The interplay between iron, haem and manganese in Porphyromonas gingivalis

Journal of Oral Biosciences

Volumn 57, Issue 2, 2015, Pages 91-101

  Butler, Catherine A ^a   Dashper, Stuart G ^a   Khan, Hasnah S G ^a   Zhang, Lianyi ^a   Reynolds, Eric C ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Metal ion homeostasis; P. gingivalis; Survival; Virulence

Indexed keywords

EID: 84929223005     PISSN: 13490079     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.job.2014.12.003     Document Type: Review

References (165)

1. N.J. Kassebaum, E. Bernabe, M. Dahiya, B. Bhandari, C.J. Murray, and W. Marcenes Global burden of severe periodontitis in 1990-2010: a systematic review and meta-regression J Dent Res 93 2014 1045 1053
2. B.A. Dye Global periodontal disease epidemiology Periodontology 2000 58 2012 10 25
3. P.E. Petersen, and P.C. Baehni Periodontal health and global public health Periodontology 2000 60 2012 7 14
4. P.I. Eke, B.A. Dye, L. Wei, G.O. Thornton-Evans, and R.J. Genco Prevalence of periodontitis in adults in the United States: 2009 and 2010 J Dent Res 91 2012 914 920
5. P.N. Papapanou The prevalence of periodontitis in the US: forget what you were told J Dent Res 91 2012 907 908
6. N. Guha, P. Boffetta, V. Wunsch Filho, J. Eluf Neto, O. Shangina, D. Zaridze, M.P. Curado, S. Koifman, E. Matos, A. Menezes, N. Szeszenia-Dabrowska, L. Fernandez, D. Mates, A.W. Daudt, J. Lissowska, R. Dikshit, and P. Brennan Oral health and risk of squamous cell carcinoma of the head and neck and esophagus: results of two multicentric case-control studies Am J Epidemiol 166 2007 1159 1173
7. M. Tezal, M.A. Sullivan, M.E. Reid, J.R. Marshall, A. Hyland, T. Loree, C. Lillis, L. Hauck, J. Wactawski-Wende, and F.A. Scannapieco Chronic periodontitis and the risk of tongue cancer Arch Otolaryngol Head Neck Surg 133 2007 450 454
8. D.S. Michaud, K. Joshipura, E. Giovannucci, and C.S. Fuchs A prospective study of periodontal disease and pancreatic cancer in US male health professionals J Natl Cancer Inst 99 2007 171 175
9. R.Z. Stolzenberg-Solomon, K.W. Dodd, M.J. Blaser, J. Virtamo, P.R. Taylor, and D. Albanes Tooth loss, pancreatic cancer, and Helicobacter pylori Am J Clin Nutr 78 2003 176 181
10. P.P. Hujoel, M. Drangsholt, C. Spiekerman, and N.S. Weiss An exploration of the periodontitis-cancer association Ann Epidemiol 13 2003 312 316
11. R.J. Genco, and T.E. Van Dyke Prevention: reducing the risk of CVD in patients with periodontitis Nat Rev Cardiol 7 2010 479 480
12. A. Spahr, E. Klein, N. Khuseyinova, C. Boeckh, R. Muche, M. Kunze, D. Rothenbacher, G. Pezeshki, A. Hoffmeister, and W. Koenig Periodontal infection and coronary heart disease Arch Intern Med 166 2006 554 559
13. E. Ioannidou, D. Kao, N. Chang, J. Burleson, and A. Dongari-Bagtzoglou Elevated serum interleukin-6 (IL-6) in solid-organ transplant recipients is positively associated with tissue destruction and IL-6 gene expression in the periodontium J Periodontol 77 2006 1871 1878
14. K. Lundberg, N. Wegner, T. Yucel-Lindberg, and P.J. Venables Periodontitis in RA-the citrullinated enolase connection Nat Rev Rheumatol 6 2010 727 730
15. E. Lalla, and P.N. Papapanou Diabetes mellitus and periodontitis: a tale of two common interrelated diseases Nat Rev Endocrinol 7 2011 738 748
16. N. Gully, R. Bright, V. Marino, C. Marchant, M. Cantley, D. Haynes, C. Butler, S. Dashper, E. Reynolds, and M. Bartold Porphyromonas gingivalis peptidylarginine deiminase, a key contributor in the pathogenesis of experimental periodontal disease and experimental arthritis PLoS One 9 2014 e100838
17. S.S. Socransky, A.D. Haffajee, M.A. Cugini, C. Smith, and R.L. Kent Microbial complexes in subgingival plaque J Clin Periodontol 25 1998 134 144
18. R. Darveau Periodontitis: a polymicrobial disruption of host homeostasis Nat Rev Microbiol 8 2010 481 490
19. G. Hajishengallis, S. Liang, A. Payne Mark, A. Hashim, R. Jotwani, A. Eskan Mehmet, L. McIntosh Megan, A. Alsam, L. Kirkwood Keith, D. Lambris John, P. Darveau Richard, and A. Curtis Michael Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement Cell Host Microbe 10 2011 497 506
