Cytokine-inducing components of periodontopathogenic bacteria

Journal of Periodontal Research

Volumn 31, Issue 6, 1996, Pages 393-407

  Wilson, Michael ^a   Reddi, Krisanavane ^a   Henderson, Brian ^a  

^a UNIVERSITY COLLEGE LONDON   (United Kingdom)

Author keywords

Cytokines; Fimbriae; Lipopolysaccharides; Membrane proteins; Polysaccharides; Porins

Indexed keywords

AUTACOID; CYTOKINE; LIPOPOLYSACCHARIDE; OUTER MEMBRANE PROTEIN;

ANIMAL; BIOSYNTHESIS; CHEMISTRY; FIBROBLAST; FIMBRIA; GRAM NEGATIVE BACTERIUM; GRAM POSITIVE BACTERIUM; HUMAN; IMMUNOLOGY; MACROPHAGE; METABOLISM; MICROBIOLOGY; MONOCYTE; PERIODONTITIS; REVIEW;

ANIMALS; BACTERIAL OUTER MEMBRANE PROTEINS; CYTOKINES; FIBROBLASTS; FIMBRIAE, BACTERIAL; GRAM-NEGATIVE BACTERIA; GRAM-POSITIVE BACTERIA; HUMANS; INFLAMMATION MEDIATORS; LIPOPOLYSACCHARIDES; MACROPHAGES; MONOCYTES; PERIODONTITIS;

EID: 0030207158     PISSN: 00223484     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1600-0765.1996.tb00508.x     Document Type: Article

References (117)

