Skip to main content
SpringerLink
Log in
Book cover

Studies on Periodontal Disease pp 107–130Cite as

Physiological Roles of a Periodontopathic Bacterial Membrane-Bound Quinol Peroxidase

  • Chapter
  • First Online:

  • 1789 Accesses

Abstract

Quinol peroxidase (QPO) catalyzes peroxidase activity using a quinol on respiratory chain as a substrate. QPO was purified from the membrane fraction of Actinobacillus actinomycetemcomitans, a bacterial species associated with a variety of human infections, including localized aggressive periodontitis (LAP). The cytoplasmic membrane of A. actinomycetemcomitans exhibited QPO-dependent peroxidase activity in the presence of NADH or succinate, known physiological substrates of the respiratory chain. QPO is an approximately 50-kDa protein that contains three heme c molecules. Cloning and sequencing shows that QPO is encoded as a bacterial cytochrome c peroxidase (BCCP) with N-terminal extensions containing an additional potential heme c-binding motif. Despite the high sequence homology to BCCP, QPO does not catalyze peroxidation by cytochrome c. A qpo null mutant exhibits an oxidative stress phenotype, suggesting that QPO plays an important role in scavenging endogenously generated reactive oxygen species (ROS) such as hydrogen peroxide. In addition, the qpo null mutant exhibits reduced production of leukotoxin (LtxA), a secreted bacterial toxin that is known to target human leukocytes and erythrocytes. Screening identified ascofuranone as a highly potent inhibitor of QPO (K i = 9.6 nM). This inhibitor also induced a dose-dependent decrease in the secretion of LtxA, with an associated reduction in the pathogenicity of A. actinomycetemcomitans for HL-60 cells. Thus, inhibitors of QPO are promising candidates as drugs for the treatment and prevention of LAP.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  1. Naqui A, Chance B, Cadenas E (1986) Reactive oxygen intermediates in biochemistry. Annu Rev Biochem 55:137–166

    CAS  PubMed  Google Scholar 

  2. Massey V, Strickland A, Mayhew SG et al (1969) The production of superoxide anion radicals in the reaction of reduced flavins and flavoproteins with molecular oxygen. Biochem Biophys Res Commun 36:891–897

    CAS  PubMed  Google Scholar 

  3. Messner KR, Imlay JA (2002) Mechanism of superoxide and hydrogen peroxide formation by fumarate reductase, succinate dehydrogenase, and aspartate oxidase. J Biol Chem 277:42563–42571

    CAS  PubMed  Google Scholar 

  4. Seaver LC, Imlay JA (2004) Are respiratory enzymes the primary sources of intracellular hydrogen peroxide? J Biol Chem 279:48742–48750

    CAS  PubMed  Google Scholar 

  5. Carlioz A, Touati D (1986) Isolation of superoxide dismutase mutants in Escherichia coli: is superoxide dismutase necessary for aerobic life? EMBO J 5:623–630

    CAS  PubMed Central  PubMed  Google Scholar 

  6. Farr SB, D’Ari R, Touani D (1986) Oxygen-dependent mutagenesis in Escherichia coli lacking superoxide dismutase. Proc Natl Acad Sci U S A 83:8268–8272

    CAS  PubMed Central  PubMed  Google Scholar 

  7. Seaver LC, Imlay JA (2001) Alkyl hydroperoxide reductase is the primary scavenger of endogenous hydrogen peroxide in Escherichia coli. J Bacteriol 183:7173–7181

    CAS  PubMed Central  PubMed  Google Scholar 

  8. Hebrard H, Viala JP, Meresse S et al (2009) Redundant hydrogen peroxide scavengers contribute to Salmonella virulence and oxidative stress resistance. J Bacteriol 191:4605–4614

    CAS  PubMed Central  PubMed  Google Scholar 

  9. Park S, You X, Imlay JA (2005) Substantial DNA damage from submicromolar intracellular hydrogen peroxide detected in Hpx-mutants of Escherichia coli. Proc Natl Acad Sci U S A 102:9317–9322

    CAS  PubMed Central  PubMed  Google Scholar 

  10. Jang S, Imlay JA (2007) Micromolar intracellular hydrogen peroxide disrupts metabolism by damaging iron–sulfur enzymes. J Biol Chem 282:929–937

    CAS  PubMed  Google Scholar 

  11. Sobata JM, Imlay JA (2011) Iron enzyme ribulose-5-phosphate 3-epimerase in Escherichia coli is rapidly damaged by hydrogen peroxide but can be protected by manganese. Proc Natl Acad Sci U S A 108:5402–5407

    Google Scholar 

  12. Anjem A, Imlay JA (2012) Mononuclear iron enzymes are primary targets of hydrogen peroxide stress. J Biol Chem 287:15544–15556

    CAS  PubMed Central  PubMed  Google Scholar 

  13. Mishra S, Imlay JA (2012) Why do bacteria use so many enzymes to scavenge hydrogen peroxide? Arch Biochem Biophys 525:145–160

    CAS  PubMed Central  PubMed  Google Scholar 

  14. Seaver LC, Imlay JA (2001) Hydrogen peroxide fluxes and compartmentalization inside growing Escherichia coli. J Bacteriol 183:7182–7189