20. G. Hajishengallis, R.P. Darveau, and M.A. Curtis The keystone-pathogen hypothesis Nat Rev Microbiol 10 2012 717 725
21. S.J. Byrne, S.G. Dashper, I.B. Darby, G.G. Adams, B. Hoffmann, and E.C. Reynolds Progression of chronic periodontitis can be predicted by the levels of Porphyromonas gingivalis and Treponema denticola in subgingival plaque Oral Microbiol Immunol 24 2009 469 477
22. L.F. Brown, J.D. Beck, and R.G. Rozier Incidence of attachment loss in community-dwelling older adults J Periodontol 65 1994 316 323
23. A.D. Haffajee, S.S. Socransky, C. Smith, and S. Dibart Relation of baseline microbial parameters to future periodontal attachment loss J Clin Periodontol 18 1991 744 750
24. A.L. Griffen, M.R. Becker, S.R. Lyons, M.L. Moeschberger, and E.J. Leys Prevalence of Porphyromonas gingivalis and periodontal health status J Clin Microbiol 36 1998 3239 3242
25. R.H. Orth, N. O'Brien-Simpson, S. Dashper, and E. Reynolds Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model Mol Oral Microbiol 26 2011 229 240
26. R.D. Pathirana, N.M. O'Brien-Simpson, G.C. Brammar, N. Slakeski, and E.C. Reynolds Kgp and RgpB, but not RgpA, are important for Porphyromonas gingivalis virulence in the murine periodontitis model Infect Immun 75 2007 1436 1442
27. Z. Ma, F.E. Jacobsen, and D.P. Giedroc Coordination chemistry of bacterial metal transport and sensing Chem Rev 109 2009 4644 4681
28. A. Van Ho, D.M. Ward, and J. Kaplan Transition metal transport in yeast Annu Rev Microbiol 56 2002 237 261
29. A.C. Rosenzweig Metallochaperones: bind and deliver Chem Biol 9 2002 673 677
30. M.A. Pennella, and D.P. Giedroc Structural determinants of metal selectivity in prokaryotic metal-responsive transcriptional regulators Biometals 18 2005 413 428
31. P. Kovacic Unifying electrostatic mechanism for metal cations in receptors and cell signaling J Recept Signal Transduct 28 2008 153 161
32. T. Olson, J. Williams, and J. Allen Influence of protein interactions on oxidation/reduction midpoint potentials of cofactors in natural and de novo metalloproteins BBA Bioenerg 1827 2013 914 922
33. G. Pratviel Oxidative DNA damage mediated by transition metal ions and their complexes A. Sigel, H. Sigel, R.K.O. Sigel, Interplay between metal ions and nucleic acids 2012 Springer Netherlands 201 216
34. E.C. Theil, and K.N. Raymond Transition-metal storage, transport and biomineralization I. Bertini, H. Gray, S. Lippard, J. Valentine, Bioinorganic chemistry 1994 University Science Books Mill Valley, California 1 37
35. S.C. Andrews, A.K. Robinson, and F. Rodríguez-Quiñones bacterial Iron homeostasis FEMS Microbiol Rev 27 2003 215 237
36. N.S. Jakubovics, and H.F. Jenkinson Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria Microbiology 147 2001 1709 1718
37. K. Wooldridge, and P. Williams Iron uptake mechanisms of pathogenic bacteria FEMS Microbiol Rev 12 1993 325 348
38. V. Braun, and H. Killmann Bacterial solutions to the iron-supply problem Trends Biochem Sci 24 1999 104 109
39. K.M. Papp-Wallace, and M.E. Maguire Manganese transport and the role of manganese in virulence Annu Rev Microbiol 60 2006 187 209
40. 2+ and bacterial pathogenesis Front Biosci 9 2004 1035 1042
41. D.G. Kehres, and M.E. Maguire Emerging themes in manganese transport, biochemistry and pathogenesis in bacteria FEMS Microbiol Rev 27 2003 263 290
42. J.E. Posey, and F.C. Gherardini Lack of a role for iron in the Lyme disease pathogen Science 288 2000 1651 1653
43. J.E. Posey, J.M. Hardham, S.J. Norris, and F.C. Gherardini Characterization of a manganese-dependent regulatory protein, TroR, from Treponema pallidum Proc Natl Acad Sci USA 96 1999 10887 10892
44. F. Archibald Manganese - its acquisition by and function in the lactic-acid bacteria CRC Crit Rev Microbiol 13 1986 63 109
45. V.C. Culotta, M. Yang, and M.D. Hall Manganese transport and trafficking: lessons learned from Saccharomyces cerevisiae Eukaryot Cell 4 2005 1159 1165
