Porphyromonas gingivalis: Keeping the pathos out of the biont

Journal of Oral Microbiology

Volumn 5, Issue 2013, 2013, Pages

  Cugini, Carla ^a,b   Klepac Ceraj, Vanja ^a,c   Rackaityte, Elze ^c   Riggs, James E ^d   Davey, Mary E ^e  

^a FORSYTH INSTITUTE   (United States)

^b HARVARD SCHOOL OF DENTAL MEDICINE   (United States)

^c WELLESLEY COLLEGE   (United States)

^d RIDER UNIVERSITY   (United States)

^e UNIVERSITY OF FLORIDA COLLEGE OF DENTISTRY   (United States)

Author keywords

Biofilm; Immunoediting hypothesis; P. gingivalis; Pathobiont; Tumor

Indexed keywords

BACTERIAL PROTEIN; IRON; VIRULENCE FACTOR;

ARTICLE; BACTERIAL GENOME; BACTERIAL VIRULENCE; BACTERIOPHAGE; BIOFILM; CLUSTERED REGULARLY INTERSPACES SHORT PALINDROM REPEAT REGION; COMMUNITY STRUCTURE; GENE LOCUS; HUMAN; MALIGNANT NEOPLASTIC DISEASE; MICROBIAL COMMUNITY; MOUTH FLORA; NONHUMAN; NUTRITIONAL ASSESSMENT; NUTRITIONAL PARAMETERS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN DEGRADATION; SPECIES COMPOSITION;

EID: 84879303332     PISSN: None     EISSN: 20002297     Source Type: Journal    
DOI: 10.3402/jom.v5i0.19804     Document Type: Article

References (127)

