Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

Identification of immunological parameters associated with the alveolar bone level in periodontal patients

  • Park, Chang-Seo (Department of Periodontology, Pusan National University School of Dentistry) ;
  • Lee, Ju-Yeon (Department of Periodontology, Pusan National University School of Dentistry) ;
  • Kim, Sung-Jo (Department of Periodontology, Pusan National University School of Dentistry) ;
  • Choi, Jeom-Il (Department of Periodontology, Pusan National University School of Dentistry)
  • Received : 2010.01.27
  • Accepted : 2010.03.11
  • Published : 2010.04.30
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: The present study was performed to clarify the relationship between periodontal disease severity and selected immunological parameters consisting of serum IgG titer against periodontopathogenic bacteria, the expression of the helper T-cell cytokine by gingival mononuclear cells, and patients' immunoreactivity to cross-reactive heat shock protein (HSP) epitope peptide from P. gingivalis HSP60. Methods: Twenty-five patients with moderate periodontitis had their gingival connective tissue harvested of gingival mononuclear cells during an open flap debridement procedure and peripheral blood was drawn by venipuncture to collect serum. The mean level of interproximal alveolar bone was calculated to be used as an index for periodontal disease severity for a given patient. Each of selected immunologic parameters was subject to statistical management to seek their correlations with the severity of periodontal disease. Results: A significant correlation could not be identified between serum IgG titers against specific bacteria (Porphyromonas gingivalis, Prevotella intermedia, Fusobacterium nucleatum, Actinobacillus actinomycetemcomitans, and Streptococcus mutans) and the severity of periodontal disease. Expression of interleukin (IL)-10 by gingival mononuclear cells was statistically significant in the group of patients who had higher levels of alveolar bone height. However, a similar correlation could not be demonstrated in cases for IL-4 or interferon-$\gamma$. Patients' serum reactivity to cross-reactive epitope peptide showed a significant correlation with the amount of alveolar bone. Conclusions: It was concluded that expression of IL-10 by gingival mononuclear cells and patients' sero-reactivity to the cross-reactive HSP peptide of P. gingivalis HSP60 were significantly correlated with alveolar bone height.

