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. 1988 Mar;56(3):619–625. doi: 10.1128/iai.56.3.619-625.1988

Suppression of murine macrophage interleukin-1 release by the polysaccharide portion of Haemophilus actinomycetemcomitans lipopolysaccharide.

T Nishihara 1, T Koga 1, S Hamada 1
PMCID: PMC259336  PMID: 3257748

Abstract

Lipopolysaccharide (LPS) was extracted from whole cells of Haemophilus actinomycetemcomitans Y4 by the hot phenol-water procedure. LPS was cleaved into its lipid A and polysaccharide moieties by hydrolysis in 1% acetic acid. The major component sugars of the polysaccharide were glucose, heptose, rhamnose, galactose, and fucose. LPS and lipid A from H. actinomycetemcomitans induced the release of interleukin-1 (IL-1) by LPS-responsive C3H/HeN murine peritoneal macrophages and cell line macrophages (P388D1 and J744.1), but not by LPS-nonresponsive C3H/HeJ peritoneal macrophages. The polysaccharide was unable to induce the release of IL-1. It suppressed the IL-1 release from LPS- and lipid A-stimulated macrophages, but not the production of cell-associated and intracellular IL-1. The addition of rhamnose, a sugar component of the polysaccharide, abrogated the inhibitory effect of the polysaccharide on IL-1 release. These results suggest the participation of a lectinlike molecule in IL-1 release.