1. Seymour GJ, Ford PJ, Cullinan MP, Leishman S, Yamazaki K. Relationship between periodontal infections and systemic disease. Clin Microbiol Infect 2007; 13(Suppl 4): 3-10.
2. Gottlieb B. The formation of the pocket: diffuse atropy of alveolar bone. J Am Dent Assoc 1928; 15: 462-74.
3. Socransky SS, Haffajee AD. Implications of periodontal microbiology for the treatment of periodontal infections. Compendium 1994: S684-5, 8-93; quiz S714-7.
4. Aas JA, Paster BJ, Stokes LN, Olsen I, Dewhirst FE. Defining the normal bacterial flora of the oral cavity. J Clin Microbiol 2005; 43: 5721-32.
5. Dewhirst FE, Chen T, Izard J, Paster BJ, Tanner AC, Yu WH, et al. The human oral microbiome. J Bacteriol 2010; 192: 5002-17.
6. Siqueira JF, Jr., Rocas IN. Community as the unit of pathogenicity: an emerging concept as to the microbial pathogenesis of apical periodontitis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2009; 107: 870-8.
7. Berezow AB, Darveau RP. Microbial shift and periodontitis. Periodontology 2000 2010; 55: 36-47.
8. Darveau RP. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 2010; 8: 481-90.
9. Baelum V, Lopez R. Defining and classifying periodontitis: need for a paradigm shift. Eur J Oral Sci 2003; 111: 2-6.
10. Lopez NJ. Occurrence of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis, and Prevotella intermedia in progressive adult periodontitis. J Periodontol 2000; 71: 948-54.
11. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Comparison of the microbiota of supra- and subgingival plaque in health and periodontitis. J Clin Periodontol 2000; 27: 648-57.
12. Haffajee AD, Cugini MA, Tanner A, Pollack RP, Smith C, Kent RL, Jr., et al. Subgingival microbiota in healthy, wellmaintained elder and periodontitis subjects. J Clin Periodontol 1998; 25: 346-53.
13. Moore WE, Moore LV. The bacteria of periodontal diseases. Periodontology 2000 1994; 5: 66-77.
14. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontology 2000 1994; 5: 78-111.
15. Ximenez-Fyvie LA, Haffajee AD, Socransky SS. Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol 2000; 27: 722-32.
16. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL, Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998; 25: 134-44.
17. Gmur R, Guggenheim B. Interdental supragingival plaque-a natural habitat of Actinobacillus actinomycetemcomitans, Bacteroides forsythus, Campylobacter rectus, and Prevotella nigrescens. J Dent Res 1994; 73: 1421-8.
18. Frisken KW, Tagg JR, Laws AJ, Orr MB. Suspected periodontopathic microorganisms and their oral habitats in young children. Oral Microbiol Immunol 1987; 2: 60-4.
19. Mombelli A, Buser D, Lang NP, Berthold H. Suspected periodontopathogens in erupting third molar sites of periodontally healthy individuals. J Clin Periodontol 1990; 17: 48-54.
20. Mazmanian SK, Round JL, Kasper DL. A microbial symbiosis factor prevents intestinal inflammatory disease. Nature 2008; 453: 620-5.
21. Round JL, Mazmanian SK. The gut microbiota shapes intestinal immune responses during health and disease. Nat Rev Immunol 2009; 9: 313-23.
22. Chow J, Mazmanian SK. A pathobiont of the microbiota balances host colonization and intestinal inflammation. Cell Host Microbe 2010; 7: 265-76.
23. Chow J, Tang H, Mazmanian SK. Pathobionts of the gastrointestinal microbiota and inflammatory disease. Current opinion in immunology 2011; 23: 473-80.
24. Choi JI, Nakagawa T, Yamada S, Takazoe I, Okuda K. Clinical, microbiological and immunological studies on recurrent periodontal disease. J Clin Periodontol 1990; 17: 426-34.
25. 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.
26. Grossi SG, Zambon JJ, Ho AW, Koch G, Dunford RG, Machtei EE, et al. Assessment of risk for periodontal disease. I. Risk indicators for attachment loss. J Periodontol 1994; 65: 260-7.
27. Lamont RJ, Jenkinson HF. Subgingival colonization by Porphyromonas gingivalis. Oral Microbiol Immunol 2000; 15: 341-9.
28. Moore WE, Moore LH, Ranney RR, Smibert RM, Burmeister JA, Schenkein HA. The microflora of periodontal sites showing active destructive progression. J Clin Periodontol 1991; 18: 729-39.
