Porphyromonas gingivalis: A clonal pathogen? Diversities in housekeeping genes and the major fimbriae gene

Journal of Oral Microbiology

Volumn 3, Issue 2011, 2011, Pages

  Enersen, Morten ^a  

^a UNIVERSITY OF OSLO   (Norway)

Author keywords

Fima genotyping; Mlst; Periodontitis; Population genetics; Porphyromonas gingivalis; Recombination

Indexed keywords

FIMBRIA PROTEIN; PROTEIN FIMA; UNCLASSIFIED DRUG;

CLONE; DNA SEQUENCE; FIMA GENE; FIMBRIA; GENETIC ASSOCIATION; GENETIC HETEROGENEITY; GENETIC RECOMBINATION; GENETIC VARIABILITY; GENOTYPE; HOUSEKEEPING GENE; HUMAN; MULTILOCUS ENZYME ELECTROPHORESIS; MULTILOCUS SEQUENCE TYPING; NONHUMAN; PERIODONTITIS; POLYMERASE CHAIN REACTION; POPULATION GENETICS; POPULATION STRUCTURE; PORPHYROMONAS GINGIVALIS; REVIEW;

EID: 84864807050     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.3402/jom.v3i0.8487     Document Type: Review

References (95)

1. Cooper JE, Feil EJ. Multilocus sequence typing - what is resolved? Trends Microbiol 2004; 12: 373-7.
2. Baker S, Hanage W, Holt K. Navigating the future of bacterial molecular epidemiology. Curr Opin Microbiol 2010; 13: 640-5.
3. Feil EJ, Spratt BG. Recombination and the population structures of bacterial pathogens. Annu Rev Microbiol 2001; 55: 561-90.
4. Feil EC, Enright MC. Analyses of clonality and the evolution of bacterial pathogens. Curr Opin Microbiol 2004; 7: 308-13.
5. Maynard Smith J, Smith NH, O'Rourke M, Spratt BG. How clonal are bacteria? Proc Natl Acad Sci U S A 1993; 90: 4384-8.
6. Maynard Smith J, Feil E, Smith NH. Population structure and evolutionary dynamics of pathogenic acteria. Bioessays 2000; 22: 1115-22.
7. Caugant DA, Bøvre K, Gaustad P, Bryn K, Holten E, Høiby EA. Multilocus genotypes determined by enzyme electrophoresis of Neisseria meningitidis isolated from patients with systemic disease and from healthy carriers. J Gen Microbiol 1986; 132: 641-52.
8. Maiden MCJ. Multilocus sequence typing of bacteria. Annu Rev Microbiol 2006; 60: 561-88.
9. Spratt BG, Hanage WP, Li B, Aanensen D, Feil E. Displaying the relatedness among isolates of bacterial species - the eBURST approach. FEMS Microbiol Lett 2004; 214: 129-34.
10. Kilian M, Frandsen EVG, Haubek D, Poulsen K. The etiology of periodontal disease revisited by population genetic analysis. Periodontol 2000-2006; 42: 158-79.
11. Maiden MC, Bygraves JA, Feil E, Morelli G, Russell JE, Urwin R, et al. Multilocus sequence typing: a portable approach to the identification of clones within populations of pathogenic microorganisms. Proc Natl Acad Sci U S A 1998; 95: 3140-5.
12. Bougnoux ME, Aanensen DM, Morand S, Théraud M, Spratt BG, d'Enfert C. Multilocus sequence typing of Candida albicans: strategies, data exchange and applications. Infect Genet Evol 2004; 3: 243-52.
13. Dodgson AR, Pujol C, Denning DW, Soll DR, Fox AJ. Multilocus sequence typing of Candida glabrata reveals geographically enriched clades. J Clin Microbiol 2003; 41: 5709-17.
14. Enright MC, Spratt BG. A multilocus sequence typing scheme for Streptococcus pneumoniae: identification of clones associated with serious invasive disease. Microbiology 1998; 144: 3049-60.
15. Dingle KE, Colles FM, Wareing DR, Ure R, Fox AJ, Bolton FE, et al. Multilocus sequence typing system for Campylobacter jejuni. J Clin Microbiol 2001; 39: 14-23.