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Selected References

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  1. Amento E. P., Kurnick J. T., Krane S. M. Interleukin 1 production by the human monocyte cell line U937 requires a lymphokine induction signal distinct from interleukin 2 or interferons. J Immunol. 1985 Jan;134(1):350–357. [PubMed] [Google Scholar]
  2. Arend W. P., Joslin F. G., Massoni R. J. Effects of immune complexes on production by human monocytes of interleukin 1 or an interleukin 1 inhibitor. J Immunol. 1985 Jun;134(6):3868–3875. [PubMed] [Google Scholar]
  3. Bakouche O., Brown D. C., Lachman L. B. Subcellular localization of human monocyte interleukin 1: evidence for an inactive precursor molecule and a possible mechanism for IL 1 release. J Immunol. 1987 Jun 15;138(12):4249–4255. [PubMed] [Google Scholar]
  4. Barker K. A., Holt S. C. The in vitro effect of Actinobacillus actinomycetemcomitans strain Y4 lipopolysaccharide on murine peritoneal macrophages. Can J Microbiol. 1983 Nov;29(11):1552–1563. doi: 10.1139/m83-238. [DOI] [PubMed] [Google Scholar]
  5. Berman M. A., Sandborg C. I., Calabia B. S., Andrews B. S., Friou G. J. Interleukin 1 inhibitor masks high interleukin 1 production in acquired immunodeficiency syndrome (AIDS). Clin Immunol Immunopathol. 1987 Jan;42(1):133–140. doi: 10.1016/0090-1229(87)90180-2. [DOI] [PubMed] [Google Scholar]
  6. Brown K. M., Muchmore A. V., Rosenstreich D. L. Uromodulin, an immunosuppressive protein derived from pregnancy urine, is an inhibitor of interleukin 1. Proc Natl Acad Sci U S A. 1986 Dec;83(23):9119–9123. doi: 10.1073/pnas.83.23.9119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Dewhirst F. E., Stashenko P. P., Mole J. E., Tsurumachi T. Purification and partial sequence of human osteoclast-activating factor: identity with interleukin 1 beta. J Immunol. 1985 Oct;135(4):2562–2568. [PubMed] [Google Scholar]
  8. Dinarello C. A. Interleukin-1. Rev Infect Dis. 1984 Jan-Feb;6(1):51–95. doi: 10.1093/clinids/6.1.51. [DOI] [PubMed] [Google Scholar]
  9. Fujiwara H., Ellner J. J. Spontaneous production of a suppressor factor by the human macrophage-like cell line U937. I. Suppression of interleukin 1, interleukin 2, and mitogen-induced blastogenesis in mouse thymocytes. J Immunol. 1986 Jan;136(1):181–185. [PubMed] [Google Scholar]
  10. Giri J. G., Lomedico P. T., Mizel S. B. Studies on the synthesis and secretion of interleukin 1. I. A 33,000 molecular weight precursor for interleukin 1. J Immunol. 1985 Jan;134(1):343–349. [PubMed] [Google Scholar]
  11. Gowen M., Wood D. D., Ihrie E. J., McGuire M. K., Russell R. G. An interleukin 1 like factor stimulates bone resorption in vitro. Nature. 1983 Nov 24;306(5941):378–380. doi: 10.1038/306378a0. [DOI] [PubMed] [Google Scholar]
  12. Haeffner-Cavaillon N., Cavaillon J. M., Moreau M., Szabó L. Interleukin 1 secretion by human monocytes stimulated by the isolated polysaccharide region of the Bordetella pertussis endotoxin. Mol Immunol. 1984 May;21(5):389–395. doi: 10.1016/0161-5890(84)90036-1. [DOI] [PubMed] [Google Scholar]
  13. Harvey W., Kamin S., Meghji S., Wilson M. Interleukin-1-like activity in capsular material from Haemophilus actinomycetemcomitans. Immunology. 1987 Mar;60(3):415–418. [PMC free article] [PubMed] [Google Scholar]
  14. Holt S. C., Tanner A. C., Socransky S. S. Morphology and ultrastructure of oral strains of Actinobacillus actinomycetemcomitans and Haemophilus aphrophilus. Infect Immun. 1980 Nov;30(2):588–600. doi: 10.1128/iai.30.2.588-600.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Iino Y., Hopps R. M. The bone-resorbing activities in tissue culture of lipopolysaccharides from the bacteria Actinobacillus actinomycetemcomitans, Bacteroides gingivalis and Capnocytophaga ochracea isolated from human mouths. Arch Oral Biol. 1984;29(1):59–63. doi: 10.1016/0003-9969(84)90043-8. [DOI] [PubMed] [Google Scholar]
  16. Kamin S., Harvey W., Wilson M., Scutt A. Inhibition of fibroblast proliferation and collagen synthesis by capsular material from Actinobacillus actinomycetemcomitans. J Med Microbiol. 1986 Nov;22(3):245–249. doi: 10.1099/00222615-22-3-245. [DOI] [PubMed] [Google Scholar]
  17. Kemp A., Mellow L., Sabbadini E. Inhibition of interleukin 1 activity by a factor in submandibular glands of rats. J Immunol. 1986 Oct 1;137(7):2245–2251. [PubMed] [Google Scholar]
  18. Kiley P., Holt S. C. Characterization of the lipopolysaccharide from Actinobacillus actinomycetemcomitans Y4 and N27. Infect Immun. 1980 Dec;30(3):862–873. doi: 10.1128/iai.30.3.862-873.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Knudsen P. J., Dinarello C. A., Strom T. B. Prostaglandins posttranscriptionally inhibit monocyte expression of interleukin 1 activity by increasing intracellular cyclic adenosine monophosphate. J Immunol. 1986 Nov 15;137(10):3189–3194. [PubMed] [Google Scholar]
