Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1987 Oct;55(10):2332–2340. doi: 10.1128/iai.55.10.2332-2340.1987

Immunosuppressive effects of Centipeda periodontii: selective cytotoxicity for lymphocytes and monocytes.

B J Shenker 1, P Berthold 1, P Dougherty 1, K K Porter 1
PMCID: PMC260709  PMID: 3653981

Abstract

We have examined soluble sonic extracts prepared from several strains of Centipeda periodontii for their ability to alter human lymphocyte function. These organisms were isolated from subgingival plaque of patients with periodontal disease. We found that sonicates from several, but not all, strains of C. periodontii caused a dose-dependent inhibition of lymphocyte responsiveness to concanavalin A, phytohemagglutinin, pokeweed mitogen, and formalinized Staphylococcus aureus. Inhibition was associated with a concomitant decrease in cell viability assessed by trypan blue exclusion, 51Cr release, and electron microscopy. The maximal number of dead cells was observed 20 to 24 h after exposure to the sonic extract. Susceptible cells include human lymphocytes (both B and T), monocytes, and erythrocytes, whereas polymorphonuclear cells, murine L-929 fibroblasts, and sheep erythrocytes were not affected. Preliminary characterization of the cytotoxic activity indicates that it is heat labile and trypsin sensitive and has an Mr of 60,000. It has been proposed that impaired host defense may play a pivotal role in the pathogenesis of periodontal diseases. The data presented in this paper suggest that immunosuppression (local or systemic or both) could be initiated by C. periodontii. This immunosuppression may alter the nature and consequences of host-parasite interactions, thereby enhancing the pathogenicity of C. periodontii itself or some other opportunistic organism.

