur. J. Biochem. 205:459-466.
46. Rundgren, M. 1977. Steady state kinetics of 4- hydroxyphenylpyruvate dioxygenase from human liver (III). J. Biol. Chem. 252:5094-5099.
47. Rundgren, M. 1982. Tritium isotope effects in the reaction catalyzed by 4-hydroxyphenylpyruvate dioxygenase from Pseudomonas sp. strain P.J. 874. Biochim. Biophys. Acta 704:59-65.
48. Russo, P. A., G. A. Mitchell, and R. M. Tanguay. 2001. Tyrosinemia: a review. Pediatr. Dev. Pathol. 4:212-221.
49. Saini, L., S. Galsworthy, M. John, and M. A. Valvano. 1999. Intracellular survival of Burkholderia cepacia complex isolates in the presence of macrophage cell activation. Microbiology 145:3465-3475.
50. Schnell, S., and H. M. Steinman. 1995. Function and stationary-phase induction of periplasmic copper-zinc superoxide dismutase and catalase/peroxidase in Caulobacter crescentus. J. Bacteriol. 177:5924-5929.
51. Schnitzler, N., H. Peltroche-Llacsahuanga, N. Bestier, J. Zundorf, R. Lutticken, and G. Haase. 1999. Effect of melanin and carotenoids of Exophiala (Wangiella) dermatitidis on phagocytosis, oxidative burst, and killing by human neutrophils. Infect. Immun. 67:94-101.
52. Scriver, C. R. 1996. Alkaptonuria: such a long journey. Nat. Genet. 14:5-6.
53. Serre, L., A. Sailland, D. Sy, P. Boudec, A. Rolland, E. Pebay-Peyroula, and C. Cohen-Addad. 1999. Crystal structure of Pseudomonas fluorescens 4-hydroxyphenylpyruvate dioxygenase: an enzyme involved in the tyrosine degradation pathway. Structure 7:977-988.
54. Shivprasad, S., and W. J. Page. 1989. Catechol formation and melanization by Na-dependent Azotobacter chroococcum: a protective mechanism for aeroadaptation? Appl. Environ Microbiol. 55:1811-1817.
55. -.. Free Radic. Biol. Med. 11:1-8.
56. Speert, D. P., D. Henry, P. Vandamme, M. Corey, and E. Mahenthiralingam. 2002. Epidemiology of Burkholderia cepacia complex in patients with cystic fibrosis, Canada. Emerg. Infect. Dis. 8:181-187.
57. Steinert, M., M. Flugel, M. Schuppler, J. H. Helbig, A. Supriyono, P. Proksch, and P. C. Luck. 2001. The Lly protein is essential for p-hydroxyphenylpyruvate dioxygenase activity in Legionella pneumophila. FEMS Microbiol. Lett. 203:41-47.
58. Tablan, O. C., T. L. Chroba, D. V. Schidlow, J. W. White, K. A. Hardy, P. H. Giligan, W. M. Morgan, L. A. Chow, W. J. Martone, and W. R. Jarvis. 1985. Pseudomonas cepacia colonization in patients with cystic fibrosis: risk factors and clinical outcome. J. Pediatr. 107:382-387.
59. Vandamme, P., B. Holmes, T. Coenye, J. Goris, E. Mahenthiralingam, J. J. LiPuma, and J. R. Govan. 2003. Burkholderia cenocepacia sp. nov. - a new twist to an old story. Res. Microbiol. 154:91-96.
60. Wang, Y., P. Aisen, and A. Casadevall. 1995. Cryptococcus neoformans melanin and virulence: mechanism of action. Infect. Immun. 63:3131-3136.
61. Wang, Y., and A. Casadevall. 1994. Susceptibility of melanized and nonmelanized Cryptococcus neoformans to nitrogen- and oxygen-derived oxidants. Infect. Immun. 62:3004-3007.
62. Wiater, L. A., A. B. Sadosky, and H. A. Shuman. 1994. Mutagenesis of Legionella pneumophila using Tn903 dlllacZ: identification of a growth-phase-regulated pigmentation gene. Mol. Microbiol. 11:641-653.
63. Wyckoff, E. E., E. J. Pishko, T. N. Kirkland, and G. T. Cole. 1995. Cloning and expression of a gene encoding a T-cell reactive protein from Coccidioides immitis: homology to 4-hydroxyphenylpyruvate dioxygenase and the mammalian F antigen. Gene 161:107-111.
64. Zughaier, S. M., H. C. Ryley, and S. K. Jackson. 1999. A melanin pigment purified from an epidemic strain of Burkholderia cepacia attenuates monocytic respiratory burst activity by scavenging superoxide anion. Infect. Immun. 67:908-913.