The inflammophilic character of the periodontitis-associated microbiota

Molecular Oral Microbiology

Volumn 29, Issue 6, 2014, Pages 248-257

  Hajishengallis, G ^a  

^a UNIVERSITY OF PENNSYLVANIA SCHOOL OF DENTAL MEDICINE   (United States)

Author keywords

P. gingivalis; Dysbiosis; Inflammation; Periodontitis; Toll like receptors

Indexed keywords

ANTIINFLAMMATORY AGENT; COLLAGEN; HEME; PEPTIDE;

ARTICLE; BACTERIAL LOAD; BIOFILM; DISEASE ASSOCIATION; DISEASE COURSE; DYSBIOSIS; ECOLOGY; HOST; HUMAN; INFLAMMATION; INFLAMMOPHILIC; MICROBIAL BIOMASS; MICROBIAL COMMUNITY; MICROBIAL GROWTH; MICROFLORA; NONHUMAN; NUTRIENT; OSTEOLYSIS; PATHOGENESIS; PERIODONTAL DISEASE; PERIODONTITIS; ALVEOLAR BONE LOSS; ANIMAL; DISEASE MODEL; HOST PATHOGEN INTERACTION; IMMUNOLOGY; MICROBIOLOGY; PORPHYROMONAS GINGIVALIS;

ALVEOLAR BONE LOSS; ANIMALS; ANTI-INFLAMMATORY AGENTS; BACTERIAL LOAD; BIOFILMS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DYSBIOSIS; HOST-PATHOGEN INTERACTIONS; HUMANS; INFLAMMATION; MICROBIOTA; PERIODONTITIS; PORPHYROMONAS GINGIVALIS;

EID: 84911397225     PISSN: 20411006     EISSN: 20411014     Source Type: Journal    
DOI: 10.1111/omi.12065     Document Type: Article

References (75)

