Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1988 Aug;56(8):2149–2155. doi: 10.1128/iai.56.8.2149-2155.1988

Effect of lipopolysaccharide on proteoglycan synthesis by adult human gingival fibroblasts in vitro.

P M Bartold 1, S J Millar 1
PMCID: PMC259537  PMID: 3165085

Abstract

The effect of lipopolysaccharide preparations from Salmonella enteritidis, Bacteroides gingivalis, and Actinobacillus actinomycetemcomitans on human gingival fibroblasts was studied. Lipopolysaccharide from all sources inhibited fibroblast proliferation in the concentration range of 0.5 to 50 micrograms/ml, with the lipopolysaccharide from A. actinomycetemcomitans having the strongest inhibitory effect. Assessment of the effect of lipopolysaccharide on gingival fibroblast metabolism indicated both total protein and proteoglycan synthesis to be inhibited with increasing concentrations of lipopolysaccharide. As for the antiproliferative effect, lipopolysaccharide from A. actinomycetemcomitans had the greatest inhibitory effect on cell synthetic activity. This inhibitory effect was determined by pulse-chase experiments to be a true depression in synthesis. Furthermore, the effect was independent of lipopolysaccharide-induced changes in cell proliferation and prostaglandin synthesis. This study confirmed the toxic effect of lipopolysaccharide on fibroblasts and, in particular, indicated that various lipopolysaccharide preparations vary in their potency to influence cell proliferation and extracellular matrix synthesis.

