Oxidative stress response in the opportunistic oral pathogen Fusobacterium nucleatum

Proteomics

Volumn 11, Issue 10, 2011, Pages 2027-2037

  Steeves, Craig H ^a   Potrykus, Joanna ^a   Barnett, David A ^b   Bearne, Stephen L ^a,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b ATLANTIC CANCER RESEARCH INSTITUTE   (Canada)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

2 DE; Anaerobe; Fusobacterium nucleatum; Microbiology; Oxidative stress; Tandem mass spectrometry

Indexed keywords

ADENOSINE TRIPHOSPHATE; ALKYL HYDROPEROXIDE REDUCTASE; CHAPERONE; FRUCTOSE BISPHOSPHATE ALDOLASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; HYDROGEN PEROXIDE; PROTEIN CLPB; PROTEIN DNAK; PROTEIN HRCA; PROTEIN HTPG; PROTEOME; REACTIVE OXYGEN METABOLITE; THIOREDOXIN REDUCTASE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIUM COLONY; BIOFILM; DENTAL CARIES; FUSOBACTERIUM NUCLEATUM; MASS SPECTROMETRY; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PERIODONTAL DISEASE; PRIORITY JOURNAL; PROTEIN MODIFICATION; TWO DIMENSIONAL GEL ELECTROPHORESIS;

BACTERIAL PROTEINS; CARBOHYDRATE METABOLISM; CHAPERONINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; FUSOBACTERIUM NUCLEATUM; HYDROGEN PEROXIDE; OXIDATIVE STRESS; OXYGEN; PROTEOME; TANDEM MASS SPECTROMETRY;

FUSOBACTERIUM NUCLEATUM; NEGIBACTERIA;

EID: 79955758639     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000631     Document Type: Article

References (77)