1. Haffajee AD, Socransky SS. Microbial etiological agents of destructive periodontal diseases. Periodontology 2000 1994; 5: 78-111.
2. Socransky SS, Haffajee AD. Microbial mechanisms in the pathogenesis of destructive periodontal diseases: a critical assessment. J Periodont Res 1991; 26: 195-212.
3. Gibbons RJ, MacDonald JB. Degradation of collagenous substrates by Bacteroides melaninogenicus. J Bacteriol 1961; 81: 614-621.
4. Tsai CC, McArthur WP, Baehni PC, Hammond BF, Taichman NS. Extraction and partial purification of a leukotoxin from a plaque-derived Gram-negative microorganism. Infect Immun 1979; 25: 427-439.
5. Kamen PR. The effects of bacterial sonicates on human keratinizing stratified squamous epithelium in vitro. J Periodont Res 1981; 16: 323-330.
6. Singer RE, Buckner BA. Butyrate and propionate: important components of toxic dental plaque extracts. Infect Immun 1981; 32: 458-463.
7. Tonzetich J, McBride J. Characterisation of volatile surphur production by pathogenic and non-pathogenic strains of oral Bacteroides. Arch Oral Biol 1981; 26: 963-969.
8. Gemmell E, Seymour GJ. Interleukin 1, interleukin 6 and transforming growth factor-β production by human gingival mononuclear cells following stimulation with Porphyromonas gingivalis and Fusobacterium nucleatum. J Periodont Res 1993; 28: 122-129.
9. Ogawa T, Uchida H, Hamada S. Porphyromonas gingivalis fimbriae and their synthetic peptides induce proinflammatory cytokines in human peripheral blood monocyte cultures. FEMS Microbiol Lett 1994; 116: 237-242.
10. Matsushita K, Nagaoka S, Arakski R, Kawabata Y, Iki K, Kawagoe M, Takada H. Immunobiological activities of a 55-kilodalton cell surface protein of Prevotella intermedia ATCC 25611. Infect Immun 1994; 62: 2459-2469.
11. Norton L, Proffit W, Moore R. In vitro bone growth inhibition in the presence of histamine and endotoxins. J Periodontol 1970; 41: 153-157.
12. Aleo JJ, DeRenzis FA, Varboncoeur A. The presence and biologic activity of cementum-bound endotoxin. J Periodontol 1974; 45: 672-675.
13. Lucas R, Cohen S, Aleo J. Histochemical study of strain L fibroblasts exposed to endotoxin - the effect on cellular organelles. J Periodontol 1979; 50: 20-22.
14. Saglie FR, Simon K, Merrill J, Koeffler HP. Lipopolysaccharide from Actinobacillus actinomycetemcomitans stimulates macrophages to produce interleukin-1 and tumor necrosis factor mRNA and protein. Oral Microbiol Immunol 1990; 5: 256-262.
15. Sismey-Durrant HJ, Hopps RM. Effect of lipopolysaccharide from Porphyromonas gingivalis on prostaglandin E2 and interleukin-1-beta release from rat periosteal and human gingival fibroblasts in vitro. Oral Microbiol Immunol 1991: 66: 378-380.
16. Tamura M, Tokuda M, Nagaoka S, Takada H. Lipopolysaccharides of Bacteroides intermedius (Prevotella intermedia) and Bacteroides (Porphyromonas) gingivalis induce interleukin-8 gene expression in human gingival fibroblast cultures. Infect Immun 1992; 60: 4932-4937.
17. Yamazaki K, Ikarashi F, Aoyagi T, Takahashi K, Nakajima T, Hara K, Seymour GJ. Direct and indirect effects of Porphyromonas gingivalis lipopolysaccharide on interleukin-6 production by human gingival fibroblasts. Oral Microbiol Immunol 1992; 7: 218-224.
18. Henderson B, Wilson M. Modulins: a new class of cytokine-inducing, proinflammatory bacterial virulence factor. Inflamm Res 1995; 44: 187-197.
19. Dinarello CA. Was the original endogenous pyrogen interleukin-1? In: Bomford R, Henderson B, eds. Interleukin-1. Inflammation and Disease. North Holland: Elsevier 1989; 17-30.
20. Meager AJ. Introduction to cytokines and their physiology. In: Henderson B, Bodmer M, eds. Therapeutic Modulation of Cytokines. Boca Raton: CRC Press, 1996; 3-36.
21. Sadlack B, Merz H, Schorle H, Schimpl A, Feller AC, Horak I. Ulcerative colitis-like disease in mice with a disrupted interleukin-1 gene. Cell 1993; 75: 253-261.