Full text

PDF
2149

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aleo J. J., De Renzis F. A., Farber P. A. In vitro attachment of human gingival fibroblasts to root surfaces. J Periodontol. 1975 Nov;46(11):639–645. doi: 10.1902/jop.1975.46.11.639. [DOI] [PubMed] [Google Scholar]
  2. Aleo J. J., De Renzis F. A., Farber P. A., Varboncoeur A. P. The presence and biologic activity of cementum-bound endotoxin. J Periodontol. 1974 Sep;45(9):672–675. doi: 10.1902/jop.1974.45.9.672. [DOI] [PubMed] [Google Scholar]
  3. Aleo J. J. Stimulation of macromolecular synthesis by endotoxin-treated 3T6 fibroblasts. Experientia. 1980 May 15;36(5):546–547. doi: 10.1007/BF01965790. [DOI] [PubMed] [Google Scholar]
  4. Bartold P. M., Boyd R. R., Page R. C. Proteoglycans synthesized by gingival fibroblasts derived from human donors of different ages. J Cell Physiol. 1986 Jan;126(1):37–46. doi: 10.1002/jcp.1041260106. [DOI] [PubMed] [Google Scholar]
  5. Bartold P. M., Page R. C. Isolation and characterization of proteoglycans synthesized by adult human gingival fibroblasts in vitro. Arch Biochem Biophys. 1987 Mar;253(2):399–412. doi: 10.1016/0003-9861(87)90193-7. [DOI] [PubMed] [Google Scholar]
  6. Bartold P. M., Page R. C. Proteoglycans synthesized by cultured fibroblasts derived from normal and inflamed human gingiva. In Vitro Cell Dev Biol. 1986 Jul;22(7):407–417. doi: 10.1007/BF02623531. [DOI] [PubMed] [Google Scholar]
  7. Bartold P. M., Wiebkin O. W., Thonard J. C. The active role of gingival proteoglycans in periodontal disease. Med Hypotheses. 1983 Dec;12(4):377–387. doi: 10.1016/0306-9877(83)90109-3. [DOI] [PubMed] [Google Scholar]
  8. Bordin S., Page R. C., Narayanan A. S. Heterogeneity of normal human diploid fibroblasts: isolation and characterization of one phenotype. Science. 1984 Jan 13;223(4632):171–173. doi: 10.1126/science.6691142. [DOI] [PubMed] [Google Scholar]
  9. Buckingham R. B., Castor C. W. The effect of bacterial products on synovial fibroblast function: hypermetabolic changes induced by endotoxin. J Clin Invest. 1972 May;51(5):1186–1194. doi: 10.1172/JCI106912. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Carroll G. J. Porcine catabolin stimulates prostaglandin E2 secretion but does not affect intracellular cyclic AMP production in pig synovial fibroblasts. Ann Rheum Dis. 1985 Sep;44(9):631–636. doi: 10.1136/ard.44.9.631. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Daly C. G., Seymour G. J., Kieser J. B. Bacterial endotoxin: a role in chronic inflammatory periodontal disease? J Oral Pathol. 1980 Jan;9(1):1–15. doi: 10.1111/j.1600-0714.1980.tb01383.x. [DOI] [PubMed] [Google Scholar]
  12. Engel D., Schroeder H. E., Page R. C. Morphological features and functional properties of human fibroblasts exposed to Actinomyces viscosus substances. Infect Immun. 1978 Jan;19(1):287–295. doi: 10.1128/iai.19.1.287-295.1978. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Genco R. J., Slots J. Host responses in periodontal diseases. J Dent Res. 1984 Mar;63(3):441–451. doi: 10.1177/00220345840630031601. [DOI] [PubMed] [Google Scholar]
  14. 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 Oct;50(1):262–270. doi: 10.1128/iai.50.1.262-270.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Hausmann E., Raisz L. G., Miller W. A. Endotoxin: stimulation of bone resorption in tissue culture. Science. 1970 May 15;168(3933):862–864. doi: 10.1126/science.168.3933.862. [DOI] [PubMed] [Google Scholar]
  16. LAGUNOFF D., WARREN G. Determination of 2-deoxy-2-sulfoaminohexose content of mucopolysaccharides. Arch Biochem Biophys. 1962 Dec;99:396–400. doi: 10.1016/0003-9861(62)90285-0. [DOI] [PubMed] [Google Scholar]
  17. Larjava H., Jalkanen M., Penttinen R., Paunio K. Enhanced synthesis of hyaluronic acid by human gingival fibroblasts exposed to human dental bacterial extract. J Periodontal Res. 1983 Jan;18(1):31–39. doi: 10.1111/j.1600-0765.1983.tb00332.x. [DOI] [PubMed] [Google Scholar]
  18. Larjava H. Metabolic change in cultured gingival fibroblasts exposed to bacterial extracts. Stimulation of hyaluronic acid synthesis. J Periodontal Res. 1984 May;19(3):230–237. doi: 10.1111/j.1600-0765.1984.tb00814.x. [DOI] [PubMed] [Google Scholar]
  19. Larjava H., Uitto V. J., Eerola E., Haapasalo M. Inhibition of gingival fibroblast growth by Bacteroides gingivalis. Infect Immun. 1987 Jan;55(1):201–205. doi: 10.1128/iai.55.1.201-205.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Lark M. W., Laterra J., Culp L. A. Close and focal contact adhesions of fibroblasts to a fibronectin-containing matrix. Fed Proc. 1985 Feb;44(2):394–403. [PubMed] [Google Scholar]