46. J.D. Aguirre, and V.C. Culotta Battles with iron: manganese in oxidative stress protection J Biol Chem 287 2012 13541 13548
47. H.-J. Tseng, Y. Srikhanta, A.G. McEwan, and M.P. Jennings Accumulation of manganese in Neisseria gonorrhoeae correlates with resistance to oxidative killing by superoxide anion and is independent of superoxide dismutase activity Mol Microbiol 40 2001 1175 1186
48. J. Cadet, T. Douki, D. Gasparutto, and J.-L. Ravanat Oxidative damage to DNA: formation, measurement and biochemical features Mutat Res - Fundam Mol Mech Mutagen 531 2003 5 23
49. M. Freitas, Lima JLFC, and E. Fernandes Optical probes for detection and quantification of neutrophils' oxidative burst. A review Anal Chim Acta 649 2009 8 23
50. P. Pacher, J.S. Beckman, and L. Liaudet Nitric oxide and peroxynitrite in health and disease Physiol Rev 87 2007 315 424
51. D.T. Sawyer, and J.S. Valentine How super is superoxide? Acc Chem Res 14 1981 393 400
52. K.H. Cheeseman, and T.F. Slater An introduction to free radical biochemistry Br Med Bull 49 1993 481 493
53. S. Stohs, and D. Bagchi Oxidative mechanisms in the toxicity of metal ions Free Radic Biol Med 18 1995 321 336
54. C.A. Genco Regulation of hemin and iron transport in Porphyromonas gingivalis Adv Dent Res 9 1995 41 47
55. P.D. Marsh The effect of growth rate and haemin on the virulence and proteolytic activity of Porphyromonas gingivalis W50 Microbiology 140 1994 861
56. A.S. McKee, A.S. McDermid, A. Baskerville, A.B. Dowsett, D.C. Ellwood, and P.D. Marsh Effect of hemin on the physiology and virulence of Bacteroides gingivalis W50 Infect Immun 52 1986 349 355
57. T. Olczak, W. Simpson, X. Liu, and C.A. Genco Iron and heme utilization in Porphyromonas gingivalis FEMS Microbiol Rev 29 2005 119 144
58. S.G. Dashper, C.A. Butler, J.P. Lissel, R.A. Paolini, B. Hoffmann, P.D. Veith, N.M. O'Brien-Simpson, S.L. Snelgrove, J.T. Tsiros, and E.C. Reynolds A novel Porphyromonas gingivalis FeoB plays a role in manganese accumulation J Biol Chem 280 2005 28095 28102
59. J.M. Roper, E. Raux, A.A. Brindley, H.L. Schubert, S.E. Gharbia, H.N. Shah, and M.J. Warren The enigma of cobalamin (Vitamin B12) biosynthesis in Porphyromonas gingivalis: identification and characterization of a functional corrin pathway J Biol Chem 275 2000 40316 40323
60. S. Hou, M.F. Reynolds, F.T. Horrigan, S.H. Heinemann, and T. Hoshi Reversible binding of heme to proteins in cellular signal transduction Acc Chem Res 39 2006 918 924
61. S.E.J. Bowman, and K.L. Bren The chemistry and biochemistry of heme c: functional bases for covalent attachment Nat Prod Rep 25 2008 1118 1130
62. S.G. Dashper, C.-S. Ang, P.D. Veith, H.L. Mitchell, A.W.H. Lo, C.A. Seers, K.A. Walsh, N. Slakeski, D. Chen, J.P. Lissel, C.A. Butler, N.M. O'Brien-Simpson, I.G. Barr, and E.C. Reynolds Response of Porphyromonas gingivalis to heme limitation in continuous culture J Bacteriol 191 2009 1044 1055
63. N. Takahashi, T. Sato, and T. Yamada Metabolic pathways for cytotoxic end product formation from glutamate- and aspartate-containing peptides by Porphyromonas gingivalis J Bacteriol 182 2000 4704 4710
64. V. Meuric, A. Rouillon, F. Chandad, and M. Bonnaure-Mallet Putative respiratory chain of Porphyromonas gingivalis Future Microbiol 5 2010 717 734
65. A. Reyes-Prieto, B. Barquera, and O. Juárez Origin and evolution of the sodium-pumping NADH: ubiquinone oxidoreductase PLoS One 9 2014 e96696
66. E. Biegel, S. Schmidt, J. González, and V. Müller Biochemistry, evolution and physiological function of the Rnf complex, a novel ion-motive electron transport complex in prokaryotes Cell Mol Life Sci 68 2011 613 634
67. C. Anaya-Bergman, A. Rosato, and J.P. Lewis Iron- and hemin-dependent gene expression of Porphyromonas gingivalis Mol Oral Microbiol 2014 10.1111/omi.12066
68. S. Dashper, C.-S. Ang, S.W. Liu, R. Paolini, P. Veith, and E. Reynolds Inhibition of Porphyromonas gingivalis biofilm by oxantel Antimicrob Agents Chemother 54 2010 1311 1314
