1887

Microbiology Society logo

Volume 153, Issue 4

catalase shares surface-predicted epitopes with mammalian catalases Free

Abstract

colonizes the murine intestine and has been associated with hepatic inflammation and neoplasia in susceptible mouse strains. In this study, the catalase of an enterohepatic was characterized for the first time. catalase is a highly conserved enzyme that may be important for bacterial survival in the mammalian intestine. Recombinant catalase was expressed in in order to verify its enzymic activity . catalase comprises 478 amino acids with a highly conserved haem-ligand domain. Three conserved motifs (R-F-Y-D, RERIPER and VVHAKG) in the haem-ligand domain and three surface-predicted motifs were identified in catalase and are shared among bacterial and mammalian catalases. catalase is present in the cytoplasmic and periplasmic compartments. Mice infected with demonstrated immune responses to murine and catalase, suggesting that catalase contains conserved structural motifs and may contribute to autoimmune responses. Antibodies to catalase recognized murine hepatocyte catalase in hepatic tissue from infected mice. Antibodies from sera of -infected mice reacted with peptides comprising two conserved surface-predicted motifs in catalase. Catalases are highly conserved enzymes in bacteria and mammals that may contribute to autoimmune responses in animals infected with catalase-producing pathogens.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): HRP, horseradish peroxidase and ROS, reactive oxygen species
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.29184-0
2007-04-01
2024-04-25
Loading full text...

Full text loading...

/deliver/fulltext/micro/153/4/1006.html?itemId=/content/journal/micro/10.1099/mic.0.29184-0&mimeType=html&fmt=ahah

