Skip to main content
NCBI home page
Infection and Immunity logoLink to Infection and Immunity
. 1997 Sep;65(9):3556–3560. doi: 10.1128/iai.65.9.3556-3560.1997

Relevance of immunoglobulin G Fc receptor polymorphism to recurrence of adult periodontitis in Japanese patients.

T Kobayashi 1, N A Westerdaal 1, A Miyazaki 1, W L van der Pol 1, T Suzuki 1, H Yoshie 1, J G van de Winkel 1, K Hara 1
PMCID: PMC175506  PMID: 9284119

Abstract

Polymorphonuclear neutrophil (PMN) phagocytic function has been shown to be impaired in some patients with periodontitis. PMN constitutively express members of two immunoglobulin G receptor (Fc gammaR) classes: Fc gammaRIIa (CD32) and Fc gammaRIIIb (CD16). Both receptors exhibit genetically determined structural and functional biallelic polymorphisms, which have been shown to influence PMN phagocytic function. In this study, we assessed the relevance of these Fc gammaR polymorphisms to susceptibility to adult periodontitis and recurrence rate. The distribution of Fc gammaRIIa and Fc gammaRIIIb genotypes of 100 Japanese patients with adult periodontitis during follow-up was compared to the distribution of genotypes in 105 race-matched healthy controls. No significant skewing of distributions of Fc gammaRIIa and Fc gammaRIIIb genotypes was observed between patients and controls. Notably, however, a significant overrepresentation of the Fc gammaRIIIb-NA2 allotype was found in patients with disease recurrence (P < 0.05; odds ratio, 4.29; 95% confidence interval, 1.19 to 16.24). Moreover, the annual rate of recurrence was significantly higher in patients with the Fc gammaRIIIb-NA2/NA2 and Fc gammaRIIIb-NA1/NA2 genotypes than in Fc gammaRIIIb-NA1/NA1 individuals (P < 0.05). Fc gammaRIIa-R/R131 individuals also exhibited higher recurrence rates, though the difference was not statistically significant (P = 0.06). These results suggest that the Fc gammaRIIIb-NA2 allotype represents a risk factor for recurrence of adult periodontitis.

Full Text

The Full Text of this article is available as a PDF (168.4 KB).