69. S. Dashper, N. O'Brien-Simpson, S.W. Liu, R. Paolini, H. Mitchell, K. Walsh, T. D'Cruze, B. Hoffmann, D. Catmull, Y. Zhu, and E. Reynolds Oxantel disrupts polymicrobial biofilm development of periodontal pathogens Antimicrob Agents Chemother 58 2014 378 385
70. T.E. Bramanti, and S.C. Holt Roles of porphyrins and host iron transport proteins in regulation of growth of Porphyromonas gingivalis W50 J Bacteriol 173 1991 7330 7339
71. V. Brochu, D. Grenier, K. Nakayama, and D. Mayrand Acquisition of iron from human transferrin by Porphyromonas gingivalis: a role for Arg- and Lys-gingipain activities Oral Microbiol Immunol 16 2001 79 87
72. V. Goulet, B. Britigan, K. Nakayama, and D. Grenier Cleavage of human transferrin by Porphyromonas gingivalis gingipains promotes growth and formation of hydroxyl radicals Infect Immun 72 2004 4351 4356
73. A. de Lillo, R. Teanpaisan, J.F. Fierro, and C.W.I. Douglas Binding and degradation of lactoferrin by Porphyromonas gingivalis, Prevotella intermedia and Prevotella nigrescens FEMS Immunol Med Microbiol 14 1996 135 143
74. J.D. Oram, and B. Reiter Inhibition of bacteria by lactoferrin and other iron-chelating agents BBA Gen Subj 170 1968 351 365
75. W. Bellamy, M. Takase, K. Yamauchi, H. Wakabayashi, K. Kawase, and M. Tomita Identification of the bactericidal domain of lactoferrin BBA Protein Struct Mol Enzymol 1121 1992 130 136
76. H. Wakabayashi, K. Yamauchi, T. Kobayashi, T. Yaeshima, K. Iwatsuki, and H. Yoshie Inhibitory effects of lactoferrin on growth and biofilm formation of Porphyromonas gingivalis and Prevotella intermedia Antimicrob Agents Chemother 53 2009 3308 3316
77. S.G. Dashper, Y. Pan, P.D. Veith, Y.-Y. Chen, E.C.Y. Toh, S.W. Liu, K.J. Cross, and E.C. Reynolds Lactoferrin inhibits Porphyromonas gingivalis proteinases and Has sustained biofilm inhibitory activity Antimicrob Agents Chemother 56 2012 1548 1556
78. S.G. Dashper, K.J. Cross, N. Slakeski, P. Lissel, P. Aulakh, C. Moore, and E.C. Reynolds Hemoglobin hydrolysis and heme acquisition by Porphyromonas gingivalis Oral Microbiol Immunol 19 2004 50 56
79. Y. Shi, D.B. Ratnayake, K. Okamoto, N. Abe, K. Yamamoto, and K. Nakayama Genetic analyses of proteolysis, hemoglobin binding, and hemagglutination of Porphyromonas gingivalis: construction of mutants with a combination of rgpA, rgpB, kgp and hagA J Biol Chem 274 1999 17955 17960
80. S. Shizukuishi, K. Tazaki, E. Inoshita, K. Kataoka, T. Hanioka, and A. Amano Effect of concentration of compounds containing iron on the growth of Porphyromonas gingivalis FEMS Microbiol Lett 131 1995 313 317
81. M. Paramaesvaran, K.-A. Nguyen, E. Caldon, J.A. McDonald, S. Najdi, G. Gonzaga, D.B. Langley, A. DeCarlo, M.J. Crossley, N. Hunter, and C.A. Collyer Porphyrin-mediated cell surface heme capture from hemoglobin by Porphyromonas gingivalis J Bacteriol 185 2003 2528 2537
82. K.D. Krewulak, and H.J. Vogel Structural biology of bacterial iron uptake BBA Biomebr 1778 2008 1781 1804
83. A.A. DeCarlo, M. Paramaesvaran, P.L.W. Yun, C. Collyer, and N. Hunter Porphyrin-mediated binding to hemoglobin by the HA2 domain of cysteine proteinases (gingipains) and hemagglutinins from the periodontal pathogen Porphyromonas gingivalis J Bacteriol 181 1999 3784 3791
84. T. Olczak, D.W. Dixon, and C.A. Genco Binding specificity of the Porphyromonas gingivalis heme and hemoglobin receptor HmuR, Gingipain K, and Gingipain R1 for heme, porphyrins, and metalloporphyrins J Bacteriol 183 2001 5599 5608
85. P.D. Veith, Y.-Y. Chen, D.G. Gorasia, D. Chen, M.D. Glew, N.M. O'Brien-Simpson, J.D. Cecil, J.A. Holden, and E.C. Reynolds Porphyromonas gingivalis outer membrane vesicles exclusively contain outer membrane and periplasmic proteins and carry a cargo enriched with virulence factors J Proteome Res 13 2014 2420 2432
86. T. Olczak, K. Siudeja, and M. Olczak Purification and initial characterization of a novel Porphyromonas gingivalis HmuY protein expressed in Escherichia coli and insect cells Protein Expr Purif 49 2006 299 306
