Activation of protective responses in oral epithelial cells by Fusobacterium nucleatum and human β-defensin-2

Journal of Medical Microbiology

Volumn 56, Issue 7, 2007, Pages 976-987

  Yin, Lei ^a   Dale, Beverly A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA CHEMOKINE; ASPARTATE AMMONIA LIGASE; BETA DEFENSIN 2; BETA DEFENSIN 4; CHEMOKINE; CHEMOKINE CCL20; CHEMOKINE CXCL2; COMPLEMENT COMPONENT C3; CYSTATHIONINE GAMMA LYASE; GELATINASE B; GLYCEROL KINASE; HYPOCALCIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 8; INTERSTITIAL COLLAGENASE; KYNURENINASE; PROTEASOME; PROTEIN SKALP; PROTEINASE INHIBITOR; SCLEROPROTEIN; SECRETORY LEUKOCYTE PROTEINASE INHIBITOR; SERINE PROTEINASE INHIBITOR; SERPINB1; SERPINB2; SERPINB3; SERPINB4; SERUM AMYLOID A; UBIQUITIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN;

ANTIMICROBIAL ACTIVITY; ARTICLE; CELL DIVISION; CHEMOTAXIS; COMMENSAL; CONTROLLED STUDY; FUSOBACTERIUM NUCLEATUM; GENE EXPRESSION; GENE FUNCTION; HUMAN; HUMAN CELL; IMMUNE RESPONSE; IMMUNOSTIMULATION; INFLAMMATION; MICROARRAY ANALYSIS; MITOSIS; MOUTH MUCOSA; MUCOSAL IMMUNITY; NUCLEOTIDE SEQUENCE; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DEGRADATION; SIGNAL TRANSDUCTION; STATISTICAL ANALYSIS; WOUND HEALING;

BETA-DEFENSINS; CELLS, CULTURED; CYTOKINES; EPITHELIAL CELLS; FUSOBACTERIUM NUCLEATUM; GENE EXPRESSION REGULATION; GINGIVA; HUMANS; IMMUNITY, NATURAL; INFLAMMATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PROTEASE INHIBITORS; PROTEINS;

EID: 34447293485     PISSN: 00222615     EISSN: None     Source Type: Journal    
DOI: 10.1099/jmm.0.47198-0     Document Type: Article

References (76)

1. Al-Shahrour, F., Minguez, P., Vaquerizas, J. M., Conde, L. & Dopazo, J. (2005). BABELOMICS: a suite of web tools for functional annotation and analysis of groups of genes in high-throughput experiments. Nucleic Acids Res 33, W460-W464.
2. Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S. & other authors (2000). Gene ontology: tool for the unification of biology. Nat Genet 25, 25-29.
3. Baldi, P. & Long, A. D. (2001). A Bayesian framework for the analysis of microarray expression data: regularized t-test and statistical inferences of gene changes. Bioinformatics 17, 509-519.
4. Banno, T., Gazel, A. & Blumenberg, M. (2005). Pathway-specific profiling identifies the NF-κB-dependent tumor necrosis factor α-regulated genes in epidermal keratinocytes. J Biol Chem 280, 18973-18980.
5. Boniotto, M., Jordan, W. J., Eskdale, J., Tossi, A., Antcheva, N., Crovella, S., Connell, N. D. & Gallagher, G. (2006). Human β-defensin 2 induces a vigorous cytokine response in peripheral blood mononuclear cells. Antimicrob Agents Chemother 50, 1433-1441.
6. Chung, W. O. & Dale, B. A. (2004). Innate immune response of oral and foreskin keratinocytes: utilization of different signaling pathways by various bacterial species. Infect Immun 72, 352-358.
7. Chung, W. O., Hansen, S. R., Rao, D. & Dale, B. A. (2004). Protease-activated receptor signaling increases epithelial antimicrobial peptide expression. J Immunol 173, 5165-5170.
8. Collier-Hyams, L. S. & Neish, A. S. (2005). Innate immune relationship between commensal flora and the mammalian intestinal epithelium. Cell Mol Life Sci 62, 1339-1348.
9. Curtis, M. A., Aduse-Opoku, J. & Rangarajan, M. (2001). Cysteine proteases of Porphyromonas gingivalis. Crit Rev Oral Biol Med 12, 192-216.