    CAS  PubMed Central  PubMed  Google Scholar 

  15. Winterbourn CC, Hampton MB, Livesey JH et al (2006) Modeling the reactions of superoxide and myeloperoxidase in the neutrophil phagosome: implications for microbial killing. J Biol Chem 281:39860–39869

    CAS  PubMed  Google Scholar 

  16. Pericone CD, Overweg K, Hermans PW et al (2000) Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68:3990–3997

    CAS  PubMed Central  PubMed  Google Scholar 

  17. Imlay JA (2009) In: Bock A, Curtiss R III, Kaper JB, Karp PD, Neidhart FC, Nystrom T, Slauch JM, Sqires CL, Ussery D (eds) EcoSal-Escherichia coli and Salmonella: cellular and molecular biology. ASM Press, Washington, DC. Available from http://www.ecosal.org

  18. Loew O (1900) A new enzyme of general occurrence in organisms. Science 11:701–702

    CAS  PubMed  Google Scholar 

  19. Zheng L, Cash VL, Flint DH et al (1998) Assembly of iron–sulfur clusters. Identification of an iscSUA-hscBA-fdx gene cluster from Azotobacter vinelandii. J Biol Chem 273:13264–13272

    CAS  PubMed  Google Scholar 

  20. Lee C, Lee SM, Mukhopadhyay P et al (2004) Redox regulation of OxyR requires specific disulfide bond formation involving a rapid kinetic reaction path. Nat Struct Mol Biol 11:1179–1185

    CAS  PubMed  Google Scholar 

  21. Herbig AF, Helmann JD (2001) Roles of metal ions and hydrogen peroxide in modulating the interaction of the Bacillus subtilis PerR peroxide regulon repressor with operator DNA. Mol Microbiol 41:849–859

    CAS  PubMed  Google Scholar 

  22. Lee JW, Helmann JD (2006) The PerR transcription factor senses H2O2 by metal-catalysed histidine oxidation. Nature 440:363–367

    CAS  PubMed  Google Scholar 

  23. Gaballa A, Helmann JD (2002) A peroxide-induced zinc uptake system plays an important role in protection against oxidative stress in Bacillus subtilis. Mol Microbiol 45:997–1005

    CAS  PubMed  Google Scholar 

  24. Herbert D, Pinsent J (1948) Crystalline bacterial catalase. Biochem J 43:193–202

    CAS  PubMed Central  PubMed  Google Scholar 

  25. Clayton RK (1959) Purified catalase from Rhodopseudomonas spheroides. Biochim Biophys Acta 36:40–47

    CAS  PubMed  Google Scholar 

  26. Bravo J, Verdaguer N, Tormo J et al (1995) Crystal structure of catalase HPII from Escherichia coli. Structure 3:491–502

    CAS  PubMed  Google Scholar 

  27. Bravo J, Mate MJ, Schneider T et al (1999) Structure of catalase HPII from Escherichia coli at 1.9 A resolution. Proteins 34:155–166

    CAS  PubMed  Google Scholar 

  28. Gouet P, Jouve HM, Dideberg O (1995) Crystal structure of Proteus mirabilis PR catalase with and without bound NADPH. J Mol Biol 249:933–954

    CAS  PubMed  Google Scholar 

  29. Murshudov GN, Melik-Adamyan WR, Grebenko AI et al (1992) Three-dimensional structure of catalase from Micrococcus lysodeikticus at 1.5 A resolution. FEBS Lett 312:127–131

    CAS  PubMed  Google Scholar 

  30. Loewen PC, Carpena X, Rovita C (2004) Structure of Helicobacter pylori catalase, with and without formic acid bound, at 1.6 A resolution. Biochemistry 43:3089–3103

    CAS  PubMed  Google Scholar 

  31. Carpena X, Perez R, Ochoa WF (2001) Crystallization and preliminary X-ray analysis of clade I catalases from Pseudomonas syringae and Listeria seeligeri. Acta Crystallogr D Biol Crystallogr 57:1184–1186

    CAS  PubMed  Google Scholar 

  32. Wada K, Tada T, Nakamura Y et al (2002) Crystallization and preliminary X-ray diffraction studies of catalase-peroxidase from Synechococcus PCC 7942. Acta Crystallogr D Biol Crystallogr 58:157–159

    PubMed  Google Scholar 

  33. Bertrand T, Eady NA, Jones JN et al (2004) Crystal structure of Mycobacterium tuberculosis catalase-peroxidase. J Biol Chem 279:38991–38999

    CAS  PubMed  Google Scholar 

  34. Carpena X, Loprasert S, Mongkolsuk S et al (2003) Catalase-peroxidase KatG of Burkholderia pseudomallei at 1.7A resolution. J Mol Biol 327:475–489

    CAS  PubMed  Google Scholar 

  35. Carpena X, Melik-Adamya W, Loewen PC et al (2004) Structure of the C-terminal domain of the catalase-peroxidase KatG from Escherichia coli. Acta Crystallogr D Biol Crystallogr 60:1824–1832

    PubMed  Google Scholar 

  36. Amara P, Andreoletti P, Jouve HM et al (2001) Ligand diffusion in the catalase from Proteus mirabilis: a molecular dynamics study. Protein Sci 10:1927–1935

