Oral bacterial DNA differ in their ability to induce inflammatory responses in human monocytic cell lines

Journal of Periodontology

Volumn 83, Issue 8, 2012, Pages 1069-1077

  Sahingur, Sinem Esra ^a   Xia, Xia Juan ^a   Schifferle, Robert E ^b  

^a VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

^b UNIVERSITY AT BUFFALO   (United States)

Author keywords

Cytokines; Fusobacterium nucleatum; Microbiology; Monocytes; Periodontitis; Porphyromonas gingivalis

Indexed keywords

AUTACOID; BACTERIAL DNA; CHLOROQUINE; CYTOKINE; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; LIPOPOLYSACCHARIDE; TLR9 PROTEIN, HUMAN; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR ALPHA;

ARTICLE; CELL LINE; CULTURE TECHNIQUE; DRUG ANTAGONISM; DRUG EFFECT; FUSOBACTERIUM NUCLEATUM; GENETICS; HUMAN; IMMUNOLOGY; MICROBIOLOGY; MONOCYTE; MOUTH; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; STREPTOCOCCUS SANGUINIS;

CELL CULTURE TECHNIQUES; CELL LINE; CHLOROQUINE; CYTOKINES; DNA, BACTERIAL; FUSOBACTERIUM NUCLEATUM; HUMANS; INFLAMMATION MEDIATORS; INTERLEUKIN-1BETA; INTERLEUKIN-6; INTERLEUKIN-8; LIPOPOLYSACCHARIDES; MONOCYTES; MOUTH; PORPHYROMONAS GINGIVALIS; SIGNAL TRANSDUCTION; STREPTOCOCCUS SANGUIS; TOLL-LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR-ALPHA;

EID: 84864917698     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2011.110522     Document Type: Article

References (50)