10. Dale, B. A., Kimball, J. R., Krisanaprakornkit, S., Roberts, F., Robinovitch, M., O'Neal, R., Valore, E. V., Ganz, T., Anderson, G. M. & Weinberg, A. (2001). Localized antimicrobial peptide expression in human gingiva. J Periodontal Res 36, 285-294.
11. Darveau, R. P., Belton, C. M., Reife, R. A. & Lamont, R. J. (1998). Local chemokine paralysis, a novel pathogenic mechanism for Porphyromonas gingivalis. Infect Immun 66, 1660-1665.
12. de Hoon, M. J., Imoto, S., Nolan, J. & Miyano, S. (2004). Open source clustering software. Bioinformatics 20, 1453-1454.
13. Doniger, S. W., Salomonis, N., Dahlquist, K. D., Vranizan, K., Lawlor, S. C. & Conklin, B. R. (2003). MAPPFinder: using Gene Ontology and GenMAPP to create a global gene-expression profile from microarray data. Genome Biol 4, R7.
14. Durr, M. & Peschel, A. (2002). Chemokines meet defensins: the merging concepts of chemoattractants and antimicrobial peptides in host defense. Infect Immun 70, 6515-6517.
15. Eisen, M. B., Spellman, P. T., Brown, P. O. & Botstein, D. (1998). Cluster analysis and display of genome-wide expression patterns. Proc Natl Acad Sci U S A 95, 14863-14868.
16. Fan, J., Heller, N. M., Gorospe, M., Atasoy, U. & Stellato, C. (2005). The role of post-transcriptional regulation in chemokine gene expression in inflammation and allergy. Eur Respir J 26, 933-947.
17. Fenno, J. C., Lee, S. Y., Bayer, C. H. & Ning, Y. (2001). The opdB locus encodes the trypsin-like peptidase activity of Treponema denticola. Infect Immun 69, 6193-6200.
18. Ferran, C., Stroka, D. M., Badrichani, A. Z., Cooper, J. T., Wrighton, C. J., Soares, M., Grey, S. T. & Bach, F. H. (1998). A20 inhibits NF-κB activation in endothelial cells without sensitizing to tumor necrosis factor-mediated apoptosis. Blood 91, 2249-2258.
19. Ganz, T. (2003). Defensins: antimicrobial peptides of innate immunity. Nat Rev Immunol 3, 710-720.
20. Gibbs, S., Fijneman, R., Wiegant, J., van Kessel, A. G., van De Putte, P. & Backendorf, C. (1993). Molecular characterization and evolution of the SPRR family of keratinocyte differentiation markers encoding small proline-rich proteins. Genomics 16, 630-637.
21. Gon, Y., Asai, Y., Hashimoto, S., Mizumura, K., Jibiki, I., Machino, T., Ra, C. & Horie, T. (2004). A20 inhibits Toll-like receptor 2- and 4-mediated interleukin-8 synthesis in airway epithelial cells. Am J Respir Cell Mol Biol 31, 330-336.
22. Greaves, D. R., Wang, W., Dairaghi, D. J., Dieu, M. C., Saint-Vis, B., Franz-Bacon, K., Rossi, D., Caux, C., McClanahan, T. & other authors (1997). CCR6, a CC chemokine receptor that interacts with macrophage inflammatory protein 3α and is highly expressed in human dendritic cells. J Exp Med 186, 837-844.
23. Handfield, M., Mans, J. J., Zheng, G., Lopez, M. C., Mao, S., Progulske-Fox, A., Narasimhan, G., Baker, H. V. & Lamont, R. J. (2005). Distinct transcriptional profiles characterize oral epithelium-microbiota interactions. Cell Microbiol 7, 811-823.
24. Harris, M. A., Clark, J., Ireland, A., Lomax, J., Ashburner, M., Foulger, R., Eilbeck, K., Lewis, S., Marshall, B. & other authors (2004). The Gene Ontology (GO) database and informatics resource. Nucleic Acids Res 32, D258-D261.
25. Hasan, L., Mazzucchelli, L., Liebi, M., Lis, M., Hunger, R. E., Tester, A., Overall, C. M. & Wolf, M. (2006). Function of liver activation-regulated chemokine/CC chemokine ligand 20 is differently affected by cathepsin B and cathepsin D processing. J Immunol 176, 6512-6522.
