Polymicrobial infection with periodontal pathogens specifically enhances microRNA miR-146a in ApoE-/- mice during experimental periodontal disease

Infection and Immunity

Volumn 79, Issue 4, 2011, Pages 1597-1605

  Nahid, Md A ^a   Rivera, Mercedes ^a   Lucas, Alexandra ^b   Chan, Edward K L ^a   Kesavalu, L ^a  

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

^b UNIVERSITY OF FLORIDA COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

INTERLEUKIN 1 RECEPTOR ASSOCIATED KINASE 1; INTERLEUKIN 1BETA; MESSENGER RNA; MICRORNA; MIR 146A; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RECEPTOR ASSOCIATED FACTOR 6; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; CYTOKINE RELEASE; HUMAN; HUMAN CELL; MIXED INFECTION; MOUSE; NONHUMAN; PERIODONTAL DISEASE; PERIODONTIUM; PORPHYROMONAS GINGIVALIS; PRIORITY JOURNAL; SPLEEN; TANNERELLA FORSYTHENSIS; TREPONEMA DENTICOLA;

ANIMALS; APOLIPOPROTEINS E; BACTEROIDES; BLOTTING, WESTERN; DISEASE MODELS, ANIMAL; GRAM-NEGATIVE BACTERIAL INFECTIONS; HUMANS; INTERLEUKIN-1BETA; MALE; MICE; MICE, KNOCKOUT; MICRORNAS; MONOCYTES; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPLEEN; TREPONEMA DENTICOLA; TUMOR NECROSIS FACTOR-ALPHA;

EID: 79953321414     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01062-10     Document Type: Article

References (52)