16. Enright MC, Spratt BG, Kalia A, Cross JH, Bessen DE. Multilocus sequence typing of Streptococcus pyogenes and the relationships between emm type and clone. Infect Immun 2001; 69: 2416-27.
17. Kotetishvili M, Stine OC, Kreger A, Morris JG Jr, Sulakvelidze A. Multilocus sequence typing for characterization of clinical and environmental Salmonella strains. J Clin Microbiol 2002; 40: 1626-35.
18. Feil EJ, Cooper JE, Grundmann H, Robinson DA, Enright MC, Berendt T, et al. How clonal is Staphylococcus aureus? J Bacteriol 2003; 185: 3307-16.
19. Meats E, Feil EJ, Stringer S, Cody AJ, Goldstein R, Kroll JS, et al. Characterisation of encapsulated and noncapsulated Haemophilus influenzae and determination of phylogenetic relationships by multilocus sequence typing. J Clin Microbiol 2003; 41: 1623-36.
20. Helgason E, Tourasse NJ, Meisal R, Caugant DA, Kolstø A-B. Multilocus sequence typing scheme for bacteria of the Bacillus cereus group. Appl Environ Microbiol 2004; 70: 191-201.
21. Urwin R, Maiden MCJ. Multi-locus sequence typing: a tool for global epidemiology. Trends Microbiol 2003; 11: 479-87.
22. Jolley K, Chan MS, Maiden MC. mlstdbNet-distributed multilocus sequence typing (MLST) databases. BMC Bioinformatics 2004; 5: 86.
23. Jolley KA, Maiden MC. BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 2010; 11: 595.
24. Listgarten MA. Structure of the microbial flora associated with periodontal health and disease in man. A light and electron microscopic study. J Periodontol 1976; 47: 1-18.
25. Kolenbrander PE, Palmer RJ JR, Rickard AH, Jakubovics N, Chalmers NI, Diaz P. Bacterial interactions and successions during plaque development. Periodontol 2000 2006; 42: 47-79.
26. Darveau RP, Tanner A, Page RC. The microbial challenge in periodontitis. Periodontol 2000 1997; 14: 12-32.
27. Holt SC, Kesavalu L, Walker S, Genco CA. Virulence factors of Porphyromonas gingivalis. Periodontol 1999; 20: 168-238.
28. Amano A. Molecular interaction of Porphyromonas gingivalis with host cells: implication for the microbial pathogenesis of periodontal disease. J Periodontol 2003; 74: 90-6.
29. Nelson KE, Fleischmann RD, DeBoy RT, Paulsen IT, Fouts DE, Eisen JA, et al. Complete genome sequence of the oral pathogenic bacterium Porphyromonas gingivalis strain W83. J Bacteriol 2003; 185: 5591-601.
30. Holt S, Ebersole J. Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the 'red complex', a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000-2005; 38: 72-122.
31. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25: 134-44.
32. Socransky SS, Haffajee AD. Periodontal microbial ecology. Periodontol 2000-2005; 38: 135-87.
33. Dzink JL, Socransky SS, Haffajee AD. The predominant cultivable microbiota of active and inactive lesions of destructive periodontal diseases. J Clin Periodontol 1988; 15: 316-23.
34. Haffajee AD, Cugini MA, Tanner A, Pollack RP, Smith C, Kent RL Jr, et al. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 1998; 25: 346-53.
35. Feng Z, Weinberg A. Role of bacteria in health and disease of periodontal tissues. Periodontol 2000-2006; 40: 50-76.
36. Mager DL, Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Distribution of selected bacterial species on intraoral surfaces. J Clin Periodontol 2003; 30: 644-54.
37. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontol 2000 1994; 5: 78-111.
38. Travis J, Pike R, Imamura T, Potempa J. Porphyromonas gingivalis proteinases as virulence factors in the development of periodontitis. J Periodontal Res 1997; 32: 120-5.