29. Masuda K, Yoshioka M, Hinode D, Nakamura R. Purification and characterization of arginine carboxypeptidase produced by Porphyromonas gingivalis. Infect Immun 2002; 70: 1807-15.
30. Masuda K, Tomita K, Hayashi H, Yoshioka M, Hinode D, Nakamura R. Consumption of peptide-derived arginine by a periodontopathogenic bacterium, Porphyromonas gingivalis. Anaerobe 2001; 7: 209-17.
31. McGraw WT, Potempa J, Farley D, Travis J. Purification, characterization, and sequence analysis of a potential virulence factor from Porphyromonas gingivalis, peptidylarginine deiminase. Infect Immun 1999; 67: 3248-56.
32. Chen Z, Potempa J, Polanowski A, Wikstrom M, Travis J. Purification and characterization of a 50-kDa cysteine proteinase (gingipain) from Porphyromonas gingivalis. J Biol Chem 1992; 267: 18896-901.
33. Rodriguez SB, Stitt BL, Ash DE. Expression of peptidylarginine deiminase from Porphyromonas gingivalis in Escherichia coli: enzyme purification and characterization. Arch Biochem Biophys 2009; 488: 14-22.
34. Endo J, Otsuka M, Ohara E, Sato M, Nakamura R. Cleavage action of a trypsin-like protease from Bacteroides gingivalis 381 on reduced egg-white lysozyme. Arch Oral Biol 1989; 34: 911-6.
35. Grenier D, La VD. Proteases of Porphyromonas gingivalis as important virulence factors in periodontal disease and potential targets for plant-derived compounds: a review article. Curr Drug Targets 2011; 12: 322-31.
36. Kuramitsu HK. Proteases of Porphyromonas gingivalis: what don't they do. Oral Microbiol Immunol 1998; 13: 263-70.
37. O-Brien-Simpson NM, Veith PD, Dashper SG, Reynolds EC. Porphyromonas gingivalis gingipains: the molecular teeth of a microbial vampire. Curr Protein Pept Sci 2003; 4: 409-26.
38. Potempa J, Banbula A, Travis J. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontology 2000 2000; 24: 153-92.
39. Takii R, Kadowaki T, Baba A, Tsukuba T, Yamamoto K. A functional virulence complex composed of gingipains, adhesins, and lipopolysaccharide shows high affinity to host cells and matrix proteins and escapes recognition by host immune systems. Infect Immun 2005; 73: 883-93.
40. Hajishengallis G, Darveau RP, Curtis MA. The keystonepathogen hypothesis. Nat Rev Microbiol 2012; 10: 717-25.
41. Hajishengallis G, Liang S, Payne MA, Hashim A, Jotwani R, Eskan MA, et al. Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 2011; 10: 497-506.
42. Colombo AV, Silva CM, Haffajee A, Colombo AP. Identification of oral bacteria associated with crevicular epithelial cells from chronic periodontitis lesions. J Med Microbiol 2006; 55: 609-15.
43. Rudney JD, Chen R. The vital status of human buccal epithelial cells and the bacteria associated with them. Arch Oral Biol 2006; 51: 291-8.
44. Zaura E, Keijser BJ, Huse SM, Crielaard W. Defining the healthy "core microbiome" of oral microbial communities. BMC Microbiol 2009; 9: 259.
45. Bik EM, Long CD, Armitage GC, Loomer P, Emerson J, Mongodin EF, et al. Bacterial diversity in the oral cavity of 10 healthy individuals. The ISME J 2010; 4: 962-74.
46. Hasturk H, Kantarci A, Goguet-Surmenian E, Blackwood A, Andry C, Serhan CN, et al. Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 2007; 179: 7021-9.
47. Frias-Lopez J, Duran-Pinedo A. Effect of periodontal pathogens on the metatranscriptome of a healthy multispecies biofilm model. J Bacteriol 2012; 194: 2082-95.
48. Kuboniwa M, Tribble GD, James CE, Kilic AO, Tao L, Herzberg MC, et al. Streptococcus gordonii utilizes several distinct gene functions to recruit Porphyromonas gingivalis into a mixed community. Mol Microbiol 2006; 60: 121-39.
49. Saito Y, Fujii R, Nakagawa KI, Kuramitsu HK, Okuda K, Ishihara K. Stimulation of Fusobacterium nucleatum biofilm formation by Porphyromonas gingivalis. Oral Microbiol Immunol 2008; 23: 1-6.
50. Kuboniwa M, Hendrickson EL, Xia Q, Wang T, Xie H, Hackett M, et al. Proteomics of Porphyromonas gingivalis within a model oral microbial community. BMC Microbiol 2009; 9: 98.
51. Hendrickson EL, Wang T, Dickinson BC, Whitmore SE, Wright CJ, Lamont RJ, et al. Proteomics of Streptococcus gordonii within a model developing oral microbial community. BMC Microbiol 2012; 12: 211.
52. Masuda T, Murakami Y, Noguchi T, Yoshimura F. Effects of various growth conditions in a chemostat on expression of virulence factors in Porphyromonas gingivalis. Appl Environ Microbiol 2006; 72: 3458-67.