26. Hasegawa, Y., Mans, J. J., Mao, S., Lopez, M. C., Baker, H. V., Handfield, M. & Lamont, R. J. (2007). Gingival epithelial cell transcriptional responses to commensal and opportunistic oral microbial species. Infect Immun 75, 2540-2547.
27. Holzhausen, M., Spolidorio, L. C. & Vergnolle, N. (2005). Role of protease-activated receptor-2 in inflammation, and its possible implications as a putative mediator of periodontitis. Mem Inst Oswaldo Cruz 100 (Suppl. 1), 177-180.
28. Holzhausen, M., Spolidorio, L. C., Ellen, R. P., Jobin, M. C., Steinhoff, M., Andrade-Gordon, P. & Vergnolle, N. (2006). Protease-activated receptor-2 activation: a major role in the pathogenesis of Porphyromonas gingivalis infection. Am J Pathol 168, 1189-1199.
29. Inano, H., Kameyama, S., Yasui, S. & Nagai, A. (1998). Granulocyte colony-stimulating factor induces neutrophil sequestration in rabbit lungs. Am J Respir Cell Mol Biol 19, 167-174.
30. Irmler, M., Thome, M., Hahne, M., Schneider, P., Hofmann, K., Steiner, V., Bodmer, J. L., Schroter, M., Burns, K. & other authors (1997). Inhibition of death receptor signals by cellular FLIP. Nature 388, 190-195.
31. Ismail, A. S. & Hooper, L. V. (2005). Epithelial cells and their neighbors. IV. Bacterial contributions to intestinal epithelial barrier integrity. Am J Physiol Gastrointest Liver Physiol 289, G779-G784.
32. Jonca, N., Guerrin, M., Hadjiolova, K., Caubet, C., Gallinaro, H., Simon, M. & Serre, G. (2002). Corneodesmosin, a component of epidermal corneocyte desmosomes, displays homophilic adhesive properties. J Biol Chem 277, 5024-5029.
33. Kelly, D., Campbell, J. I., King, T. P., Grant, G., Jansson, E. A., Courts, A. G., Pettersson, S. & Conway, S. (2004). Commensal anaerobic gut bacteria attenuate inflammation by regulating nuclear-cytoplasmic shuttling of PPAR-γ and RelA. Nat Immunol 5, 104-112.
34. Kelly, D., Conway, S. & Aminov, R. (2005). Commensal gut bacteria: mechanisms of immune modulation. Trends Immunol 26, 326-333.
35. Kinane, D. F., Shiba, H., Stathopoulou, P. G., Zhao, H., Lappin, D. F., Singh, A., Eskan, M. A., Beckers, S., Waigel, S. & other authors (2006). Gingival epithelial cells heterozygous for Toll-like receptor 4 polymorphisms Asp299Gly and Thr399Ile are hypo-responsive to Porphyromonas gingivalis. Genes Immun 7, 190-200.
36. Kolenbrander, P. E. (2000). Oral microbial communities: biofilms, interactions, and genetic systems. Annu Rev Microbiol 54, 413-437.
37. Kolenbrander, P. E., Andersen, R. N., Blehert, D. S., Egland, P. G., Foster, J. S. & Palmer, R. J., Jr (2002). Communication among oral bacteria. Microbiol Mol Biol Rev 66, 486-505.
38. Krisanaprakornkit, S., Weinberg, A., Perez, C. N. & Dale, B. A. (1998). Expression of the peptide antibiotic human β-defensin 1 in cultured gingival epithelial cells and gingival tissue. Infect Immun 66, 4222-4228.
39. Krisanaprakornkit, S., Kimball, J. R., Weinberg, A., Darveau, R. P., Bainbridge, B. W. & Dale, B. A. (2000). Inducible expression of human β-defensin 2 by Fusobacterium nucleatum in oral epithelial cells: multiple signaling pathways and role of commensal bacteria in innate immunity and the epithelial barrier. Infect Immun 68, 2907-2915.
40. Krisanaprakornkit, S., Kimball, J. R. & Dale, B. A. (2002). Regulation of human β-defensin-2 in gingival epithelial cells: the involvement of mitogen-activated protein kinase pathways, but not the NF-κB transcription factor family. J Immunol 168, 316-324.
41. Lamont, R. J., Chan, A., Belton, C. M., Izutsu, K. T., Vasel, D. & Weinberg, A. (1995). Porphyromonas gingivalis invasion of gingival epithelial cells. Infect Immun 63, 3878-3885.