39. Lamont RJ, Jenkinson H. Life below the gum line: pathogenic mechanisms of Porphyromonas gingivalis. Microbiol Mol Biol Rev 1998; 62: 1244-63.
40. Imamura T. The role of gingipains in the pathogenesis of periodontal disease. J Periodontol 2003; 74: 111-8.
41. O'Brien Simpson NM, Veith PD, Dashper SG, Reynolds EC. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Prot Pept Sci 2003; 4: 409-26.
42. Lamont RJ, Jenkinson HF. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 2000; 15: 341-9.
43. Li L, Michel R, Cohen J, Decarlo A, Kozarov E. Intracellular survival and vascular cell-to-cell transmission of Porphyromonas gingivalis. BMC Microbiol 2008; 8: 26.
44. Hajishengallis G. Porphyromonas gingivalis - host interactions: open war or intelligent guerilla tactics? Microbes and Infection 2009; 11: 637-45.
45. Scannapieco FA, Bush RB, Paju S. Associations between periodontal disease and risk for atherosclerosis, cardiovascular disease, and stroke. A systematic review. Ann Periodontol 2003; 8: 38-53.
46. Kozarov EV, Dorn BR, Shelburne CE, Dunn WA Jr, Progulske-Fox A. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 2005; 25: 17-8.
47. Kozarov E, Sweier D, Shelburne C, Progulske-Fox A, Lopatin D. Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect 2006; 8: 687-93.
48. Wada K, Kamisaki Y. Roles of oral bacteria in cardiovascular diseases. From molecular mechanisns to clinical cases: involvement of Porphyromonas gingivalis in the deveopment of human aortic aneurysm. J Pharmacol Sci 2010; 113: 115-9.
49. Nakano K, Wada K, Nomura R, Nemoto H, Inaba H, Kojima A, et al. Characterization of aortic aneurysms in cardiovascular disease patients harboring Porphyromonas gingivalis. Oral Diseases 2011; 17: 370-8.
50. Hamada S, Amano A, Kimura S, Nakagawa I, Kawabata S, Morisaki I. The importance of fimbriae in the virulence and ecology of some oral bacteria. Oral Microbiol Immunol 1998; 13: 129-38.
51. Amano A, Nakagawa I, Okahashi N, Hamada N. Variations of Porphyromonas gingivalis fimbriae in relation to microbial pathogenesis. J Periodontal Res 2004; 39: 136-42.
52. Hamada N, Sojar HT, Cho M, Genco RJ. Isolation and characterization of minor fimbria from Porphyromonas gingivalis. Infect Immun 1996; 59: 4788-94.
53. Dickinson DP, Kubiniec MA, Yoshimura F, Genco RJ. Molecular cloning and sequencing of the gene encoding the fimbrial subunit protein of Bacteroides gingivalis. J Bacteriol 1988; 170: 1658-65.
54. Lee JY, Sojar HT, Bedi GS, Genco RJ. Porphyromonas (Bacteroides) gingivalis fimbrillin: size, amino-terminal sequence, and antigenic heterogeneity. Infect Immun 1991; 59: 383-9.
55. Fujiwara T, Morishima S, Takahashi I, Hamada S. Molecular cloning and sequencing of the fimbrillin gene of Porphyromonas gingivalis strains and characterization of recombinant proteins. Biochem Biophys Res Commun 1993; 197: 241-7.
56. Amano A, Nakagawa I, Kataoka K, Morisaki I, Hamada S. Distribution of Porphyromonas gingivalis strains with fimA genotypes in periodontitis patients. J Clin Microbiol 1999; 37: 1426-30.
57. Nakagawa I, Amano A, Kimura RK, Nakamura T, Kawabata S, Hamada S. Distribution and molecular characterization of Porphyromonas gingivalis carrying a new type of fimA gene. J Clin Microbiol 2000; 38: 1909-14.
