Roles of the host oxidative immune response and bacterial antioxidant rubrerythrin during Porphyromonas gingivalis infection

PLoS Pathogens

Volumn 2, Issue 7, 2006, Pages 0712-0725

  Mydel, Piotr ^a,b,e   Takahashi, Yusuke ^b,c   Yumoto, Hiromichi ^b,d   Sztukowska, Maryta ^a,e   Kubica, Malgorzata ^a   Gibson III, Frank C ^b   Kurtz Jr , Donald M ^f   Travis, Jim ^e   Collins, L Vincent ^g   Nguyen, Ky Anh ^e   Genco, Caroline Attardo ^b   Potempa, Jan ^a,e  

^a JAGIELLONIAN UNIVERSITY   (Poland)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c KANAGAWA DENTAL COLLEGE   (Japan)

^d UNIVERSITY OF TOKUSHIMA   (Japan)

^e University of Georgia ^*  (United States)

^f UNIVERSITY OF GEORGIA   (United States)

^g UNIVERSITY OF GOTHENBURG   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANT; CYTOKINE; MICROBICIDE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; RUBRERYTHRIN; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; FERREDOXIN; RUBRERYTHRIN PROTEIN, BACTERIA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BACTEREMIA; BACTERIAL GENE; BACTERIAL INFECTION; BACTERIAL STRAIN; BACTERICIDAL ACTIVITY; CELL PROLIFERATION; CONTROLLED STUDY; CYTOKINE RELEASE; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; LEUKOCYTE ACTIVATION; MOBILIZATION; MOUSE; NEUTROPHIL; NONHUMAN; OSTEOLYSIS; OXIDATIVE STRESS; PATHOLOGY; PHAGOCYTOSIS; PORPHYROMONAS GINGIVALIS; RBR GENE; RESPIRATORY BURST; SAMPLING; ANIMAL; C57BL MOUSE; DISEASE MODEL; GENETICS; IMMUNOLOGY; METABOLISM; MOUSE MUTANT; MUCOSAL IMMUNITY;

BACTERIA (MICROORGANISMS); PORPHYROMONAS GINGIVALIS;

ANIMALS; ANTIOXIDANTS; BACTERIAL PROTEINS; BACTEROIDACEAE INFECTIONS; DISEASE MODELS, ANIMAL; FEMALE; FERREDOXINS; HUMANS; IMMUNITY, MUCOSAL; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NADPH OXIDASE; NEUTROPHILS; OXIDATIVE STRESS; PORPHYROMONAS GINGIVALIS; RESPIRATORY BURST;

EID: 33746619299     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.0020076     Document Type: Article

References (88)

1. Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L (2000) Neutrophils: Molecules, functions and pathophysiological aspects. Lab Invest 80: 617-653.
2. Belaaouaj A, Kim KS, Shapiro SD (2000) Degradation of outer membrane protein A in Escherichia coli killing by neutrophil elastase. Science 289: 1185-1188.
3. Lopez-Boado YS, Espinola M, Bahr S, Belaaouaj A (2004) Neutrophil serine proteinases cleave bacterial flagellin, abrogating its host response-inducing activity. J Immunol 172: 509-515.
4. Weinrauch Y, Drujan D, Shapiro SD, Weiss J, Zychlinsky A (2002) Neutrophil elastase targets virulence factors of enterobacteria. Nature 417: 91-94.
5. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y, et al. (2004) Neutrophil extracellular traps kill bacteria. Science 303: 1532-1535.
6. Lekstrom-Himes JA, Gallin JI (2000) Immunodeficiency diseases caused by defects in phagocytes. N Engl J Med 343: 1703-1714.
7. Roos D, van Bruggen R, Meischl C (2003) Oxidative killing of microbes by neutrophils. Microbes Infect 5: 1307-1315.
8. Goldblatt D, Thrasher AJ (2000) Chronic granulomatous disease. Clin Exp Immunol 122: 1-9.
9. Babior BM (2004) NADPH oxidase. Curr Opin Immunol 16: 42-47.
10. Winkelstein JA, Marino MC, Johnston RB, Boyle J, Curnutte, et al. (2000) Chronic granulomatous disease. Report on a national registry of 368 patients. Medicine (Baltimore) 79: 155-169.
11. Cohen MS, Leong PA, Simpson DM (1985) Phagocytic cells in periodontal defense. Periodontal status of patients with chronic granulomatous disease of childhood. J Periodontol 56: 611-617.
12. + flux. Nature 416: 291-297.
13. + channel is essential for innate immunity. Nature 427: 853-858.
14. Nizet V, Gallo RL (2003) Cathelicidins and innate defense against invasive bacterial infection. Scand J Infect Dis 35: 670-676.
15. Deas DE, Mackey SA, McDonnell HT (2003) Systemic disease and periodontitis: Manifestations of neutrophil dysfunction. Periodontol 2000 32: 82-104.
16. Hart TC, Shapira L, Van Dyke TE (1994) Neutrophil defects as risk factors for periodontal diseases. J Periodontol 65: 521-529.
17. Loesche WJ, Grossman NS (2001) Periodontal disease as a specific, albeit chronic, infection: Diagnosis and treatment. Clin Microbiol Rev 14: 727-752.
18. Van Dyke TE, Hoop G (1991) Neutrophil function and oral disease. Crit Rev Oral Biol Med 1: 117-133.
19. Cutler CW, Kalmar JR, Genco CA (1995) Pathogenic strategies of the oral anaerobe, Porphyromonas gingivalis. Trends Microbiol 3: 45-51.
20. Johnson NA, McKenzie R, McLean L, Sowers LC, Fletcher HM (2004) 8-oxo-7,8-dihydroguanine is removed by a nucleotide excision repair-like mechanism in Porphyromonas gingivalis W83. J Bacteriol 186: 7697-7703.
21. Nakayama K (1994) Rapid viability loss on exposure to air in a superoxide dismutase-deficient mutant of Porphyromonas gingivalis. J Bacteriol 176: 1939-1943.
22. Sztukowska M, Bugno M, Potempa J, Travis J, Kurtz DM Jr (2002) Role of Rbr in the oxidative stress response of Porphyromonas gingivalis. Mol Microbiol 44: 479-488.
23. Coulter ED, Shenvi NV, Kurtz DM Jr (1999) NADH peroxidase activity of rubrerythrin. Biochem Biophys Res Commun 255: 317-323.
24. Lumppio HL, Shenvi NV, Summers AO, Voordouw G, Kurtz DM Jr. (2001) Rubrerythrin and rubredoxin oxidoreductase in Desulfovibrio vulgaris. A novel oxidative stress protection system. J Bacteriol 183: 101-108.
25. Weinberg WV, Jenney FE Jr, Cui X, Adams MWW (2004) Rubrerythrin from the hyperthermophilic archaeon Pyrococcus furiosus is a rubredoxin-dependent iron-containing peroxidase. J Bacteriol 186: 7888-7895.
26. Smalley JW, Birss AJ, Silver J (2000) The periodontal pathogen Porphyromonas gingivalis harnesses the chemistry of the m-oxo bishaem of iron protophyrin IX to protect against hydrogen peroxide. FEMS Microbiol Lett 183: 159-164.