1. Piovano, S., Bacteriology of most frequent oral anaerobic infections. Anaerobe 1999, 5, 221-227.
2. Kolenbrander, P. E., Palmer, R. J., Rickard, A. H., Jakubovics, N. S. et al., Bacterial interactions and successions during plaque development. Periodontology 2000 2006, 42, 47-79.
3. Kolenbrander, P. E., London, J., Adhere today, here tomorrow: oral bacterial adherence. J. Bacteriol. 1993, 175, 3247-3252.
4. Zilm, P. S., Rogers, A. H., Co-adhesion and biofilm formation by Fusobacterium nucleatum in response to growth pH. Anaerobe 2007, 13, 146-152.
5. Bradshaw, D. J., Marsh, P. D., Watson, G. K., Allison, C., Role of Fusobacterium nucleatum and coaggregation in anaerobe survival in planktonic and biofilm oral microbial communities during aeration. Infect. Immun. 1998, 66, 4729-4732.
6. Kraus, F. W., Nickerson, J. F., Perry, W. I., Walker, A. P., Peroxide and peroxidogenic bacteria in human saliva. J. Bacteriol. 1957, 73, 727-735.
7. Barnard, J. P., Stinson, M. W., Influence of environmental conditions on hydrogen peroxide formation by Streptococcus gordonii. Infect. Immun. 1999, 67, 6558-6564.
8. Ryan, C. S., Kleinberg, I., Bacteria in human mouths involved in the production and utilization of hydrogen peroxide. Arch. Oral Biol. 1995, 40, 753-763.
9. Sheikhi, M., Bouhafs, R. K., Hammarstrom, K. J., Jarstrand, C., Lipid peroxidation caused by oxygen radicals from Fusobacterium-stimulated neutrophils as a possible model for the emergence of periodontitis. Oral Dis. 2001, 7, 41-46.
10. Shin, J., Ji, S., Choi, Y., Ability of oral bacteria to induce tissue-destructive molecules from human neutrophils. Oral Dis. 2008, 14, 327-334.
11. Saito, Y., Fujii, R., Nakagawa, K. I., Kuramitsu, H. K. et al., Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol. Immunol. 2008, 23, 1-6.
12. Diaz, P. I., Zilm, P. S., Rogers, A. H., Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments. Microbiology 2002, 148, 467-472.
13. Bradshaw, D. J., Marsh, P. D., Allison, C., Schilling, K. M., Effect of oxygen, inoculum composition and flow rate on development of mixed-culture oral biofilms. Microbiology 1996, 142, 623-629.
14. Gursoy, U. K., Pollanen, M., Kononen, E., Uitto, V. J., Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J. Periodontol. 2010, 81, 1084-1091.
15. Cabiscol, E., Tamarit, J., Ros, J., Oxidative stress in bacteria and protein damage by reactive oxygen species. Int. Microbiol. 2000, 3, 3-8.
16. Diaz, P. I., Zilm, P. S., Rogers, A. H., The response to oxidative stress of Fusobacterium nucleatum grown in continuous culture. FEMS Microbiol. Lett. 2000, 187, 31-34.
17. Rolfe, R. D., The role of probiotic cultures in the control of gastrointestinal health. J. Nutr. 2000, 130, 396S-402S.
18. Kapatral, V., Anderson, I., Ivanova, N., Reznik, G. et al., Genome sequence and analysis of the oral bacterium Fusobacterium nucleatum strain ATCC 25586. J. Bacteriol. 2002, 184, 2005-2018.
19. Kapatral, V., Ivanova, N., Anderson, I., Reznik, G. et al., Genome analysis of F. nucleatum sub spp vincentii and its comparison with the genome of F. nucleatum ATCC 25586. Genome Res. 2003, 13, 1180-1189.
20. Karpathy, S. E., Qin, X., Gioia, J., Jiang, H. et al., Genome sequence of Fusobacterium nucleatum subspecies polymorphum - a genetically tractable fusobacterium. PLoS ONE 2007, 2, e659.
21. Imlay, J. A., Cellular defenses against superoxide and hydrogen peroxide. Annu. Rev. Biochem. 2008, 77, 755-776.
22. da Silva, V. L., Diniz, C. G., dos Santos, S. G., Gomes, R. M. et al., Physiological alterations of a Fusobacterium nucleatum strain exposed to oxidative stress. J. Appl. Microbiol. 2007, 103, 20-26.
23. Silva, V. L., Diniz, C. G., Cara, D. C., Santos, S. G. et al., Enhanced pathogenicity of Fusobacterium nucleatum adapted to oxidative stress. Microb. Pathog. 2005, 39, 131-138.
24. Imlay, J. A., Pathways of oxidative damage. Annu. Rev. Microbiol. 2003, 57, 395-418.
25. Santos, S. G., Diniz, C. G., Silva, V. L., Martins, W. A. et al., Effects of oxidative stress on the virulence profile of Prevotella intermedia during experimental infection in gnotobiotic mice. J. Med. Microbiol. 2007, 56, 289-297.
26. Nandakumar, R., Madayiputhiya, N., Fouad, A. F., Proteomic analysis of endodontic infections by liquid chromatography-tandem mass spectrometry. Oral Microbiol. Immunol. 2009, 24, 347-352.
27. Zilm, P. S., Bagley, C. J., Rogers, A. H., Milne, I. R., Gully, N. J., The proteomic profile of Fusobacterium nucleatum is regulated by growth pH. Microbiology 2007, 153, 148-159.