58. Nakagawa I, Amano A, Ohara-Nemoto Y, Endoh N, Morisaki I, Kimura S, et al. Identification of a new variant of fimA gene of Porphyromonas gingivalis and its distribution in adults and disabled populations with periodontitis. J Periodontal Res 2002; 37: 425-32.
59. Amano A, Kubinowa M, Nakagawa I, Akiyama S, Morisaki I, Hamada S. Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status. J Dent Res 2000; 79: 1664-8.
60. Beikler T, Peters U, Prajaneh S, Prior K, Ehmke B, Fleming TF. Prevalence of Porphyromonas gingivalis fimA genotypes in Caucasians. Eur J Oral Sci 2003; 111: 390-4.
61. Missailidis CG, Emeda JE, Ota-Tsuzuki C, Anzai D, Mayer MPA. Distribution of fimA genotypes of Porphyromonas gingivalis in subjects with various periodontal conditions. Oral Microbiol Immunol 2004; 19: 224-9.
62. Miura M, Hamachi T, Fujise O, Maeda K. The prevalence and pathogenic differences of Porphyromonas gingivalis fimA genotypes in patients with aggressive periodontitis. J Periodontal Res 2005; 40: 147-52.
63. Nakagawa I, Amano A, Kubinowa M, Nakamura T, Kawabata S, Hamada S. Functional differences among FimA variants of Porphyromonas gingivalis and their effects on adhesion to and invasion of human epithelial cells. Infect Immun 2002; 70: 277-85.
64. Neiders ME, Chen PB, Suido H, Reynolds HS, Zambon JJ, Shlossman M, et al. Heterogeneity of virulence among strains of Bacteroides gingivalis. J Periodontal Res 1989; 24: 192-8.
65. Genco CA, Van Dyke T, Amar S. Animal models for Porphyromonas gingivalis-mediated periodontal disease. Trends Microbiol 1998; 6: 444-9.
66. Nakano K, Kubinowa M, Nakagawa I, Yamamura T, Nomura R, Okahashi N, et al. Comparison of inflammatory changes caused by Porphyromonas gingivalis with distinct fimA genotypes in a mouse abscess model. Oral Microbiol Immunol 2004; 19: 205-9.
67. Kato T, Kawai S, Nakano K, Inaba H, Kubinowa M, Nakagawa I, et al. Virulence of Porphyromonas gingivalis is altered by substitution of fimbria gene with different genotype. Cell Microbiol 2007; 9: 753-65.
68. Umeda JE, Missailidis C, Longo PL, Anzai D, Wikstrom M, Mayer MPA. Adhesion and invasion to epithelial cells by fimA genotypes of Porphyromonas gingivalis. Oral Microbiol Immunol 2006; 21: 415-9.
69. Inaba H, Nakano K, Kato T, Nomura R, Kawai S, Kubinowa M, et al. Heterogenic virulence and related factors among clinical isolates of Porphyromonas gingivalis with type II fimbriae. Oral Microbiol Immunol 2008; 23: 29-35.
70. Nakano K, Inaba H, Nomura R, Nemoto H, Takeuchi H, Toda K, et al. Distribution of Porphyromonas gingivalis fimA genotypes in cardiovascular specimens from Japanese patients. Oral Microbiol Immunol 2008; 23: 170-2.
71. Rôças IN, Siqueira Jr JF Distribution of Porphyromonas gingivalis fimA genotypes in primary endodontic infections. Oral Surg Oral Med Oral Path Oral Radiol Endod 2010; 10: 474-8.
72. Wang Q, Zhou X, Zheng Q, Wang Y, Tang L, Huang D. Distribution of Porphyromonas gingivalis fimA genotypes in chronic apical periodontitis associated with symptoms. J Endodontics 2010; 36: 1790-5.
73. Loos BG, Dyer DW, Whittam TS, Selander RK. Genetic structure of populations of Porphyromonas gingivalis associated with periodontitis and other oral infections. Infect Immun 1993; 61: 204-12.
74. Menard C, Mouton C. Clonal diversity of the taxon Porphyromonas gingivalis assessed by random amplified polymorphic DNA fingerprinting. Infect Immun 1995; 63: 2522-31.