1. Cochran DL. Inflammation and bone loss in periodontal disease. J Periodontol 2008;79(Suppl. 8):1569-1576.
2. Sahingur SE, Cohen RE. Analysis of host responses and risk for disease progression. Periodontol 2000 2004;34:57-83. (Pubitemid 41794530)
3. Scannapieco FA. Periodontal inflammation: From gingivitis to systemic disease? Compend Contin Educ Dent 2004;25(7 Suppl. 1)16-25.
4. Mahanonda R, Pichyangkul S. Toll-like receptors and their role in periodontal health and disease. Periodontol 2000 2007;43:41-55.
5. Barksby HE, Nile CJ, Jaedicke KM, Taylor JJ, Preshaw PM. Differential expression of immunoregulatory genes in monocytes in response to Porphyromonas gingivalis and Escherichia coli lipopolysaccharide. Clin Exp Immunol 2009;156:479-487.
6. Hajishengallis G, Tapping RI, Harokopakis E, et al. Differential interactions of fimbriae and lipopolysaccharide from Porphyromonas gingivalis with the Tolllike receptor 2-centred pattern recognition apparatus. Cell Microbiol 2006;8:1557-1570. (Pubitemid 44350015)
7. Liu R, Desta T, Raptis M, Darveau RP, Graves DTP. P. gingivalis and E. coli lipopolysaccharides exhibit different systemic but similar local induction of inflammatory markers. J Periodontol 2008;79:1241-1247.
8. Asagiri M, Hirai T, Kunigami T, et al. Cathepsin K-dependent toll-like receptor 9 signaling revealed in experimental arthritis. Science 2008;319:624-627. (Pubitemid 351197065)
9. Ewald SE, Barton GM. Nucleic acid sensing Toll-like receptors in autoimmunity. Curr Opin Immunol 2011; 23:3-9.
10. Hirsch I, Caux C, Hasan U, Bendriss-Vermare N, Olive D. Impaired Toll-like receptor 7 and 9 signaling: From chronic viral infections to cancer. Trends Immunol 2010;31:391-397.
11. Sahingur SE, Xia XJ, Alamgir S, Honma K, Sharma A, Schenkein HA. DNA from Porphyromonas gingivalis and Tannerella forsythia induce cytokine production in human monocytic cell lines. Mol Oral Microbiol 2010; 25:123-135.
12. Nonnenmacher C, Dalpke A, Zimmermann S, Flores- De-Jacoby L, Mutters R, Heeg K. DNA from periodontopathogenic bacteria is immunostimulatory for mouse and human immune cells. Infect Immun 2003; 71:850-856. (Pubitemid 36150780)
13. Takeshita A, Imai K, Hanazawa S. CpG motifs in Porphyromonas gingivalis DNA stimulate interleukin- 6 expression in human gingival fibroblasts. Infect Immun 1999;67:4340-4345. (Pubitemid 29400405)
14. Kajita K, Honda T, Amanuma R, et al. Quantitative messenger RNA expression of Toll-like receptors and interferon-alpha1 in gingivitis and periodontitis. Oral Microbiol Immunol 2007;22:398-402. (Pubitemid 47621818)
15. Holla LI, Vokurka J, Hrdlickova B, Augustin P, Fassmann A. Association of Toll-like receptor 9 haplotypes with chronic periodontitis in Czech population. J Clin Periodontol 2010;37:152-159.
16. Sahingur SE, Xia XJ, Gunsolley J, Schenkein HA, Genco RJ, De Nardin E. Single nucleotide polymorphisms of pattern recognition receptors and chronic periodontitis. J Periodontal Res 2011;46:184-192.
17. Socransky SS, Haffajee AD, Smith C, et al. Use of checkerboard DNA-DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 2004;19:352-362. (Pubitemid 39487668)
18. Huang CB, Altimova Y, Strange S, Ebersole JL. Polybacterial challenge effects on cytokine/chemokine production by macrophages and dendritic cells. Inflamm Res 2011;60:119-125.
19. Dickinson BC, Moffatt CE, Hagerty D, et al. Interaction of oral bacteria with gingival epithelial cell multilayers. Mol Oral Microbiol 2011;26:210-220.
20. Sheikhi M, Gustafsson A, Jarstrand C. Cytokine, elastase and oxygen radical release by Fusobacterium nucleatum-activated leukocytes: A possible pathogenic factor in periodontitis. J Clin Periodontol 2000; 27:758-762.
21. Polak D, Wilensky A, Shapira L, et al. Mouse model of experimental periodontitis induced by Porphyromonas gingivalis/Fusobacterium nucleatum infection: Bone loss and host response. J Clin Periodontol 2009;36: 406-410.
22. Fardini Y, Chung P, Dumm R, Joshi N, Han YW. Transmission of diverse oral bacteria to murine placenta: Evidence for the oral microbiome as a potential source of intrauterine infection. Infect Immun 2010;78: 1789-1796.
23. Han YW, Fardini Y, Chen C, et al. Term stillbirth caused by oral Fusobacterium nucleatum. Obstet Gynecol 2010;115:442-445.
24. Dharmani P, Strauss J, Ambrose C, Allen-Vercoe E, Chadee K. Fusobacterium nucleatum infection of colonic cells stimulates MUC2 mucin and tumor necrosis factor alpha. Infect Immun 2011;79:2597-2607.
25. Strauss J, Kaplan GG, Beck PL, et al. Invasive potential of gut mucosa-derived Fusobacterium nucleatum positively correlates with IBD status of the host. Inflamm Bowel Dis 2011;17:1971-1978.
26. González OA, Li M, Ebersole JL, Huang CB. HIV-1 reactivation induced by the periodontal pathogens Fusobacterium nucleatum and Porphyromonas gingivalis involves Toll-like receptor 2 [corrected] and 9 activation in monocytes/macrophages. Clin Vaccine Immunol 2010;17:1417-1427.