28. Zilm, P. S., Mira, A., Bagley, C. J., Rogers, A. H., Effect of alkaline growth pH on the expression of cell envelope proteins in Fusobacterium nucleatum. Microbiology 2010, 156, 1783-1794.
29. Al-Haroni, M., Skaug, N., Bakken, V., Cash, P., Proteomic analysis of ampicillin-resistant oral Fusobacterium nucleatum. Oral Microbiol. Immunol. 2008, 23, 36-42.
30. Potrykus, J., Mahaney, B., White, R. L., Bearne, S. L., Proteomic investigation of glucose metabolism in the butyrate-producing gut anaerobe Fusobacterium varium. Proteomics 2007, 7, 1839-1853.
31. Bradford, M. M., A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
32. Anderson, N. L., Two Dimensional Gel Electrophoresis: Operation of the ISO-DALT System, Large Scale Biology Press, Rockville, MD 1991.
33. Potrykus, J., White, R. L., Bearne, S. L., Proteomic investigation of amino acid catabolism in the indigenous gut anaerobe Fusobacterium varium. Proteomics 2008, 8, 2691-2703.
34. Seo, Y. H., Carroll, K. S., Profiling protein thiol oxidation in tumor cells using sulfenic acid-specific antibodies. Proc. Natl. Acad. Sci. USA 2009, 106, 16163-16168.
35. Blostein, R., Rutter, W. J., Comparative studies of liver and muscle aldolase. II. Immunochemical and chromatographic differentiation. J. Biol. Chem. 1963, 238, 3280-3285.
36. Noltmann, E. A., Gubler, C. J., Kuby, S. A., Glucose 6-phosphate dehydrogenase (Zwischenferment). I. Isolation of the crystalline enzyme from yeast. J. Biol. Chem. 1961, 236, 1225-1230.
37. Rippa, M., Signorini, M., 6-Phosphogluconate dehydrogenase from Candida utilis. Methods Enzymol. 1975, 41, 237-240.
38. Anda, P., Gebbia, J. A., Backenson, P. B., Coleman, J. L., Benach, J. L., A glyceraldehyde-3-phosphate dehydrogenase homolog in Borrelia burgdorferi and Borrelia hermsii. Infect. Immun. 1996, 64, 262-268.
39. Ferdinand, W., The isolation and specific activity of rabbit-muscle glyceraldehyde phosphate dehydrogenase. Biochem. J. 1964, 92, 578-585.
40. Lowry, O. H., Passonneau, J. V., Phosphoglucomutase kinetics with the phosphates of fructose, glucose, mannose, ribose, and galactose. J. Biol. Chem. 1969, 244, 910-916.
41. Bergmeyer, H. U., Gawehn, K., Grassel, M., in: Bergmeyer, H. U. (Ed.), Methods of Enzymatic Analysis, Academic Press, Inc., New York, NY 1974, pp. 499-500.
42. Poole, L. B., Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch. Biochem. Biophys. 2005, 433, 240-254.
43. Seaver, L. C., Imlay, J. A., Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J. Bacteriol. 2001, 183, 7173-7181.
44. Chuang, M. H., Wu, M. S., Lin, J. T., Chiou, S. H., Proteomic analysis of proteins expressed by Helicobacter pylori under oxidative stress. Proteomics 2005, 5, 3895-3901.
45. Mitsumoto, A., Takanezawa, Y., Okawa, K., Iwamatsu, A., Nakagawa, Y., Variants of peroxiredoxins expression in response to hydroperoxide stress. Free Rad. Biol. Med. 2001, 30, 625-635.
46. Rabilloud, T., Chevallet, M., Luche, S., Leize-Wagner, E., Oxidative stress response: a proteomic view. Expert Rev. Proteomics 2005, 2, 949-956.
47. Weber, H., Engelmann, S., Becher, D., Hecker, M., Oxidative stress triggers thiol oxidation in the glyceraldehyde-3-phosphate dehydrogenase of Staphylococcus aureus. Mol. Microbiol. 2004, 52, 133-140.
48. Wagner, E., Luche, S., Penna, L., Chevallet, M. et al., A method for detection of overoxidation of cysteines: peroxiredoxins are oxidized in vivo at the active-site cysteine during oxidative stress. Biochem. J. 2002, 366, 777-785.
49. Woo, H. A., Kang, S. W., Kim, H. K., Yang, K. S. et al., Reversible oxidation of the active site cysteine of peroxiredoxins to cysteine sulfinic acid. Immunoblot detection with antibodies specific for the hyperoxidized cysteine-containing sequence. J. Biol. Chem. 2003, 278, 47361-47364.
50. Wolf, C., Hochgrafe, F., Kusch, H., Albrecht, D. et al., Proteomic analysis of antioxidant strategies of Staphylococcus aureus: diverse responses to different oxidants. Proteomics 2008, 8, 3139-3153.
51. Lim, J. C., Choi, H. I., Park, Y. S., Nam, H. W. et al., Irreversible oxidation of the active-site cysteine of peroxiredoxin to cysteine sulfonic acid for enhanced molecular chaperone activity. J. Biol. Chem. 2008, 283, 28873-28880.
52. Chuang, M. H., Wu, M. S., Lo, W. L., Lin, J. T. et al., The antioxidant protein alkylhydroperoxide reductase of Helicobacter pylori switches from a peroxide reductase to a molecular chaperone function. Proc. Natl. Acad. Sci. USA 2006, 103, 2552-2557.