  20. Koga T., Nishihara T., Fujiwara T., Nisizawa T., Okahashi N., Noguchi T., Hamada S. Biochemical and immunobiological properties of lipopolysaccharide (LPS) from Bacteroides gingivalis and comparison with LPS from Escherichia coli. Infect Immun. 1985 Mar;47(3):638–647. doi: 10.1128/iai.47.3.638-647.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Koga T., Odaka C., Moro I., Fujiwara T., Nishihara T., Okahashi N., Hamada S. Local Shwartzman activity of lipopolysaccharides from several selected strains of suspected periodontopathic bacteria. J Periodontal Res. 1987 Mar;22(2):103–107. doi: 10.1111/j.1600-0765.1987.tb01547.x. [DOI] [PubMed] [Google Scholar]
  22. Korn J. H., Brown K. M., Downie E., Liao Z. H., Rosenstreich D. L. Augmentation of IL 1-induced fibroblast PGE2 production by a urine-derived IL 1 inhibitor. J Immunol. 1987 May 15;138(10):3290–3294. [PubMed] [Google Scholar]
  23. Kunkel S. L., Chensue S. W., Phan S. H. Prostaglandins as endogenous mediators of interleukin 1 production. J Immunol. 1986 Jan;136(1):186–192. [PubMed] [Google Scholar]
  24. Kurt-Jones E. A., Beller D. I., Mizel S. B., Unanue E. R. Identification of a membrane-associated interleukin 1 in macrophages. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1204–1208. doi: 10.1073/pnas.82.4.1204. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Lotz M., Tsoukas C. D., Fong S., Dinarello C. A., Carson D. A., Vaughan J. H. Release of lymphokines after infection with Epstein Barr virus in vitro. II. A monocyte-dependent inhibitor of interleukin 1 downregulates the production of interleukin 2 and interferon-gamma in rheumatoid arthritis. J Immunol. 1986 May 15;136(10):3643–3648. [PubMed] [Google Scholar]
  26. Mandell R. L. A longitudinal microbiological investigation of Actinobacillus actinomycetemcomitans and Eikenella corrodens in juvenile periodontitis. Infect Immun. 1984 Sep;45(3):778–780. doi: 10.1128/iai.45.3.778-780.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Mandell R. L., Socransky S. S. A selective medium for Actinobacillus actinomycetemcomitans and the incidence of the organism in juvenile periodontitis. J Periodontol. 1981 Oct;52(10):593–598. doi: 10.1902/jop.1981.52.10.593. [DOI] [PubMed] [Google Scholar]
  28. Matsushima K., Taguchi M., Kovacs E. J., Young H. A., Oppenheim J. J. Intracellular localization of human monocyte associated interleukin 1 (IL 1) activity and release of biologically active IL 1 from monocytes by trypsin and plasmin. J Immunol. 1986 Apr 15;136(8):2883–2891. [PubMed] [Google Scholar]
  29. Mizel S. B., Mizel D. Purification to apparent homogeneity of murine interleukin 1. J Immunol. 1981 Mar;126(3):834–837. [PubMed] [Google Scholar]
  30. Mizel S. B. Physicochemical characterization of lymphocyte-activating factor (LAF). J Immunol. 1979 Jun;122(6):2167–2172. [PubMed] [Google Scholar]
  31. Nishihara T., Fujiwara T., Koga T., Hamada S. Chemical composition and immunobiological properties of lipopolysaccharide and lipid-associated proteoglycan from Actinobacillus actinomycetemcomitans. J Periodontal Res. 1986 Sep;21(5):521–530. doi: 10.1111/j.1600-0765.1986.tb01488.x. [DOI] [PubMed] [Google Scholar]
  32. Nishihara T., Koga T., Hamada S. Extracellular proteinaceous substances from Haemophilus actinomycetemcomitans induce mitogenic responses in murine lymphocytes. Oral Microbiol Immunol. 1987 Mar;2(1):48–52. doi: 10.1111/j.1399-302x.1987.tb00269.x. [DOI] [PubMed] [Google Scholar]
  33. Oppenheim J. J., Togawa A., Chedid L., Mizel S. Components of mycobacteria and muramyl dipeptide with adjuvant activity induce lymphocyte activating factor. Cell Immunol. 1980 Mar 1;50(1):71–81. doi: 10.1016/0008-8749(80)90007-6. [DOI] [PubMed] [Google Scholar]
  34. Sato K., Fujii Y., Asano S., Ohtsuki T., Kawakami M., Kasono K., Tsushima T., Shizume K. Recombinant human interleukin 1 alpha and beta stimulate mouse osteoblast-like cells (MC3T3-E1) to produce macrophage-colony stimulating activity and prostaglandin E2. Biochem Biophys Res Commun. 1986 Nov 26;141(1):285–291. doi: 10.1016/s0006-291x(86)80366-7. [DOI] [PubMed] [Google Scholar]
  35. Scala G., Kuang Y. D., Hall R. E., Muchmore A. V., Oppenheim J. J. Accessory cell function of human B cells. I. Production of both interleukin 1-like activity and an interleukin 1 inhibitory factor by an EBV-transformed human B cell line. J Exp Med. 1984 Jun 1;159(6):1637–1652. doi: 10.1084/jem.159.6.1637. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. 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]
  37. Slots J., Reynolds H. S., Genco R. J. Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun. 1980 Sep;29(3):1013–1020. doi: 10.1128/iai.29.3.1013-1020.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Sveen K., Skaug N. Bone resorption stimulated by lipopolysaccharides from Bacteroides, Fusobacterium and Veillonella, and by the lipid A and the polysaccharide part of Fusobacterium lipopolysaccharide. Scand J Dent Res. 1980 Dec;88(6):535–542. doi: 10.1111/j.1600-0722.1980.tb01264.x. [DOI] [PubMed] [Google Scholar]
  39. Tiku K., Tiku M. L., Liu S., Skosey J. L. Normal human neutrophils are a source of a specific interleukin 1 inhibitor. J Immunol. 1986 May 15;136(10):3686–3692. [PubMed] [Google Scholar]
  40. Wilson M., Kamin S., Harvey W. Bone resorbing activity of purified capsular material from Actinobacillus actinomycetemcomitans. J Periodontal Res. 1985 Sep;20(5):484–491. doi: 10.1111/j.1600-0765.1985.tb00831.x. [DOI] [PubMed] [Google Scholar]

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