Keywords

References

  1. Socransky SS, Haffajee AD. The nature of periodontal diseases. Ann Periodontol 1997;2:3-10. https://doi.org/10.1902/annals.1997.2.1.3
  2. Ishikawa I, Nakashima K, Koseki T, Nagasawa T, Watanabe H, Arakawa S, et al. Induction of the immune response to periodontopathic bacteria and its role in the pathogenesis of periodontitis. Periodontol 2000 1997;14:79-111. https://doi.org/10.1111/j.1600-0757.1997.tb00193.x
  3. Ebersole JL, Taubman MA, Smith DJ, Frey DE. Human immune responses to oral microorganisms: patterns of systemic antibody levels to Bacteroides species. Infect Immun 1986;51:507-13.
  4. Naito Y, Okuda K, Takazoe I. Immunoglobulin G response to subgingival gram-negative bacteria in human subjects. Infect Immun 1984;45:47-51.
  5. Ebersole JL, Taubman MA. The protective nature of host responses in periodontal diseases. Periodontol 2000 1994;5:112-41. https://doi.org/10.1111/j.1600-0757.1994.tb00021.x
  6. Socransky SS, Haffajee AD, Cugini MA, Smith C, Kent RL Jr. Microbial complexes in subgingival plaque. J Clin Periodontol 1998;25:134-44. https://doi.org/10.1111/j.1600-051X.1998.tb02419.x
  7. Naito Y, Okuda K, Takazoe I, Watanabe H, Ishikawa I. The relationship between serum IgG levels to subgingival gram-negative bacteria and degree of periodontal destruction. J Dent Res 1985;64:1306-10. https://doi.org/10.1177/00220345850640111101
  8. Kojima T, Yano K, Ishikawa I. Relationship between serum antibody levels and subgingival colonization of Porphyromonas gingivalis in patients with various types of periodontitis. J Periodontol 1997;68:618-25. https://doi.org/10.1902/jop.1997.68.7.618
  9. Taubman MA, Haffajee AD, Socransky SS, Smith DJ, Ebersole JL. Longitudinal monitoring of humoral antibody in subjects with destructive periodontal diseases. J Periodontal Res 1992;27:511-21. https://doi.org/10.1111/j.1600-0765.1992.tb01825.x
  10. Taubman MA, Kawai T. Involvement of T-lymphocytes in periodontal disease and in direct and indirect induction of bone resorption. Crit Rev Oral Biol Med 2001;12:125-35. https://doi.org/10.1177/10454411010120020301
  11. Kawai T, Matsuyama T, Hosokawa Y, Makihira S, Seki M, Karimbux NY, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006;169:987-98. https://doi.org/10.2353/ajpath.2006.060180
  12. Liu D, Yao S, Wise GE. Effect of interleukin-10 on gene expression of osteoclastogenic regulatory molecules in the rat dental follicle. Eur J Oral Sci 2006;114:42-9. https://doi.org/10.1111/j.1600-0722.2006.00283.x
  13. Al-Rasheed A, Scheerens H, Rennick DM, Fletcher HM, Tatakis DN. Accelerated alveolar bone loss in mice lacking interleukin-10. J Dent Res 2003;82:632-5. https://doi.org/10.1177/154405910308200812
  14. Al-Rasheed A, Scheerens H, Srivastava AK, Rennick DM, Tatakis DN. Accelerated alveolar bone loss in mice lacking interleukin-10: late onset. J Periodontal Res 2004;39:194-8. https://doi.org/10.1111/j.1600-0765.2004.00724.x
  15. Sasaki H, Okamatsu Y, Kawai T, Kent R, Taubman M, Stashenko P. The interleukin-10 knockout mouse is highly susceptible to Porphyromonas gingivalis-induced alveolar bone loss. J Periodontal Res 2004;39:432-41. https://doi.org/10.1111/j.1600-0765.2004.00760.x
  16. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, et al. T-cell-mediated regulation of osteoclasto-genesis by signalling cross-talk between RANKL and IFN-gamma. Nature 2000;408:600-5. https://doi.org/10.1038/35046102
  17. Teng YT, Mahamed D, Singh B. Gamma interferon positively modulates Actinobacillus actinomycetemcomitans-specific RANKL+ CD4+ Th-cell-mediated alveolar bone destruction in vivo. Infect Immun 2005;73:3453-61. https://doi.org/10.1128/IAI.73.6.3453-3461.2005
  18. Baker PJ, Dixon M, Evans RT, Dufour L, Johnson E, Roopenian DC. CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infect Immun 1999;67:2804-9.
  19. Mahamed DA, Marleau A, Alnaeeli M, Singh B, Zhang X, Penninger JM, et al. G(-) anaerobes-reactive CD4+ T-cells trigger RANKL-mediated enhanced alveolar bone loss in diabetic NOD mice. Diabetes 2005;54:1477-86. https://doi.org/10.2337/diabetes.54.5.1477
  20. Young DB. Stress proteins and the immune response. Antonie Van Leeuwenhoek 1990;58:203-8. https://doi.org/10.1007/BF00548934
  21. Lamb JR, Bal V, Mendez-Samperio P, Mehlert A, So A, Rothbard J, et al. Stress proteins may provide a link between the immune response to infection and autoimmunity. Int Immunol 1989;1:191-6. https://doi.org/10.1093/intimm/1.2.191