    CAS  PubMed Central  PubMed  Google Scholar 

  37. Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61:192–208

    CAS  PubMed  Google Scholar 

  38. Hillar A, Peters B, Pauls R et al (2000) Modulation of the activities of catalase-peroxidase HPI of Escherichia coli by site-directed mutagenesis. Biochemistry 59:5868–5875

    Google Scholar 

  39. Regelsberger G, Jakopitsch C, Engleder M et al (1999) Spectral and kinetic studies of the oxidation of monosubstituted phenols and anilines by recombinant Synechocystis catalase-peroxidase compound I. Biochemistry 38:10480–10488

    CAS  PubMed  Google Scholar 

  40. Singh R, Wiseman B, Deemagam T (2008) Comparative study of catalase-peroxidases (KatGs). Arch Biochem Biophys 471:207–214

    CAS  PubMed  Google Scholar 

  41. Christman MF, Stolz G, Ames BN (1989) OxyR, a positive regulator of hydrogen peroxide-inducible genes in Escherichia coli and Salmonella typhimurium, is homologous to a family of bacterial regulatory proteins. Proc Natl Acad Sci U S A 86:3484–3488

    CAS  PubMed Central  PubMed  Google Scholar 

  42. Bsat N, Herbig A, Casillas-Martinez L et al (1998) Bacillus subtilis contains multiple Fur homologues: identification of the iron uptake (Fur) and peroxide regulon (PerR) repressors. Mol Microbiol 29:189–198

    CAS  PubMed  Google Scholar 

  43. Bol DK, Yasbin RE (1994) Analysis of the dual regulatory mechanisms controlling expression of the vegetative catalase gene of Bacillus subtilis. J Bacteriol 176:6744–6748

    CAS  PubMed Central  PubMed  Google Scholar 

  44. Hahn JS, Oh SY, Chater KF et al (2000) H2O2-sensitive fur-like repressor CatR regulating the major catalase gene in Streptomyces coelicolor. J Biol Chem 275:38254–38260

    CAS  PubMed  Google Scholar 

  45. Zou P, Borovok I, Ortiz de Orué Lucana D, Muller D et al (1999) The mycelium-associated Streptomyces reticuli catalase-peroxidase, its gene and regulation by FurS. Microbiology 145:549–559

    CAS  PubMed  Google Scholar 

  46. LeBlanc JJ, Brassinga AK, Ewann F et al (2008) An ortholog of OxyR in Legionella pneumophila is expressed postexponentially and negatively regulates the alkyl hydroperoxide reductase (ahpC2D) operon. J Bacteriol 190:3444–3455

    CAS  PubMed Central  PubMed  Google Scholar 

  47. Loewen PC, Switala J (1988) Purification and characterization of spore-specific catalase-2 from Bacillus subtilis. Biochem Cell Biol 66:707–714

    CAS  PubMed  Google Scholar 

  48. Engelmann S, Lindner C, Hecker M (1995) Cloning, nucleotide sequence, and regulation of katE encoding a sigma B-dependent catalase in Bacillus subtilis. J Bacteriol 177:5598–5605

    CAS  PubMed Central  PubMed  Google Scholar 

  49. Brunder W, Schmidt H, Karch H (1996) KatP, a novel catalase-peroxidase encoded by the large plasmid of enterohaemorrhagic Escherichia coli O157:H7. Microbiology 142(Pt 11):3305–3315

    CAS  PubMed  Google Scholar 

  50. Sha Z, Stabel TJ, Mayfield JE (1994) Brucella abortus catalase is a periplasmic protein lacking a standard signal sequence. J Bacteriol 176:7375–7377

    CAS  PubMed Central  PubMed  Google Scholar 

  51. Whittenbury R (1964) Hydrogen peroxide formation and catalase activity in the lactic acid bacteria. J Gen Microbiol 35:13–26

    CAS  PubMed  Google Scholar 

  52. Johnston MA, Delwiche EA (1965) Distribution and characteristics of the catalases of Lactobacillaceae. J Bacteriol 90:347–351

    CAS  PubMed Central  PubMed  Google Scholar 

  53. Kono Y, Fridovich I (1983) Inhibition and reactivation of Mn-catalase. Implications for valence changes at the active site manganese. J Biol Chem 258:13646–13648

    CAS  PubMed  Google Scholar 

  54. Allgood GS, Perry JJ (1986) Characterization of a manganese-containing catalase from the obligate thermophile Thermoleophilum album. J Bacteriol 168:563–567

    CAS  PubMed Central  PubMed  Google Scholar 

  55. Jacquamet L, Michaud-Soret I, Debaecker-Petit N et al (1997) Magnetization studies of the reduced active form of the catalase from Thermus thermophilus. Angew Chem Int Ed Engl 36:1626–1628

    CAS  Google Scholar 

  56. Robbe-Saule V, Coynault C, Ibanez-Ruiz M et al (2001) Identification of a non-haem catalase in Salmonella and its regulation by RpoS (sigmaS). Mol Microbiol 39:1533–1545

    CAS  PubMed  Google Scholar 

  57. Amo T, Atomi H, Imanaka T (2002) Unique presence of a manganese catalase in a hyperthermophilic archaeon, Pyrobaculum calidifontis VA1. J Bacteriol 184:3305–3312

    CAS  PubMed Central  PubMed  Google Scholar 

  58. Barynin VV, Whittaker MM, Antonyuk SV et al (2001) Crystal structure of manganese catalase from Lactobacillus plantarum. Structure 9:725–738