87. H. Wójtowicz, T. Guevara, C. Tallant, M. Olczak, A. Sroka, J. Potempa, M. Solà, T. Olczak, and F.X. Gomis-Rüth Unique structure and stability of HmuY, a novel heme-binding protein of Porphyromonas gingivalis PLoS Pathog 5 2009 e1000419
88. W. Simpson, T. Olczak, and C.A. Genco Characterization and expression of HmuR, a TonB-dependent hemoglobin receptor of Porphyromonas gingivalis J Bacteriol 182 2000 5737 5748
89. J.W. Smalley, D.P. Byrne, A.J. Birss, H. Wojtowicz, A. Sroka, J. Potempa, and T. Olczak HmuY haemophore and gingipain proteases constitute a unique syntrophic system of haem acquisition by Porphyromonas gingivalis PLoS One 6 2011 e17182
90. J.P. Lewis, K. Plata, F. Yu, A. Rosato, and C. Anaya Transcriptional organization, regulation and role of the Porphyromonas gingivalis W83 hmu haemin-uptake locus Microbiology 152 2006 3367 3382
91. J.-L. Gao, K.-A. Nguyen, and N. Hunter Characterization of a hemophore-like protein from Porphyromonas gingivalis J Biol Chem 285 2010 40028 40038
92. T.E. Bramanti, and S.C. Holt Effect of porphyrins and host iron transport proteins on outer membrane protein expression in Porphyromonas (Bacteroides) gingivalis: identification of a novel 26 kDa hemin-repressible surface protein Microb Pathog 13 1992 61 73
93. S.G. Dashper, A. Hendtlass, N. Slakeski, C. Jackson, K.J. Cross, L. Brownfield, R. Hamilton, I. Barr, and E.C. Reynolds Characterization of a novel outer membrane hemin-binding protein of Porphyromonas gingivalis J Bacteriol 182 2000 6456 6462
94. M. Shoji, Y. Shibata, T. Shiroza, H. Yukitake, B. Peng, Y.Y. Chen, K. Sato, M. Naito, Y. Abiko, E.C. Reynolds, and K. Nakayama Characterization of hemin-binding protein 35 (HBP35) in Porphyromonas gingivalis: its cellular distribution, thioredoxin activity and role in heme utilization BMC Microbiol 10 2010 152
95. N. Slakeski, S.G. Dashper, P. Cook, C. Poon, C. Moore, and E.C. Reynolds A Porphyromonas gingivalis genetic locus encoding a heme transport system Oral Microbiol Immunol 15 2000 388 392
96. J.W. Smalley, A.J. Birss, A.S. McKee, and P.D. Marsh Haemin-binding proteins of Porphyromonas gingivalis W50 grown in a chemostat under haemin-limitation J Gen Microbiol 139 1993 2145 2150
97. N.M. O'Brien-Simpson, R.D. Pathirana, G.D. Walker, and E.C. Reynolds Porphyromonas gingivalis RgpA-Kgp proteinase-adhesin complexes penetrate gingival tissue and induce proinflammatory cytokines or apoptosis in a concentration-dependent manner Infect Immun 77 2009 1246 1261
98. N.M. O'Brien-Simpson, P.D. Veith, S.G. Dashper, and E.C. Reynolds Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire Curr Protein Pept Sci 4 2003 409 426
99. M.L. Cartron, S. Maddocks, P. Gillingham, C.J. Craven, and S.C. Andrews Feo - transport of ferrous iron into bacteria Biometals 19 2006 143 157
100. T.C. Marlovits, W. Haase, C. Herrmann, S.G. Aller, and V.M. Unger The membrane protein FeoB contains an intramolecular G protein essential for Fe (II) uptake in bacteria Proc Natl Acad Sci USA 99 2002 16243 16248
101. M.R. Ash, A. Guilfoyle, R.J. Clarke, M. Guss, M.J. Maher, and M. Jormakka Potassium-activated GTPase reaction in the G protein-coupled ferrous iron transporter B J Biol Chem 285 2010 14594 14602
102. J. He, H. Miyazaki, C. Anaya, F. Yu, W.A. Yeudall, and J.P. Lewis Role of Porphyromonas gingivalis FeoB2 in metal uptake and oxidative stress protection Infect Immun 74 2006 4214 4223
103. D. Duy, J. Soll, and K. Philippar Solute channels of the outer membrane: from bacteria to chloroplasts Biol Chem 388 2007 879 889
104. H. Nikaido Molecular basis of bacterial outer membrane permeability revisited Microbiol Mol Biol Rev 67 2003 593 656
105. T.H. Hohle, W.L. Franck, G. Stacey, and M.R. O'Brian Bacterial outer membrane channel for divalent metal ion acquisition Proc Natl Acad Sci USA 108 2011 15390 15395
106. J.W. Smalley, J. Silver, P.J. Marsh, and A.J. Birss The periodontopathogen Porphyromonas gingivalis binds iron protoporphyrin IX in the mu-oxo dimeric form: an oxidative buffer and possible pathogenic mechanism Biochem J 331 1998 681 685