27. Genco CA, Cutler CW, Kapczynski D, Maloney K, Arnold RR (1991) A novel mouse model to study the virulence of and host response to Porphyromonas (Bacteroides) gingivalis. Infect Immun 59: 1255-1263.
28. Genco CA, Kapczynsk DR, Cutler CW, Arko RJ, Arnold RR (1992) Influence of immunization on Porphyromonas gingivalis colonization and invasion in the mouse chamber model. Infect Immun 60: 1447-1454.
29. Jarstrand C, Wiernik A, Revesz L (2000) Significance of oxygen availability for release of oxygen free radicals and lysozyme by neutrophils. J Clin Lab Immunol 32: 37-39.
30. Isogai E, Isogai H, Matuo K, Hirose K, Kowashi Y, et al. (2003) Sensitivity of genera Porphyromonas and Prevotella to the bactericidal action of C-terminal domain of human CAP18 and its analogues. Oral Microbiol Immunol 18: 329-332.
31. Klempner MS (1984) Interactions of polymorphonuclear leukocytes with anaerobic bacteria. Rev Infect Dis 6 (Suppl 1): S40-S44.
32. Van Amersfoort ES, Van Berkel TJ, Kuiper J (2003) Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin Microbiol Rev 16: 379-414.
33. Gyurko R, Boustany G, Huang PL, Kantarci A, Van Dyke TE, et al. (2003) Mice lacking inducible nitric oxide synthase demonstrate impaired killing of Porphyromonas gingivalis. Infect Immun 71: 4917-4924.
34. Banbula A, Bugno M, Kuster A, Heinrich PC, Travis J, et al. (1999) Rapid and efficient inactivation of IL-6 by gingipains, lysine- and arginine-specific proteinases from Porphyromonas gingivalis. Biochem Biophys Res Commun 261: 598-602.
35. Calkins CC, Platt K, Potempa J, Travis J (1998) Inactivation of tumor necrosis factor-alpha by proteinases (gingipains) from the periodontal pathogen, Porphyromonas gingivalis. Implications of immune evasion. J Biol Chem 273: 6611-6614.
36. Fletcher J, Nair S, Poole S, Henderson B, Wilson M (1998) Cytokine degradation by biofilms of Porphyromonas gingivalis. Curr Microbiol 36: 216-219.
37. Schmekel B, Karlsson SE, Linden M, Sundstrom C, Tegner H, et al. (1990) Myeloperoxidase in human lung lavage. I. A marker of local neutrophil activity. Inflammation 14: 447-454.
38. Dykens JA, Baginski TJ (1998) Urinary 8-hydroxydeoxyguanosine excretion as a non-invasive marker of neutrophil activation in animal models of inflammatory bowel disease. Scand J Gastroenterol 33: 628-636.
39. Caimi G, Hoffmann E, Montana M, Incalcaterra E, Dispensa F, et al. (2005) Plasma markers of platelet and polymorphonuclear leukocyte activation in young adults with acute myocardial infarction. Clin Hemorheol Microcirc 32: 67-74.
40. Miyasaki KT, Nemirovskiy E (1997) Myeloperoxidase isoform activities released by human neutrophils in response to dental and periodontal bacteria. Oral Microbiol Immunol 12: 27-32.
41. Keatings VM, Barnes PJ (1997) Granulocyte activation markers in induced sputum: Comparison between chronic obstructive pulmonary disease, asthma, and normal subjects. Am J Respir Crit Care Med 155: 449-453.
42. Holzer W, Petersen F, Strittmatter W, Matzku S, von Hoegen I (1996) A fusion protein of IL-8 and a Fab antibody fragments binds to IL-8 receptors and induces neutrophil activation. Cytokine 8: 214-221.
43. Grisham MB, Everse J, Janssen HF (1988) Endotoxemia and neutrophil activation in vivo. Am J Physiol 254: H1017-H1022.
44. Yamamoto C, Yoneda T, Yoshikawa M, Fu A, Tokuyama T, et al. (1997) Airway inflammation in COPD assessed by sputum levels of interleukin-8. Chest 112: 505-510.
45. Tauber E, Herouy Y, Goetz M, Urbanek R, Hagel E, et al. (1999) Assessment of serum myeloperoxidase in children with bronchial asthma. Allergy 54: 177-182.
46. Franck T, Grulke S, Deby-Dupont G, Deby C, Duvivier H, et al. (2005) Development of an enzyme-linked immunosorbent assay for specific equine neutrophil myeloperoxidase measurement in blood. J Vet Diagn Invest 17: 412-419.