    CAS  PubMed  Google Scholar 

  59. Antonyuk SV, Melik-Adamyan VR, Popov AN et al (2000) Three-dimensional structure of dimanganese catalase from Thermus thermophilus at 1 A resolution. Kristallografiya 45:111–122

    CAS  Google Scholar 

  60. Beyer WF Jr, Fridovich I (1985) Pseudocatalase from Lactobacillus plantarum: evidence for a homopentameric structure containing two atoms of manganese per subunit. Biochemistry 24:6460–6467

    CAS  PubMed  Google Scholar 

  61. Shank M, Barynin V, Dismukes GC (1994) Protein coordination to manganese determines the high catalytic rate of dimanganese catalases. Comparison to functional catalase mimics. Biochemistry 33:15433–15436

    CAS  PubMed  Google Scholar 

  62. Passardi F, Theiler G, Zamocky M et al (2007) PeroxiBase: the peroxidase database. Phytochemistry 68:1605–1611

    CAS  PubMed  Google Scholar 

  63. Kono Y, Fridovich I (1983) Functional significance of manganese catalase in Lactobacillus plantarum. J Bacteriol 155:742–746

    CAS  PubMed Central  PubMed  Google Scholar 

  64. Martin JE, Imlay JA (2011) The alternative aerobic ribonucleotide reductase of Escherichia coli, NrdEF, is a manganese-dependent enzyme that enables cell replication during periods of iron starvation. Mol Microbiol 80:319–334

    CAS  PubMed Central  PubMed  Google Scholar 

  65. Patzer SI, Hantke K (2001) Dual repression by Fe2+-Fur and Mn2+-MntR of the mntH gene, encoding an NRAMP-like Mn2+ transporter in Escherichia coli. J Bacteriol 183:4806–4813

    CAS  PubMed Central  PubMed  Google Scholar 

  66. Tardat B, Touati D (1991) Two global regulators repress the anaerobic expression of MnSOD in Escherichia coli::Fur (ferric uptake regulation) and Arc (aerobic respiration control). Mol Microbiol 5:455–465

    CAS  PubMed  Google Scholar 

  67. Kim K, Kim IH, Lee KY et al (1988) The isolation and purification of a specific “protector” protein which inhibits enzyme inactivation by a thiol/Fe(III)/O2 mixed-function oxidation system. J Biol Chem 263:4704–4711

    CAS  PubMed  Google Scholar 

  68. Cha MK, Kim HK, Kim IH et al (1995) Thioredoxin-linked “thiol peroxidase” from periplasmic space of Escherichia coli. J Biol Chem 270:28635–28641

    CAS  PubMed  Google Scholar 

  69. Baker LM, Poole LB (2003) Catalytic mechanism of thiol peroxidase from Escherichia coli. Sulfenic acid formation and overoxidation of essential CYS61. J Biol Chem 278:9203–9211

    CAS  PubMed  Google Scholar 

  70. Choi J, Choi S, Cha MK et al (2003) Crystal structure of Escherichia coli thiol peroxidase in the oxidized state: insights into intramolecular disulfide formation and substrate binding in atypical 2-Cys peroxiredoxins. J Biol Chem 278:49478–49486

    CAS  PubMed  Google Scholar 

  71. Hall A, Sankaran B, Poole LB et al (2009) Structural changes common to catalysis in the Tpx peroxiredoxin subfamily. J Mol Biol 393:867–881

    CAS  PubMed Central  PubMed  Google Scholar 

  72. Zhou Y, Wan XY, Wang HL et al (1997) Bacterial scavengase p20 is structurally and functionally related to peroxiredoxins. Biochem Biophys Res Commun 233:848–852

    CAS  PubMed  Google Scholar 

  73. Cha MK, Kim W, Lim CJ et al (2004) Escherichia coli periplasmic thiol peroxidase acts as lipid hydroperoxide peroxidase and the principal antioxidative function during anaerobic growth. J Biol Chem 279:8769–8778

    CAS  PubMed  Google Scholar 

  74. Tao K (2008) Subcellular localization and in vivo oxidation-reduction kinetics of thiol peroxidase in Escherichia coli. FEMS Microbiol Lett 289:41–45

    CAS  PubMed  Google Scholar 

  75. Atack JM, Harvey P, Jones MA et al (2008) The Campylobacter jejuni thiol peroxidases Tpx and Bcp both contribute to aerotolerance and peroxide-mediated stress resistance but have distinct substrate specificities. J Bacteriol 190:5279–5290

    CAS  PubMed Central  PubMed  Google Scholar 

  76. Comtois SL, Gidley MD, Kelly DJ (2003) Role of the thioredoxin system and the thiol-peroxidases Tpx and Bcp in mediating resistance to oxidative and nitrosative stress in Helicobacter pylori. Microbiology 149:121–129

    CAS  PubMed  Google Scholar 

  77. La Carbona S, Sauvageot N, Giard JC et al (2007) Comparative study of the physiological roles of three peroxidases (NADH peroxidase, alkyl hydroperoxide reductase and thiol peroxidase) in oxidative stress response, survival inside macrophages and virulence of Enterococcus faecalis. Mol Microbiol 66:1148–1163