107. A. Amano, T. Ishimoto, H. Tamagawa, and S. Shizukuishi Role of superoxide dismutase in resistance of Porphyromonas gingivalis to killing by polymorphonuclear leukocytes Infect Immun 60 1992 712 714
108. J. Ueshima, M. Shoji, D.B. Ratnayake, K. Abe, S. Yoshida, K. Yamamoto, and K. Nakayama Purification, gene cloning, gene expression, and mutants of Dps from the obligate anaerobe Porphyromonas gingivalis Infect Immun 71 2003 1170 1178
109. J.-L. Gao, Y. Lu, G. Browne, Y.a.p. BC-M, J. Trewhella, N. Hunter, and K.-A. Nguyen The role of heme binding by DNA-protective protein from starved cells (Dps) in the tolerance of Porphyromonas gingivalis to heme toxicity J Biol Chem 287 2012 42243 42258
110. N. Johnson, Y. Liu, and H. Fletcher Alkyl hydroperoxide peroxidase subunit C (ahpC) protects against organic peroxides but does not affect the virulence of Porphyromonas gingivalis W83 Oral Microbiol Immunol 19 2004 233 239
111. P. Mydel, Y. Takahashi, H. Yumoto, M. Sztukowska, M. Kubica, F.C. Gibson III, D.M. Kurtz Jr, J. Travis, L.V. Collins, and K.-A. Nguyen Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection PLoS Pathog 2 2006 e76
112. P.E. Kolenbrander, R.J. Palmer Jr, S. Periasamy, and N.S. Jakubovics Oral multispecies biofilm development and the key role of cell-cell distance Nat Rev Microbiol 8 2010 471 480
113. M. Kuboniwa, E.L. Hendrickson, Q. Xia, T. Wang, H. Xie, M. Hackett, and R.J. Lamont Proteomics of Porphyromonas gingivalis within a model oral microbial community BMC Microbiol 9 2009 98
114. K.H. Tan, C.A. Seers, S.G. Dashper, H.L. Mitchell, J.S. Pyke, V. Meuric, N. Slakeski, S.M. Cleal, J.L. Chambers, M.J. McConville, and E.C. Reynolds Porphyromonas gingivalis and Treponema denticola exhibit metabolic symbioses PLoS Pathog 10 2014 e1003955
115. Z. Zainal-Abidin, P.D. Veith, S.G. Dashper, Y. Zhu, D.V. Catmull, Y.Y. Chen, D.C. Heryanto, D. Chen, J.S. Pyke, K. Tan, H.L. Mitchell, and E.C. Reynolds Differential proteomic analysis of a polymicrobial biofilm J Proteome Res 11 2012 4449 4464
116. C.S. Ang, P.D. Veith, S.G. Dashper, and E.C. Reynolds Application of 16O/18O reverse proteolytic labeling to determine the effect of biofilm culture on the cell envelope proteome of Porphyromonas gingivalis W50 Proteomics 8 2008 1645 1660
117. L.M. Mashburn, A.M. Jett, D.R. Akins, and M. Whiteley Staphylococcus aureus serves as an iron source for Pseudomonas aeruginosa during in vivo coculture J Bacteriol 187 2005 554 566
118. Y. Zhu, S.G. Dashper, Y.-Y. Chen, S. Crawford, N. Slakeski, and E.C. Reynolds Porphyromonas gingivalis and Treponema denticola synergistic polymicrobial biofilm development PLoS One 8 2013 e71727
119. M.R. Simionato, C.M. Tucker, M. Kuboniwa, G. Lamont, D.R. Demuth, G.D. Tribble, and R.J. Lamont Porphyromonas gingivalis genes involved in community development with Streptococcus gordonii Infect Immun 74 2006 6419 6428
120. P.I. Diaz, P.S. Zilm, and A.H. Rogers Fusobacterium nucleatum supports the growth of Porphyromonas gingivalis in oxygenated and carbon-dioxide-depleted environments Microbiology 148 2002 467 472
121. N.A. Burgess, D.F. Kirke, P. Williams, K. Winzer, K.R. Hardie, N.L. Meyers, J. Aduse-Opoku, M.A. Curtis, and M. Camara LuxS-dependent quorum sensing in Porphyromonas gingivalis modulates protease and haemagglutinin activities but is not essential for virulence Microbiology 148 2002 763 772
122. W.O. Chung, Y. Park, R.J. Lamont, R. McNab, B. Barbieri, and D.R. Demuth Signaling system in Porphyromonas gingivalis based on a LuxS protein J Bacteriol 183 2001 3903 3909
123. J. Frias, E. Olle, and M. Alsina Periodontal pathogens produce quorum sensing signal molecules Infect Immun 69 2001 3431 3434
124. L. Guo, X. He, and W. Shi Intercellular communications in multispecies oral microbial communities Front Microbiol 5 2014 10.3389/fmicb.2014.00328
125. J.P. Lewis Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms Periodontology 2000 52 2010 94 116