22. Kuhn R, Lohler J, Rennick D, Rajewsky K, Muller W. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993; 75: 263-274.
23. 1 gene results in multifocal inflammatory disease. Nature 1992; 359: 693-699.
24. Pettipher ER, Higgs GA, Henderson B. Interleukin-1 induces leukocyte infiltration and cartilage proteoglycan degradation in the synovial joint. Proc Natl Acad Sci USA 1986; 83: 8749-8753.
25. Henderson B, Pettipher ER. Arthitogenic actions of recombinant IL-1 and tumour necrosis factor in the rabbit; evidence for synergistic interactions between cytokines in vivo. Clin Exp Immunol 1989; 75: 306-310
26. Opal S. Interleukin-1 receptor antagonist. In: Henderson B, Bodmer M, eds. Therapeutic Modulation of Cytokines. Boca Raton: CRC Press, 1996; 197-219.
27. Henderson B, Poole S. Modulation of cytokine function: therapeutic applications. Adv Pharmacol 1994;25: 53-115.
28. Elliott MJ, Maini RN, Feldmann M, Long-Fox A, Charles P, Katsikis P. Treatment of rheumatoid arthritis with chimeric monoclonal antibodies to TNFα. Arth Rheum 1993; 36: 1681-1690.
29. Henderson B. Cytokine and proteinase inhibitors in the modulation of connective tissue destruction in rheumatoid arthritis. Clin Immunother 1994; 2: 167-174.
30. Masada MP, Persson R, Kenney JS, Lee SW, Page R, Allison AC. Measurement of interleukin-α and -1β in gingival crevicular fluids: Implications for the pathogenesis of periodontal disease. J Periodont Res 1990; 25: 156-163.
31. Rossomando EF, Kennedy JE, Hadjimichael J. Tumour necrosis factor alpha in gingival crevicuiar fluid as a possible indicator of periodontal disease in humans. Arch Oral Biol 1990; 35: 431-434.
32. Reinhardt RA, Masada MP, Kaldahl WB, et al. Gingival fluid IL-1 and IL-6 levels in refractory periodontitis. J Clin Periodontol 1993; 20: 225-231.
33. Jandinski JJ, Stashenko P, Feder LS, et al. Localization of interleukin-1 β in human periodontal tissues. J Periodontol 1991; 62: 36-43.
34. Matsuki Y, Yamamoto T, Hara K. Localization of interleukin-1 (IL-1) mRNA expressing macrophages in human inflamed gingiva and IL-1 activity in gingival crevicular fluid. J Periodont Res 1993; 28: 35-42.
35. Kjeldsen M, Holmstrup P, Bendtzen K. Marginal periodontitis and cytokines; review of the literature. J Periodontol 1993; 64: 1013-1022.
36. Tufano MA, Cipollaro de L'Ero G, Ianniello R, Galdiero M, Galdiero F. Protein A and other surface components of Staphylococcus aureus stimulate production of IL-Iα, IL-4, IL-6, TNF and IFNγ. Eur Cvtokine Netw 1991; 2: 361-366.
37. Riesenfeld-Om I, Wolpe S, Garcia-Bustos JF, Hoffmann MK, Tuomanen E. Production of interleukin-1 but not tumor necrosis factor by human monocytes stimulated with pneumococcal cell surface components. Infect Immun 1989; 57: 1890-1893.
38. Bhakdi S, Klonisch T, Nuber P, Fischer W. Stimulation of monokine production by lipoteichoic acids. Infect Immun 1991; 59: 4614-4620.
39. Standiford TJ, Arenberg DA, Danforth JM, Kunkel SL, VanOtteren GM, Stricter RM. Lipoteichoic acid induces secretion of interleukin-8 from human blood monocytes: a cellular and molecular analysis. Infect Immun 1994; 62: 119-125
40. Moreno C, Taverne J, Mehlert A, et al. Lipoarabinomannan from Mycobacterium tuberculosis induces the production of tumour necrosis factor from human and murine macrophages. Clin Exp Immunol 1988; 76: 240-245.
41. Barnes PF, Chatterjee D, Abrams JS, et al. Cytokine production induced by Mycobacterium tuberculosis lipoarabinomannan: relationship to chemical structure. J Immunol 1992; 149: 541-547.
42. Wallis RS, Paranjape R, Phillips M. Identification by two-dimensional gel electrophoresis, of a 58 kilodalton tumor necrosis factor-inducing protein of Mycobacterium tuberculosis. Infect Immun 1993; 61: 627-632.