53. Litwin CM, Calderwood SB. Role of iron in regulation of virulence genes. Clin Microbiol Rev 1993; 6: 137-49. 54. Wang R, Kaplan A, Guo L, Shi W, Zhou X, Lux R, et al. The influence of iron availability on human salivary microbial community composition. Microb Ecol 2012; 64: 152-61.
54. Wang R, Kaplan A, Guo L, Shi W, Zhou X, Lux R, et al. The influence of iron availability on human salivary microbial community composition. Microb Ecol 2012; 64: 152-61.
55. Zainal-Abidin Z, Veith PD, Dashper SG, Zhu Y, Catmull DV, Chen YY, et al. Differential proteomic analysis of a polymicrobial biofilm. J Proteome Res 2012; 11: 4449-64. 56. Lewis JP. Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms. Periodontology 2000 2010; 52: 94-116.
56. Lewis JP. Metal uptake in host-pathogen interactions: role of iron in Porphyromonas gingivalis interactions with host organisms. Periodontology 2000 2010; 52: 94-116.
57. Olczak T, Simpson W, Liu X, Genco CA. Iron and heme utilization in Porphyromonas gingivalis. FEMS Microbiol Rev 2005; 29: 119-44.
58. Berlutti F, Ajello M, Bosso P, Morea C, Petrucca A, Antonini G, et al. Both lactoferrin and iron influence aggregation and biofilm formation in Streptococcus mutans. Biometals 2004; 17: 271-8.
59. Dashper SG, Pan Y, Veith PD, Chen YY, Toh EC, Liu SW, et al. Lactoferrin inhibits Porphyromonas gingivalis proteinases and has sustained biofilm inhibitory activity. Antimicrobial Agents Chemother 2012; 56: 1548-56.
60. Baumgartner S, Imfeld T, Schicht O, Rath C, Persson RE, Persson GR. The impact of the stone age diet on gingival conditions in the absence of oral hygiene. J Periodontol 2009; 80: 759-68.
61. Adegboye AR, Twetman S, Christensen LB, Heitmann BL. Intake of dairy calcium and tooth loss among adult Danish men and women. Nutrition 2012; 28: 779-84.
62. Laine ML, Crielaard W. Functional foods/ingredients and periodontal diseases. Eur J Nutr 2012; 51(Suppl 2): S27-30.
63. Hosokawa Y, Hosokawa I, Ozaki K, Nakanishi T, Nakae H, Matsuo T. Catechins inhibit CCL20 production in IL-17Astimulated human gingival fibroblasts. Cell Physiol Biochem 2009; 24: 391-6.
64. Hosokawa Y, Hosokawa I, Ozaki K, Nakanishi T, Nakae H, Matsuo T. Catechins inhibit CXCL10 production from oncostatin M-stimulated human gingival fibroblasts. J Nutr Biochem 2010; 21: 659-64.
65. Kushiyama M, Shimazaki Y, Murakami M, Yamashita Y. Relationship between intake of green tea and periodontal disease. J Periodontol 2009; 80: 372-7.
66. Bodet C, Grenier D, Chandad F, Ofek I, Steinberg D,Weiss EI. Potential oral health benefits of cranberry. Crit Rev Food Sci Nutr 2008; 48: 672-80.
67. Petti S, Scully C. Polyphenols, oral health and disease: A review. J Dent 2009; 37: 413-23.
68. Rizzo A, Bevilacqua N, Guida L, Annunziata M, Romano Carratelli C, Paolillo R. Effect of resveratrol and modulation of cytokine production on human periodontal ligament cells. Cytokine 2012; 60: 197-204.
69. Gonzalez OA, Escamilla C, Danaher RJ, Dai J, Ebersole JL, Mumper RJ, et al. Antibacterial effects of blackberry extract target periodontopathogens. J Periodontal Res 2012; 48: 80-6.
70. Breitbart M. Marine viruses: truth or dare. Ann Rev Mar Sci 2012; 4: 425-48.
71. Breitbart M, Rohwer F. Here a virus, there a virus, everywhere the same virus? Trends Microbiol 2005; 13: 278-84.
72. Rohwer F, Thurber RV. Viruses manipulate the marine environment. Nature 2009; 459: 207-12.
73. Hitch G, Pratten J, Taylor PW. Isolation of bacteriophages from the oral cavity. Lett Appl Microbiol 2004; 39: 215-9.
74. Sandmeier H, van Winkelhoff AJ, Bar K, Ankli E, Maeder M, Meyer J. Temperate bacteriophages are common among Actinobacillus actinomycetemcomitans isolates from periodontal pockets. J Periodontal Res 1995; 30: 418-25.
75. Pride DT, Salzman J, Haynes M, Rohwer F, Davis-Long C, White RA, 3rd, et al. Evidence of a robust resident bacteriophage population revealed through analysis of the human salivary virome. ISME J 2012; 6: 915-26.
76. Roberts AP, Mullany P. Genetic basis of horizontal gene transfer among oral bacteria. Periodontology 2000 2006; 42: 36-46.
