Interleukin-1β is internalised by viable Aggregatibacter actinomycetemcomitans biofilm and locates to the outer edges of nucleoids

Cytokine

Volumn 60, Issue 2, 2012, Pages 565-574

  Paino, Annamari ^a   Lohermaa, Elina ^a   Sormunen, Raija ^b   Tuominen, Heidi ^a   Korhonen, Jari ^c   Pöllänen, Marja T ^d   Ihalin, Riikka ^a  

^a UNIVERSITY OF TURKU   (Finland)

^b UNIVERSITY OF OULU   (Finland)

^c ÅBO AKADEMI UNIVERSITY   (Finland)

^d UNIVERSITY OF TURKU   (Finland)

Author keywords

Aggregatibacter actinomycetemcomitans; Bacterial DNA binding protein HU; Biofilm host interaction; Interleukin 1 ; Organotypic gingival mucosa

Indexed keywords

INTERLEUKIN 1BETA;

AGGREGATIBACTER ACTINOMYCETEMCOMITANS; APOPTOSIS; ARTICLE; BACTERIAL GENE; BIOFILM; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE EXPRESSION; IMMUNOELECTRON MICROSCOPY; INTERNALIZATION; KERATINOCYTE; MASS SPECTROMETRY; NICK END LABELING; NONHUMAN; PERIODONTOSIS; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN LOCALIZATION;

ACTINOBACILLUS ACTINOMYCETEMCOMITANS; ACTINOBACILLUS INFECTIONS; AMINO ACID SEQUENCE; APOPTOSIS; BACTERIAL ADHESION; BIOFILMS; CELL PROLIFERATION; DNA, BACTERIAL; ENDOCYTOSIS; EPITHELIAL CELLS; GINGIVA; HU PARANEOPLASTIC ENCEPHALOMYELITIS ANTIGENS; HUMANS; INTERLEUKIN-1BETA; KERATINOCYTES; MICROBIAL VIABILITY; MOLECULAR SEQUENCE DATA; MUCOUS MEMBRANE; PENICILLINS; PROTEIN BINDING; STREPTOMYCIN;

BACTERIA (MICROORGANISMS);

EID: 84866757439     PISSN: 10434666     EISSN: 10960023     Source Type: Journal    
DOI: 10.1016/j.cyto.2012.07.024     Document Type: Article

References (54)