43. Mangan DF, Wahl SM, Sultzer BM, Mergenhagen SE. Stimulation of human monocytes by endotoxin-associated protein: inhibition of programmed cell death (apotosis) and potential significance in adjuvanticity. Infect Immun 1992; 60: 1684-1686.
44. Tufano MA, Rossano F, Catalanotti P, et al. Immunobiological activities of Helicobacterpylori porins. Infect Immun 1994; 62: 1392-1399.
45. Galdiero F, Cipollaro de L'Ero G, Bendetto N, Galdiero M, Tufano MA. Release of cytokines induced by Salmonella typhimurium porins. Infect Immun 1993; 61: 155-161.
46. Tufano MA, Rossano F, Catalanotti P, et al. Properties of Yersinia enterocolitica porins: interference with biological functions of phagocytes, nitric oxide production and selective cytokine release. Inst Pasteur Res Microbiol 1994; 145: 297-307.
47. Czarny A, Witkowska D, Mulczyk M. Induction of tumor necrosis factor and interleukin-6 by outer membrane proteins of Shigella in spleen cells and macrophages of mice. Arch Immunol Ther Exp 1993; 41: 153-157.
48. Radolf JD, Norgard MV, Brandt ME, Isaacs RD, Thompson PA, Beutier B. Lipoproteins of Borrelia burgdorferi and Treponema pallidum activate cachectin/tumor necrosis factor synthesis: analysis using a CAT reporter construct. J Immunol 1991; 147: 1968-1974.
49. Timeerman CP, Matsson E, Martinez-Martinez L, et al. Induction of release of tumor necrosis factor from human monocytes by staphylococci and staphylococcal peptidoglycans. Infect Immun 161: 4167-4172.
50. Keller R, Gustafson JE, Keist R. The macrophage response to bacteria. Modulation of macrophage functional activity by peptidoglycan from Moraxella (Branhamella) catarrhalis. Clin Exp Immunol 1992; 89: 384-389.
51. Onta T, Sashida M, Fujii N. Sugawara S, Rikiishi H, Kumagai K. Induction of acute arthritis in mice by peptidoglycan derived from Gram-positive bacteria and its possible role in cytokine production. Microbiol Immunol 1993; 37: 573-582.
52. Dokter WHA, Dijkstras A. Koopmans SB, et al. G(Anh)MTetra, a natural bacterial cell wall breakdown product, induces interleukin-1β and interleukin-6 expression in human monocytes. J Biol Chem 1994; 269: 4201-4206.
53. Dokter WHA, Dijkstra AJ, Koopmans SB, et al. G(Anh)MTetra, a naturally occurring 1,6-anhydro muramyl dipeptide, induces granulocyte colony-stimulating factor expression in human monocytes: a molecular analysts. Infect Immun 1994; 62: 2953-2957.
54. Takada H, Kimura S, Hamada S. Induction of inflammatory cytokines by a soluble moiety prepared from an enzyme lysate of Actinomyces viscosus cell walls. J Med Microbiol 1993; 38: 395-400.
55. Linder H, Engberg I, Hoschutsky H, Mattsby-Baltzer I. Svanborg C. Adhesion-dependent activation of mucosal interleukin-6 production. Infect Immun 1991; 59: 4357-4362.
56. Hedges S, Svensson M, Svanborg C. Interleukin-6 response of epithelial cell lines to bacterial stimulation in vitro. Infect Immun 1992; 60: 1295-1301.
57. Mai UEH, Perez-Perez GI, Wahl LM, Wahl SM, Blaser MJ, Smith PD. Soluble surface proteins from Helicobacter pylori activate monocytes/macrophages by lipopolysaccharide-independent mechanism. J Clin Invest 1991; 87: 894-900.
58. Soell M, Holveck F, Scholler M, Wachsman D, Klein J-P, Binding of Streptococcus mutans SR protein to human monocytes: production of tumor necrosis factor, interleukin-1 and interleukin-6. Infect Immun 1994; 62: 1805-1812.
59. Bhakdi S, Mubly M, Korom S, Schmidt G. Effects of Escherichia coli hemolysin on human monocytes: cytocidal action and stimulation of interleukin-1 release. J Clin Invest 1990; 85: 1746-1753.
60. Bhakdi S, Muhly M, Korom S, Hugo F. Release of interleukin-1β associated with potent cytocidal action of staphylococcal alpha-toxin on human monocytes. Infect Immun 1989; 57: 3512-3519.
61. Houldsworth S, Andrew PW, Mitchell TJ. Pneumolysin stimulates production of tumor necrosis factor alpha and interleukin-1β by human mononuclear phagocytes. Infect Immun 1994; 62: 1501-1503.