    PubMed  Google Scholar 

  78. Tartaglia LA, Storz G, Ames BN (1989) Identification and molecular analysis of oxyR-regulated promoters important for the bacterial adaptation to oxidative stress. J Mol Biol 210:709–719

    CAS  PubMed  Google Scholar 

  79. Jacobson FS, Morgan RW, Christman MF et al (1989) An alkyl hydroperoxide reductase from Salmonella typhimurium involved in the defense of DNA against oxidative damage. Purification and properties. J Biol Chem 264:1488–1496

    CAS  PubMed  Google Scholar 

  80. Neidhardt FC, Varghn V, Phillips TA et al (1983) Gene-protein index of Escherichia coli K-12. Microbiol Rev 47:231–284

    CAS  PubMed Central  PubMed  Google Scholar 

  81. Andrews SC, Harrison PM, Guest JR (1991) A molecular analysis of the 53.3 minute region of the Escherichia coli linkage map. J Gen Microbiol 137:61–367

    Google Scholar 

  82. Clarke DJ, Mackay CL, Campopiano DJ et al (2009) Interrogating the molecular details of the peroxiredoxin activity of the Escherichia coli bacterioferritin comigratory protein using high-resolution mass spectrometry. Biochemistry 48:3904–3914

    CAS  PubMed  Google Scholar 

  83. Liao SJ, Yang CY, Chin KH et al (2009) Insights into the alkyl peroxide reduction pathway of Xanthomonas campestris bacterioferritin comigratory protein from the trapped intermediate-ligand complex structures. J Mol Biol 390:951–966

    CAS  PubMed  Google Scholar 

  84. Clarke DJ, Ortega XP, Mackay CL et al (2010) Subdivision of the bacterioferritin comigratory protein family of bacterial peroxiredoxins based on catalytic activity. Biochemistry 49:1319–1330

    CAS  PubMed  Google Scholar 

  85. Wang G, Adriana A, Olczak AA et al (2005) Contribution of the Helicobacter pylori thiol peroxidase bacterioferritin comigratory protein to oxidative stress resistance and host colonization. Infect Immun 73:378–384

    CAS  PubMed Central  PubMed  Google Scholar 

  86. Jeong W, Cha MK, Kim IH (2000) Thioredoxin-dependent hydroperoxide peroxidase activity of bacterioferritin comigratory protein (BCP) as a new member of the thiol-specific antioxidant protein (TSA)/alkyl hydroperoxide peroxidase C (AhpC) family. J Biol Chem 275:2924–2930

    CAS  PubMed  Google Scholar 

  87. Wang G, Hong Y, Johnson MK et al (2006) Lipid peroxidation as a source of oxidative damage in Helicobacter pylori: protective roles of peroxiredoxins. Biochim Biophys Acta 1760:1596–1603

    CAS  PubMed  Google Scholar 

  88. Johnson NA, McKenzie RM, Fletcher HM (2011) The bcp gene in the bcp-recA-vimA-vimE-vimF operon is important in oxidative stress resistance in Porphyromonas gingivalis W83. Mol Oral Microbiol 26:62–77

    CAS  PubMed  Google Scholar 

  89. Foumier M, Aubert C, Dermoun Z et al (2006) Response of the anaerobe Desulfovibrio vulgaris Hildenborough to oxidative conditions: proteome and transcript analysis. Biochimie 88:85–94

    Google Scholar 

  90. Lynch RE, Fridovich I (1978) Permeation of the erythrocyte stroma by superoxide radical. J Biol Chem 253:4697–4699

    CAS  PubMed  Google Scholar 

  91. Korshunov SS, Imlay JA (2002) A potential role for periplasmic superoxide dismutase in blocking the penetration of external superoxide into the cytosol of Gram-negative bacteria. Mol Microbiol 43:95–106

    CAS  PubMed  Google Scholar 

  92. Korshunov S, Imlay JA (2006) Detection and quantification of superoxide formed within the periplasm of Escherichia coli. J Bacteriol 188:6326–6334

    CAS  PubMed Central  PubMed  Google Scholar 

  93. De Groote MA, Granger D, Xu Y et al (1995) Genetic and redox determinants of nitric oxide cytotoxicity in a Salmonella typhimurium model. Proc Natl Acad Sci U S A 92:6399–6403

    PubMed Central  PubMed  Google Scholar 

  94. Balashova NV, Park DH, Patel JK et al (2007) Interaction between leukotoxin and Cu, Zn superoxide dismutase in Aggregatibacter actinomycetemcomitans. Infect Immun 75:4490–4497

    CAS  PubMed Central  PubMed  Google Scholar 

  95. Cattoir V, Lemenand O, Avril JL et al (2006) The sodA gene as a target for phylogenetic dissection of the genus Haemophilus and accurate identification of human clinical isolates. Int J Med Microbiol 296:531–540

    CAS  PubMed  Google Scholar 

  96. Zambon JJ (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 12:1–20

    CAS  PubMed  Google Scholar 

  97. Scannapieco FA, Bush RB, Paju S (2003) Periodontal disease as a risk factor for adverse pregnancy outcomes. A systematic review. Ann Periodontol 8:70–78