1. Zambon J.J. Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 1985, 12(1):1-20.
2. Socransky S.S., Haffajee A.D. The bacterial etiology of destructive periodontal disease: current concepts. J Periodontol 1992, 63(4 Suppl.):322-331.
3. Kozarov E.V., Dorn B.R., Shelburne C.E., Dunn W.A., Progulske-Fox A. Human atherosclerotic plaque contains viable invasive Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis. Arterioscler Thromb Vasc Biol 2005, 25(3):e17-e18.
4. Haraszthy V.I., Zambon J.J., Trevisan M., Zeid M., Genco R.J. Identification of periodontal pathogens in atheromatous plaques. J Periodontol 2000, 71(10):1554-1560.
5. Stashenko P., Fujiyoshi P., Obernesser M.S., Prostak L., Haffajee A.D., Socransky S.S. Levels of interleukin 1beta in tissue from sites of active periodontal disease. J Clin Periodontol 1991, 18(7):548-554.
6. Gamonal J., Acevedo A., Bascones A., Jorge O., Silva A. Levels of interleukin-1beta, -8, and -10 and RANTES in gingival crevicular fluid and cell populations in adult periodontitis patients and the effect of periodontal treatment. J Periodontol 2000, 71(10):1535-1545.
7. Kelk P., Claesson R., Chen C., Sjöstedt A., Johansson A. IL-1beta secretion induced by Aggregatibacter (actinobacillus) actinomycetemcomitans is mainly caused by the leukotoxin. Int J Med Microbiol 2008, 298(5-6):529-541.
8. Matsuki Y., Yamamoto T., Hara K. Interleukin-1 mRNA-expressing macrophages in human chronically inflamed gingival tissues. Am J Pathol 1991, 138(6):1299-1305.
9. Stathopoulou P.G., Benakanakere M.R., Galicia J.C., Kinane D.F. Epithelial cell pro-inflammatory cytokine response differs across dental plaque bacterial species. J Clin Periodontol 2010, 37(1):24-29.
10. Belibasakis G.N., Johansson A., Wang Y., Chen C., Lagergard T., Kalfas S., et al. Cytokine responses of human gingival fibroblasts to Actinobacillus actinomycetemcomitans cytolethal distending toxin. Cytokine 2005, 30(2):56-63.
11. Yang J., Hooper W.C., Phillips D.J., Talkington D.F. Interleukin-1beta responses to Mycoplasma pneumoniae infection are cell-type specific. Microb Pathog 2003, 34(1):17-25.
12. Friedlander R.M., Gagliardini V., Rotello R.J., Yuan J. Functional role of interleukin 1beta (IL-1beta) in IL-1beta-converting enzyme-mediated apoptosis. J Exp Med 1996, 184(2):717-724.
13. Fratelli M., Gagliardini V., Galli G., Gnocchi P., Ghiara P., Ghezzi P. Autocrine interleukin-1beta regulates both proliferation and apoptosis in EL4-6.1 thymoma cells. Blood 1995, 85(12):3532-3537.
14. Eskan M.A., Benakanakere M.R., Rose B.G., Zhang P., Zhao J., Stathopoulou P., et al. Interleukin-1beta modulates proinflammatory cytokine production in human epithelial cells. Infect Immun 2008, 76(5):2080-2089.
15. Mogi M., Otogoto J., Ota N., Inagaki H., Minami M., Kojima K. Interleukin 1beta, interleukin 6, beta 2-microglobulin, and transforming growth factor-alpha in gingival crevicular fluid from human periodontal disease. Arch Oral Biol 1999, 44(6):535-539.
16. Dickinson B.C., Moffatt C.E., Hagerty D., Whitmore S.E., Brown T.A., Graves D.T., et al. Interaction of oral bacteria with gingival epithelial cell multilayers. Mol Oral Microbiol 2011, 26(3):210-220.
17. Oscarsson J., Karched M., Thay B., Chen C., Asikainen S. Proinflammatory effect in whole blood by free soluble bacterial components released from planktonic and biofilm cells. BMC Microbiol 2008, 8:206.
18. Reddi K., Wilson M., Poole S., Meghji S., Henderson B. Relative cytokine-stimulating activities of surface components of the oral periodontopathogenic bacterium Actinobacillus actinomycetemcomitans. Cytokine 1995, 7(6):534-541.
19. Sfakianakis A., Barr C.E., Kreutzer D.L. Actinobacillus actinomycetemcomitans-induced expression of IL-1alpha and IL-1beta in human gingival epithelial cells: Role in IL-8 expression. Eur J Oral Sci 2001, 109(6):393-401.
20. Sliepen I., Van Damme J., Van Essche M., Loozen G., Quirynen M., Teughels W. Microbial interactions influence inflammatory host cell responses. J Dent Res 2009, 88(11):1026-1030.
21. Dongari-Bagtzoglou A.I., Ebersole J.L. Production of inflammatory mediators and cytokines by human gingival fibroblasts following bacterial challenge. J Periodontal Res 1996, 31(2):90-98.
22. Darveau R.P. Periodontitis: a polymicrobial disruption of host homeostasis. Nat Rev Microbiol 2010, 8(7):481-490.
23. Steinberg T., Dannewitz B., Tomakidi P., Hoheisel J.D., Mussig E., Kohl A., et al. Analysis of interleukin-1beta-modulated mRNA gene transcription in human gingival keratinocytes by epithelia-specific cDNA microarrays. J Periodontal Res 2006, 41(5):426-446.
24. Kanangat S., Bronze M.S., Meduri G.U., Postlethwaite A., Stentz F., Tolley E., et al. Enhanced extracellular growth of Staphylococcus aureus in the presence of selected linear peptide fragments of human interleukin (IL)-1beta and IL-1 receptor antagonist. J Infect Dis 2001, 183(1):65-69.
25. Kanangat S., Postlethwaite A., Cholera S., Williams L., Schaberg D. Modulation of virulence gene expression in Staphylococcus aureus by interleukin-1beta: novel implications in bacterial pathogenesis. Microbes Infect 2007, 9(3):408-415.
26. Paino A., Tuominen H., Jääskeläinen M., Alanko J., Nuutila J., Asikainen S.E., et al. Trimeric form of intracellular ATP synthase subunit beta of Aggregatibacter actinomycetemcomitans binds human interleukin-1beta. PLoS One 2011, 6(4):e18929.