62. Flegel WA, Muller F, Daubener W, Fischer H-G, Hadding U, Northoff H. Cytokine response by human monocytes to Clostridium difficile toxin A and toxin B. Infect Immun 1991; 59: 3659-3666.
63. Manthey CL, Vogel SN. Interactions of lipopolysaccharide with macrophages. Immunol Ser 1994; 60: 63-81.
64. Hamada S, Takada H, Ogawa T, Fujiwara T, Mihara J. Lipopolysaccharides of oral anaerobes associated with chronic inflammation: chemical and immunomodulating properties. Intern Rev Immunol 1990; 6: 247-261.
65. Fujiwara T, Nishihara T, Koga T, Hamada S. Serological properties and immunobiological activities of lipopolysaccharides from black-pigmented and related oral Bacteroides species. J Gen Microbiol 1988; 134: 2867-2876.
66. Garrison SW, Nichols FC. LPS-elicited secretory responses in monocytes: altered release of PGE2 but not IL-1 beta in patients with adult periodontitis. J Periodont Res 1989; 24: 88-95.
67. Payne JB, Peluso JF Jr, Nichols FC. Longitudinal evaluation of peripheral blood monocyte secretory function in periodontitis-resistant and periodontitis-susceptible patients. Arch Oral Biol 1993; 38: 309-317.
68. Takada H, Mihara J. Morisaki I, Hamada S. Production of cytokines by human gingival fibroblasts. In: Hamada S, Holt SC, McGhee JR, eds. Periodontal Disease; pathogens and host immune responses Quintessence Publishing Co. Tokyo, 1991; 265-276.
69. Hamada S, Koga T, Nishihara T, Fujiwara T, Okahashi N. Characterization and immunobiologic activities of lipopolysaccharides from periodontal bacteria. Adv Dent Res 1988: 2: 284-291.
70. Nishihara T, Koga T, Hamada S. Production of an interleukin-1 inhibitor by cell line P388D1 murine macrophages stimulated with Haemophilus actinomycetemcomitans lipopolysaccharide. Infect Immun 1988; 56: 2801-2807.
71. McFarlane CG, Reynolds JJ, Meikle MC. The release of interleukin-1 beta, tumor necrosis factor-alpha and interferon-gamma by cultured peripheral blood mononuclear cells from patients with periodontitis. J Periodont Res 1990; 25: 207-214
72. Lindemann RA, Miyasaki KT, Wolinsky LE. Induction of activated lymphocyte killing by bacteria associated with periodontal disease. J Dent Res 1988; 67: 846-850.
73. Reddi K, Wilson M, Poole S, Meghji S, Henderson B. Relative cytokine-stimulating activities of surface components of the periodontopathogenic bacterium Actinobacillus aclinomycetemcomitans. Cytokine 1996; 7: 534-541.
74. Okahashi N, Koga T, Nishihara T, Fujiwara T, Hamada S. Immunobiological properties of lipopolysaccharides isolated from Fusobacterium nucleatum and F. necrophorum. J Gen Microbiol 1988; 134: 1707-1715.
75. Hanazawa S, Nakada K, Ohmori Y, Miyoshi T, Amano S, Kitano S. Functional role of interleukin 1 in periodontal disease: induction of interleukin 1 production by Bacteroides gingivalis lipopolysaccharide in peritoneal macrophages from C3H/HeN and C3H/HeJ mice. Infect Immun 1985; 50: 262-270.
76. Isogai H, Isogai E, Fujii N, Oguma K, Kagota W. Takano K. Histological changes and some in vitro biological activities induced by lipopolysaccharide from Bacteroides gingivalis. Zent Bakteriol Mickrobiol Hyg Ser A 1988; 269: 64-77.
77. Bramanti TE, Wong GG, Weintraub ST, Holt SC. Chemical characterization and biologic properties of lipopolysaccharide from Bacteroides gingivalis strains W50, W83 and ATCC 33277. Oral Microbiol Immunol 1989; 4: 183-192.
78. Hernichel-Gorbach E, Kornman KS, Holt SC, et al. Host responses in patients with generalised refractory periodontitis. J Periodontol 1994; 65: 8-16.
79. Shapira L, Takashiba S, Amar S, Van Dyke TE. Porphyromonas gingivalis lipopolysaccharide stimulation of human monocytes: dependence on serum and CD14 receptor. Oral Microbiol Immunol 1994; 9: 112-117.
80. Wright SD, Ramos RA, Tobias PS, Ulevitch RJ, Mathison JC. CD14: a receptor for complexes of lipopolysaccharide and LPS binding protein. Science 1990; 249: 1431- 1433.