Full text

PDF
2332

Images in this article

2336Image
on p.2336

Selected References

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

  1. Arneborn P., Biberfeld G. T-lymphocyte subpopulations in relation to immunosuppression in measles and varicella. Infect Immun. 1983 Jan;39(1):29–37. doi: 10.1128/iai.39.1.29-37.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Asaro J. P., Nisengard R., Beutner E. H., Neiders M. Experimental periodontal disease. Immediate hypersensitivity. J Periodontol. 1983 Jan;54(1):23–28. doi: 10.1902/jop.1983.54.1.23. [DOI] [PubMed] [Google Scholar]
  3. Bradford M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem. 1976 May 7;72:248–254. doi: 10.1016/0003-2697(76)90527-3. [DOI] [PubMed] [Google Scholar]
  4. Budtz-Jörgensen E., Kelstrup J., Funder-Nielsen T. D., Knudsen A. M. Leukocyte migration inhibition by bacterial antigens in patients with periodontal disease. J Periodontal Res. 1977 Jan;12(1):21–29. doi: 10.1111/j.1600-0765.1977.tb00105.x. [DOI] [PubMed] [Google Scholar]
  5. Burckhardt J. J., Gaegauf-Zollinger R., Schmid R., Guggenheim B. Alveolar bone loss in rats after immunization with Actinomyces viscosus. Infect Immun. 1981 Mar;31(3):971–977. doi: 10.1128/iai.31.3.971-977.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Carrow E. W., Domer J. E. Immunoregulation in experimental murine candidiasis: specific suppression induced by Candida albicans cell wall glycoprotein. Infect Immun. 1985 Jul;49(1):172–181. doi: 10.1128/iai.49.1.172-181.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Frandsen E. V., Reinholdt J., Kilian M. Enzymatic and antigenic characterization of immunoglobulin A1 proteases from Bacteroides and Capnocytophaga spp. Infect Immun. 1987 Mar;55(3):631–638. doi: 10.1128/iai.55.3.631-638.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Frøland S. S. Bacterial infections in the compromised host. Scand J Infect Dis Suppl. 1984;43:7–16. [PubMed] [Google Scholar]
  9. Genco R. J., Mashimo P. A., Krygier G., Ellison S. A. Antibody-mediated effects on the periodontium. J Periodontol. 1974 May;45(5):330–337. doi: 10.1902/jop.1974.45.5.330. [DOI] [PubMed] [Google Scholar]
  10. Ginsburg I., Tsai C. C., Wrenn S. M., Taichman N. S. Phospholipids inhibit cytotoxic effects of Actinobacillus actinomycetemcomitans leukotoxin on human polymorphonuclear leukocytes. Inflammation. 1982 Dec;6(4):365–370. doi: 10.1007/BF00917307. [DOI] [PubMed] [Google Scholar]
  11. Hoffenbach A., Lagrange P. H., Bach M. A. Deficit of interleukin 2 production associated with impaired T-cell proliferative responses in Mycobacterium lepraemurium infection. Infect Immun. 1983 Jan;39(1):109–116. doi: 10.1128/iai.39.1.109-116.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  12. Ivanyi L., Lehner T. Stimulation of lymphocyte transformation by bacterial antigens in patients with periodontal disease. Arch Oral Biol. 1970 Nov;15(11):1089–1096. doi: 10.1016/0003-9969(70)90121-4. [DOI] [PubMed] [Google Scholar]
  13. Kantzler G. B., Lauteria S. F., Cusumano C. L., Lee J. D., Ganguly R., Waldman R. H. Immunosuppression during influenza virus infection. Infect Immun. 1974 Nov;10(5):996–1002. doi: 10.1128/iai.10.5.996-1002.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kato K., Yamamoto K., Kimura T., Azuma I., Askenase P. W. Suppression of BCG cell wall-induced delayed-type hypersensitivity by pretreatment with killed BCG: induction of nonspecific suppressor T cells by the adjuvant portion (MDP) and of specific suppressor T cells by the antigen portion (TAP). J Immunol. 1984 Jun;132(6):2790–2795. [PubMed] [Google Scholar]
  15. Kauffman C. A., Phair J. P., Linnemann C. C., Jr, Schiff G. M. Cell-mediated immunity in humans during viral infection. I. Effect of rubella on dermal hypersensitivity, phytohemagglutinin response, and T lymphocyte numbers. Infect Immun. 1974 Jul;10(1):212–215. doi: 10.1128/iai.10.1.212-215.1974. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Kleinhenz M. E., Ellner J. J., Spagnuolo P. J., Daniel T. M. Suppression of lymphocyte responses by tuberculous plasma and mycobacterial arabinogalactan. Monocyte dependence and indomethacin reversibility. J Clin Invest. 1981 Jul;68(1):153–162. doi: 10.1172/JCI110231. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lehner T., Wilton J. M., Ivanyi L., Manson J. D. Immunological aspects of juvenile periodontitis (periodontosis). J Periodontal Res. 1974;9(5):261–272. doi: 10.1111/j.1600-0765.1974.tb00681.x. [DOI] [PubMed] [Google Scholar]