27. Kar S., Edgar R., Adhya S. Nucleoid remodeling by an altered HU protein: reorganization of the transcription program. Proc Natl Acad Sci USA 2005, 102(45):16397-16402.
28. Rouviere-Yaniv J., Gros F. Characterization of a novel, low-molecular-weight DNA-binding protein from Escherichia coli. Proc Natl Acad Sci USA 1975, 72(9):3428-3432.
29. Drlica K., Rouviere-Yaniv J. Histonelike proteins of bacteria. Microbiol Rev 1987, 51(3):301-319.
30. Oberto J., Nabti S., Jooste V., Mignot H., Rouviere-Yaniv J. The HU regulon is composed of genes responding to anaerobiosis, acid stress, high osmolarity and SOS induction. PLoS One 2009, 4(2):e4367.
31. Berger M., Farcas A., Geertz M., Zhelyazkova P., Brix K., Travers A., et al. Coordination of genomic structure and transcription by the main bacterial nucleoid-associated protein HU. EMBO Rep 2010, 11(1):59-64.
32. Alberti-Segui C., Arndt A., Cugini C., Priyadarshini R., Davey M.E. HU protein affects transcription of surface polysaccharide synthesis genes in Porphyromonas gingivalis. J Bacteriol 2010, 192(23):6217-6229.
33. Davey M.E., Duncan M.J. Enhanced biofilm formation and loss of capsule synthesis: deletion of a putative glycosyltransferase in Porphyromonas gingivalis. J Bacteriol 2006, 188(15):5510-5523.
34. Wang Y., Shi W., Chen W., Chen C. Type IV pilus gene homologs pilABCD are required for natural transformation in Actinobacillus actinomycetemcomitans. Gene 2003, 312:249-255.
35. Chen C., Kittichotirat W., Chen W., Downey J.S., Si Y., Bumgarner R. Genome sequence of naturally competent Aggregatibacter actinomycetemcomitans serotype a strain D7S-1. J Bacteriol 2010, 192(10):2643-2644.
36. Karched M., Paul-Satyaseela M., Asikainen S. A simple viability-maintaining method produces homogenic cell suspensions of autoaggregating wild-type Actinobacillus actinomycetemcomitans. J Microbiol Methods 2007, 68(1):46-51.
37. Green H., Fuchs E., Watt F. Differentiated structural components of the keratinocyte. Cold Spring Harb Symp Quant Biol 1982, 46(Pt 1):293-301.
38. Kaplan J.B., Meyenhofer M.F., Fine D.H. Biofilm growth and detachment of Actinobacillus actinomycetemcomitans. J Bacteriol 2003, 185(4):1399-1404.
39. Gursoy U.K., Pöllänen M., Könönen E., Uitto V.J. Biofilm formation enhances the oxygen tolerance and invasiveness of Fusobacterium nucleatum in an oral mucosa culture model. J Periodontol 2010, 81(7):1084-1091.
40. Oksanen J., Hormia M. An organotypic in vitro model that mimics the dento-epithelial junction. J Periodontol 2002, 73(1):86-93.
41. Mäkelä M., Salo T., Larjava H. MMP-9 from TNF alpha-stimulated keratinocytes binds to cell membranes and type I collagen: a cause for extended matrix degradation in inflammation?. Biochem Biophys Res Commun 1998, 253(2):325-335.
42. Slot J.W., Geuze H.J. A new method of preparing gold probes for multiple-labeling cytochemistry. Eur J Cell Biol 1985, 38(1):87-93.
43. Paul-Satyaseela M., Karched M., Bian Z., Ihalin R., Boren T., Arnqvist A., et al. Immunoproteomics of Actinobacillus actinomycetemcomitans outer-membrane proteins reveal a highly immunoreactive peptidoglycan-associated lipoprotein. J Med Microbiol 2006, 55(Pt 7):931-942.
44. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.J. Protein measurement with the folin phenol reagent. J Biol Chem 1951, 193(1):265-275.
45. O'Connell K.L., Stults J.T. Identification of mouse liver proteins on two-dimensional electrophoresis gels by matrix-assisted laser desorption/ionization mass spectrometry of in situ enzymatic digests. Electrophoresis 1997, 18(3-4):349-359.
46. Zimmerman S.B., Murphy L.D. Release of compact nucleoids with characteristic shapes from Escherichia coli. J Bacteriol 2001, 183(17):5041-5049.
47. Tardif F., Ross G., Rouabhia M. Gingival and dermal fibroblasts produce interleukin-1beta converting enzyme and interleukin-1beta but not interleukin-18 even after stimulation with lipopolysaccharide. J Cell Physiol 2004, 198(1):125-132.
48. Belibasakis G., Johansson A., Wang Y., Claesson R., Chen C., Asikainen S., et al. Inhibited proliferation of human periodontal ligament cells and gingival fibroblasts by Actinobacillus actinomycetemcomitans: involvement of the cytolethal distending toxin. Eur J Oral Sci 2002, 110(5):366-373.
49. Damek-Poprawa M., Haris M., Volgina A., Korostoff J., Dirienzo J.M. Cytolethal distending toxin damages the oral epithelium of gingival explants. J Dent Res 2011, 90(7):874-879.
50. Smith J.L., Bayles D.O. The contribution of cytolethal distending toxin to bacterial pathogenesis. Crit Rev Microbiol 2006, 32(4):227-248.
51. Kang P., Korostoff J., Volgina A., Grzesik W., DiRienzo J.M. Differential effect of the cytolethal distending toxin of Actinobacillus actinomycetemcomitans on co-cultures of human oral cells. J Med Microbiol 2005, 54(Pt 8):785-794.
52. Alaoui-El-Azher M., Mans J.J., Baker H.V., Chen C., Progulske-Fox A., Lamont R.J., et al. Role of the ATM-checkpoint kinase 2 pathway in CDT-mediated apoptosis of gingival epithelial cells. PLoS One 2010, 5(7):e11714.
53. Wising C., Azem J., Zetterberg M., Svensson L.A., Ahlman K., Lagergard T. Induction of apoptosis/necrosis in various human cell lineages by Haemophilus ducreyi cytolethal distending toxin. Toxicon 2005, 45(6):767-776.
54. Chen C., Kittichotirat W., Si Y., Bumgarner R. Genome sequence of Aggregatibacter actinomycetemcomitans serotype c strain D11S-1. J Bacteriol 2009, 191(23):7378-7379.