81. Schumann RR, Leong SR, Flaggs GW, et al. Structure and function of lipopolysaccharide binding protein. Science 1990; 249: 1429-1431.
82. Ogawa T, Uchida H, Amino K. Immunobiological activities of chemically defined lipid A from lipopolysaccharides of Porphyromonas gingivalis. Microbiology 1994; 140: 1209-1216.
83. Dinarello CA, Thompson RC. Blocking IL-1: interleukin-1 receptor antagonist in vivo and in vitro. Immunol Today 1991; 12: 404-410.
84. Hanazawa S, Kawata Y Takeshita A, et al. Expression of monocyte chemoattractant protein 1 (MCP-1) in adult periodontal disease: increased monocyte chemotactic activity in crevicular fluids and induction of MCP-1 expression in gingival tissues. Infect Immun 1993, 61: 5219-5224.
85. Christ WJ, Asano O, Robidoux ALC, et al. E5531, a pure endotoxin antagonist of high potency. Science 1995; 268: 80-83.
86. Wilson M, Moore J, Kieser JB. Identity of limulus amoebocyte lysate-active root surface materials from periodontally-involved teeth. J Clin Periodont 1986; 13: 743-747.
87. Maidwell-Smith M, Wilson M, Kieser JB. Lipopolysaccharide (endotoxin) from individual periodontally involved teeth. J Clin Periodontol 1987; 14: 453-456
88. Takahashi T, Nishihara T, Ishihara Y, et al. Mutine macrophage interleukin-1 release by capsularlike serotype-specific polysaccharide antigens of Actinobacillus actinomycetemcomitans. Infect Immun 1991; 59: 18-23.
89. Naito Y, Ohno J, Takazoe I, Okuda K. The relationship between polysaccharide antigen and interleukin-1 beta producing activity in Porphyromonas gingivalis. Bull Tokyo Dent Coll 1992; 33: 187-195.
90. Nishihara T, Koga T, Hamada S. Suppression of murine macrophage interleukin-1 release by the polysaccharide portion of Haemophilus actinomycetemcomitans lipopolysaccharide. Infect Immun 1988; 56: 619-625.
91. Hirose K. Stimulatory effects of Bacteroides gingivalis fimbriae on production of fibroblast-derived thymocyteactivating factor (FTAF) by human gingival fibroblasts. J Meikai Univ School Dent 1990; 19: 127-136.
92. Reddi K, Wilson M, Poole S, Henderson B. Comparison of the pro-inflammatory cytokine-stimulating activity of the surface-associated material of periodontopathogenic bacteria. J Periodont Res 1996; 31: 120-130.
93. Wilson M, Meghji S, Barber P, Henderson B. Biological activities of surface-associated material from Porphyromonas gingivalis. FEMS Immunol Med Microbiol 1993: 6: 147-155
94. Reddi K, Poole S, Nair S, Meghji S, Henderson B, Wilson M. Lipid A-associated proteins from periodontopathogenic bacteria induce interleukin-6 production by human gingival fibroblasts and monocytes. FEMS Immunol Med Microbiol 1995; 11: 137-144.
95. OgawaT, Kusumoto Y, Uchida H, Nagashima S, Ogo H, Hamada S. Immunobiological activities of synthetic peptide segments of fimbrial protein from Porphyromonas gingivalis. Biochem Biophys Res Comm 1991; 180: 1335-1341.
96. Murakami Y, Hanazawa S, Nishida K, Iwasaka H, Kitano S. N-acetyl-D-galactosamine inhibits TNF-alpha gene expression induced in mouse peritoneal macrophages by fimbriae of Porphyromonas (Bacteroides) gingivalis, an oral anaerobe. Biochem Biophys Res Comm 1993; 192: 826-832.
97. Hanazawa S, Murakami Y, Hirose K. Bacteroides (Porphyromonas) gingivalis fimbriae activate mouse peritoneal macrophages and induce gene expression and production of interleukin-1. Infect Immun 1991; 59: 1972-1977.
98. Kawata Y, Hanazawa S, Amano S, et al. Porphyromonas gingivalis fimbriae stimulate bone resorption in vitro. Infect Immun 1994; 62: 3012-3016.
99. Hanazawa S, Murakami Y, Takeshita A, et al. Porphyromonas gingivalis fimbriae induce expression of the neutrophil chemotactic factor KC gene of mouse peritoneal macrophages; role of protein kinase C. Infect Immun 1992 Apr; 60: 1544-1549.