53. Fujiwara, N., Nakano, M., Kato, S., Yoshihara, D. et al., Oxidative modification to cysteine sulfonic acid of Cys111 in human copper-zinc superoxide dismutase. J. Biol. Chem. 2007, 282, 35933-35944.
54. Dalle-Donne, I., Rossi, R., Colombo, G., Giustarini, D., Milzani, A., Protein S-glutathionylation: a regulatory device from bacteria to humans. Trends Biochem. Sci. 2009, 34, 85-96.
55. Carlsson, J., Larsen, J. T., Edlund, M. B., Utilization of glutathione (L-gamma-glutamyl-L-cysteinylglycine) by Fusobacterium nucleatum subspecies nucleatum. Oral Microbiol. Immunol. 1994, 9, 297-300.
56. Klatt, P., Lamas, S., Regulation of protein function by S-glutathiolation in response to oxidative and nitrosative stress. Eur. J. Biochem. 2000, 267, 4928-4944.
57. Thomas, J. G., Baneyx, F., ClpB and HtpG facilitate de novo protein folding in stressed Escherichia coli cells. Mol. Microbiol. 2000, 36, 1360-1370.
58. Hwang, N. R., Yim, S. H., Kim, Y. M., Jeong, J. et al., Oxidative modifications of glyceraldehyde-3-phosphate dehydrogenase play a key role in its multiple cellular functions. Biochem. J. 2009, 423, 253-264.
59. Maller, N. C., Schroder, E., Eaton, P., Glyceraldehyde 3-phosphate dehydrogenase is unlikely to mediate hydrogen peroxide signaling: studies with a novel anti-dimedone sulfenic acid antibody. Antioxid. Redox Signal. 2011, 14, 49-60.
60. Grant, C. M., Metabolic reconfiguration is a regulated response to oxidative stress. J. Biol. 2008, 7, 1.0-1.4.
61. Ralser, M., Wamelink, M. M., Kowald, A., Gerisch, B. et al., Dynamic rerouting of the carbohydrate flux is key to counteracting oxidative stress. J. Biol. 2007, 6, 10.00-10.18.
62. Schmalhausen, E. V., Nagradova, N. K., Boschi-Muller, S., Branlant, G., Muronetz, V. I., Mildly oxidized GAPDH: the coupling of the dehydrogenase and acyl phosphatase activities. FEBS Lett. 1999, 452, 219-222.
63. Arutyunova, E. I., Danshina, P. V., Domnina, L. V., Pleten, A. P., Muronetz, V. I., Oxidation of glyceraldehyde-3-phosphate dehydrogenase enhances its binding to nucleic acids. Biochem. Biophys. Res. Commun. 2003, 307, 547-552.
64. Maeda, K., Nagata, H., Yamamoto, Y., Tanaka, M. et al., Glyceraldehyde-3-phosphate dehydrogenase of Streptococcus oralis functions as a coadhesin for Porphyromonas gingivalis major fimbriae. Infect. Immun. 2004, 72, 1341-1348.
65. Palop, A., Rutherford, G. C., Marquis, R. E., Inactivation of enzymes within spores of Bacillus megaterium ATCC 19213 by hydroperoxides. Can. J. Microbiol. 1998, 44, 465-470.
66. Gharbia, S. E., Shah, N., Glucose utilization and growth response to protein hydrolysates by Fusobacterium species. Curr. Microbiol. 1988, 17, 229-234.
67. Bolstad, A. I., Jensen, H. B., Bakken, V., Taxonomy, biology, and periodontal aspects of Fusobacterium nucleatum. Clin. Microbiol. Rev. 1996, 9, 55-71.
68. Shah, H. N., Gharbia, S. E., Ecological events in subgingival dental plaque with reference to Bacteroides and Fusobacterium species. Infection 1989, 17, 264-268.
69. Robrish, S. A., Oliver, C., Thompson, J., Amino acid-dependent transport of sugars by Fusobacterium nucleatum ATCC 10953. J. Bacteriol. 1987, 169, 3891-3897.
70. Nystrom, T., Role of oxidative carbonylation in protein quality control and senescence. EMBO J. 2005, 24, 1311-1317.
71. Kumsta, C., Jakob, U., Redox-regulated chaperones. Biochemistry 2009, 48, 4666-4676.
72. Okano, S., Shibata, Y., Shiroza, T., Abiko, Y., Proteomics-based analysis of a counter-oxidative stress system in Porphyromonas gingivalis. Proteomics 2006, 6, 251-258.
73. Doyle, S. M., Wickner, S., Hsp104 and ClpB: protein disaggregating machines. Trends Biochem. Sci. 2009, 34, 40-48.
74. Kwon, H. Y., Kim, E. H., Tran, T. D., Pyo, S. N., Rhee, D. K., Reduction-sensitive and cysteine residue-mediated Streptococcus pneumoniae HrcA oligomerization in vitro. Mol. Cells 2009, 27, 149-157.
75. Wen, Z. T., Suntharaligham, P., Cvitkovitch, D. G., Burne, R. A., Trigger factor in Streptococcus mutans is involved in stress tolerance, competence development, and biofilm formation. Infect. Immun. 2005, 73, 219-225.
76. Deuerling, E., Patzelt, H., Vorderwulbecke, S., Rauch, T. et al., Trigger factor and DnaK possess overlapping substrate pools and binding specificities. Mol. Microbiol. 2003, 47, 1317-1328.
77. Choi-Rhee, E., Cronan, J. E., The biotin carboxylase-biotin carboxyl carrier protein complex of Escherichia coli acetyl-CoA carboxylase. J. Biol. Chem. 2003, 278, 30806-30812.