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. 1996 Nov;64(11):4450–4455. doi: 10.1128/iai.64.11.4450-4455.1996

Monocyte chemoattractant protein 1 and interleukin-8 production in mononuclear cells stimulated by oral microorganisms.

Y Jiang 1, T R Russell 1, D T Graves 1, H Cheng 1, S H Nong 1, S M Levitz 1
PMCID: PMC174397  PMID: 8890191

Abstract

Chemokines are a family of low-molecular-weight proinflammatory cytokines that stimulate recruitment of leukocytes. The chemokines interleukin-8 (IL-8) and monocyte chemoattractant protein 1 (MCP-1) are relatively specific chemoattractants for neutrophils and monocytes, respectively. Chemokine expression contributes to the presence of different leukocyte populations observed in normal and pathologic states. In the present studies, peripheral blood mononuclear cells (PBMC) were stimulated by microbes (Candida albicans, Streptococcus mutans, Porphyromonas gingivalis, and Actinobacillus actinomycetemcomitans) selected based upon their importance as oral pathogens. IL-8 and MCP-1 gene expression and protein release were determined by Northern blot (RNA blot) analysis and enzyme-linked immunosorbent assay. C. albicans, P. gingivalis, and A. actinomycetemcomitans induced high levels of production of both MCP-1 and IL-8. S. mutans was a strong inducer of MCP-1, but it did not stimulate significant production of IL-8. C. albicans, S. mutans, and A. actinomycetemcomitans were 500 to 5,000 times more potent than P. gingivalis in terms of MCP-1 production. In general, the microbe-to-PBMC ratios required for maximum gene expression of MCP-1 were lower than those for IL-8. However, for actual protein release of MCP-1 versus IL-8, differences in the effects of various microbe concentrations were observed only for A. actinomycetemcomitans. These results demonstrate that different oral pathogens induce specific dose-dependent patterns of chemokine gene expression and release. Such patterns may help explain the immunopathology of oral infections, particularly with regard to inflammatory leukocyte recruitment.