1. Aas, J. A., B. J. Paster, L. N. Stokes, I. Olsen, and F. E. Dewhirst. 2005. Defining the normal bacterial flora of the oral cavity. J. Clin. Microbiol. 43:5721-5732.
2. Ambros, V. 2004. The functions of animal microRNAs. Nature 431:350-355.
3. Bellon, M., Y. Lepelletier, O. Hermine, and C. Nicot. 2009. Deregulation of microRNA involved in hematopoiesis and the immune response in HTLV-I adult T-cell leukemia. Blood 113:4914-4917.
4. Bodet, C., F. Chandad, and D. Grenier. 2006. Inflammatory responses of a macrophage/epithelial cell co-culture model to mono and mixed infections with Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia. Microbes Infect. 8:27-35.
5. Cameron, J. E., et al. 2008. Epstein-Barr virus growth/latency III program alters cellular microRNA expression. Virology 382:257-266.
6. Cao, H., et al. 2010. MicroRNAs play a critical role in tooth development. J. Dent. Res. 89:779-784.
7. Cremer, T. J., et al. 2009. MiR-155 induction by F. novicida but not the virulent F. tularensis results in SHIP down-regulation and enhanced proinflammatory cytokine response. PLoS One 4:e8508.
8. Fassi, F. L., et al. 2010. Helicobacter pylori induces miR-155 in T cells in a cAMP-Foxp3-dependent manner. PLoS One 5:e9500
9. Fehri, L. F., et al. 2009. Helicobacter pylori-induced modification of the histone H3 phosphorylation status in gastric epithelial cells reflects its impact on cell cycle regulation. Epigenetics 4:577-586.
10. Fenno, J. C., and B. C. McBride. 1998. Virulence factors of oral treponemes. Anaerobe 4:1-17.
11. Forner, L., T. Larsen, M. Kilian, and P. Holmstrup. 2006. Incidence of bacteremia after chewing, tooth brushing and scaling in individuals with periodontal inflammation. J. Clin. Periodontol. 33:401-407.
12. Friedman, R. C., K. K. Farh, C. B. Burge, and D. P. Bartel. 2009. Most mammalian mRNAs are conserved targets of microRNAs. Genome Res. 19:92-105.
13. Ghosh, T. K., et al. 2006. Toll-like receptor (TLR) 2-9 agonists-induced cytokines and chemokines. I. Comparison with T cell receptor-induced responses. Cell. Immunol. 243:48-57.
14. Gibson, F. C., et al. 2004. Innate immune recognition of invasive bacteria accelerates atherosclerosis in apolipoprotein E-deficient mice. Circulation 109:2801-2806.
15. Guha, M., and N. Mackman. 2001. LPS induction of gene expression in human monocytes. Cell. Signal. 13:85-94.
16. Haraszthy, V. I., J. J. Zambon, M. Trevisan, M. Zeid, and R. J. Genco. 2000. Identification of periodontal pathogens in atheromatous plaques. J. Periodontol. 71:1554-1560.
17. Holt, S. C., L. Kesavalu, S. Walker, and C. A. Genco. 1999. Virulence factors of Porphyromonas gingivalis. Periodontol. 2000 20:168-238.
18. Hou, J., et al. 2009. MicroRNA-146a feedback inhibits RIG-I-dependent type I IFN production in macrophages by targeting TRAF6, IRAK1, and IRAK2. J. Immunol. 183:2150-2158.
19. Kesavalu, L., et al. 2007. Rat model of polymicrobial infection, immunity, and alveolar bone resorption in periodontal disease. Infect. Immun. 75:1704-1712.
20. Kinane, D. F., M. P. Riggio, K. F. Walker, D. MacKenzie, and B. Shearer. 2005. Bacteraemia following periodontal procedures. J. Clin. Periodontol. 32:708-713.
21. Kozarov, E., D. Sweier, C. Shelburne, A. Progulske-Fox, and D. Lopatin. 2006. Detection of bacterial DNA in atheromatous plaques by quantitative PCR. Microbes Infect. 8:687-693.
22. Lalla, E., et al. 2003. Oral infection with a periodontal pathogen accelerates early atherosclerosis in apolipoprotein E-null mice. Arterioscler. Thromb. Vasc. Biol. 23:1405-1411.
23. Lee, R. C., R. L. Feinbaum, and V. Ambros. 1993. The C. elegans heterochronic gene lin-4 encodes small RNAs with antisense complementarity to lin-14. Cell 75:843-854.
24. Li, L., S. S. Chang, and Y. Liu. 2010. RNA interference pathways in filamentous fungi. Cell. Mol. Life Sci. 67:3849-3863.
25. Li, L., X. P. Chen, and Y. J. Li. 2010. MicroRNA-146a and human disease. Scand. J. Immunol. 71:227-231.
26. Liu, Y. C., U. H. Lerner, and Y. T. Teng. 2010. Cytokine responses against periodontal infection: protective and destructive roles. Periodontol. 2000 52:163-206.
27. Liu, Z., et al. 2010. Up-regulated microRNA-146a negatively modulate Helicobacter pylori-induced inflammatory response in human gastric epithelial cells. Microbes Infect. 12:854-863.