47. Kristjansson G, Venge P, Wanders A, Loof L, Hallgren R (2004) Clinical and subclinical intestinal inflammation assessed by the mucosal patch technique: Studies of mucosal neutrophil and eosinophil activation in inflammatory bowel diseases and irritable bowel syndrome. Gut 53: 1806-1812.
48. Lau D, Mollnau H, Eiserich JP, Freeman BA, Daiber A, et al. (2005) Myeloperoxidase mediates neutrophil activation by association with CD11b/CD18 integrins. Proc Natl Acad Sci U S A 102: 431-436.
49. Fleming TJ, Fleming ML, Malek TR (1993) Selective expression of Ly-6G on myeloid lineage cells in mouse bone marrow. RB6-8C5 mAb to granulocyte- differentiation antigen (Gr-1) detects members of the Ly-6 family. J Immunol 151: 2399-2408.
50. Gibson FC 3rd, Genco CA (2001) Prevention of Porphyromonas gingivalis-induced oral bone loss following immunization with gingipain R1. Infec Immun 69: 7959-7963.
51. Thompson HL, Wilton JM (1991) Effects of anaerobiosis and aerobiosis on interactions of human polymorphonuclear leukocytes with the dental plaque bacteria Streptococcus mutans, Capnocytophaga ochracea, and Bacteroides gingivalis. Infect. Immun 59: 932-940.
52. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, et al. (2005) HIF-1a expression regulates the bactericidal capacity of phagocytes. J Clin Invest 115: 1806-1815.
53. Mayer-Scholl A, Hurwitz R, Brinkmann V, Schmid M, Jungblut P, et al. (2005) Human neutrophils kill Bacillus anthracis. PLoS Pathog 1: e23. DOI: 10.1371/journal.ppat.0010023
54. MacMicking J, Xie QW, Nathan C (1997) Nitric oxide and macrophage function. Annu Rev Immunol 15: 323-350.
55. van der Veen RC, Dietlin TA, Hofman FM, Pen L, Segal BH, et al. (2000) Superoxide prevents nitric oxide-mediated suppression of helper T lymphocytes: Decreased autoimmune encephalomyelitis in nicotinamide adenine dinucleotide phosphate oxidase knockout mice. J Immunol 164: 5177-5183.
56. van der Veen RC, Dietlin TA, Karapetian A, Holland SM, Hofman FM (2004) Extra-cellular superoxide promotes T cell expansion through inactivation of nitric oxide. J Neuroimmunol 153: 183-189.
57. Ramsey KH, Sigar IM, Rana SV, Gupta J, Holland SM, et al. (2001) Role for inducible nitric oxide synthase in protection from chronic Chlamydia trachomatis urogenital disease in mice and its regulation by oxygen free radicals. Infect Immun 69: 7374-7379.
58. Kleinert H, Schwarz PM, Forstermann U (2003) Regulation of the expression of inducible nitric oxide synthase. Biol Chem 384: 1343-1364.
59. Aktan F. (2004) iNOS-mediated nitric oxide production and its regulation. Life Sci 75: 639-653.
60. Brune B (2005) The intimate relation between nitric oxide and superoxide in apoptosis and cell survival. Antioxid Redox Signal 7: 497-507.
61. Nathan C. (2003) Specificity of a third kind: Reactive oxygen and nitrogen intermediates in cell signaling. J Clin Invest 111: 769-778.
62. Isenberg JS, Tabatabai N, Spinelli HM (2005) Nitric oxide modulation of low-density mononuclear cell transendothelial migration. Microsurgery 25: 452-456.
63. Razavi HM, Wang le F, Weicker S, Rohan M, Law C, et al. (2004) Pulmonary neutrophil infiltration in murine sepsis: Role of inducible nitric oxide synthase. Am J Respir Crit Care Med 170: 227-233.
64. Yasui K, Kobayashi N, Yamazaki T, Agematsu K, Matsuzaki S, et al. (2005) Superoxide dismutase (SOD) as a potential inhibitory mediator of inflammation via neutrophil apoptosis. Free Radic Res 39: 755-762.
65. Ward C, Wong TH, Murray J, Rahman I, Haslett C, et al. (2000) Induction of human neutrophil apoptosis by nitric oxide donors: Evidence for a caspase-dependent, cyclic-GMP-independent, mechanism. Biochem Pharmacol 59: 305-314.
66. Sato E, Simpson KL, Grisham MB, Koyama S, Robbins RA (2000) Reactive nitrogen and oxygen species attenuate interleukin-8-induced neutrophil chemotactic activity in vitro. J Biol Chem 275: 10826-10830.