  18. Madsen M., Johnsen H. E., Hansen P. W., Christiansen S. E. Isolation of human T and B lymphocytes by E-rosette gradient centrifugation. Characterization of the isolated subpopulations. J Immunol Methods. 1980;33(4):323–336. doi: 10.1016/0022-1759(80)90003-4. [DOI] [PubMed] [Google Scholar]
  19. Maleckar J. R., Kierszenbaum F. Inhibition of mitogen-induced proliferation of mouse T and B lymphocytes by bloodstream forms of Trypanosoma cruzi. J Immunol. 1983 Feb;130(2):908–911. [PubMed] [Google Scholar]
  20. Males B. M., Berthold P., Dougherty P. A., Listgarten M. A. Helical flagellation in Centipeda periodontii, a gram-negative, anaerobic bacillus from periodontitis lesions. J Gen Microbiol. 1984 Jan;130(1):185–191. doi: 10.1099/00221287-130-1-185. [DOI] [PubMed] [Google Scholar]
  21. Mammo W., Singh G., Dolby A. E. Enhanced cellular immune response to type I collagen in patients with periodontal disease. Int Arch Allergy Appl Immunol. 1982;67(2):149–154. doi: 10.1159/000233006. [DOI] [PubMed] [Google Scholar]
  22. Mehra V., Convit J., Rubinstein A., Bloom B. R. Activated suppressor T cells in leprosy. J Immunol. 1982 Nov;129(5):1946–1951. [PubMed] [Google Scholar]
  23. Middlebrook J. L., Dorland R. B. Bacterial toxins: cellular mechanisms of action. Microbiol Rev. 1984 Sep;48(3):199–221. doi: 10.1128/mr.48.3.199-221.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Mosley R. L., Murphy J. W., Cox R. A. Immunoadsorption of Cryptococcus-specific suppressor T-cell factors. Infect Immun. 1986 Mar;51(3):844–850. doi: 10.1128/iai.51.3.844-850.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Musher D. M., Schell R. F., Jones R. H., Jones A. M. Lymphocyte transformation in syphilis: an in vitro correlate of immune suppression in vivo? Infect Immun. 1975 Jun;11(6):1261–1264. doi: 10.1128/iai.11.6.1261-1264.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Okada H., Kida T., Yamagami H. Identification and distribution of immunocompetent cells in inflamed gingiva of human chronic periodontitis. Infect Immun. 1983 Jul;41(1):365–374. doi: 10.1128/iai.41.1.365-374.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Olson G. B., Dent P. B., Rawls W. E., South M. A., Montgomery J. R., Melnick J. L., Good R. A. Abnormalities of in vitro lymphocyte responses during rubella virus infections. J Exp Med. 1968 Jul 1;128(1):47–68. doi: 10.1084/jem.128.1.47. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Patters M. R., Chen P., McKenna J., Genco R. J. Lymphoproliferative responses to oral bacteria in humans with varying severities of periodontal disease. Infect Immun. 1980 Jun;28(3):777–784. doi: 10.1128/iai.28.3.777-784.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. REYNOLDS E. S. The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol. 1963 Apr;17:208–212. doi: 10.1083/jcb.17.1.208. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Reiner N. E., Finke J. H. Interleukin 2 deficiency in murine Leishmaniasis donovani and its relationship to depressed spleen cell responses to phytohemagglutinin. J Immunol. 1983 Sep;131(3):1487–1491. [PubMed] [Google Scholar]
  31. Rivas V., Rogers T. J. Studies on the cellular nature of Candida albicans-induced suppression. J Immunol. 1983 Jan;130(1):376–379. [PubMed] [Google Scholar]
  32. Rosen F. S., Cooper M. D., Wedgwood R. J. The primary immunodeficiencies (1). N Engl J Med. 1984 Jul 26;311(4):235–242. doi: 10.1056/NEJM198407263110406. [DOI] [PubMed] [Google Scholar]
  33. Rosen F. S., Cooper M. D., Wedgwood R. J. The primary immunodeficiencies. (2). N Engl J Med. 1984 Aug 2;311(5):300–310. doi: 10.1056/NEJM198408023110506. [DOI] [PubMed] [Google Scholar]
  34. Rylander H., Lindhe J., Ahlstedt S. Experimental gingivitis in immunized dogs. J Periodontal Res. 1976 Nov;11(6):339–348. doi: 10.1111/j.1600-0765.1976.tb00088.x. [DOI] [PubMed] [Google Scholar]
  35. Sallay K., Listgarten M., Sanavi F., Ring I., Nowotny A. Bacterial invasion of oral tissues of immunosuppressed rats. Infect Immun. 1984 Mar;43(3):1091–1093. doi: 10.1128/iai.43.3.1091-1093.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Schwab J. H. Suppression of the immune response by microorganisms. Bacteriol Rev. 1975 Jun;39(2):121–143. doi: 10.1128/br.39.2.121-143.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Scott P. A., Farrell J. P. Experimental cutaneous leishmaniasis. I. Nonspecific immunodepression in BALB/c mice infected with Leishmania tropica. J Immunol. 1981 Dec;127(6):2395–2400. [PubMed] [Google Scholar]
