Skip to main content
PMC home page
Infection and Immunity logoLink to Infection and Immunity
. 1993 May;61(5):1917–1925. doi: 10.1128/iai.61.5.1917-1925.1993

Similar mechanisms of action of defined polysaccharides and lipopolysaccharides: characterization of binding and tumor necrosis factor alpha induction.

M Otterlei 1, A Sundan 1, G Skjåk-Braek 1, L Ryan 1, O Smidsrød 1, T Espevik 1
PMCID: PMC280784  PMID: 8478081

Abstract

Little has been reported about the effects of different polysaccharides on cytokine production from human monocytes. In this study, we show that several well-defined polysaccharides, including polymers with different sizes of beta 1-4-linked D-mannuronic acid (poly-M, high-M alginate, and M-blocks) and cellulose oxidized in the C-6 position, induced human monocytes to produce tumor necrosis factor alpha (TNF-alpha). Poly-M was the most efficient polysaccharide tested and, on a weight basis, was approximately as efficient as lipopolysaccharide (LPS) from Escherichia coli. TNF-alpha production was shown to depend strongly on the molecular weights of poly-M and high-M alginate, with maximal TNF-alpha production occurring at molecular weights above 50,000 and 200,000, respectively. G-blocks, alpha 1-4-linked L-guluronic acid polymers that did not induce cytokine production from monocytes, reduced the cytokine production induced by the beta 1-4-linked polyuronic acids and LPS. Furthermore, both G-blocks and LPS were found to inhibit the binding of poly-M to monocytes, as measured by flow cytometry. In addition, we found that the binding of LPS to monocytes was inhibited by G-blocks, M-blocks, and poly-M. Our results indicate that beta 1-4-linked polyuronic acids and LPS may stimulate monocytes to produce TNF-alpha by similar mechanisms and may bind to a common receptor.