1. Abe, T., Hosur, K.B., Hajishengallis, E. et al. (2012) Local complement-targeted intervention in periodontitis: proof-of-concept using a C5a receptor (CD88) antagonist. J Immunol 189: 5442-5448.
2. Abusleme, L., Dupuy, A.K., Dutzan, N. et al. (2013) The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. ISME J 7: 1016-1025.
3. Armitage, G.C. (2002) Classifying periodontal diseases - a long-standing dilemma. Periodontol 2000 30: 9-23.
4. Assuma, R., Oates, T., Cochran, D., Amar, S. and Graves, D.T. (1998) IL-1 and TNF antagonists inhibit the inflammatory response and bone loss in experimental periodontitis. J Immunol 160: 403-409.
5. Baker, P.J., Carter, S., Dixon, M., Evans, R.T. and Roopenian, D.C. (1999) Serum antibody response to oral infection precedes but does not prevent Porphyromonas gingivalis-induced alveolar bone loss in mice. Oral Microbiol Immunol 14: 194-196.
6. Belibasakis, G.N., Bao, K. and Bostanci, N. (2014) Transcriptional profiling of human gingival fibroblasts in response to multi-species in vitro subgingival biofilms. Mol Oral Microbiol 29: 174-183. Doi: 10.1111/omi.12053. [Epub ahead of print].
7. Bostanci, N. and Belibasakis, G.N. (2012) Porphyromonas gingivalis: an invasive and evasive opportunistic oral pathogen. FEMS Microbiol Lett 333: 1-9.
8. Bostanci, N., Saygan, B., Emingil, G., Atilla, G. and Belibasakis, G.N. (2011) Effect of periodontal treatment on receptor activator of NF-κB ligand and osteoprotegerin levels and relative ratio in gingival crevicular fluid. J Clin Periodontol 38: 428-433.
9. Brecx, M.C., Nalbandian, J., Ooya, K., Kornman, K.S. and Robertson, P.B. (1985) Morphological studies on periodontal disease in the cynomolgus monkey. II. Light microscopic observations on ligature-induced periodontitis. J Periodontal Res 20: 165-175.
10. Chaves, E.S., Jeffcoat, M.K., Ryerson, C.C. and Snyder, B. (2000) Persistent bacterial colonization of Porphyromonas gingivalis, Prevotella intermedia, and Actinobacillus actinomycetemcomitans in periodontitis and its association with alveolar bone loss after 6 months of therapy. J Clin Periodontol 27: 897-903.
11. Colombo, A.P., Bennet, S., Cotton, S.L. et al. (2012) Impact of periodontal therapy on the subgingival microbiota of severe periodontitis: comparison between good responders and individuals with refractory periodontitis using the human oral microbe identification microarray. J Periodontol 83: 1279-1287.
12. Curtis, M.A., Zenobia, C. and Darveau, R.P. (2011) The relationship of the oral microbiotia to periodontal health and disease. Cell Host Microbe 10: 302-306.
13. Darveau, R.P. (2010) Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 8: 481-490.
14. Darveau, R.P., Hajishengallis, G. and Curtis, M.A. (2012) Porphyromonas gingivalis as a potential community activist for disease. J Dent Res 91: 816-820.
15. Dewhirst, F.E., Chen, T., Izard, J. et al. (2010) The human oral microbiome. J Bacteriol 192: 5002-5017.
16. Divaris, K., Monda, K.L., North, K.E. et al. (2013) Exploring the genetic basis of chronic periodontitis: a genome-wide association study. Hum Mol Genet 22: 2312-2324.
17. Doungudomdacha, S., Rawlinson, A. and Douglas, C.W. (2000) Enumeration of Porphyromonas gingivalis, Prevotella intermedia and Actinobacillus actinomycetemcomitans in subgingival plaque samples by a quantitative-competitive PCR method. J Med Microbiol 49: 861-874.
18. Duran-Pinedo, A.E., Chen, T., Teles, R. et al. (2014) Community-wide transcriptome of the oral microbiome in subjects with and without periodontitis. ISME J 8: 1659-1672. Mar 6 [Epub ahead of print].
19. Eskan, M.A., Jotwani, R., Abe, T. et al. (2012) The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat Immunol 13: 465-473.
20. Graves, D. (2008) Cytokines that promote periodontal tissue destruction. J Periodontol 79: 1585-1591.
21. Graves, D.T., Fine, D., Teng, Y.T., Van Dyke, T.E. and Hajishengallis, G. (2008) The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol 35: 89-105.
22. Griffen, A.L., Beall, C.J., Firestone, N.D. et al. (2011) CORE: a phylogenetically-curated 16S rDNA database of the core oral microbiome. PLoS ONE 6: e19051.
23. Griffen, A.L., Beall, C.J., Campbell, J.H. et al. (2012) Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. ISME J 6: 1176-1185.
24. Haffajee, A.D., Cugini, M.A., Tanner, A. et al. (1998) Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 25: 346-353.
25. Hajishengallis, G. (2014a) Aging and its impact on innate immunity and inflammation: implications for periodontitis. J Oral Biosci 56: 30-37.
26. Hajishengallis, G. (2014b) Immunomicrobial pathogenesis of periodontitis: keystones, pathobionts, and host response. Trends Immunol 35: 3-11.