Selected References

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

  1. Bredius R. G., Derkx B. H., Fijen C. A., de Wit T. P., de Haas M., Weening R. S., van de Winkel J. G., Out T. A. Fc gamma receptor IIa (CD32) polymorphism in fulminant meningococcal septic shock in children. J Infect Dis. 1994 Oct;170(4):848–853. doi: 10.1093/infdis/170.4.848. [DOI] [PubMed] [Google Scholar]
  2. Bredius R. G., Fijen C. A., De Haas M., Kuijper E. J., Weening R. S., Van de Winkel J. G., Out T. A. Role of neutrophil Fc gamma RIIa (CD32) and Fc gamma RIIIb (CD16) polymorphic forms in phagocytosis of human IgG1- and IgG3-opsonized bacteria and erythrocytes. Immunology. 1994 Dec;83(4):624–630. [PMC free article] [PubMed] [Google Scholar]
  3. Bredius R. G., de Vries C. E., Troelstra A., van Alphen L., Weening R. S., van de Winkel J. G., Out T. A. Phagocytosis of Staphylococcus aureus and Haemophilus influenzae type B opsonized with polyclonal human IgG1 and IgG2 antibodies. Functional hFc gamma RIIa polymorphism to IgG2. J Immunol. 1993 Aug 1;151(3):1463–1472. [PubMed] [Google Scholar]
  4. Clark M. R., Clarkson S. B., Ory P. A., Stollman N., Goldstein I. M. Molecular basis for a polymorphism involving Fc receptor II on human monocytes. J Immunol. 1989 Sep 1;143(5):1731–1734. [PubMed] [Google Scholar]
  5. Gosselin E. J., Brown M. F., Anderson C. L., Zipf T. F., Guyre P. M. The monoclonal antibody 41H16 detects the Leu 4 responder form of human Fc gamma RII. J Immunol. 1990 Mar 1;144(5):1817–1822. [PubMed] [Google Scholar]
  6. Gunsolley J. C., Califano J. V., Koertge T. E., Burmeister J. A., Cooper L. C., Schenkein H. A. Longitudinal assessment of early onset periodontitis. J Periodontol. 1995 May;66(5):321–328. doi: 10.1902/jop.1995.66.5.321. [DOI] [PubMed] [Google Scholar]
  7. Hirschfeld L., Wasserman B. A long-term survey of tooth loss in 600 treated periodontal patients. J Periodontol. 1978 May;49(5):225–237. doi: 10.1902/jop.1978.49.5.225. [DOI] [PubMed] [Google Scholar]
  8. Holm G. Smoking as an additional risk for tooth loss. J Periodontol. 1994 Nov;65(11):996–1001. doi: 10.1902/jop.1994.65.11.996. [DOI] [PubMed] [Google Scholar]
  9. Huizinga T. W., Kleijer M., Tetteroo P. A., Roos D., von dem Borne A. E. Biallelic neutrophil Na-antigen system is associated with a polymorphism on the phospho-inositol-linked Fc gamma receptor III (CD16). Blood. 1990 Jan 1;75(1):213–217. [PubMed] [Google Scholar]
  10. Jefferis R., Kumararatne D. S. Selective IgG subclass deficiency: quantification and clinical relevance. Clin Exp Immunol. 1990 Sep;81(3):357–367. doi: 10.1111/j.1365-2249.1990.tb05339.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Looney R. J., Abraham G. N., Anderson C. L. Human monocytes and U937 cells bear two distinct Fc receptors for IgG. J Immunol. 1986 Mar 1;136(5):1641–1647. [PubMed] [Google Scholar]
  12. Lu H., Wang M., Gunsolley J. C., Schenkein H. A., Tew J. G. Serum immunoglobulin G subclass concentrations in periodontally healthy and diseased individuals. Infect Immun. 1994 May;62(5):1677–1682. doi: 10.1128/iai.62.5.1677-1682.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Löe H., Anerud A., Boysen H., Smith M. The natural history of periodontal disease in man. The rate of periodontal destruction before 40 years of age. J Periodontol. 1978 Dec;49(12):607–620. doi: 10.1902/jop.1978.49.12.607. [DOI] [PubMed] [Google Scholar]
  14. MacFarlane G. D., Herzberg M. C., Wolff L. F., Hardie N. A. Refractory periodontitis associated with abnormal polymorphonuclear leukocyte phagocytosis and cigarette smoking. J Periodontol. 1992 Nov;63(11):908–913. doi: 10.1902/jop.1992.63.11.908. [DOI] [PubMed] [Google Scholar]
  15. McFall W. T., Jr Tooth loss in 100 treated patients with periodontal disease. A long-term study. J Periodontol. 1982 Sep;53(9):539–549. doi: 10.1902/jop.1982.53.9.539. [DOI] [PubMed] [Google Scholar]
  16. Ory P. A., Clark M. R., Kwoh E. E., Clarkson S. B., Goldstein I. M. Sequences of complementary DNAs that encode the NA1 and NA2 forms of Fc receptor III on human neutrophils. J Clin Invest. 1989 Nov;84(5):1688–1691. doi: 10.1172/JCI114350. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Ory P. A., Goldstein I. M., Kwoh E. E., Clarkson S. B. Characterization of polymorphic forms of Fc receptor III on human neutrophils. J Clin Invest. 1989 May;83(5):1676–1681. doi: 10.1172/JCI114067. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Osborne J. M., Chacko G. W., Brandt J. T., Anderson C. L. Ethnic variation in frequency of an allelic polymorphism of human Fc gamma RIIA determined with allele specific oligonucleotide probes. J Immunol Methods. 1994 Aug 1;173(2):207–217. doi: 10.1016/0022-1759(94)90299-2. [DOI] [PubMed] [Google Scholar]