27. Dalpke A, Frank J, Peter M, Heeg K. Activation of tolllike receptor 9 by DNA from different bacterial species. Infect Immun 2006;74:940-946. (Pubitemid 43185528)
28. De Nardo D, De Nardo CM, Nguyen T, Hamilton JA, Scholz GM. Signaling crosstalk during sequential TLR4 and TLR9 activation amplifies the inflammatory response of mouse macrophages. J Immunol 2009;183: 8110-8118.
29. Mäkelä SM, Strengell M, Pietilä TE, Osterlund P, Julkunen I. Multiple signaling pathways contribute to synergistic TLR ligand-dependent cytokine gene expression in human monocyte-derived macrophages and dendritic cells. J Leukoc Biol 2009;85:664-672.
30. Theiner G, Rössner S, Dalpke A, et al. TLR9 cooperates with TLR4 to increase IL-12 release by murine dendritic cells. Mol Immunol 2008;45:244-252. (Pubitemid 47331637)
31. Hajishengallis G, Martin M, Schifferle RE, Genco RJ. Counteracting interactions between lipopolysaccharide molecules with differential activation of toll-like receptors. Infect Immun 2002;70:6658-6664. (Pubitemid 35387895)
32. Yumoto H, Chou HH, Takahashi Y, Davey M, Gibson FC 3rd, Genco CA. Sensitization of human aortic endothelial cells to lipopolysaccharide via regulation of Toll-like receptor 4 by bacterial fimbria-dependent invasion. Infect Immun 2005;73:8050-8059. (Pubitemid 41740292)
33. Kuznik A, Bencina M, Svajger U, Jeras M, Rozman B, Jerala R. Mechanism of endosomal TLR inhibition by antimalarial drugs and imidazoquinolines. J Immunol 2011;186:4794-4804.
34. Pollreisz A, Huang Y, Roth GA, et al. Enhanced monocyte migration and pro-inflammatory cytokine production by Porphyromonas gingivalis infection. J Periodontal Res 2010;45:239-245.
35. Nassar H, Chou HH, Khlgatian M, Gibson FC 3rd, Van Dyke TE, Genco CA. Role for fimbriae and lysinespecific cysteine proteinase gingipain K in expression of interleukin-8 and monocyte chemoattractant protein in Porphyromonas gingivalis-infected endothelial cells. Infect Immun 2002;70:268-276. (Pubitemid 34028627)
36. Konopka L, Wierzbicki M, Brzezińska-B1aszczyk E. Lipopolysaccharide from Porphyromonas gingivalis stimulates rat mast cells to cysteinyl leukotriene generation and upregulates Toll-like receptor -2 and -4 expression. Int J Immunopathol Pharmacol 2010; 23:803-810.
37. Patni S, Wynen LP, Seager AL, Morgan G, White JO, Thornton CA. Expression and activity of Toll-like receptors 1-9 in the human term placenta and changes associated with labor at term. Biol Reprod 2009;80:243-248.
38. Estrada-Gutierrez G, Gomez-Lopez N, Zaga-Clavellina V, et al. Interaction between pathogenic bacteria and intrauterine leukocytes triggers alternative molecular signaling cascades leading to labor in women. Infect Immun 2010;78:4792-4799.
39. Neta GI, von Ehrenstein OS, Goldman LR, et al. Umbilical cord serum cytokine levels and risks of small-for-gestational-age and preterm birth. Am J Epidemiol 2010;171:859-867.
40. Thaxton JE, Romero R, Sharma S. TLR9 activation coupled to IL-10 deficiency induces adverse pregnancy outcomes. J Immunol 2009;183:1144-1154.
41. Martinez-Martinez RE, Abud-Mendoza C, Patiño-Marin N, Rizo-Rodríguez JC, Little JW, Loyola-Rodríguez JP. Detection of periodontal bacterial DNA in serum and synovial fluid in refractory rheumatoid arthritis patients. J Clin Periodontol 2009;36:1004-1010.
42. Haraszthy VI, Zambon JJ, Trevisan M, Zeid M, Genco RJ. Identification of periodontal pathogens in atheromatous plaques. J Periodontol 2000;71:1554-1560.
43. Gaetti-Jardim E Jr., Marcelino SL, Feitosa AC, Romito GA, Avila-Campos MJ. Quantitative detection of periodontopathic bacteria in atherosclerotic plaques from coronary arteries. J Med Microbiol 2009;58: 1568-1575.
44. Heeg K, Dalpke A, Peter M, Zimmermann S. Structural requirements for uptake and recognition of CpG oligonucleotides. Int J Med Microbiol 2008;298:33-38. (Pubitemid 350216551)
45. Paik S, Senty L, Das S, Noe JC, Munro CL, Kitten T. Identification of virulence determinants for endocarditis in Streptococcus sanguinis by signature-tagged mutagenesis. Infect Immun 2005;73:6064-6074. (Pubitemid 41193045)
46. Banks J, Poole S, Nair SP, et al. Streptococcus sanguinis secretes CD14-binding proteins that stimulate cytokine synthesis: A clue to the pathogenesis of infective (bacterial) endocarditis? Microb Pathog 2002;32:105-116. (Pubitemid 34971615)
47. Bhan U, Ballinger MN, Zeng X, Newstead MJ, Cornicelli MD, Standiford TJ. Cooperative interactions between TLR4 and TLR9 regulate interleukin-23 and -17 production in a murine model of Gram-negative bacterial pneumonia. PLoS One 2010;5:e9896.
48. Holley MM, Zhang Y, Lehrmann E, Wood WH, Becker KG, Kielian T. Toll-like receptor 2 (TLR2)-TLR9 crosstalk dictates IL-12 family cytokine production in microglia. Glia 2012:60:29-42.
49. Hornung V, Ablasser A, Charrel-Dennis M, et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1- activating inflammasome with ASC. Nature 2009;458: 514-518.
50. Takaoka A, Wang Z, Choi MK, et al. DAI (DLM-1/ZBP1) is a cytosolic DNA sensor and an activator of innate immune response. Nature 2007;448:501-505. (Pubitemid 47123520)