Periodontitis induced by Porphyromonas gingivalis drives periodontal microbiota dysbiosis and insulin resistance via an impaired adaptive immune response

Gut

Volumn 66, Issue 5, 2016, Pages 872-885

  Blasco Baque, Vincent ^a,b,c,d   Garidou, Lucile ^a,b,c   Pomié, Céline ^a,b,c   Escoula, Quentin ^a,b,c   Loubieres, Pascale ^a,b,c,d   Le Gall David, Sandrine ^e   Lemaitre, Mathieu ^d   Nicolas, Simon ^a,b,c   Klopp, Pascale ^a,b,c   Waget, Aurélie ^a,b,c   Azalbert, Vincent ^a,b,c   Colom, André ^a,b,c   Bonnaure Mallet, Martine ^e   Kemoun, Philippe ^d   Serino, Matteo ^a,b,c   Burcelin, Rémy ^a,b,c  

^a CHU RANGUEIL   (France)

^b University Hospital of Toulouse   (France)

^c UNIVERSITÉ PAUL SABATIER   (France)

^d UNIVERSITÉ DE TOULOUSE   (France)

^e UNIVERSITÉ DE RENNES 1   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTIVE IMMUNITY; ADOPTIVE TRANSFER; ALVEOLAR BONE LOSS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DYSBIOSIS; FEMALE; FUSOBACTERIUM NUCLEATUM; GLUCOSE METABOLISM; HYPERGLYCEMIA; IMMUNOCOMPETENT CELL; INSULIN RESISTANCE; MOUSE; NONHUMAN; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PREVOTELLA INTERMEDIA; PRIORITY JOURNAL; ANIMAL; BACTEROIDACEAE INFECTION; BLOOD; C57BL MOUSE; CELL TRANSPLANTATION; COMPLICATION; CYTOLOGY; DISEASE MODEL; GINGIVA; IMMUNOLOGY; LIPID DIET; LYMPH NODE; LYMPHOCYTE; MICROBIOLOGY; MICROFLORA; PATHOLOGY; RANDOMIZATION; SPLEEN; VACCINATION;

GAMMA INTERFERON; INTERLEUKIN 6; LIPOPOLYSACCHARIDE;

ADAPTIVE IMMUNITY; ANIMALS; BACTEROIDACEAE INFECTIONS; CELL TRANSPLANTATION; DIET, HIGH-FAT; DISEASE MODELS, ANIMAL; DYSBIOSIS; FEMALE; GINGIVA; HYPERGLYCEMIA; INSULIN RESISTANCE; INTERFERON-GAMMA; INTERLEUKIN-6; LIPOPOLYSACCHARIDES; LYMPH NODES; LYMPHOCYTES; MICE; MICE, INBRED C57BL; MICROBIOTA; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RANDOM ALLOCATION; SPLEEN; VACCINATION;

EID: 84958595584     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2015-309897     Document Type: Article

References (50)