  19. Oshrain H. I., Telsey B., Mandel I. D. Neutrophil chemotaxis in refractory cases of periodontitis. J Clin Periodontol. 1987 Jan;14(1):52–55. doi: 10.1111/j.1600-051x.1987.tb01514.x. [DOI] [PubMed] [Google Scholar]
  20. Parren P. W., Warmerdam P. A., Boeije L. C., Arts J., Westerdaal N. A., Vlug A., Capel P. J., Aarden L. A., van de Winkel J. G. On the interaction of IgG subclasses with the low affinity Fc gamma RIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J Clin Invest. 1992 Oct;90(4):1537–1546. doi: 10.1172/JCI116022. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Rascu A., Repp R., Westerdaal N. A., Kalden J. R., van de Winkel J. G. Clinical relevance of Fc gamma receptor polymorphisms. Ann N Y Acad Sci. 1997 Apr 5;815:282–295. doi: 10.1111/j.1749-6632.1997.tb52070.x. [DOI] [PubMed] [Google Scholar]
  22. Salmon J. E., Edberg J. C., Brogle N. L., Kimberly R. P. Allelic polymorphisms of human Fc gamma receptor IIA and Fc gamma receptor IIIB. Independent mechanisms for differences in human phagocyte function. J Clin Invest. 1992 Apr;89(4):1274–1281. doi: 10.1172/JCI115712. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Salmon J. E., Edberg J. C., Kimberly R. P. Fc gamma receptor III on human neutrophils. Allelic variants have functionally distinct capacities. J Clin Invest. 1990 Apr;85(4):1287–1295. doi: 10.1172/JCI114566. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Sanders L. A., Feldman R. G., Voorhorst-Ogink M. M., de Haas M., Rijkers G. T., Capel P. J., Zegers B. J., van de Winkel J. G. Human immunoglobulin G (IgG) Fc receptor IIA (CD32) polymorphism and IgG2-mediated bacterial phagocytosis by neutrophils. Infect Immun. 1995 Jan;63(1):73–81. doi: 10.1128/iai.63.1.73-81.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sanders L. A., van de Winkel J. G., Rijkers G. T., Voorhorst-Ogink M. M., de Haas M., Capel P. J., Zegers B. J. Fc gamma receptor IIa (CD32) heterogeneity in patients with recurrent bacterial respiratory tract infections. J Infect Dis. 1994 Oct;170(4):854–861. doi: 10.1093/infdis/170.4.854. [DOI] [PubMed] [Google Scholar]
  26. Satoh T., Kobayashi M., Kaneda M., Tanihiro M., Okada K., Ueda K. Genotypical classification of neutrophil Fc gamma receptor III by polymerase chain reaction-single-strand conformation polymorphism. Blood. 1994 Jun 1;83(11):3312–3315. [PubMed] [Google Scholar]
  27. Warmerdam P. A., van de Winkel J. G., Gosselin E. J., Capel P. J. Molecular basis for a polymorphism of human Fc gamma receptor II (CD32). J Exp Med. 1990 Jul 1;172(1):19–25. doi: 10.1084/jem.172.1.19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Warmerdam P. A., van de Winkel J. G., Vlug A., Westerdaal N. A., Capel P. J. A single amino acid in the second Ig-like domain of the human Fc gamma receptor II is critical for human IgG2 binding. J Immunol. 1991 Aug 15;147(4):1338–1343. [PubMed] [Google Scholar]
  29. Wilson M. E., Hamilton R. G. Immunoglobulin G subclass response of localized juvenile periodontitis patients to Actinobacillus actinomycetemcomitans Y4 lipopolysaccharide. Infect Immun. 1992 May;60(5):1806–1812. doi: 10.1128/iai.60.5.1806-1812.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Wilton J. M., Hurst T. J., Sterne J. A., Caves J., Tilley C., Powell J. R. Elevated levels of the IgG2 subclass in serum from patients with a history of destructive periodontal disease. A case-control study. J Clin Periodontol. 1992 May;19(5):318–321. doi: 10.1111/j.1600-051x.1992.tb00652.x. [DOI] [PubMed] [Google Scholar]
  31. Wolff L., Dahlén G., Aeppli D. Bacteria as risk markers for periodontitis. J Periodontol. 1994 May;65(5 Suppl):498–510. doi: 10.1902/jop.1994.65.5s.498. [DOI] [PubMed] [Google Scholar]
  32. de Haas M., Kleijer M., van Zwieten R., Roos D., von dem Borne A. E. Neutrophil Fc gamma RIIIb deficiency, nature, and clinical consequences: a study of 21 individuals from 14 families. Blood. 1995 Sep 15;86(6):2403–2413. [PubMed] [Google Scholar]
  33. van de Winkel J. G., Capel P. J. Human IgG Fc receptor heterogeneity: molecular aspects and clinical implications. Immunol Today. 1993 May;14(5):215–221. doi: 10.1016/0167-5699(93)90166-I. [DOI] [PubMed] [Google Scholar]

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

RESOURCES