  38. Seymour G. J., Cole K. L., Powell R. N. Analysis of lymphocyte populations extracted from chronically inflamed human periodontal tissues. II. Blastogenic response. J Periodontal Res. 1985 Nov;20(6):571–579. doi: 10.1111/j.1600-0765.1985.tb00841.x. [DOI] [PubMed] [Google Scholar]
  39. Shenker B. J., DiRienzo J. M. Suppression of human peripheral blood lymphocytes by Fusobacterium nucleatum. J Immunol. 1984 May;132(5):2357–2362. [PubMed] [Google Scholar]
  40. Shenker B. J., Kushner M. E., Tsai C. C. Inhibition of fibroblast proliferation by Actinobacillus actinomycetemcomitans. Infect Immun. 1982 Dec;38(3):986–992. doi: 10.1128/iai.38.3.986-992.1982. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. Shenker B. J., Listgarten M. A., Taichman N. S. Suppression of human lymphocyte responses by oral spirochetes: a monocyte-dependent phenomenon. J Immunol. 1984 Apr;132(4):2039–2045. [PubMed] [Google Scholar]
  42. Shenker B. J., McArthur W. P., Tsai C. C. Immune suppression induced by Actinobacillus actinomycetemcomitans. I. Effects on human peripheral blood lymphocyte responses to mitogens and antigens. J Immunol. 1982 Jan;128(1):148–154. [PubMed] [Google Scholar]
  43. Shenker B. J., Tsai C. C., Taichman N. S. Suppression of lymphocyte responses by Actinobacillus actinomycetemcomitans. J Periodontal Res. 1982 Sep;17(5):462–465. doi: 10.1111/j.1600-0765.1982.tb02027.x. [DOI] [PubMed] [Google Scholar]
  44. Stashenko P., Resmini L. M., Haffajee A. D., Socransky S. S. Helper and suppressor T cells in periodontal disease. J Periodontal Res. 1985 Sep;20(5):515–521. doi: 10.1111/j.1600-0765.1985.tb00835.x. [DOI] [PubMed] [Google Scholar]
  45. Stashenko P., Resmini L. M., Haffajee A. D., Socransky S. S. T cell responses of periodontal disease patients and healthy subjects to oral microorganisms. J Periodontal Res. 1983 Nov;18(6):587–600. doi: 10.1111/j.1600-0765.1983.tb00396.x. [DOI] [PubMed] [Google Scholar]
  46. Strugnell R. A., Faine S., Graves S. Response of syphilitic rabbits to reinfection with homologous and heterologous Treponema pallidum strains. Infect Immun. 1984 Sep;45(3):561–565. doi: 10.1128/iai.45.3.561-565.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  47. Taichman N. S., Dean R. T., Sanderson C. J. Biochemical and morphological characterization of the killing of human monocytes by a leukotoxin derived from Actinobacillus actinomycetemcomitans. Infect Immun. 1980 Apr;28(1):258–268. doi: 10.1128/iai.28.1.258-268.1980. [DOI] [PMC free article] [PubMed] [Google Scholar]
  48. Taichman N. S., Wilton J. M. Leukotoxicity of an extract from Actinobacillus actinomycetemcomitans for human gingival polymorphonuclear leukocytes. Inflammation. 1981 Mar;5(1):1–12. doi: 10.1007/BF00910774. [DOI] [PubMed] [Google Scholar]
  49. Taubman M. A., Yoshie H., Wetherell J. R., Jr, Ebersole J. L., Smith D. J. Immune response and periodontal bone loss in germfree rats immunized and infected with Actinobacillus actinomycetemcomitans. J Periodontal Res. 1983 Jul;18(4):393–401. doi: 10.1111/j.1600-0765.1983.tb00375.x. [DOI] [PubMed] [Google Scholar]
  50. Tew J. G., Marshall D. R., Moore W. E., Best A. M., Palcanis K. G., Ranney R. R. Serum antibody reactive with predominant organisms in the subgingival flora of young adults with generalized severe periodontitis. Infect Immun. 1985 May;48(2):303–311. doi: 10.1128/iai.48.2.303-311.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  51. Tew J. G., Smibert R. M., Scott E. A., Burmeister J. A., Ranney R. R. Serum antibodies in young adult humans reactive with periodontitis associated treponemes. J Periodontal Res. 1985 Nov;20(6):580–590. doi: 10.1111/j.1600-0765.1985.tb00842.x. [DOI] [PubMed] [Google Scholar]
  52. Tsai C. C., Shenker B. J., DiRienzo J. M., Malamud D., Taichman N. S. Extraction and isolation of a leukotoxin from Actinobacillus actinomycetemcomitans with polymyxin B. Infect Immun. 1984 Feb;43(2):700–705. doi: 10.1128/iai.43.2.700-705.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Wahl L. M., Katona I. M., Wilder R. L., Winter C. C., Haraoui B., Scher I., Wahl S. M. Isolation of human mononuclear cell subsets by counterflow centrifugal elutriation (CCE). I. Characterization of B-lymphocyte-, T-lymphocyte-, and monocyte-enriched fractions by flow cytometric analysis. Cell Immunol. 1984 May;85(2):373–383. doi: 10.1016/0008-8749(84)90251-x. [DOI] [PubMed] [Google Scholar]
  54. Weir D. M., Blackwell C. C. Interaction of bacteria with the immune system. J Clin Lab Immunol. 1983 Jan;10(1):1–12. [PubMed] [Google Scholar]

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

RESOURCES