Full text

PDF
1919

Selected References

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

  1. Aarden L. A., De Groot E. R., Schaap O. L., Lansdorp P. M. Production of hybridoma growth factor by human monocytes. Eur J Immunol. 1987 Oct;17(10):1411–1416. doi: 10.1002/eji.1830171004. [DOI] [PubMed] [Google Scholar]
  2. Arenzana-Seisdedos F., Virelizier J. L. Interferons as macrophage-activating factors. II. Enhanced secretion of interleukin 1 by lipopolysaccharide-stimulated human monocytes. Eur J Immunol. 1983 Jun;13(6):437–440. doi: 10.1002/eji.1830130602. [DOI] [PubMed] [Google Scholar]
  3. Atkins E. D., Mackie W., Smolko E. E. Crystalline structures of alginic acids. Nature. 1970 Feb 14;225(5233):626–628. doi: 10.1038/225626a0. [DOI] [PubMed] [Google Scholar]
  4. Brakenhoff J. P., de Groot E. R., Evers R. F., Pannekoek H., Aarden L. A. Molecular cloning and expression of hybridoma growth factor in Escherichia coli. J Immunol. 1987 Dec 15;139(12):4116–4121. [PubMed] [Google Scholar]
  5. Bøyum A. Isolation of lymphocytes, granulocytes and macrophages. Scand J Immunol. 1976 Jun;Suppl 5:9–15. [PubMed] [Google Scholar]
  6. Cavaillon J. M., Fitting C., Caroff M., Haeffner-Cavaillon N. Dissociation of cell-associated interleukin-1 (IL-1) and IL-1 release induced by lipopolysaccharide and lipid A. Infect Immun. 1989 Mar;57(3):791–797. doi: 10.1128/iai.57.3.791-797.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Chokri M., Freudenberg M., Galanos C., Poindron P., Bartholeyns J. Antitumoral effects of lipopolysaccharides, tumor necrosis factor, interferon and activated macrophages: synergism and tissue distribution. Anticancer Res. 1989 Jul-Aug;9(4):1185–1190. [PubMed] [Google Scholar]
  8. Daley L., Pier G. B., Liporace J. D., Eardley D. D. Polyclonal B cell stimulation and interleukin 1 induction by the mucoid exopolysaccharide of Pseudomonas aeruginosa associated with cystic fibrosis. J Immunol. 1985 May;134(5):3089–3093. [PubMed] [Google Scholar]
  9. Di Luzio N. R., Williams D. L., McNamee R. B., Edwards B. F., Kitahama A. Comparative tumor-inhibitory and anti-bacterial activity of soluble and particulate glucan. Int J Cancer. 1979 Dec 15;24(6):773–779. doi: 10.1002/ijc.2910240613. [DOI] [PubMed] [Google Scholar]
  10. Espevik T., Nissen-Meyer J. A highly sensitive cell line, WEHI 164 clone 13, for measuring cytotoxic factor/tumor necrosis factor from human monocytes. J Immunol Methods. 1986 Dec 4;95(1):99–105. doi: 10.1016/0022-1759(86)90322-4. [DOI] [PubMed] [Google Scholar]
  11. Espevik T., Otterlei M., Skjåk-Braek G., Ryan L., Wright S. D., Sundan A. The involvement of CD14 in stimulation of cytokine production by uronic acid polymers. Eur J Immunol. 1993 Jan;23(1):255–261. doi: 10.1002/eji.1830230140. [DOI] [PubMed] [Google Scholar]
  12. Feist W., Ulmer A. J., Musehold J., Brade H., Kusumoto S., Flad H. D. Induction of tumor necrosis factor-alpha release by lipopolysaccharide and defined lipopolysaccharide partial structures. Immunobiology. 1989 Oct;179(4-5):293–307. doi: 10.1016/S0171-2985(89)80036-1. [DOI] [PubMed] [Google Scholar]
  13. Gearing A. J., Bird C. R., Bristow A., Poole S., Thorpe R. A simple sensitive bioassay for interleukin-1 which is unresponsive to 10(3) U/ml of interleukin-2. J Immunol Methods. 1987 May 4;99(1):7–11. doi: 10.1016/0022-1759(87)90025-1. [DOI] [PubMed] [Google Scholar]
  14. Haeffner-Cavaillon N., Chaby R., Cavaillon J. M., Szabó L. Lipopolysaccharide receptor on rabbit peritoneal macrophages. I. Binding characteristics. J Immunol. 1982 May;128(5):1950–1954. [PubMed] [Google Scholar]
  15. Lebbar S., Cavaillon J. M., Caroff M., Ledur A., Brade H., Sarfati R., Haeffner-Cavaillon N. Molecular requirement for interleukin 1 induction by lipopolysaccharide-stimulated human monocytes: involvement of the heptosyl-2-keto-3-deoxyoctulosonate region. Eur J Immunol. 1986 Jan;16(1):87–91. doi: 10.1002/eji.1830160117. [DOI] [PubMed] [Google Scholar]