75. Ali RW, Martin L, Haffajee AD, Socransky SS. Detection of identical ribotypes of Porphyromonas gingivalis in patients residing in the United States, Sudan, Romania and Norway. Oral Microbiol Immunol 1997; 12: 106-11.
76. Frandsen EV, Poulsen K, Curtis MA, Kilian M. Evidence of recombination in Porphyromonas gingivalis and random distribution of putative virulence markers. Infect Immun 2001; 69: 4479-85.
77. Koehler A, Karch H, Beikler T, Flemmig TF, Suerbaum S, Schmidt H. Multilocus sequence analysis of Porphyromonas gingivalis indicates frequent recombination. Microbiology 2003; 149: 2407-15.
78. Enersen M, Olsen I, Caugant DA. Multilocus sequence typing of Porphyromonas gingivalis strains from different geographic origins. J Clin Microbiol 2006; 44: 35-41.
79. Enersen M, Olsen I, Kvalheim Ø, Caugant DA. fimA genotypes and multilocus sequence types of Porphyromonas gingivalis from patients with periodontitis. J Clin Microbiol 2008; 46: 31-42.
80. Jolley KA, Feil EJ, Chan MS, Maiden MC. Sequence type analysis and recombinational tests (START). Bioinformatics 2001; 17: 1230-1.
81. Enersen M. Population structure of the periodontal pathogen Porhyromonas gingivalis: diversity in housekeeping genes and the major fimbrae gene. Thesis. University of Oslo, Oslo, Norway; 2008.
82. Haubold B, Hudson RR. LIAN 3.0: detecting linkage disequilibrium in multilocus data. Bioinformatics 2000; 16: 847-8.
83. Maynard Smith J. Analyzing the mosaic structure of genes. J Mol Evol 1992; 34: 126-9.
84. Enersen M, Olsen I, Caugant DA. Genetic diversity of Porphyromonas gingivalis isolates from single 'refractory' periodontitis sites. Appl Environ Microbiol 2008; 74: 5817-21.
85. Huson DH. SplitsTree: analyzing and visualizing evolutionary data. Bioinformatics 1998; 14: 68-73.
86. Loos BG, Van Winkelhoff AJ, Dunford RG, Genco RJ, De Graaff J, Dickinson DP, et al. A statistical approach to the ecology of Porphyromonas gingivalis. J Dent Res 1992; 71: 353-8.
87. Socransky SS, Haffajee AD. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 1992; 63: 322-31.
88. Tribble GA, Lamont GJ, Progulske-Fox A, Lamont RJ. Conjugal transfer of chromosomal DNA contributes to genetic variation in the oral pathogen Porphyromonas gingivalis. J Bacteriol 2007; 189: 6382-8.
89. Zhang YJ, Yasui S, Yoshimura F, Ishikawa I. Multiple restriction fragment length polymorphism genotypes of Porphyromonas gingivalis in single periodontal pockets. Oral Microbiol Immunol 1995; 10: 125-8.
90. Leys EJ, Smith JH, Lyons SR, Griffen AL. Identification of Porphyromonas gingivalis strains by heteroduplex analysis and detection of multiple strains. J Clin Microbiol 1999; 37: 3906-11.
91. Haffajee AD, Uzel NG, Arguello EI, Torresyap G, Guerrero DM, Socransky SS. Clinical and microbiological changes associated with the use of combined antimicrobial therapies to treat 'refractory' peridontitis. J Clin Periodontol 2004; 31: 869-71.
92. Armitage GC. The development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999; 4: 1-6.
93. Hanage WP, Fraser C, Spratt BG. The impact of homologous recombination on the generation of diversity in bacteria. J Theor Biol 2006; 239: 210-9.
94. Fraser C, Hanage WP, Spratt BG. Recombination and the nature of bacterial speciation. Science 2007; 315: 476-80.
95. Feil EJ, Li BC, Aanensen DM, Hanage WP, Spratt BG. eBURST: inferring patterns of evolutionary descent among clusters of related bacterial genotypes from multilocus sequence typing data. J Bacteriol 2004; 186: 1518-30.