126. S. Silver, and L.T. Phung Bacterial heavy metal resistance: new surprises Annu Rev Microbiol 50 1996 753 789
127. L. Escolar, J. Perez-Martin, and V. de Lorenzo Opening the iron box: transcriptional metalloregulation by the Fur protein J Bacteriol 181 1999 6223 6229
128. K. Hantke Iron and metal regulation in bacteria Curr Opin Microbiol 4 2001 172 177
129. A. Bagg, and J. Neilands Ferric uptake regulation protein acts as a repressor, employing iron (II) as a cofactor to bind the operator of an iron transport operon in Escherichia coli Biochemistry (Mosc) 26 1987 5471 5477
130. M. Coy, and J.B. Neilands Structural dynamics and functional domains of the Fur protein Biochemistry (Mosc) 30 1991 8201 8210
131. E. Pohl, J.C. Haller, A. Mijovilovich, W. Meyer-Klaucke, E. Garman, and M.L. Vasil Architecture of a protein central to iron homeostasis: crystal structure and spectroscopic analysis of the ferric uptake regulator Mol Microbiol 47 2003 903 915
132. C. Dian, S. Vitale, G.A. Leonard, C. Bahlawane, C. Fauquant, D. Leduc, C. Muller, H. de Reuse, I. Michaud-Soret, and L. Terradot The structure of the Helicobacter pylori ferric uptake regulator Fur reveals three functional metal binding sites Mol Microbiol 79 2011 1260 1275
133. Z. Ma, M.J. Faulkner, and J.D. Helmann Origins of specificity and cross-talk in metal ion sensing by Bacillus subtilis Fur Mol Microbiol 86 2012 1144 1155
134. C.A. Butler, S.G. Dashper, Z. Zhang, C.A. Seers, H.L. Mitchell, D.V. Catmull, M.D. Glew, J.E. Heath, Y. Tan, H.S.G. Khan, and E.C. Reynolds The Porphyromonas gingivalis ferric uptake regulator orthologue binds hemin and regulates hemin-responsive biofilm development PLoS One 9 2014 e111168 10.1371/journal.pone.0111168
135. S. Pellicer, A. González, M.L. Peleato, J.I. Martinez, M.F. Fillat, and M.T. Bes Site-directed mutagenesis and spectral studies suggest a putative role of FurA from Anabaena sp. PCC 7120 as a heme sensor protein FEBS J 279 2012 2231 2246
136. A. Smith, N.I. Hooper, N. Shipulina, and W.T. Morgan Heme binding by a bacterial repressor protein, the gene product of the ferric uptake regulation (fur) gene of Escherichia coli J Protein Chem 15 1996 575 583
137. C.E. James, Y. Hasegawa, Y. Park, V. Yeung, G.D. Tribble, M. Kuboniwa, D.R. Demuth, and R.J. Lamont LuxS involvement in the regulation of genes coding for hemin and iron acquisition systems in Porphyromonas gingivalis Infect Immun 74 2006 3834 3844
138. J. Boyd, M.N. Oza, and J.R. Murphy Molecular cloning and DNA sequence analysis of a diphtheria tox iron-dependent regulatory element (dtxR) from Corynebacterium diphtheriae Proc Natl Acad Sci USA 87 1990 5968 5972
139. X. Qiu, C.L. Verlinde, S. Zhang, M.P. Schmitt, R.K. Holmes, and W.G. Hol Three-dimensional structure of the diphtheria toxin repressor in complex with divalent cation co-repressors Structure 3 1995 87 100
140. M.M. Spiering, D. Ringe, J.R. Murphy, and M.A. Marletta Metal stoichiometry and functional studies of the diphtheria toxin repressor Proc Natl Acad Sci USA 100 2003 3808 3813
141. X. Qiu, E. Pohl, R.K. Holmes, and W.G. Hol High-resolution structure of the diphtheria toxin repressor complexed with cobalt and manganese reveals an SH3-like third domain and suggests a possible role of phosphate as co-corepressor Biochemistry (Mosc) 35 1996 12292 12302
142. J.A. D'Aquino, and D. Ringe Determinants of the SRC homology domain 3-like fold J Bacteriol 185 2003 4081 4086
143. M.D. Feese, B.P. Ingason, J. Goranson-Siekierke, R.K. Holmes, and W.G. Hol Crystal structure of the iron-dependent regulator from Mycobacterium tuberculosis at 2.0-A resolution reveals the Src homology domain 3-like fold and metal binding function of the third domain J Biol Chem 276 2001 5959 5966
144. J.F. Love, J.C. VanderSpek, and J.R. Murphy The SRC homology 3-like domain of the diphtheria toxin repressor (DtxR) modulates repressor activation through interaction with the ancillary metal ion-binding site J Bacteriol 185 2003 2251 2258