42. Liu, L., Wang, L., Jia, H. P., Zhao, C., Heng, H. H., Schutte, B. C., McCray, P. B., Jr & Ganz, T. (1998). Structure and mapping of the human β-defensin HBD-2 gene and its expression at sites of inflammation. Gene 222, 237-244.
43. Lourbakos, A., Potempa, J., Travis, J., D'Andrea, M. R., Andrade-Gordon, P., Santulli, R., Mackie, E. J. & Pike, R. N. (2001). Arginine-specific protease from Porphyromonas gingivalis activates protease-activated receptors on human oral epithelial cells and induces interleukin-6 secretion. Infect Immun 69, 5121-5130.
44. Lu, Q., Jin, L., Darveau, R. P. & Samaranayake, L. P. (2004). Expression of human β-defensins-1 and -2 peptides in unresolved chronic periodontitis. J Periodontal Res 39, 221-227.
45. Macpherson, A. J. & Harris, N. L. (2004). Interactions between commensal intestinal bacteria and the immune system. Nat Rev Immunol 4, 478-485.
46. Magert, H. J., Drogemuller, K. & Raghunath, M. (2005). Serine proteinase inhibitors in the skin: role in homeostasis and disease. Curr Protein Pept Sci 6, 241-254.
47. McMichael, J. W., Maxwell, A. I., Hayashi, K., Taylor, K., Wallace, W. A., Govan, J. R., Dorin, J. R. & Sallenave, J. M. (2005). Antimicrobial activity of murine lung cells against Staphylococcus aureus is increased in vitro and in vivo after elafin gene transfer. Infect Immun 73, 3609-3617.
48. Mizutani, H., Black, R. & Kupper, T. S. (1991). Human keratinocytes produce but do not process pro-interleukin-1 (IL-1) beta. Different strategies of IL-1 production and processing in monocytes and keratinocytes. J Clin Invest 87, 1066-1071.
49. Mondino, A. & Blasi, F. (2004). uPA and uPAR in fibrinolysis, immunity and pathology. Trends Immunol 25, 450-455.
50. Neish, A. S., Gewirtz, A. T., Zeng, H., Young, A. N., Hobert, M. E., Karmali, V., Rao, A. S. & Madara, J. L. (2000). Prokaryotic regulation of epithelial responses by inhibition of IκB-α ubiquitination. Science 289, 1560-1563.
51. Niyonsaba, F., Ogawa, H. & Nagaoka, I. (2004). Human β-defensin-2 functions as a chemotactic agent for tumour necrosis factor-α-treated human neutrophils. Immunology 111, 273-281.
52. Niyonsaba, F., Ushio, H., Nagaoka, I., Okumura, K. & Ogawa, H. (2005). The human β-defensins (-1, -2, -3, -4) and cathelicidin LL-37 induce IL-18 secretion through p38 and ERK MAPK activation in primary human keratinocytes. J Immunol 175, 1776-1784.
53. Ogura, Y., Bonen, D. K., Inohara, N., Nicolae, D. L., Chen, F. F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R. & other authors (2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature 411, 603-606.
54. Pfaffl, M. W. (2001). A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29, e45.
55. Qin, J., Qian, Y., Yao, J., Grace, C. & Li, X. (2005). SIGIRR inhibits interleukin-1 receptor- and Toll-like receptor 4-mediated signaling through different mechanisms. J Biol Chem 280, 25233-25241.
56. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S. & Medzhitov, R. (2004). Recognition of commensal microflora by Toll-like receptors is required for intestinal homeostasis. Cell 118, 229-241.
57. Saeed, A. I., Sharov, V., White, J., Li, J., Liang, W., Bhagabati, N., Braisted, J., Klapa, M., Currier, T. & other authors (2003). TM4: a free, open-source system for microarray data management and analysis. Biotechniques 34, 374-378.
58. Saito, T., Ishihara, K., Kato, T. & Okuda, K. (1997). Cloning, expression, and sequencing of a protease gene from Bacteroides forsythus ATCC 43037 in Escherichia coli. Infect Immun 65, 4888-4891.
59. Sallenave, J. M., Cunningham, G. A., James, R. M., McLachlan, G. & Haslett, C. (2003). Regulation of pulmonary and systemic bacterial lipopolysaccharide responses in transgenic mice expressing human elafin. Infect Immun 71, 3766-3774.