27. Hajishengallis, G. and Lambris, J.D. (2011) Microbial manipulation of receptor crosstalk in innate immunity. Nat Rev Immunol 11: 187-200.
28. Hajishengallis, G. and Lamont, R.J. (2012) Beyond the red complex and into more complexity: the Polymicrobial Synergy and Dysbiosis (PSD) model of periodontal disease etiology. Mol Oral Microbiol 27: 409-419.
29. Hajishengallis, G. and Lamont, R.J. (2014) Breaking bad: manipulation of the host response by Porphyromonas gingivalis. Eur J Immunol 44: 328-338.
30. Hajishengallis, G., Liang, S., Payne, M.A. et al. (2011) Low-abundance biofilm species orchestrates inflammatory periodontal disease through the commensal microbiota and complement. Cell Host Microbe 10: 497-506.
31. Hajishengallis, G., Darveau, R.P. and Curtis, M.A. (2012) The keystone-pathogen hypothesis. Nat Rev Microbiol 10: 717-725.
32. Hasturk, H., Kantarci, A., Goguet-Surmenian, E. et al. (2007) Resolvin E1 regulates inflammation at the cellular and tissue level and restores tissue homeostasis in vivo. J Immunol 179: 7021-7029.
33. Hasturk, H., Kantarci, A. and Van Dyke, T.E. (2012) Paradigm shift in the pharmacological management of periodontal diseases. Front Oral Biol 15: 160-176.
34. Holt, S.C., Ebersole, J., Felton, J., Brunsvold, M. and Kornman, K.S. (1988) Implantation of Bacteroides gingivalis in nonhuman primates initiates progression of periodontitis. Science 239: 55-57.
35. Jiao, Y., Darzi, Y., Tawaratsumida, K. et al. (2013) Induction of bone loss by pathobiont-mediated nod1 signaling in the oral cavity. Cell Host Microbe 13: 595-601.
36. Jorth, P., Turner, K.H., Gumus, P., Nizam, N., Buduneli, N. and Whiteley, M. (2014) Metatranscriptomics of the human oral microbiome during health and disease. MBio 5: e01012-e01014.
37. Jusko, M., Potempa, J., Karim, A.Y. et al. (2012) A metalloproteinase karilysin present in the majority of Tannerella forsythia isolates inhibits all pathways of the complement system. J Immunol 188: 2338-2349.
38. Kesavalu, L., Sathishkumar, S., Bakthavatchalu, V. et al. (2007) Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect Immun 75: 1704-1712.
39. Kinane, D.F. and Hart, T.C. (2003) Genes and gene polymorphisms associated with periodontal disease. Crit Rev Oral Biol Med 14: 430-449.
40. Kinane, D.F., Demuth, D.R., Gorr, S.U., Hajishengallis, G.N. and Martin, M.H. (2007) Human variability in innate immunity. Periodontol 2000 45: 14-34.
41. Kirkwood, K.L., Cirelli, J.A., Rogers, J.E. and Giannobile, W.V. (2007) Novel host response therapeutic approaches to treat periodontal diseases. Periodontol 2000 43: 294-315.
42. Kornman, K.S., Holt, S.C. and Robertson, P.B. (1981) The microbiology of ligature-induced periodontitis in the cynomolgus monkey. J Periodontal Res 16: 363-371.
43. Krauss, J.L., Potempa, J., Lambris, J.D. and Hajishengallis, G. (2010) Complementary Tolls in the periodontium: how periodontal bacteria modify complement and Toll-like receptor responses to prevail in the host. Periodontol 2000 52: 141-162.
44. Kumar, P.S., Leys, E.J., Bryk, J.M., Martinez, F.J., Moeschberger, M.L. and Griffen, A.L. (2006) Changes in periodontal health status are associated with bacterial community shifts as assessed by quantitative 16S cloning and sequencing. J Clin Microbiol 44: 3665-3673.
45. Laine, M.L., Crielaard, W. and Loos, B.G. (2012) Genetic susceptibility to periodontitis. Periodontol 2000 58: 37-68.
46. Liang, S., Krauss, J.L., Domon, H. et al. (2011) The C5a receptor impairs IL-12-dependent clearance of Porphyromonas gingivalis and is required for induction of periodontal bone loss. J Immunol 186: 869-877.
47. Lindroth, A.M. and Park, Y.J. (2013) Epigenetic biomarkers: a step forward for understanding periodontitis. J Periodontal Implant Sci 43: 111-120.
48. Maekawa, T. and Hajishengallis, G. (2014) Topical treatment with probiotic Lactobacillus brevis CD2 inhibits experimental periodontal inflammation and bone loss. J Periodontal Res. doi: 10.1111/jre.12164 [Epub ahead of print].
49. Maekawa, T., Abe, T., Hajishengallis, E. et al. (2014a) Genetic and intervention studies implicating complement C3 as a major target for the treatment of periodontitis. J Immunol 192: 6020-6027. doi:10.4049/jimmunol.1400569.
50. Maekawa, T., Krauss, J.L., Abe, T. et al. (2014b) Porphyromonas gingivalis manipulates complement and TLR signaling to uncouple bacterial clearance from inflammation and promote dysbiosis. Cell Host Microbe 15: 768-778.
51. Marsh, P.D. (2003) Are dental diseases examples of ecological catastrophes? Microbiology 149: 279-294.