28. Livak, K. J., and T. D. Schmittgen. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-delta delta C(T)) method. Methods 25:402-408.
29. Mizel, S. B., and J. A. Snipes. 2002. Gram-negative flagellin-induced selftolerance is associated with a block in interleukin-1 receptor-associated kinase release from Toll-like receptor 5. J. Biol. Chem. 277:22414-22420.
30. Mustapha, I. Z., S. Debrey, M. Oladubu, and R. Ugarte. 2007. Markers of systemic bacterial exposure in periodontal disease and cardiovascular disease risk: a systematic review and meta-analysis. J. Periodontol. 78:2289-2302.
31. Nahid, A. M., and S. Sugii. 2006. Binding of porcine ficolin-alpha to lipopolysaccharides from Gram-negative bacteria and lipoteichoic acids from Gram-positive bacteria. Dev. Comp. Immunol. 30:335-343.
32. Nahid, M. A., K. M. Pauley, M. Satoh, and E. K. Chan. 2009. miR-146a is critical for endotoxin-induced tolerance. Implication in innate immunity. J. Biol. Chem. 284:34590-34599.
33. Nahid, M. A., M. Satoh, and E. K. Chan. 2011. Mechanistic role of microRNA-146a in endotoxin-induced differential cross-regulation of TLR signaling. J. Immunol. 186:1723-1734. [Epub ahead of print.]
34. Narayanan, D., et al. 2005. The distribution of Tannerella forsythia in an adolescent and adult population. J. Periodontal Res. 40:482-488.
35. Okada, H., and S. Murakami. 1998. Cytokine expression in periodontal health and disease. Crit. Rev. Oral Biol. Med. 9:248-266.
36. Okuda, K., et al. 2001. Detection of Treponema denticola in atherosclerotic lesions. J. Clin. Microbiol. 39:1114-1117.
37. Paquette, D. W., N. Brodala, and T. C. Nichols. 2007. Cardiovascular disease, inflammation, and periodontal infection. Periodontol. 2000 44:113-126.
38. Paster, B. J., et al. 2001. Bacterial diversity in human subgingival plaque. J. Bacteriol. 183:3770-3783.
39. Potempa, J., A. Banbula, and J. Travis. 2000. Role of bacterial proteinases in matrix destruction and modulation of host responses. Periodontol. 2000 24:153-192.
40. Sahingur, S. E., et al. 2010. DNA from Porphyromonas gingivalis and Tannerella forsythia induce cytokine production in human monocytic cell lines. Mol. Oral Microbiol. 25:123-135.
41. Sathishkumar, S., et al. 2008. Extracorporeal shock wave therapy induces alveolar bone regeneration. J. Dent. Res. 87:687-691.
42. Scannapieco, F. A., R. B. Bush, and S. Paju. 2003. Associations between periodontal disease and risk for nosocomial bacterial pneumonia and chronic obstructive pulmonary disease. A systematic review. Ann. Periodontol. 8:54-69.
43. Shaffer, J. P. 1986. Modified sequentially rejective multiple test procedures. J. Am. Stat. Assoc. 81:826-831.
44. Socransky, S. S., and A. D. Haffajee. 2005. Periodontal microbial ecology. Periodontol. 2000 38:135-187.
45. Socransky, S. S., A. D. Haffajee, M. A. Cugini, C. Smith, and R. L. Kent, Jr. 1998. Microbial complexes in subgingival plaque. J. Clin. Periodontol. 25: 134-144.
46. Taganov, K. D., M. P. Boldin, K. J. Chang, and D. Baltimore. 2006. NFkappaB-dependent induction of microRNA miR-146, an inhibitor targeted to signaling proteins of innate immune responses. Proc. Natl. Acad. Sci. U. S. A. 103:12481-12486.
47. Urbich, C., A. Kuehbacher, and S. Dimmeler. 2008. Role of microRNAs in vascular diseases, inflammation, and angiogenesis. Cardiovasc. Res. 79:581-588.
48. Van Amersfoort, E. S., T. J. Van Berkel, and J. Kuiper. 2003. Receptors, mediators, and mechanisms involved in bacterial sepsis and septic shock. Clin. Microbiol. Rev. 16:379-414.
49. Weber, C., A. Schober, and A. Zernecke. 2010. MicroRNAs in arterial remodelling, inflammation and atherosclerosis. Curr. Drug Targets 11:950-956.
50. Wightman, B., I. Ha, and G. Ruvkun. 1993. Posttranscriptional regulation of the heterochronic gene lin-14 by lin-4 mediates temporal pattern formation in C. elegans. Cell 75:855-862.
51. Williams, A. E., M. M. Perry, S. A. Moschos, H. M. Larner-Svensson, and M. A. Lindsay. 2008. Role of miRNA-146a in the regulation of the innate immune response and cancer. Biochem. Soc. Trans. 36:1211-1215.
52. Zaric, S., et al. 2010. Impaired immune tolerance to Porphyromonas gingivalis lipopolysaccharide promotes neutrophil migration and decreased apoptosis. Infect. Immun. 78:4151-4156.