References

  1. Avenaud P., Le Bail B., Mayo K., Marais A., Fawaz R., Bioulac-Sage P., Megraud F. 2003; Natural history of Helicobacter hepaticus infection in conventional A/J mice, with special reference to liver involvement. Infect Immun 71:3667–3672 [CrossRef]
     [Google Scholar]
  2. Bai Y., Zhang Y. L., Jin J. F., Wang J. D., Zhang Z. S., Zhou D. Y. 2003; Recombinant Helicobacter pylori catalase. World J Gastroenterol 9:1119–1122
     [Google Scholar]
  3. Basu M., Czinn S. J., Blanchard T. G. 2004; Absence of catalase reduces long-term survival of Helicobacter pylori in macrophage phagosomes. Helicobacter 9:211–216 [CrossRef]
     [Google Scholar]
  4. Beers R. F. Jr, Sizer I. W. 1952; A spectrophotometric method for measuring the breakdown of hydrogen peroxide by catalase. J Biol Chem 195:133–140
     [Google Scholar]
  5. Bergman M., Del Prete G., Appelmelk B., van Kooyk Y. 2006; Helicobacter pylori phase variation, immune modulation and gastric autoimmunity. Nat Rev Microbiol 4:151–159 [CrossRef]
     [Google Scholar]
  6. Brown S. M., Howell M. L., Vasil M. L., Anderson A. J., Hassett D. J. 1995; Cloning and characterization of the katB gene of Pseudomonas aeruginosa encoding a hydrogen peroxide-inducible catalase: purification of KatB, cellular localization, and demonstration that it is essential for optimal resistance to hydrogen peroxide. J Bacteriol 177:6536–6544
     [Google Scholar]
  7. Chen M., Chen J., Liao W., Zhu S., Yu J., Leung W. K., Hu P., Sung J. J. Y. 2003; Immunization with attenuated Salmonella typhimurium producing catalase in protection against gastric Helicobacter pylori infection in mice. Helicobacter 8:613–625 [CrossRef]
     [Google Scholar]
  8. Corpet F. 1988; Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890 [CrossRef]
     [Google Scholar]
  9. Dassanayake R. P., Griep M. A., Duhamel G. E. 2005; The cytolethal distending toxin B sub-unit of Helicobacter hepaticus is a Ca2+- and Mg2+-dependent neutral nuclease. FEMS Microbiol Lett 251:219–225 [CrossRef]
     [Google Scholar]
  10. D'Elios M. M., Appelmelk B. J., Amedei A., Bergman M. P., Prete G. D. 2004; Gastric autoimmunity: the role of Helicobacter pylori and molecular mimicry. Trends Mol Med 10:316–323 [CrossRef]
     [Google Scholar]
  11. Fita I., Rossmann M. G. 1985; The active center of catalase. J Mol Biol 185:21–37 [CrossRef]
     [Google Scholar]
  12. Foltz C. J., Fox J. G., Cahill R., Murphy J. C., Yan L., Shames B., Schauer D. B. 1998; Spontaneous inflammatory bowel disease in multiple mutant mouse lines: association with colonization by Helicobacter hepaticus . Helicobacter 3:69–78 [CrossRef]
     [Google Scholar]
  13. Fox J. G., Dewhirst F. E., Tully J. G., Paster B. J., Yan L., Taylor N. S., Gorelick P. L., Ward J. M., Collins M. J. Jr 1994; Helicobacter hepaticus sp. nov., a microaerophilic bacterium isolated from livers and intestinal mucosal scrapings from mice. J Clin Microbiol 32:1238–1245
     [Google Scholar]
  14. Fox J. G., Li X., Yan L., Cahill R. J., Hurley R., Lewis R., Murphy J. C. 1996; Chronic proliferative hepatitis in A/JCr mice associated with persistent Helicobacter hepaticus infection: a model of Helicobacter -induced carcinogenesis. Infect Immun 64:1548–1558
     [Google Scholar]
  15. Ge Z., Feng Y., Whary M. T., Nambiar P. R., Xu S., Ng V., Taylor N. S., Fox J. G. 2005; Cytolethal distending toxin is essential for Helicobacter hepaticus colonization in outbred Swiss Webster mice. Infect Immun 73:3559–3567 [CrossRef]
     [Google Scholar]
  16. Guex N., Peitsch M. C. 1997; SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18:2714–2723 [CrossRef]
     [Google Scholar]
  17. Hagen T. M., Huang S., Curnutte J., Fowler P., Martinez V., Wehr C. M., Ames B. N., Chisari F. V. 1994; Extensive oxidative DNA damage in hepatocytes of transgenic mice with chronic active hepatitis destined to develop hepatocellular carcinoma. Proc Natl Acad Sci U S A 91:12808–12812 [CrossRef]
     [Google Scholar]
  18. Harris A. G., Hazell S. L. 2003; Localisation of Helicobacter pylori catalase in both the periplasm and cytoplasm, and its dependence on the twin-arginine target protein, KapA, for activity. FEMS Microbiol Lett 229:283–289 [CrossRef]