145. G. Wang, G.P. Wylie, P.D. Twigg, D.L. Caspar, J.R. Murphy, and T.M. Logan Solution structure and peptide binding studies of the C-terminal src homology 3-like domain of the diphtheria toxin repressor protein Proc Natl Acad Sci USA 96 1999 6119 6124
146. G.P. Wylie, V. Rangachari, E.A. Bienkiewicz, V. Marin, N. Bhattacharya, J.F. Love, J.R. Murphy, and T.M. Logan Prolylpeptide binding by the prokaryotic SH3-like domain of the diphtheria toxin repressor: a regulatory switch Biochemistry (Mosc) 44 2005 40 51
147. Y.-C. Su, K.-H. Chin, H.-C. Hung, G.-H. Shen, A.H.J. Wang, and S.-H. Chou Structure of Stenotrophomonas maltophilia FeoA complexed with zinc: a unique prokaryotic SH3-domain protein that possibly acts as a bacterial ferrous iron-transport activating factor Acta Crystallogr F - Struct Biol Cryst Commun 66 2010 636 642
148. G.M. Rodriguez, M.I. Voskuil, B. Gold, G.K. Schoolnik, and I. Smith IdeR, an essential gene in Mycobacterium tuberculosis: role of IdeR in iron-dependent gene expression, iron metabolism, and oxidative stress response Infect Immun 70 2002 3371 3381
149. Q. Que, and J.D. Helmann Manganese homeostasis in Bacillus subtilis is regulated by MntR, a bifunctional regulator related to the diphtheria toxin repressor family of proteins Mol Microbiol 35 2000 1454 1468
150. P.J. Hill, A. Cockayne, P. Landers, J.A. Morrissey, C.M. Sims, and P. Williams SirR, a novel iron-dependent repressor in Staphylococcus epidermidis Infect Immun 66 1998 4123 4129
151. 2+) permease in Streptococcus gordonii is regulated by a diphtheria toxin metallorepressor-like protein ScaR Mol Microbiol 38 2000 140 153
152. Y.L. Low, N.S. Jakubovics, J.C. Flatman, H.F. Jenkinson, and A.W. Smith Manganese-dependent regulation of the endocarditis-associated virulence factor EfaA of Enterococcus faecalis J Med Microbiol 52 2003 113 119
153. E. Rolerson, A. Swick, L. Newlon, C. Palmer, Y. Pan, B. Keeshan, and G. Spatafora The SloR/Dlg metalloregulator modulates Streptococcus mutans virulence gene expression J Bacteriol 188 2006 5033 5044
154. E. Guedon, and J.D. Helmann Origins of metal ion selectivity in the DtxR/MntR family of metalloregulators Mol Microbiol 48 2003 495 506
155. H. Xie, and C. Zheng OxyR activation in Porphyromonas gingivalis in response to a hemin-limited environment Infect Immun 80 2012 3471 3480
156. P.I. Diaz, N. Slakeski, E.C. Reynolds, R. Morona, A.H. Rogers, and P.E. Kolenbrander Role of oxyR in the oral anaerobe Porphyromonas gingivalis J Bacteriol 188 2006 2454 2462
157. J.M. Sobota, and J.A. Imlay 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 USA 108 2011 5402 5407
158. A. Amano, S. Shizukuishi, H. Tamagawa, K. Iwakura, S. Tsunasawa, and A. Tsunemitsu Characterization of superoxide dismutases purified from either anaerobically maintained or aerated Bacteroides gingivalis J Bacteriol 172 1990 1457 1463
159. M.C. Lynch, and H.K. Kuramitsu Role of superoxide dismutase activity in the physiology of Porphyromonas gingivalis Infect Immun 67 1999 3367 3375
160. K. Nakayama The superoxide dismutase-encoding gene of the obligately anaerobic bacterium Bacteroides gingivalis Gene 96 1990 149 150
161. S. Sugio, B.Y. Hiraoka, and F. Yamakura Crystal structure of cambialistic superoxide dismutase from Porphyromonas gingivalis Eur J Biochem 267 2000 3487 3495
162. P.S. Novichkov, A.E. Kazakov, D.A. Ravcheev, S.A. Leyn, G.Y. Kovaleva, R.A. Sutormin, M.D. Kazanov, W. Riehl, A.P. Arkin, I. Dubchak, and D.A. Rodionov RegPrecise 3.0 - a resource for genome-scale exploration of transcriptional regulation in bacteria BMC Genomics 14 2013 745
163. L.S. Busenlehner, M.A. Pennella, and D.P. Giedroc The SmtB/ArsR family of metalloregulatory transcriptional repressors: structural insights into prokaryotic metal resistance FEMS Microbiol Rev 27 2003 131 143
164. N.L. Brown, J.V. Stoyanov, S.P. Kidd, and J.L. Hobman The MerR family of transcriptional regulators FEMS Microbiol Rev 27 2003 145 163
165. L. Cuthbertson, and J.R. Nodwell The TetR family of regulators Microbiol Mol Biol Rev 77 2013 440 475