    PubMed  Google Scholar 

  98. Roos D, van Bruggen R, Meischl C (2003) Oxidative killing of microbes by neutrophiles. Microbes Infect 5:1307–1315

    CAS  PubMed  Google Scholar 

  99. Dongari AI, Miyasaki KT (1991) Sensitivity of Actinobacillus actinomycetemcomitans and Haemophyllus aphrophilus to oxidative killing. Oral Microbiol Immunol 6:363–372

    CAS  PubMed  Google Scholar 

  100. Imlay JA (2002) How oxygen damages microbes: oxygen tolerance and obligate anaerobiosis. Adv Microb Physiol 46:111–153

    CAS  PubMed  Google Scholar 

  101. Smith AH, Imlay JA, Mackie RI (2003) Increasing the oxidative stress response allows Escherichia coli to overcome inhibitory effects of condensed tannins. Appl Environ Microbiol 69:3406–3411

    CAS  PubMed Central  PubMed  Google Scholar 

  102. Imlay JA (2003) Pathway of oxidative damage. Annu Rev Microbiol 57:395–418

    CAS  PubMed  Google Scholar 

  103. Soballe B, Poole RK (2000) Ubiquinone limits oxidative stress in Escherichia coli. Microbiology 146:787–796

    CAS  PubMed  Google Scholar 

  104. Messner KR, Imlay JA (1999) The identification of primary sites of superoxide and hydrogen peroxide formation in the aerobic respiratory chain and sulfide reductase complex of Escherichia coli. J Biol Chem 274:10119–10128

    CAS  PubMed  Google Scholar 

  105. Gonzalez-Flecha B, Demple B (1995) Metabolic sources of hydrogen peroxide in aerobically growing Escherichia coli. J Biol Chem 270:13681–13687

    CAS  PubMed  Google Scholar 

  106. Imlay JA, Fridovich I (1991) Assay of metabolic superoxide production in Escherichia coli. J Biol Chem 266:6957–6965

    CAS  PubMed  Google Scholar 

  107. Imlay JA (1995) A metabolic enzyme that rapidly produces superoxide, fumarate reductase of Escherichia coli. J Biol Chem 270:19767–19777

    CAS  PubMed  Google Scholar 

  108. Thomson VJ, Bhattacharjee MK, Fine DH et al (1999) Direct selection of IS903 transposon insertions by use of broad-host range vector: isolation of catalase-deficient mutants of Actinobacillus actinomycetemcomitans. J Bacteriol 181:7298–7307

    CAS  PubMed Central  PubMed  Google Scholar 

  109. Ellfolk N, Soininen R (1970) Pseudomonas cytochrome c peroxidase. I. Purification procedure. Acta Chem Scand 24:2126–2136

    CAS  PubMed  Google Scholar 

  110. Alves T, Besson S, Duarte LC et al (1999) A cytochreome c peroxidase from Pseudomonas nautica 617 active at high ionic strength: expression, purification and characterization. Biochim Biophys Acta 1434:248–259

    CAS  PubMed  Google Scholar 

  111. Pettigrew GW (1991) The cytochrome c peroxidase of Paracoccus denitrificans. Biochim Biophys Acta 1058:25–27

    CAS  PubMed  Google Scholar 

  112. Hu W, De Smet L, Van Beeumen J et al (1998) Characterization of cytochreome c-556 from the purple phototrophic bacterium Rhodobacter capsulatus as a cytochrome c peroxidase. Eur J Biochem 258:29–36

    CAS  PubMed  Google Scholar 

  113. Arciero DM, Hooper AB (1994) A di-heme cytochrome c peroxidase from Nitrosomonas europaea catalytically active in both the oxidized and half-reduced states. J Biol Chem 269:11878–11886

    CAS  PubMed  Google Scholar 

  114. Zahn JA, Arciero DM, Hooper AB et al (1997) Cytochrome c peroxidase from Methylococcus capsulatus Bath. Arch Microbiol 168:362–372

    CAS  PubMed  Google Scholar 

  115. Fulop V, Ridout CJ, Greenwood C et al (1995) Crystal structure of the di-haem cytochrome c peroxidase from Pseudomonas aeruginosa. Structure 3:1225–1233

    CAS  PubMed  Google Scholar 

  116. Dias JM, Alves T, Bonifacio C et al (2004) Structural basis for the mechanism of Ca2+ activation of the di-heme cytochrome c peroxidase from Pseudomonas nautica 617. Structure 12:961–973

    CAS  PubMed  Google Scholar 

  117. Shimizu H, Schuller DJ, Lanzilotta WN et al (2001) Crystal structure of Nitrosomonas europaea cytochrome c peroxidase and the structural basis for ligand switching in bacterial di-heme peroxidases. Biochemistry 40:13483–13490

    CAS  PubMed  Google Scholar 

  118. De Smetl L, Savvides SN, Van Horen E et al (2006) Structural and mutagenesis studies on the cytochrome c peroxidase from Rhodobacter capsulatus provide new insights into structure-function relationship of bacterial di-heme peroxidases. J Biol Chem 281:4371–4379

    Google Scholar 

  119. Echalier A, Goodhew CF, Pettigrew GW et al (2006) Activation and catalysis of the di-heme cytochrome c peroxidase from Paracoccus pantotrophus. Structure 14:107–117

    CAS  PubMed  Google Scholar 

  120. Gilmour R, Goodhew CF, Pettigrew GW et al (1994) The kinetics of the oxidation of cytochrome c by Paracoccus cytochrome c peroxidase. Biochem J 300:907–914