100. Shenker BJ, Vitale L, Slots J. Immunosuppressive effects of Prevotella intermedia on in vitro human lymphocyte activation. Infect Immun 1991; 59: 4583-4589.
101. Kirby AC, Meghi S, Nair S, et al. The potent bone resorbing mediator of Actinobacillus actinomycetemcomitans is homologons to the molecular chaperone GroEL. J Clin Invest 1996; 96: 1185-1194.
102. White PA, Wilson M, Nair SP, Kirby AC, Reddi K, Henderson B. Characterization of an antiproliferative surface-associated protein from Actinobacillus actinomycetemcomitans which can be neutralised by sera from a proportion of patients with localised juvenile periodontitis. Infect Immun 1995; 63: 2612-2618.
103. Lindemann RA, Economou JS. Actinobacillus actinomycetemcomitans and Bacteroides gingivalis activate human peripheral monocytes to produce interleukin-1 and tumor necrosis factor. J Periodontol 1988; 59: 728-730.
104. Bom-van Noorloos A-A, van der Meer JW, van de Gevel JS, Schepens E, van Steenbergen TJ, Burger EH. Bacteroides gingivalis stimulates bone resorption via interleukin-1 production by mononuclear cells. The relative role for B. gingivalis endotoxin. J Clin Periodontol 1990; 17: 409-413.
105. Walsh LJ, Stritzel F, Yamazaki K, Bird PS, Gemmell E, Seymour GJ. Interleukin-1 and interleukin-1 inhibitor production by human adherent cells stimulated with periodontopathic bacteria. Arch Oral Biol 1989; 34: 679-683.
106. Yamazaki K, Polak B, Bird PS, Gemmell E, Hara K. Seymour GJ. Effects of periodontopathic bacteria on IL-1 and IL-1 inhibitor production by human polymorphonuclear neutrophils. Oral Microbiol Immunol 1989; 4: 193-198.
107. Ohmori Y, Hanazawa S, Amano S, Miyoshi T, Hirose K, Kitano S. Spontaneous production of thymocyte-activating factor by human gingival fibroblasts and its autoregulatory effect on their proliferation. Infect Immun 1987; 55: 947-954.
108. Woolverton CJ, Bryson CL, Redshaw PA, Paquet A. Immunomodulating activities of sodium-dodecyl-sulphate-extracted antigens from Actinobacillus actinomycetemcomitans serotype b. Microb Ecol Hlth Dis 1994; 7: 275-282.
109. Kurita-Ochiai T, Ochiai K, Ikeda T. Immunosuppressive effect induced by Actinobacillus actinomycetemcomitans: effect on immunoglobulin production and lymphokine synthesis. Oral Microbiol Immunol 1992; 7: 338-343.
110. Rossano F, Rizo A, Sanges MR, Ero GC, Tufano MA. Human monocytes and gingival fibroblasts release tumour necrosis factor-alpha, interleukin-1 alpha and interleukm-6 in response to particulate and soluble fractions of Prevotella melaninogenica and Fusobacterium nucleatum. Int J Clin Lab Res 1993; 23: 165-168.
111. Rothe J, Lesslauer W, Lotscher H, et al. Mice lacking the tumour necrosis factor receptor 1 are resistant to TNF-mediated toxicity but highly susceptible to infection by Listeria monocytogenes. Nature 1993; 364: 798-802.
112. Haziot A, Rong G-W, Silver J, Goyert SM. Recombinant soluble CD 14 mediates the activation of endothelial cells by lipopolysaccharide. J Immunol 1993; 151: 1500-1507.
113. Schutt C, Schilling T, Grunwald U, Schonfeld W, Kruger C. Endotoxin-neutralising capacity of soluble CD 14. Res Immunol 1992; 143: 71-77.
114. Watanabe K, Tanaka Y. Morimoto I, et al. Interleukin-4 as a potent inhibitor of bone resorption. Biochem Biophys Res Commun 1990; 172: 1035-1041.
115. Ruscetti FW, Dubois CM, Jacobsen SE, Keller JR. Transforming growth factor beta and interleukin-1: a paradigm for opposing regulation of haemopoiesis. Baillieres Clin Haematol 1992; 5: 703-721.
116. Ruschen C, Lemm G, Warnatz H. Spontaneous and LPS-stimulated production of intracellular IL-1 beta by synovial macrophages in rheumatoid arthritis is inhibited by IFNγ. Clin Exp Immunol 1989; 76: 246-251.
117. Page R. The role of inflammatory mediators in the pathogenesis of periodontal disease. J Periodont Res 1991; 26: 230-242.