  21. Lucas R. M., Subramoniam A., Aleo J. J. Intracellular localization of bacterial lipopolysaccharide using the avidin biotin complex method at the electron microscopic level. J Periodontol. 1985 Sep;56(9):553–557. doi: 10.1902/jop.1985.56.9.553. [DOI] [PubMed] [Google Scholar]
  22. Millar S. J., Goldstein E. G., Levine M. J., Hausmann E. Modulation of bone metabolism by two chemically distinct lipopolysaccharide fractions from Bacteroides gingivalis. Infect Immun. 1986 Jan;51(1):302–306. doi: 10.1128/iai.51.1.302-306.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Morales T. I., Wahl L. M., Hascall V. C. The effect of bacterial lipopolysaccharides on the biosynthesis and release of proteoglycans from calf articular cartilage cultures. J Biol Chem. 1984 Jun 10;259(11):6720–6729. [PubMed] [Google Scholar]
  24. Narayanan A. S., Page R. C. Biochemical characterization of collagens synthesized by fibroblasts derived from normal and diseased human gingiva. J Biol Chem. 1976 Sep 25;251(18):5464–5471. [PubMed] [Google Scholar]
  25. Narayanan A. S., Page R. C., Kuzan F. Collagens synthesized in vitro by diploid fibroblasts obtained from chronically inflamed human connective tissue. Lab Invest. 1978 Jul;39(1):61–65. [PubMed] [Google Scholar]
  26. Pitaru S., Soldinger M., Madgar D., Metzger Z. Bacterial endotoxin inhibits migration, attachment, and orientation of human gingival fibroblasts in vitro and delays collagen gel contraction. J Dent Res. 1987 Sep;66(9):1449–1455. doi: 10.1177/00220345870660090801. [DOI] [PubMed] [Google Scholar]
  27. ROE J. H. The determination of sugar in blood and spinal fluid with anthrone reagent. J Biol Chem. 1955 Jan;212(1):335–343. [PubMed] [Google Scholar]
  28. Saito H., Yamagata T., Suzuki S. Enzymatic methods for the determination of small quantities of isomeric chondroitin sulfates. J Biol Chem. 1968 Apr 10;243(7):1536–1542. [PubMed] [Google Scholar]
  29. Scannapieco F. A., Millar S. J., Reynolds H. S., Zambon J. J., Levine M. J. Effect of anaerobiosis on the surface ultrastructure and surface proteins of Actinobacillus actinomycetemcomitans (Haemophilus actinomycetemcomitans). Infect Immun. 1987 Sep;55(9):2320–2323. doi: 10.1128/iai.55.9.2320-2323.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Schmidt J. A., Mizel S. B., Cohen D., Green I. Interleukin 1, a potential regulator of fibroblast proliferation. J Immunol. 1982 May;128(5):2177–2182. [PubMed] [Google Scholar]
  31. Seppä H., Grotendorst G., Seppä S., Schiffmann E., Martin G. R. Platelet-derived growth factor in chemotactic for fibroblasts. J Cell Biol. 1982 Feb;92(2):584–588. doi: 10.1083/jcb.92.2.584. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Slots J., Genco R. J. Black-pigmented Bacteroides species, Capnocytophaga species, and Actinobacillus actinomycetemcomitans in human periodontal disease: virulence factors in colonization, survival, and tissue destruction. J Dent Res. 1984 Mar;63(3):412–421. doi: 10.1177/00220345840630031101. [DOI] [PubMed] [Google Scholar]
  33. Smith G. L. Synergistic action of bacterial lipopolysaccharides on serum-stimulated DNA synthesis in mouse embryo fibroblasts. Proc Soc Exp Biol Med. 1976 Oct;153(1):187–192. doi: 10.3181/00379727-153-39507. [DOI] [PubMed] [Google Scholar]
  34. Stevens R. H., Gatewood C., Hammond B. F. Cytotoxicity of the bacterium Actinobacillus actinomycetemcomitans extracts in human gingival fibroblasts. Arch Oral Biol. 1983;28(11):981–987. doi: 10.1016/0003-9969(83)90051-1. [DOI] [PubMed] [Google Scholar]
  35. Stevens R. H., Sela M. N., Shapira J., Hammond B. F. Detection of a fibroblast proliferation inhibitory factor from Capnocytophaga sputigena. Infect Immun. 1980 Jan;27(1):271–275. doi: 10.1128/iai.27.1.271-275.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Vaheri A., Ruoslahti E., Sarvas M., Nurminen M. Mitogenic effect by lipopolysaccharide and pokeweed lectin on density-inhibited chick embryo fibroblasts. J Exp Med. 1973 Dec 1;138(6):1356–1364. doi: 10.1084/jem.138.6.1356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wilson M. E. Effects of bacterial endotoxins on neutrophil function. Rev Infect Dis. 1985 May-Jun;7(3):404–418. doi: 10.1093/clinids/7.3.404. [DOI] [PubMed] [Google Scholar]
  38. Yanagishita M., Hascall V. C. Biosynthesis of proteoglycans by rat granulosa cells cultured in vitro. J Biol Chem. 1979 Dec 25;254(24):12355–12364. [PubMed] [Google Scholar]

Articles from Infection and Immunity are provided here courtesy of American Society for Microbiology (ASM)

RESOURCES