    CAS  PubMed Central  PubMed  Google Scholar 

  121. Hu W, Van Driessche G, Devreese B et al (1997) Structural characterization of Paracoccus denitrificans cytochrome c peroxidase and assignment of the low and high potential heme sites. Biochemistry 36:7958–7966

    CAS  PubMed  Google Scholar 

  122. McGinnity DF, Devreese B, Prazeres S et al (1996) A single histidine is required for activity of cytochrome c peroxidase from Paracoccus denitrificans. J Biol Chem 271:11126–11133

    CAS  PubMed  Google Scholar 

  123. Samyn B, Van Craenenbroeck K, De Smet L et al (1995) A reinvestigation of the covalent structure of Pseudomonas aeruginosa cytochrome c peroxidase. FEBS Lett 377:145–149

    CAS  PubMed  Google Scholar 

  124. Foote N, Turner R, Brittain T et al (1992) A quantitative model for the mechanism of action of the cytochrome c peroxidase of Pseudomonas aeruginosa. Biochem J 283:839–843

    CAS  PubMed Central  PubMed  Google Scholar 

  125. Ellfolk N, Ronnberg M, Osterlund K (1991) Structural and functional features of Pseudomonas cytochrome c peroxidase. Biochim Biophys Acta 1080:68–77

    CAS  PubMed  Google Scholar 

  126. Goodhew CF, Wilson IB, Hunter DJ et al (1990) The cellular location and specificity of bacterial cytochrome c peroxidases. Biochem J 271:707–712

    CAS  PubMed Central  PubMed  Google Scholar 

  127. Foote N, Peterson J, Gadsby PM et al (1985) Redox-linked spin-state changes in the di-haem cytochrome c-551 peroxidase from Pseudomonas aeruginosa. Biochem J 230:227–237

    CAS  PubMed Central  PubMed  Google Scholar 

  128. Ellfolk N, Ronnberg M, Aasa R et al (1983) Properties and function of the two hemes in Pseudomonas cytochrome c peroxidase. Biochim Biophys Acta 743:23–30

    CAS  PubMed  Google Scholar 

  129. Ronnberg M, Ellfolk N (1979) Heme-linked properties of Pseudomonas cytochrome c peroxidase. Evidence for non-equivalence of the hemes. Biochim Biophys Acta 581:325–333

    CAS  PubMed  Google Scholar 

  130. Foote N, Peterson J, Gadsby PM et al (1984) A study of the oxidized form of Pseudomonas aeruginosa cytochrome c-551 peroxidase with the use of magnetic circular dichroism. Biochem J 223:369–378

    CAS  PubMed Central  PubMed  Google Scholar 

  131. Bradley AL, Chobot SE, Arciero DM et al (2004) A distinctive electrocatalytic response from the cytochrome c peroxidase of Nitrosomonas europaea. J Biol Chem 279:13297–13300

    CAS  PubMed  Google Scholar 

  132. Unden G, Bongaerts J (1997) Alternative respiratory pathways of Escherichia coli: energetics and transcriptional regulation in response to electron acceptors. Biochim Biophys Acta 1320:217–234

    CAS  PubMed  Google Scholar 

  133. Kita K, Konishi K, Anraku Y (1984) Terminal oxidases of Escherichia coli aerobic respiratory chain. I. Purification and properties of cytochrome b 562-o complex from cells in the early exponential phase of aerobic growth. J Biol Chem 259:3368–3374

    CAS  PubMed  Google Scholar 

  134. Yamada H, Takashima E, Konishi K (2007) Molecular characterization of the membrane-bound quinol peroxidase functionally connected to the respiratory chain. FEBS J 274:853–866

    CAS  PubMed  Google Scholar 

  135. Gilmour R, Prazeres S, McGinnity DF et al (1995) The affinity and specificity of Ca2+-binding sites of cytochrome c peroxidase from Paracoccus denitrificans. Eur J Biochem 234:878–886

    CAS  PubMed  Google Scholar 

  136. Hirokawa T, Boon-Chieng S, Mitaku S (1998) SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14:378–379

    CAS  PubMed  Google Scholar 

  137. Kita K, Konishi K, Anraku Y (1984) Terminal oxidases of Escherichia coli aerobic respiratory chain. II. Purification and properties of cytochrome b 558-d complex from cells grown with limited oxygen and evidence of branched electron-carrying systems. J Biol Chem 259:3375–3381

    CAS  PubMed  Google Scholar 

  138. Takashima E, Konishi K (2008) Characterization of a quinol peroxidase mutant in Aggregatibacter actinomycetemcomitans. FEMS Microbiol Lett 286:66–70

    CAS  PubMed  Google Scholar 

  139. Slots J, Ting M (2002) Systemic antibiotics in the treatment of periodontal disease. Periodontol 2000 28:106–176

    PubMed  Google Scholar 

  140. Van Winkelhoff AT, Slots J (1999) Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in nonoral infections. Periodontol 2000 20:122–135

    PubMed  Google Scholar 

  141. Kachlany SC, Fine DH, Figurski DH (2000) Secretion of RTX leukotoxin by Actinobacillus actinomycetemcomitans. Infect Immun 68:6094–6100