  22. Choi JI, Chung SW, Kang HS, Rhim BY, Kim SJ. Establishment of Porphyromonas gingivalis heat-shock-protein-specific T-cell lines from atherosclerosis patients. J Dent Res 2002;81:344-8. https://doi.org/10.1177/154405910208100511
  23. Choi JI, Chung SW, Kang HS, Rhim BY, Park YM, Kim US, et al. Epitope mapping of Porphyromonas gingivalis heatshock protein and human heat-shock protein in human atherosclerosis. J Dent Res 2004;83:936-40. https://doi.org/10.1177/154405910408301209
  24. Chung SW, Kang HS, Park HR, Kim SJ, Choi JI. Immune responses to heat shock protein in Porphyromonas gingivalis-infected periodontitis and atherosclerosis patients. J Periodontal Res 2003;38:388-93. https://doi.org/10.1034/j.1600-0765.2003.00664.x
  25. Ueki K, Tabeta K, Yoshie H, Yamazaki K. Self-heat shock protein 60 induces tumour necrosis factor-alpha in monocyte-derived macrophage: possible role in chronic inflammatory periodontal disease. Clin Exp Immunol 2002;127:72-7. https://doi.org/10.1046/j.1365-2249.2002.01723.x
  26. Moudgil KD, Durai M. Regulation of autoimmune arthritis by self-heat-shock proteins. Trends Immunol 2008;29:412-8. https://doi.org/10.1016/j.it.2008.06.003
  27. van Eden W, van der Zee R, Prakken B. Heat-shock proteins induce T-cell regulation of chronic inflammation. Nat Rev Immunol 2005;5:318-30. https://doi.org/10.1038/nri1593
  28. Durai M, Gupta RS, Moudgil KD. The T cells specific for the carboxyl-terminal determinants of self (rat) heatshock protein 65 escape tolerance induction and are involved in regulation of autoimmune arthritis. J Immunol 2004;172:2795-802.
  29. Durai M, Kim HR, Bala KK, Moudgil KD. T cells against the pathogenic and protective epitopes of heat-shock protein 65 are crossreactive and display functional similarity: novel aspect of regulation of autoimmune arthritis. J Rheumatol 2007;34:2134-43.
  30. Quintana FJ, Carmi P, Mor F, Cohen IR. DNA fragments of the human 60-kDa heat shock protein (HSP60) vaccinate against adjuvant arthritis: identification of a regulatory HSP60 peptide. J Immunol 2003;171:3533-41.
  31. Lee JY, Lee JY, Kim SJ, Choi JI. Production and characterization of cross-reactive anti-Porphyromonas gingivalis heat shock protein 60 monoclonal antibody. J Korean Acad Periodontol 2008;38:565-78.
  32. Ishikawa I, Watanabe H, Horibe M, Izumi Y. Diversity of IgG antibody responses in the patients with various types of periodontitis. Adv Dent Res 1988;2:334-8.
  33. Horibe M, Watanabe H, Ishikawa I. Effect of periodontal treatments on serum IgG antibody titers against periodontopathic bacteria. J Clin Periodontol 1995;22:510-5. https://doi.org/10.1111/j.1600-051X.1995.tb00798.x
  34. Anderson DM, Ebersole JL, Novak MJ. Functional properties of nonhuman primate antibody to Porphyromonas gingivalis. Infect Immun 1995;63:3245-52.
  35. Arenzana-Seisdedos F, Virelizier JL, Fiers W. Interferons as macrophage-activating factors. III. Preferential effects of interferon-gamma on the interleukin 1 secretory potential of fresh or aged human monocytes. J Immunol 1985;134:2444-8.
  36. te Velde AA, Huijbens RJ, Heije K, de Vries JE, Figdor CG. Interleukin-4 (IL-4) inhibits secretion of IL-1 beta, tumor necrosis factor alpha, and IL-6 by human monocytes. Blood 1990;76:1392-7.
  37. Bettelli E, Das MP, Howard ED, Weiner HL, Sobel RA, Kuchroo VK. IL-10 is critical in the regulation of autoim-mune encephalomyelitis as demonstrated by studies of IL-10- and IL-4-deficient and transgenic mice. J Immunol 1998;161:3299-306.
  38. Kucharzik T, Lugering N, Weigelt H, Adolf M, Domschke W, Stoll R. Immunoregulatory properties of IL-13 in patients with inflammatory bowel disease; comparison with IL-4 and IL-10. Clin Exp Immunol 1996;104:483-90. https://doi.org/10.1046/j.1365-2249.1996.39750.x
  39. Sasaki H, Hou L, Belani A, Wang CY, Uchiyama T, Muller R, et al. IL-10, but not IL-4, suppresses infection-stimulated bone resorption in vivo. J Immunol 2000;165:3626-30.
  40. Shinnick TM, Vodkin MH, Williams JC. The Mycobacterium tuberculosis 65-kilodalton antigen is a heat shock protein which corresponds to common antigen and to the Escherichia coli GroEL protein. Infect Immun 1988;56:446-51.

Cited by

  1. Vaccines against periodontitis: a forward-looking review vol.40, pp.4, 2010, https://doi.org/10.5051/jpis.2010.40.4.153
  2. Pathological Characteristics of Periodontal Disease in Patients with Chronic Kidney Disease and Kidney Transplantation vol.20, pp.14, 2010, https://doi.org/10.3390/ijms20143413