77. Pride DT, Salzman J, Relman DA. Comparisons of clustered regularly interspaced short palindromic repeats and viromes in human saliva reveal bacterial adaptations to salivary viruses. Environ Microbiol 2012; 14: 2564-76.
78. Enersen M. Porphyromonas gingivalis: a clonal pathogen?: Diversities in housekeeping genes and the major fimbriae gene. J Oral Microbiol 2011; 3. doi: 10.3402/jom.v3i0.8487.
79. 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.
80. Naito M, Hirakawa H, Yamashita A, Ohara N, Shoji M, Yukitake H, et al. Determination of the genome sequence of Porphyromonas gingivalis strain ATCC 33277 and genomic comparison with strain W83 revealed extensive genome rearrangements in P. gingivalis. DNA Res 2008; 15: 215-25.
81. Tribble GD, Rigney TW, Dao DH, Wong CT, Kerr JE, Taylor BE, et al. Natural competence is a major mechanism for horizontal DNA transfer in the oral pathogen Porphyromonas gingivalis. MBio 2012; 3.
82. Slots J. Human viruses in periodontitis. Periodontology 2000 2010; 53: 89-110.
83. Willner D, Furlan M, Haynes M, Schmieder R, Angly FE, Silva J, et al. Metagenomic analysis of respiratory tract DNA viral communities in cystic fibrosis and non-cystic fibrosis individuals. PLoS ONE 2009; 4: e7370.
84. Klepac-Ceraj V, Lemon KP, Martin TR, Allgaier M, Kembel SW, Knapp AA, et al. Relationship between cystic fibrosis respiratory tract bacterial communities and age, genotype, antibiotics and Pseudomonas aeruginosa. Environ Microbiol 2010; 12: 1293-303.
85. Blainey PC, Milla CE, Cornfield DN, Quake SR. Quantitative analysis of the human airway microbial ecology reveals a pervasive signature for cystic fibrosis. Sci Transl Med 2012; 4: 153ra30.
86. Barrangou R, Fremaux C, Deveau H, Richards M, Boyaval P, Moineau S, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315: 1709-12.
87. Bhaya D, Davison M, Barrangou R. CRISPR-Cas systems in bacteria and archaea: versatile small RNAs for adaptive defense and regulation. Annu Rev Genet 2011; 45: 273-97.
88. Stern A, Mick E, Tirosh I, Sagy O, Sorek R. CRISPR targeting reveals a reservoir of common phages associated with the human gut microbiome. Genome Res 2012; 22: 1985-94. doi: 10.1101/gr.138297.112. Epub 2012 Jun 25.
89. Pride DT, Sun CL, Salzman J, Rao N, Loomer P, Armitage GC, et al. Analysis of streptococcal CRISPRs from human saliva reveals substantial sequence diversity within and between subjects over time. Genome Res 2011; 21: 126-36.
90. van der Ploeg JR. Analysis of CRISPR in Streptococcus mutans suggests frequent occurrence of acquired immunity against infection by M102-like bacteriophages. Microbiology 2009; 155: 1966-76.
91. Rho M, Wu YW, Tang H, Doak TG, Ye Y. Diverse CRISPRs evolving in human microbiomes. PLoS Genet 2012; 8: e1002441.
92. Visser MB, Ellen RP. New insights into the emerging role of oral spirochaetes in periodontal disease. Clin Microbiol Infect 2011; 17: 502-12.
93. Davey ME, O'Toole GA. Microbial biofilms: from ecology to molecular genetics. Microbiol Mol Biol Rev 2000; 64: 847-67.
94. Hibbing ME, Fuqua C, Parsek MR, Peterson SB. Bacterial competition: surviving and thriving in the microbial jungle. Nat Rev Microbiol 2010; 8: 15-25.
95. Stoodley P, Sauer K, Davies DG, Costerton JW. Biofilms as complex differentiated communities. Annu Rev Microbiol 2002; 56: 187-209.
96. Medzhitov R, Schneider DS, Soares MP. Disease tolerance as a defense strategy. Science 2012; 335: 936-41.
97. Schreiber RD, Old LJ, Smyth MJ. Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 2011; 331: 1565-70.
98. Motz GT, Coukos G. The parallel lives of angiogenesis and immunosuppression: cancer and other tales. Nat Rev Immunol 2011; 11: 702-11.
99. Dvorak HF. Tumors: wounds that do not heal. Similarities between tumor stroma generation and wound healing. N Engl J Med 1986; 315: 1650-9.
100. Fine DH, Markowitz K, Furgang D, Fairlie K, Ferrandiz J, Nasri C, et al. Macrophage inflammatory protein-1alpha: a salivary biomarker of bone loss in a longitudinal cohort study of children at risk for aggressive periodontal disease? J Periodontol 2009; 80: 106-13.
101. Page RC, Engel LD, Narayanan AS, Clagett JA. Chronic inflammatory gingival and periodontal disease. JAMA 1978; 240: 545-50.