    CAS  PubMed Central  PubMed  Google Scholar 

  142. Lally ET, Hill RB, Kieba IR et al (1999) The interaction between RTX toxins and target cells. Trends Microbiol 7:356–361

    CAS  PubMed  Google Scholar 

  143. Takashima E, Yamada H, Konishi K (2007) Bacterial multi-heme peroxidase. In: Mohan RM (ed) Research advances in biochemistry, vol 1. Global Research Network, Kerala, pp 21–27

    Google Scholar 

  144. Herren CD, Rocha ER, Smith CJ (2003) Genetic analysis of an important oxidative stress locus in the anaerobe Bacteroides fragilis. Gene 316:167–175

    CAS  PubMed  Google Scholar 

  145. Partridge JD, Poole RK, Green J (2007) The Escherichia coli yhjA gene, encoding a predicted cytochrome c peroxidase, is regulated by FNR and OxyR. Microbiology 153:1499–1507

    CAS  PubMed  Google Scholar 

  146. Charoensuk K, Irie A, Lertwattanasakul N et al (2011) Physiological importance of cytochrome c peroxidase in ethanologenic thermotoletant Zymomonas mobilis. J Mol Microbiol Biotechnol 20:70–82

    CAS  PubMed  Google Scholar 

  147. Poole LB (2005) Bacterial defenses against oxidants: mechanistic features of cysteine-based peroxidases and their flavoprotein reductases. Arch Biochem Biophys 433:240–254

    CAS  PubMed  Google Scholar 

  148. Takashima E, Yamada H, Yajima A et al (2010) A quinol peroxidase inhibitor prevents secretion of a leukotoxin from Aggregatibacter actinomycetemcomitans. J Periodontal Res 45:123–128

    CAS  PubMed  Google Scholar 

  149. Ui H, Ishiyama A, Sekiguchi H et al (2007) Selective and potent in vitro antimalarial activities found in four microbial metabolites. J Antibiot (Tokyo) 60:220–222

    CAS  Google Scholar 

  150. Minagawa N, Yabu Y, Kita K et al (1997) An antibiotic, ascofuranone, specifically inhibits respiration and in vitro growth of long slender bloodstream forms of Trypanosoma brucei brucei. Mol Biochem Parasitol 84:271–280

    CAS  PubMed  Google Scholar 

  151. Yabu Y, Yoshida A, Suzuki T et al (2003) The efficacy of ascofuranone in a consecutive treatment on Trypanosoma brucei brucei in mice. Parasitol Int 52:155–164

    CAS  PubMed  Google Scholar 

  152. Toledano MB, Kullik I, Trinh F et al (1994) Redox-dependent shift of OxyR-DNA contacts along an extended DNA-binding site: a mechanism for differential promoter selection. Cell 78:897–909

    CAS  PubMed  Google Scholar 

  153. Haubek D, Ennibi OK, Abdellaoui L et al (2002) Attachment loss in Moroccan early onset periodontitis patients and infection with the JP2-type of Actinobacillus actinomycetemcomitans. J Clin Periodontol 29:657–660

    PubMed  Google Scholar 

  154. Cho HJ, Kang JH, Kwak JY et al (2007) Ascofuranone suppresses PMA-mediated matrix metalloproteinase-9 gene activation through the Ras/Raf/MEK/ERK and Ap1-dependent mechanisms. Carcinogenesis 28:1104–1110

    CAS  PubMed  Google Scholar 

  155. Yabu Y, Minagawa N, Kita K et al (1998) Oral and intraperitoneal treatment of Trypanosoma brucei brucei with a combination of ascofuranone and glycerol, in mice. Parasitol Int 47:131–137

    CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Nippon Dental University School of Life Dentistry at Tokyo, 1-9-20 Fujimi, Chiyoda-ku, Tokyo, 102-8159, Japan

    Kiyoshi Konishi

Authors
  1. Kiyoshi Konishi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Kiyoshi Konishi .

Editor information

Editors and Affiliations

  1. Department of Preventive Dentistry, Okayama University Graduate School of Medicine and Pharmaceutical Sciences, Okayama, Japan

    Daisuke Ekuni

  2. Dept of Science and Clinical Specialty Odontostomatology & Biochemistry, Polytechnical University of Marche Faculty of Medicine, Ancona, Italy

    Maurizio Battino

  3. Department of Preventive Dentistry, Okayama Univ Graduate School of Medicine Dentistry and Pharmaceutical Sciences, Okayama, Japan

    Takaaki Tomofuji

  4. Dept of Oral Biological & Medical Scienc Laboratory of Periodontal Biology, University of British Columbia Faculty of Dentistry, Vancouver, British Columbia, Canada

    Edward E. Putnins

Rights and permissions

Reprints and permissions

Copyright information

© 2014 Springer Science+Business Media New York

About this chapter

Cite this chapter

Konishi, K. (2014). Physiological Roles of a Periodontopathic Bacterial Membrane-Bound Quinol Peroxidase. In: Ekuni, D., Battino, M., Tomofuji, T., Putnins, E. (eds) Studies on Periodontal Disease. Oxidative Stress in Applied Basic Research and Clinical Practice. Humana Press, New York, NY. https://doi.org/10.1007/978-1-4614-9557-4_8

Download citation

Publish with us

Policies and ethics

Search

Navigation