67. van Pelt LJ, Huisman MV, Weening RS, von dem Borne AE, Roos D, et al. (1996) A single dose of granulocyte-macrophage colony-stimulating factor induces systemic interleukin-8 release and neutrophil activation in healthy volunteers. Blood 87: 5305-5313.
68. Segal BH, Ding L, Holland SM (2003) Phagocyte NADPH oxidase, but not inducible nitric oxide synthase, is essential for early control of Burkholderia cepacia and Chromobacterium violaceum infection in mice. Infect Immun 71: 205-210.
69. Messina CGM, Reeves EP, Roes J, Segal AW (2002) Catalase negative Staphylococcus aureus retain virulence in mouse model of chronic granulomatous disease. FEBS Lett 518: 107-110.
70. Belaaouaj A, McCarthy R, Baumann M, Gao Z, Ley TJ, et al. (1998) Mice lacking neutrophil elastase reveal impaired host defence against gram negative bacterial sepsis. Nat Med 4: 615-618.
71. Tkalcevic J, Novelli M, Phylactides M, Iredale JP, Segal AW, et al. (2000) Impaired immunity and enhanced resistance to endotoxin in the absence of neutrophil elastase and cathepsin G. Immunity 12: 201-210.
72. Mastroeni P, Vazquez-Torres A, Fang FC, Xu Y, Khan S, et al. (2000) Antimicrobial actions of the NADPH phagocyte oxidase and inducible nitric oxide synthase in experimental salmonellosis. II. Effects on microbial proliferation and host survival in vivo. J Exp Med 192: 237-248.
73. Ogawa T, Asai Y, Yamamoto H, Taiji Y, Jinno T, et al. (2000) Immunobiological activities of a chemically synthesized lipid A of Porphyromonas gingivalis. FEMS Immunol Med Microbiol 28: 273-281.
74. O'Reilly M, Newcomb DE, Remick D (1999) Endotoxin, sepsis, and the primrose path. Shock 12: 411-420.
75. Kobayashi SD, Vovich JM, Braughton KR, Whitnry AR, Nauseef WM, et al. (2004) Gene expression profiling provides insight into the pathophysiology of chronic granulomatous disease. J Immunol 172: 636-643.
76. Reth M (2002) Hydrogen peroxide as second messenger in lymphocyte activation. Nat Immunol 3: 1129-1134.
77. Perez HD, Kelly E, Elfman F, Armitage G, Winkler J (1991) Defective polymorphonuclear leukocyte formyl peptide receptor(s) in juvenile periodontitis. J Clin Invest 87: 971-976.
78. Cainciola LJ, Genco RJ, Patters MR, McKenna J, van Oss CJ (1977) Defective polymorphonuclear leukocyte function in a human periodontal disease. Nature 265: 445-447.
79. Hewitt C, McCormick D, Linden G, Turk D, Stern I, et al. (2004) The role of cathepsin C in Papillon-Lefavre syndrome, prepubertal periodontitis, and aggressive periodontitis. Hum Mutat 23: 222-228.
80. Putsep K, Carlsson G, Boma HG, Andersson M (2002) Deficiency of antibacterial peptides in patients with morbus Kostmann: An observation study. Lancet 360: 1144-1149.
81. Gronert K, Kantarci A, Levy BD, Clish CB, Odparlik S, et al. (2004) A molecular defect in intracellular lipid signaling in human neutrophils in localized aggressive periodontal tissue damage. J Immunol 172 : 1856-1861.
82. Miyasaki KT. (1991) The neutrophil: mechanisms of controlling periodontal bacteria. J Periodontol 62: 761-774.
83. White NJ (2003) Melioidosis. Lancet 361: 1715-1722.
84. Eberl L, Tummler B (2004) Pseudomonas aeruginosa and Burkholderia cepacia in cystic fibrosis: Genome evolution, interactions and adaptation. Int J Med. Microbiol 294: 123-131.
85. Crushell E, Harty S, Sharif F, Bourke B (2004) Enteric Campylobacter: purging its secrets? Pediatr Res 55: 3-12.
86. Finegold SM (1977) Anaerobic bacteria in human diseases. New York: Academic Press. 710 p.
87. Segal AW, Geisow M, Garcia R, Harper A, Miller R (1981) The respiratory of phagocytic cells is associated with a rise in vacuolar pH. Nature 290: 406-409.
88. Baker PJ, Evans RT, Roopenian DC (1994) Oral infection with Porphyromonas gingivalis and induced alveolar bone loss in immunocompetent and severe combined immunodeficient mice. Arch Oral Biol 39: 1035-1040.