     [Google Scholar]
  19. Harris A. G., Hinds F. E., Beckhouse A. G., Kolesnikow T., Hazell S. L. 2002; Resistance to hydrogen peroxide in Helicobacter pylori : role of catalase (KatA) and Fur, and functional analysis of a novel gene product designated ‘KatA-associated protein’, KapA (HP0874). Microbiology 148:3813–3825
     [Google Scholar]
  20. Hazell S. L., Graham D. Y., Evans D. J. Jr 1991; Helicobacter pylori catalase. J Gen Microbiol 137:57–61 [CrossRef]
     [Google Scholar]
  21. Herbert D. P. J. 1948; Crystalline bacterial catalase. Biochem J 43:193–202
     [Google Scholar]
  22. Hoffman C. S., Wright A. 1985; Fusions of secreted proteins to alkaline phosphatase: an approach for studying protein secretion. Proc Natl Acad Sci U S A 82:5107–5111 [CrossRef]
     [Google Scholar]
  23. Hooft R. W., Vriend G., Sander C., Abola E. E. 1996; Errors in protein structures. Nature 381:272
     [Google Scholar]
  24. Hynes S. O., Keenan J. I., Ferris J. A., Annuk H., Moran A. P. 2005; Lewis epitopes on outer membrane vesicles of relevance to Helicobacter pylori pathogenesis. Helicobacter 10:146–156 [CrossRef]
     [Google Scholar]
  25. Inouye H., Barnes W., Beckwith J. 1982; Signal sequence of alkaline phosphatase of Escherichia coli . J Bacteriol 149:434–439
     [Google Scholar]
  26. Klotz M. G., Hutcheson S. W. 1992; Multiple periplasmic catalases in phytopathogenic strains of Pseudomonas syringae . Appl Environ Microbiol 58:2468–2473
     [Google Scholar]
  27. Klotz M. G., Klassen G. R., Loewen P. C. 1997; Phylogenetic relationships among prokaryotic and eukaryotic catalases. Mol Biol Evol 14:951–958 [CrossRef]
     [Google Scholar]
  28. Kono Y., Fridovich I. 1983; Isolation and characterization of the pseudocatalase of Lactobacillus plantarum . J Biol Chem 258:6015–6019
     [Google Scholar]
  29. Loewen P. C., Carpena X., Rovira C., Ivancich A., Perez-Luque R., Haas R., Odenbreit S., Nicholls P., Fita I. 2004; Structure of Helicobacter pylori catalase, with and without formic acid bound, at 1.6 Å resolution. Biochemistry 43:3089–3103 [CrossRef]
     [Google Scholar]
  30. Mayfield J. E., Duvall M. R. 1996; Anomalous phylogenies based on bacterial catalase gene sequences. J Mol Evol 42:469–471 [CrossRef]
     [Google Scholar]
  31. Miura H., Tobe T., Miura K., Kobayashi K., Higashi T. 2000; Identification of epitopes for cross-reaction, auto-reaction and autoantibodies to catalase. J Autoimmun 15:433–440 [CrossRef]
     [Google Scholar]
  32. Murthy M. R., Sicignano A., Tanaka N., Rossmann M. G., Reid T. J. III 1981; Structure of beef liver catalase. J Mol Biol 152:465–499 [CrossRef]
     [Google Scholar]
  33. Orth T., Kellner R., Diekmann O., Faust J., Mayet W. J., Meyer zum Buschenfelde K. H. 1998; Identification and characterization of autoantibodies against catalase and alpha-enolase in patients with primary sclerosing cholangitis. Clin Exp Immunol 112:507–515 [CrossRef]
     [Google Scholar]
  34. Peitsch M. C., Wells T. N., Stampf D. R., Sussman J. L. 1995; The Swiss-3DImage collection and PDB-Browser on the World-Wide Web. Trends Biochem Sci 20:82–84 [CrossRef]
     [Google Scholar]
  35. Pena J. A., Rogers A. B., Ge Z., Ng V., Li S. Y., Fox J. G., Versalovic J. 2005; Probiotic Lactobacillus spp. diminish Helicobacter hepaticus -induced inflammatory bowel disease in interleukin-10-deficient mice. Infect Immun 73:912–920 [CrossRef]
     [Google Scholar]
  36. Pitson S. M., Mendz G. L., Srinivasan S., Hazell S. L. 1999; The tricarboxylic acid cycle of Helicobacter pylori . Eur J Biochem 260:258–267 [CrossRef]
     [Google Scholar]
  37. Pratt J. S., Sachen K. L., Wood H. D., Eaton K. A., Young V. B. 2006; Modulation of host immune responses by the cytolethal distending toxin of Helicobacter hepaticus . Infect Immun 74:4496–4504 [CrossRef]
     [Google Scholar]
  38. Putnam C. D., Arvai A. S., Bourne Y., Tainer J. A. 2000; Active and inhibited human catalase structures: ligand and NADPH binding and catalytic mechanism. J Mol Biol 296:295–309 [CrossRef]
     [Google Scholar]
  39. Radcliff F. J., Hazell S. L., Kolesnikow T., Doidge C., Lee A. 1997; Catalase, a novel antigen for Helicobacter pylori vaccination. Infect Immun 65:4668–4674