52. Miller, D.P., Bell, J.K., McDowell, J.V. et al. (2012) Structure of factor H-binding protein B (FhbB) of the periopathogen, Treponema denticola: insights into progression of periodontal disease. J Biol Chem 287: 12715-12722.
53. Moore, W.E., Holdeman, L.V., Smibert, R.M., Hash, D.E., Burmeister, J.A. and Ranney, R.R. (1982) Bacteriology of severe periodontitis in young adult humans. Infect Immun 38: 1137-1148.
54. Moore, W.E., Moore, L.H., Ranney, R.R., Smibert, R.M., Burmeister, J.A. and Schenkein, H.A. (1991) The microflora of periodontal sites showing active destructive progression. J Clin Periodontol 18: 729-739.
55. Moutsopoulos, N.M., Konkel, J., Sarmadi, M. et al. (2014) Defective neutrophil recruitment in leukocyte adhesion deficiency type I disease causes local IL-17-driven inflammatory bone loss. Sci Transl Med 6: 229ra240.
56. Orth, R.K., O'Brien-Simpson, N.M., Dashper, S.G. and Reynolds, E.C. (2011) Synergistic virulence of Porphyromonas gingivalis and Treponema denticola in a murine periodontitis model. Mol Oral Microbiol 26: 229-240.
57. Page, R.C. and Schroeder, H.E. (1982) Periodontitis in Man and Other Animals - A Comparative Review. Basel, Switzerland: Karger.
58. Page, R.C., Lantz, M.S., Darveau, R. et al. (2007) Immunization of Macaca fascicularis against experimental periodontitis using a vaccine containing cysteine proteases purified from Porphyromonas gingivalis. Oral Microbiol Immunol 22: 162-168.
59. Polak, D., Wilensky, A., Shapira, L. et al. (2009) Mouse model of experimental periodontitis induced by P. gingivalis/F. nucleatum infection: bone loss and host response. J Clin Periodontol 36: 406-410.
60. Popadiak, K., Potempa, J., Riesbeck, K. and Blom, A.M. (2007) Biphasic effect of gingipains from Porphyromonas gingivalis on the human complement system. J Immunol 178: 7242-7250.
61. Potempa, J. and Pike, R.N. (2009) Corruption of innate immunity by bacterial proteases. J Innate Immun 1: 70-87.
62. Ramsey, M.M., Rumbaugh, K.P. and Whiteley, M. (2011) Metabolite cross-feeding enhances virulence in a model polymicrobial infection. PLoS Pathog 7: e1002012.
63. Ricklin, D., Hajishengallis, G., Yang, K. and Lambris, J.D. (2010) Complement: a key system for immune surveillance and homeostasis. Nat Immunol 11: 785-797.
64. Settem, R.P., El-Hassan, A.T., Honma, K., Stafford, G.P. and Sharma, A. (2012) Fusobacterium nucleatum and Tannerella forsythia induce synergistic alveolar bone loss in a mouse periodontitis model. Infect Immun 80: 2436-2443.
65. Socransky, S.S. and Haffajee, A.D. (1994) Evidence of bacterial etiology: a historical perspective. Periodontol 2000 5: 7-25.
66. Stabholz, A., Soskolne, W.A. and Shapira, L. (2010) Genetic and environmental risk factors for chronic periodontitis and aggressive periodontitis. Periodontol 2000 53: 138-153.
67. Takeuchi, H., Hirano, T., Whitmore, S.E., Morisaki, I., Amano, A. and Lamont, R.J. (2013) The serine phosphatase SerB of Porphyromonas gingivalis suppresses IL-8 production by dephosphorylation of NF-κB RelA/p65. PLoS Pathog 9: e1003326.
68. Tan, K.H., Seers, C.A., Dashper, S.G. et al. (2014) Porphyromonas gingivalis and Treponema denticola exhibit metabolic symbioses. PLoS Pathog 10: e1003955.
69. Tanner, A.C., Kent, R. Jr and Kanasi, E. (2007) Clinical characteristics and microbiota of progressing slight chronic periodontitis in adults. J Clin Periodontol 34: 917-930.
70. Venketaraman, V., Lin, A.K., Le, A., Kachlany, S.C., Connell, N.D. and Kaplan, J.B. (2008) Both leukotoxin and poly-N-acetylglucosamine surface polysaccharide protect Aggregatibacter actinomycetemcomitans cells from macrophage killing. Microb Pathog 45: 173-180.
71. Wang, M., Krauss, J.L., Domon, H. et al. (2010) Microbial hijacking of complement-toll-like receptor crosstalk. Sci Signal 3: ra11.
72. Wingrove, J.A., DiScipio, R.G., Chen, Z., Potempa, J., Travis, J. and Hugli, T.E. (1992) Activation of complement components C3 and C5 by a cysteine proteinase (gingipain-1) from Porphyromonas (Bacteroides) gingivalis. J Biol Chem 267: 18902-18907.
73. Yilmaz, O. (2008) The chronicles of Porphyromonas gingivalis: the microbium, the human oral epithelium and their interplay. Microbiology 154: 2897-2903.
74. Zenobia, C., Hasturk, H., Nguyen, D., Van Dyke, T.E., Kantarci, A. and Darveau, R.P. (2014) Porphyromonas gingivalis lipid A phosphatase activity is critical for colonization and increasing the commensal load in the rabbit ligature model. Infect Immun 82: 650-659.
75. Zhou, Q., Leeman, S.E. and Amar, S. (2011) Signaling mechanisms in the restoration of impaired immune function due to diet-induced obesity. Proc Natl Acad Sci USA 108: 2867-2872.