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Selected References

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  1. Colotta F., Borré A., Wang J. M., Tattanelli M., Maddalena F., Polentarutti N., Peri G., Mantovani A. Expression of a monocyte chemotactic cytokine by human mononuclear phagocytes. J Immunol. 1992 Feb 1;148(3):760–765. [PubMed] [Google Scholar]
  2. Gesser B., Deleuran B., Lund M., Vestergård C., Lohse N., Deleuran M., Jensen S. L., Pedersen S. S., Thestrup-Pedersen K., Larsen C. G. Interleukin-8 induces its own production in CD4+ T lymphocytes: a process regulated by interleukin 10. Biochem Biophys Res Commun. 1995 May 25;210(3):660–669. doi: 10.1006/bbrc.1995.1711. [DOI] [PubMed] [Google Scholar]
  3. Graves D. T., Jiang Y. Chemokines, a family of chemotactic cytokines. Crit Rev Oral Biol Med. 1995;6(2):109–118. doi: 10.1177/10454411950060020101. [DOI] [PubMed] [Google Scholar]
  4. Haapasalo M. Black-pigmented gram-negative anaerobes in endodontic infections. FEMS Immunol Med Microbiol. 1993 Mar;6(2-3):213–217. doi: 10.1111/j.1574-695X.1993.tb00329.x. [DOI] [PubMed] [Google Scholar]
  5. Hanazawa S., Kawata Y., Takeshita A., Kumada H., Okithu M., Tanaka S., Yamamoto Y., Masuda T., Umemoto T., Kitano S. 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 Dec;61(12):5219–5224. doi: 10.1128/iai.61.12.5219-5224.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Jun K. C., Barua P. K., Zambon J. J., Neiders M. E. Proteolytic activity in black-pigmented bacteroides species. J Endod. 1989 Oct;15(10):463–467. doi: 10.1016/s0099-2399(89)80025-1. [DOI] [PubMed] [Google Scholar]
  7. Leonard E. J., Skeel A., Yoshimura T., Rankin J. Secretion of monocyte chemoattractant protein-1 (MCP-1) by human mononuclear phagocytes. Adv Exp Med Biol. 1993;351:55–64. doi: 10.1007/978-1-4615-2952-1_7. [DOI] [PubMed] [Google Scholar]
  8. Levitz S. M., Tabuni A., Nong S. H., Golenbock D. T. Effects of interleukin-10 on human peripheral blood mononuclear cell responses to Cryptococcus neoformans, Candida albicans, and lipopolysaccharide. Infect Immun. 1996 Mar;64(3):945–951. doi: 10.1128/iai.64.3.945-951.1996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Liebler J. M., Kunkel S. L., Burdick M. D., Standiford T. J., Rolfe M. W., Strieter R. M. Production of IL-8 and monocyte chemotactic peptide-1 by peripheral blood monocytes. Disparate responses to phytohemagglutinin and lipopolysaccharide. J Immunol. 1994 Jan 1;152(1):241–249. [PubMed] [Google Scholar]
  10. Martich G. D., Danner R. L., Ceska M., Suffredini A. F. Detection of interleukin 8 and tumor necrosis factor in normal humans after intravenous endotoxin: the effect of antiinflammatory agents. J Exp Med. 1991 Apr 1;173(4):1021–1024. doi: 10.1084/jem.173.4.1021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Paterson R. C., Watts A. Pulp responses to two strains of bacteria isolated from human carious dentine (L. plantarum) (NCTC 1406) and S. mutans (NCTC 10919). Int Endod J. 1992 May;25(3):134–141. doi: 10.1111/j.1365-2591.1992.tb00776.x. [DOI] [PubMed] [Google Scholar]
  12. Rahimi P., Wang C. Y., Stashenko P., Lee S. K., Lorenzo J. A., Graves D. T. Monocyte chemoattractant protein-1 expression and monocyte recruitment in osseous inflammation in the mouse. Endocrinology. 1995 Jun;136(6):2752–2759. doi: 10.1210/endo.136.6.7750500. [DOI] [PubMed] [Google Scholar]
  13. Shapira L., Takashiba S., Amar S., Van Dyke T. E. Porphyromonas gingivalis lipopolysaccharide stimulation of human monocytes: dependence on serum and CD14 receptor. Oral Microbiol Immunol. 1994 Apr;9(2):112–117. doi: 10.1111/j.1399-302x.1994.tb00044.x. [DOI] [PubMed] [Google Scholar]
  14. Stabholz A., Sela M. N. The role of oral microorganisms in the pathogenesis of periapical pathosis. I. Effect of Streptococcus mutans and its cellular constituents on the dental pulp and periapical tissue of cats. J Endod. 1983 May;9(5):171–175. doi: 10.1016/S0099-2399(83)80089-2. [DOI] [PubMed] [Google Scholar]
  15. Strieter R. M., Chensue S. W., Standiford T. J., Basha M. A., Showell H. J., Kunkel S. L. Disparate gene expression of chemotactic cytokines by human mononuclear phagocytes. Biochem Biophys Res Commun. 1990 Jan 30;166(2):886–891. doi: 10.1016/0006-291x(90)90893-r. [DOI] [PubMed] [Google Scholar]
  16. Sylvester I., Rankin J. A., Yoshimura T., Tanaka S., Leonard E. J. Secretion of neutrophil attractant/activation protein by lipopolysaccharide-stimulated lung macrophages determined by both enzyme-linked immunosorbent assay and N-terminal sequence analysis. Am Rev Respir Dis. 1990 Mar;141(3):683–688. doi: 10.1164/ajrccm/141.3.683. [DOI] [PubMed] [Google Scholar]
  17. 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 Nov;60(11):4932–4937. doi: 10.1128/iai.60.11.4932-4937.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Tanner A., Stillman N. Oral and dental infections with anaerobic bacteria: clinical features, predominant pathogens, and treatment. Clin Infect Dis. 1993 Jun;16 (Suppl 4):S304–S309. doi: 10.1093/clinids/16.supplement_4.s304. [DOI] [PubMed] [Google Scholar]
  19. Tonetti M. S., Imboden M. A., Gerber L., Lang N. P., Laissue J., Mueller C. Localized expression of mRNA for phagocyte-specific chemotactic cytokines in human periodontal infections. Infect Immun. 1994 Sep;62(9):4005–4014. doi: 10.1128/iai.62.9.4005-4014.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Tsai C. C., McArthur W. P., Baehni P. C., Hammond B. F., Taichman N. S. Extraction and partial characterization of a leukotoxin from a plaque-derived Gram-negative microorganism. Infect Immun. 1979 Jul;25(1):427–439. doi: 10.1128/iai.25.1.427-439.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Van Dyke T. E., Bartholomew E., Genco R. J., Slots J., Levine M. J. Inhibition of neutrophil chemotaxis by soluble bacterial products. J Periodontol. 1982 Aug;53(8):502–508. doi: 10.1902/jop.1982.53.8.502. [DOI] [PubMed] [Google Scholar]
  22. Yamaguchi N., Kawasaki M., Yamashita Y., Nakashima K., Koga T. Role of the capsular polysaccharide-like serotype-specific antigen in resistance of Actinobacillus actinomycetemcomitans to phagocytosis by human polymorphonuclear leukocytes. Infect Immun. 1995 Dec;63(12):4589–4594. doi: 10.1128/iai.63.12.4589-4594.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Yoshimura T., Takeya M., Takahashi K., Kuratsu J., Leonard E. J. Production and characterization of mouse monoclonal antibodies against human monocyte chemoattractant protein-1. J Immunol. 1991 Oct 1;147(7):2229–2233. [PubMed] [Google Scholar]
  24. Yu X., Antoniades H. N., Graves D. T. Expression of monocyte chemoattractant protein 1 in human inflamed gingival tissues. Infect Immun. 1993 Nov;61(11):4622–4628. doi: 10.1128/iai.61.11.4622-4628.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Yu X., Barnhill R. L., Graves D. T. Expression of monocyte chemoattractant protein-1 in delayed type hypersensitivity reactions in the skin. Lab Invest. 1994 Aug;71(2):226–235. [PubMed] [Google Scholar]
  26. Zambon J. J., DeLuca C., Slots J., Genco R. J. Studies of leukotoxin from Actinobacillus actinomycetemcomitans using the promyelocytic HL-60 cell line. Infect Immun. 1983 Apr;40(1):205–212. doi: 10.1128/iai.40.1.205-212.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]

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