1. Kolb H, Eizirik DL. Resistance to type 2 diabetes mellitus: a matter of hormesis? Nat Rev Endocrinol 2012;8:183-92.
2. Albandar JM, Rams TE. Global epidemiology of periodontal diseases: an overview. Periodontol 2000 2002;29:7-10.
3. D'Aiuto F, Sabbah W, Netuveli G, et al. Association of the metabolic syndrome with severe periodontitis in a large US population-based survey. J Clin Endocrinol Metab 2008;93:3989-94.
4. Vergnes JN. Treating periodontal disease may improve metabolic control in diabetics. Evid Based Dent 2010;11:73-4.
5. Borrell LN, Kunzel C, Lamster I, et al. Diabetes in the dental office: using NHANES III to estimate the probability of undiagnosed disease. J Periodontal Res 2007;42:559-65.
6. Serino M, Blasco-Baque V, Nicolas S, et al. Far from the eyes, close to the heart: dysbiosis of gut microbiota and cardiovascular consequences. Curr Cardiol Rep 2014;16:540.
7. Ley RE, Bäckhed F, Turnbaugh P, et al. Obesity alters gut microbial ecology. Proc Natl Acad Sci USA 2005;102:11070-5.
8. Serino M, Fernández-Real JM, García-Fuentes E, et al. The gut microbiota profile is associated with insulin action in humans. Acta Diabetol 2013;50:753-61.
9. Preshaw PM, Alba AL, Herrera D, et al. Periodontitis and diabetes: a two-way relationship. Diabetologia 2012;55:21-31.
10. Cani PD, Amar J, Iglesias MA, et al. Metabolic endotoxemia initiates obesity and insulin resistance. Diabetes 2007;56:1761-72.
11. Amar J, Burcelin R, Ruidavets JB, et al. Energy intake is associated with endotoxemia in apparently healthy men. Am J Clin Nutr 2008;87:1219-23.
12. Lakhssassi N, Elhajoui N, Lodter JP, et al. Antimicrobial susceptibility variation of 50 anaerobic periopathogens in aggressive periodontitis: an interindividual variability study. Oral Microbiol Immunol 2005;20:244-52.
13. Blasco-Baque V, Kémoun P, Loubieres P, et al. Impact of periodontal disease on arterial pressure in diabetic mice. Ann Cardiol Angeiol (Paris) 2012;61:173-7.
14. Koren O, Spor A, Felin J, et al. Human oral, gut, and plaque microbiota in patients with atherosclerosis. Proc Natl Acad Sci USA 2011;108(Suppl 1):4592-8.
15. Rodrigues PH, Reyes L, Chadda AS, et al. Porphyromonas gingivalis strain specific interactions with human coronary artery endothelial cells: a comparative study. PLoS ONE 2012;7(12):e52606.
16. Reichert S, Haffner M, Keyßer G, et al. Detection of oral bacterial DNA in synovial fluid. J Clin Periodontol 2013;40:591-8. .
17. Michaud DS, Izard J, Wilhelm-Benartzi CS, et al. Plasma antibodies to oral bacteria and risk of pancreatic cancer in a large European prospective cohort study. Gut 2013;62:1764-70.
18. Furusho H, Miyauchi M, Hyogo H, et al. Dental infection of Porphyromonas gingivalis exacerbates high fat diet-induced steatohepatitis in mice. J Gastroenterol 2013;48:1259-70.
19. Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006;444:860-7.
20. Nicholson JK, Holmes E, Kinross J, et al. Host-gut microbiota metabolic interactions. Science 2012;336:1262-7.
21. Burcelin R, Garidou L, Pomié C. Immuno-microbiota cross and talk: the new paradigm of metabolic diseases. Semin Immunol 2012;24:67-74.
22. Blasco-Baque V, Serino M, Vergnes JN, et al. High-fat diet induces periodontitis in mice through lipopolysaccharides (LPS) receptor signaling: protective action of estrogens. PLoS ONE 2012;7:e48220.
23. Cani PD, Delzenne NM, Amar J, et al. Role of gut microflora in the development of obesity and insulin resistance following high-fat diet feeding. Pathol Biol (Paris) 2008;56:305-9.
24. Serino M, Luche E, Gres S, et al. Metabolic adaptation to a high-fat diet is associated with a change in the gut microbiota. Gut 2012;61:543-53.
25. Segata N, Izard J, Waldron L, et al. Metagenomic biomarker discovery and explanation. Genome Biol 2011;12:R60.
26. Wade-Gueye NM, Boudiffa M, Laroche N, et al. Mice lacking bone sialoprotein (BSP) lose bone after ovariectomy and display skeletal site-specific response to intermittent PTH treatment. Endocrinology 2010;151:5103-13.
27. Wilensky A, Gabet Y, Yumoto H, et al. Three-dimensional quantification of alveolar bone loss in Porphyromonas gingivalis-infected mice using micro-computed tomography. J Periodontol 2005;76:1282-6.