  16. Lei M. G., Morrison D. C. Specific endotoxic lipopolysaccharide-binding proteins on murine splenocytes. II. Membrane localization and binding characteristics. J Immunol. 1988 Aug 1;141(3):1006–1011. [PubMed] [Google Scholar]
  17. Lesley J., He Q., Miyake K., Hamann A., Hyman R., Kincade P. W. Requirements for hyaluronic acid binding by CD44: a role for the cytoplasmic domain and activation by antibody. J Exp Med. 1992 Jan 1;175(1):257–266. doi: 10.1084/jem.175.1.257. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Liabakk N. B., Nustad K., Espevik T. A rapid and sensitive immunoassay for tumor necrosis factor using magnetic monodisperse polymer particles. J Immunol Methods. 1990 Dec 5;134(2):253–259. doi: 10.1016/0022-1759(90)90387-b. [DOI] [PubMed] [Google Scholar]
  19. Loppnow H., Brade H., Dürrbaum I., Dinarello C. A., Kusumoto S., Rietschel E. T., Flad H. D. IL-1 induction-capacity of defined lipopolysaccharide partial structures. J Immunol. 1989 May 1;142(9):3229–3238. [PubMed] [Google Scholar]
  20. Matthews N. Tumour-necrosis factor from the rabbit. II. Production by monocytes. Br J Cancer. 1978 Aug;38(2):310–315. doi: 10.1038/bjc.1978.203. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Mosmann T. R., Cherwinski H., Bond M. W., Giedlin M. A., Coffman R. L. Two types of murine helper T cell clone. I. Definition according to profiles of lymphokine activities and secreted proteins. J Immunol. 1986 Apr 1;136(7):2348–2357. [PubMed] [Google Scholar]
  22. Mosmann T. Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods. 1983 Dec 16;65(1-2):55–63. doi: 10.1016/0022-1759(83)90303-4. [DOI] [PubMed] [Google Scholar]
  23. Männel D. N., Falk W. Optimal induction of tumor necrosis factor production in human monocytes requires complete S-form lipopolysaccharide. Infect Immun. 1989 Jul;57(7):1953–1958. doi: 10.1128/iai.57.7.1953-1958.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Otterlei M., Ostgaard K., Skjåk-Braek G., Smidsrød O., Soon-Shiong P., Espevik T. Induction of cytokine production from human monocytes stimulated with alginate. J Immunother (1991) 1991 Aug;10(4):286–291. doi: 10.1097/00002371-199108000-00007. [DOI] [PubMed] [Google Scholar]
  25. Parent J. B. Core-specific receptors for lipopolysaccharide on hepatocytes. Prog Clin Biol Res. 1989;286:131–144. [PubMed] [Google Scholar]
  26. Parent J. B. Membrane receptors on rat hepatocytes for the inner core region of bacterial lipopolysaccharides. J Biol Chem. 1990 Feb 25;265(6):3455–3461. [PubMed] [Google Scholar]
  27. Pier G. B., Matthews W. J., Jr, Eardley D. D. Immunochemical characterization of the mucoid exopolysaccharide of Pseudomonas aeruginosa. J Infect Dis. 1983 Mar;147(3):494–503. doi: 10.1093/infdis/147.3.494. [DOI] [PubMed] [Google Scholar]
  28. Seljelid R., Figenschau Y., Bøgwald J., Rasmussen L. T., Austgulen R. Evidence that tumor necrosis induced by aminated beta 1-3D polyglucose is mediated by a concerted action of local and systemic cytokines. Scand J Immunol. 1989 Dec;30(6):687–694. doi: 10.1111/j.1365-3083.1989.tb02477.x. [DOI] [PubMed] [Google Scholar]
  29. Simpson J. A., Smith S. E., Dean R. T. Alginate inhibition of the uptake of Pseudomonas aeruginosa by macrophages. J Gen Microbiol. 1988 Jan;134(1):29–36. doi: 10.1099/00221287-134-1-29. [DOI] [PubMed] [Google Scholar]
  30. Skjåk-Braek G., Grasdalen H., Larsen B. Monomer sequence and acetylation pattern in some bacterial alginates. Carbohydr Res. 1986 Oct 15;154:239–250. doi: 10.1016/s0008-6215(00)90036-3. [DOI] [PubMed] [Google Scholar]
  31. Wright S. D., Jong M. T. Adhesion-promoting receptors on human macrophages recognize Escherichia coli by binding to lipopolysaccharide. J Exp Med. 1986 Dec 1;164(6):1876–1888. doi: 10.1084/jem.164.6.1876. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Wright S. D., Ramos R. A., Tobias P. S., Ulevitch R. J., Mathison J. C. CD14, a receptor for complexes of lipopolysaccharide (LPS) and LPS binding protein. Science. 1990 Sep 21;249(4975):1431–1433. doi: 10.1126/science.1698311. [DOI] [PubMed] [Google Scholar]

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

RESOURCES