     [Google Scholar]
  40. Roozendaal C., Zhao M. H., Horst G., Lockwood C. M., Kleibeuker J. H., Limburg P. C., Nelis G. F., Kallenberg C. G. 1998; Catalase and alpha-enolase: two novel granulocyte autoantigens in inflammatory bowel disease (IBD. Clin Exp Immunol 112:10–16 [CrossRef]
     [Google Scholar]
  41. Schwede T., Kopp J., Guex N., Peitsch M. C. 2003; SWISS-MODEL: an automated protein homology-modeling server. Nucleic Acids Res 31:3381–3385 [CrossRef]
     [Google Scholar]
  42. Sha Z., Stabel T. J., Mayfield J. E. 1994; Brucella abortus catalase is a periplasmic protein lacking a standard signal sequence. J Bacteriol 176:7375–7377
     [Google Scholar]
  43. Sipowicz M. A., Chomarat P., Diwan B. A., Anver M. A., Awasthi Y. C., Ward J. M., Rice J. M., Kasprzak K. S., Wild C. P., Anderson L. M. 1997; Increased oxidative DNA damage and hepatocyte overexpression of specific cytochrome P450 isoforms in hepatitis of mice infected with Helicobacter hepaticus . Am J Pathol 151:933–941
     [Google Scholar]
  44. Smith P. K., Krohn R. I., Hermanson G. T., Mallia A. K., Gartner F. H., Provenzano M. D., Fujimoto E. K., Goeke N. M., Olson B. J., Klenk D. C. 1985; Measurement of protein using bicinchoninic acid. Anal Biochem 150:76–85 [CrossRef]
     [Google Scholar]
  45. Suerbaum S., Josenhans C., Sterzenbach T., Drescher B., Brandt P., Bell M., Droge M., Fartmann B., Fischer H. P. other authors 2003; The complete genome sequence of the carcinogenic bacterium Helicobacter hepaticus . Proc Natl Acad Sci U S A 100:7901–7906 [CrossRef]
     [Google Scholar]
  46. Visick K. L., Ruby E. G. 1998; The periplasmic, group III catalase of Vibrio fischeri is required for normal symbiotic competence and is induced both by oxidative stress and by approach to stationary phase. J Bacteriol 180:2087–2092
     [Google Scholar]
  47. von Ossowski I., Hausner G., Loewen P. C. 1993; Molecular evolutionary analysis based on the amino acid sequence of catalase. J Mol Evol 37:71–76 [CrossRef]
     [Google Scholar]
  48. Wang D. H., Tsutsui K., Sano K., Masuoka N., Kira S. 2001; cDNA cloning and expression of mutant catalase from the hypocatalasemic mouse: comparison with the acatalasemic mutant. Biochim Biophys Acta 1522:217–220 [CrossRef]
     [Google Scholar]
  49. Ward J. M., Anver M. R., Haines D. C., Benveniste R. E. 1994a; Chronic active hepatitis in mice caused by Helicobacter hepaticus . Am J Pathol 145:959–968
     [Google Scholar]
  50. Ward J. M., Fox J. G., Anver M. R., Haines D. C., George C. V., Collins M. J., Gorelick P. L., Nagashima K., Gonda M. A. & other authors (1994b). Chronic active hepatitis and associated liver tumors in mice caused by a persistent bacterial infection with a novel Helicobacter species. J Natl Cancer Inst 86:1222–1227 [CrossRef]
     [Google Scholar]
  51. Ward J. M., Benveniste R. E., Fox C. H., Battles J. K., Gonda M. A., Tully J. G. 1996; Autoimmunity in chronic active Helicobacter hepatitis of mice. Serum antibodies and expression of heat shock protein 70 in liver. Am J Pathol 148:509–517
     [Google Scholar]
  52. Woodbury W., Spencer A. K., Stahman M. A. 1971; An improved procedure using ferricyanide for detecting catalase isozymes. Anal Biochem 44:301–305 [CrossRef]
     [Google Scholar]
  53. Yamanishi S., Iizumi T., Watanabe E., Shimizu M., Kamiya S., Nagata K., Kumagai Y., Fukunaga Y., Takahashi H. 2006; Implications for induction of autoimmunity via activation of B-1 cells by Helicobacter pylori urease. Infect Immun 74:248–256 [CrossRef]
     [Google Scholar]
  54. Zamocky M., Koller F. 1999; Understanding the structure and function of catalases: clues from molecular evolution and in vitro mutagenesis. Prog Biophys Mol Biol 72:19–66 [CrossRef]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.29184-0
Loading
Helicobacter hepaticus catalase shares surface-predicted epitopes with mammalian catalases
Microbiology 153, 1006 (2007); https://doi.org/10.1099/mic.0.29184-0
/content/journal/micro/10.1099/mic.0.29184-0
/content/journal/micro/10.1099/mic.0.29184-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error