28. Serino M, Waget A, Marsollier N, et al. Lipid-induced peroxidation in the intestine is involved in glucose homeostasis imbalance in mice. PLoS ONE 2011;6:e21184.
29. Hitchon CA, Chandad F, Ferucci ED, et al. Antibodies to porphyromonas gingivalis are associated with anticitrullinated protein antibodies in patients with rheumatoid arthritis and their relatives. J Rheumatol 2010;37:1105-12.
30. Caraux G, Pinloche S. PermutMatrix: a graphical environment to arrange gene expression profiles in optimal linear order. Bioinformatics 2005;21:1280-1.
31. Tarkkila L, Kari K, Furuholm J, et al. Periodontal disease-associated micro-organisms in peri-menopausal and post-menopausal women using or not using hormone replacement therapy. A two-year follow-up study. BMC Oral Health 2010;10:10.
32. Saito T, Shimazaki Y. Metabolic disorders related to obesity and periodontal disease. Periodontol 2000 2007;43:254-66.
33. Clais S, Boulet G, Kerstens M, et al. Importance of biofilm formation and dipeptidyl peptidase IV for the pathogenicity of clinical Porphyromonas gingivalis isolates. Pathog Dis 2014;70:408-13.
34. Zhu M, Belkina AC, DeFuria J, et al. B cells promote obesity-associated periodontitis and oral pathogen-associated inflammation. J Leukoc Biol 2014;96:349-57.
35. Amano A, Chen C, Honma K, et al. Genetic characteristics and pathogenic mechanisms of periodontal pathogens. Adv Dent Res 2014;26:15-22.
36. Amano A. Disruption of epithelial barrier and impairment of cellular function by Porphyromonas gingivalis. Front Biosci 2007;12:3965-74.
37. Deleon-Pennell KY, de Castro Brás LE, Lindsey ML. Circulating Porphyromonas gingivalis lipopolysaccharide resets cardiac homeostasis in mice through a matrix metalloproteinase-9-dependent mechanism. Physiol Rep 2013;1:e00079.
38. Wang PL, Ohura K. Porphyromonas gingivalis lipopolysaccharide signaling in gingival fibroblasts-CD14 and Toll-like receptors. Crit Rev Oral Biol Med 2002;13:132-42.
39. Na HS, Lim EJ, Jeong SY, et al. Plasminogen activator inhibitor type 1 expression induced by lipopolysaccharide of Porphyromonas gingivalis in human gingival fibroblast. J Microbiol 2014;52:154-60.
40. Kato H, Taguchi Y, Tominaga K, et al. Porphyromonas gingivalis LPS inhibits osteoblastic differentiation and promotes pro-inflammatory cytokine production in human periodontal ligament stem cells. Arch Oral Biol 2014;59:167-75.
41. Luche E, Cousin B, Garidou L, et al. Metabolic endotoxemia directly increases the proliferation of adipocyte precursors at the onset of metabolic diseases through a CD14-dependent mechanism. Mol Metab 2013;2:281-91.
42. Borrell LN, Papapanou PN. Analytical epidemiology of periodontitis. J Clin Periodontol 2005;32(Suppl 6):132-58.
43. Arimatsu K, Yamada H, Miyazawa H, et al. Oral pathobiont induces systemic inflammation and metabolic changes associated with alteration of gut microbiota. Sci Rep 2014;4:4828.
44. Bostanci N, Thurnheer T, Belibasakis GN. Involvement of the TREM-1/DAP12 pathway in the innate immune responses to Porphyromonas gingivalis. Mol Immunol 2011;49:387-94.
45. Yanagita M, Mori K, Kobayashi R, et al. Immunomodulation of dendritic cells differentiated in the presence of nicotine with lipopolysaccharide from Porphyromonas gingivalis. Eur J Oral Sci 2012;120:408-14.
46. Krämer B, Kebschull M, Nowak M, et al. Role of the NK cell-activating receptor CRACC in periodontitis. Infect Immun 2013;81:690-6.
47. Cheng WC, Hughes FJ, Taams LS. The presence, function and regulation of IL-17 and Th17 cells in periodontitis. J Clin Periodontol 2014;41:541-9.
48. Zelkha SA, Freilich RW, Amar S. Periodontal innate immune mechanisms relevant to atherosclerosis and obesity. Periodontol 2000 2010;54:207-21.
49. de Aquino SG, Abdollahi-Roodsaz S, Koenders MI, et al. Periodontal Pathogens Directly Promote Autoimmune Experimental Arthritis by Inducing a TLR2- and IL-1-Driven Th17 Response. J Immunol 2014;192:4103-11.
50. Hayashi C, Gudino CV, Gibson FC 3rd, et al. Review: Pathogen-induced inflammation at sites distant from oral infection: bacterial persistence and induction of cell-specific innate immune inflammatory pathways. Mol Oral Microbiol 2010;25:305-16.