102. Abe N, Kadowaki T, Okamoto K, Nakayama K, Ohishi M, Yamamoto K. Biochemical and functional properties of lysinespecific cysteine proteinase (Lys-gingipain) as a virulence factor of Porphyromonas gingivalis in periodontal disease. J Biochem 1998; 123: 305-12.
103. Guzik K, Bzowska M, Smagur J, Krupa O, Sieprawska M, Travis J, et al. A new insight into phagocytosis of apoptotic cells: proteolytic enzymes divert the recognition and clearance of polymorphonuclear leukocytes by macrophages. Cell Death Differ 2007; 14: 171-82.
104. Guzik K, Potempa J. Friendly fire against neutrophils: proteolytic enzymes confuse the recognition of apoptotic cells by macrophages. Biochimie 2008; 90: 405-15.
105. Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, et al. HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 2010; 207: 2439-53.
106. McGaha TL, Huang L, Lemos H, Metz R, Mautino M, Prendergast GC, et al. Amino acid catabolism: a pivotal regulator of innate and adaptive immunity. Immunol Rev 2012; 249: 135-57.
107. Yang B, Wang X, Ren X. Amino acid metabolism related to immune tolerance by MDSCs. Int Rev Immunol 2012; 31: 177-83.
108. Chapple IL. Reactive oxygen species and antioxidants in inflammatory diseases. J Clin Periodontol 1997; 24: 287-96.
109. Daghigh F, Borghaei RC, Thornton RD, Bee JH. Human gingival fibroblasts produce nitric oxide in response to proinflammatory cytokines. J Periodontol 2002; 73: 392-400.
110. Mahanonda R, Sa-Ard-Iam N, Montreekachon P, Pimkhaokham A, Yongvanichit K, Fukuda MM, et al. IL-8 and IDO expression by human gingival fibroblasts via TLRs. J Immunol 2007; 178: 1151-7.
111. Costerton W, Veeh R, Shirtliff M, Pasmore M, Post C, Ehrlich G. The application of biofilm science to the study and control of chronic bacterial infections. J Clin Invest 2003; 112: 1466-77.
112. Gaddis DE, Michalek SM, Katz J. TLR4 signaling via MyD88 and TRIF differentially shape the CD4- T cell response to Porphyromonas gingivalis hemagglutinin B. J Immunol 2011; 186: 5772-83.
113. Myneni SR, Settem RP, Connell TD, Keegan AD, Gaffen SL, Sharma A. TLR2 signaling and Th2 responses drive Tannerella forsythia-induced periodontal bone loss. J Immunol 2011; 187: 501-9.
114. Lambert G, Estevez-Salmeron L, Oh S, Liao D, Emerson BM, Tlsty TD, et al. An analogy between the evolution of drug resistance in bacterial communities and malignant tissues. Nat Rev Cancer 2011; 11: 375-82.
115. Amaral L, Engi H, Viveiros M, Molnar J. Review. Comparison of multidrug resistant efflux pumps of cancer and bacterial cells with respect to the same inhibitory agents. In Vivo 2007; 21: 237-44.
116. Kvist M, Hancock V, Klemm P. Inactivation of efflux pumps abolishes bacterial biofilm formation. Appl Envroment Microbiol 2008; 74: 7376-82.
117. Rohwer N, Cramer T. Hypoxia-mediated drug resistance: novel insights on the functional interaction of HIFs and cell death pathways. Drug Resist Updat 2011; 14: 191-201.
118. Mah TF, Pitts B, Pellock B, Walker GC, Stewart PS, O'Toole GA. A genetic basis for Pseudomonas aeruginosa biofilm antibiotic resistance. Nature 2003; 426: 306-10.
119. Schaible B, Taylor CT, Schaffer K. Hypoxia increases antibiotic resistance in Pseudomonas aeruginosa through altering the composition of multidrug efflux pumps. Antimicrob Agents Chemother 2012; 56: 2114-8.
120. Quesnel B. Dormant tumor cells as a therapeutic target? Cancer Lett 2008; 267: 10-7.
121. Lewis K. Persister cells. Annu Rev Microbiol 2010; 64: 357-72.
122. Drisko CH. Nonsurgical periodontal therapy. Periodontology 2000 2001; 25: 77-88.
123. Cobb CM. Microbes, inflammation, scaling and root planing, and the periodontal condition. J Dent Hyg 2008; 82(Suppl 3): 4-9.
124. Rossi DJ, Jamieson CH, Weissman IL. Stems cells and the pathways to aging and cancer. Cell 2008; 132: 681-96.
125. Mellman I, Coukos G, Dranoff G. Cancer immunotherapy comes of age. Nature 2011; 480: 480-9.
126. Pardoll D, Drake C. Immunotherapy earns its spot in the ranks of cancer therapy. J Exp Med 2012; 209: 201-9.
127. Drake CG, Antonarakis ES. Current status of immunological approaches for the treatment of prostate cancer. Curr Opin Urol 2012; 22: 197-202.