60. Sansonetti, P. J. (2004). War and peace at mucosal surfaces. Nat Rev Immunol 4, 953-964.
61. Socransky, S. S., Haffajee, A. D., Cugini, M. A., Smith, C. & Kent, R. L., Jr (1998). Microbial complexes in subgingival plaque. J Clin Periodontal 25, 134-144.
62. Strober, W., Murray, P. J., Kitani, A. & Watanabe, T. (2006). Signalling pathways and molecular interactions of NODI and NOD2. Nat Rev Immunol 6, 9-20.
63. Tien, M. T., Girardin, S. E., Regnault, B., Le Bourhis, L., Dillies, M. A., Coppee, J. Y., Bourdet-Sicard, R., Sansonetti, P. J. & Pedron, T. (2006). Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epithelial cells. J Immunol 176, 1228-1237.
64. Tonetti, M. S., Imboden, M. A. & Lang, N. P. (1998). Neutrophil migration into the gingival sulcus is associated with transepithelial gradients of interleukin-8 and ICAM-1. J Periodontal 69, 1139-1147.
65. Uehara, A., Sugawara, S., Muramoto, K. & Takada, H. (2002). Activation of human oral epithelial cells by neutrophil proteinase 3 through protease-activated receptor-2. J Immunol 169, 4594-4603.
66. van der Reijden, W. A., Bosch-Tijhof, C. J., Strooker, H. & van Winkelhoff, A. J. (2006). prtH in Tannerella forsythensis is not associated with periodontitis. J Periodontal 77, 586-590.
67. Wald, D., Qin, J., Zhao, Z., Qian, Y., Naramura, M., Tian, L., Towne, J., Sims, J. E., Stark, G. R. & Li, X. (2003). SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling. Nat Immunol 4, 920-927.
68. Wehkamp, J., Harder, J., Wehkamp, K., Wehkamp-von Meissner, B., Schlee, M., Enders, C., Sonnenborn, U., Nuding, S., Bengmark, S. & other authors (2004). NF-κB- and AP-1-mediated induction of human beta defensin-2 in intestinal epithelial cells by Escherichia coli Nissle 1917: a novel effect of a probiotic bacterium. Infect Immun 72, 5750-5758.
69. Wertz, I. E., O'Rourke, K. M., Zhou, H., Eby, M., Aravind, L., Seshagiri, S., Wu, P., Wiesmann, C., Baker, R. & other authors (2004). De-ubiquitination and ubiquitin ligase domains of A20 downregulate NF-kB signalling. Nature 430, 694-699.
70. Whitney, A. R., Diehn, M., Popper, S. J., Alizadeh, A. A., Boldrick, J. C., Relman, D. A. & Brown, P. O. (2003). Individuality and variation in gene expression patterns in human blood. Proc Natl Acad Sci U S A 100, 1896-1901.
71. Wolach, B., Gavrieli, R. & Pomeranz, A. (2000). Effect of granulocyte and granulocyte macrophage colony stimulating factors (G-CSF and GM-CSF) on neonatal neutrophil functions. Pediatr Res 48, 369-373.
72. Wright, G. W. & Simon, R. M. (2003). A random variance model for detection of differential gene expression in small microarray experiments. Bioinformatics 19, 2448-2455.
73. Yang, D., Chertov, O., Bykovskaia, S. N., Chen, Q., Buffo, M. J., Shogan, J., Anderson, M., Schroder, J. M., Wang, J. M. & other authors (1999). β-defensins: linking innate and adaptive immunity through dendritic and T cell CCR6. Science 286, 525-528.
74. Yang, D., Biragyn, A., Hoover, D. M., Lubkowski, J. & Oppenheim, J. J. (2004). Multiple roles of antimicrobial defensins, cathelicidins, and eosinophil-derived neurotoxin in host defense. Annu Rev Immunol 22, 181-215.
75. Zhou, Q. & Amar, S. (2006). Identification of proteins differentially expressed in human monocytes exposed to Porphyromonas gingivalis and its purified components by high-throughput immunoblotting. Infect Immun 74, 1204-1214.
76. Zhu, J., Nathan, C., Jin, W., Sim, D., Ashcroft, G. S., Wahl, S. M., Lacomis, L., Erdjument-Bromage, H., Tempst, P. & other authors (2002). Conversion of proepithelin to epithelins: roles of SLPI and elastase in host defense and wound repair. Cell 111, 867-878.