Abstract
The present study was performed to estimate the observed frequencies of the immunoglobulin heavy-chain (Gm) and light-chain (Km) allotypes among patients with early-onset periodontitis (EOP) and their effect on the IgG2 subclass responses against Actinobacillus actinomycetemcomitans Y4 and Porphyromonas gingivalis 381, respectively. Sixty-nine EOP patients, including 11 with localized juvenile periodontitis (LJP), 19 who had LJP, 15 with LJP-rapidly progressing periodontitis (RPP), and 24 with RPP, were examined for the Gm and Km allotypes by a hemagglutination inhibition test. Levels of immunoglobulin G2 (IgG2) antibodies against the two organisms were determined by enzyme-linked immunosorbent assay. Fifty race- and age-matched, periodontally healthy subjects were also included as a control group. The observed frequencies of the Gm haplotype afnb and Km(1) were significantly higher in the RPP and LJP groups, respectively. The G2m(n)+ group of those with RPP and the Km(1)+ group of those with LJP had significantly higher levels of IgG2 antibodies to A. actinomycetemcomitans and P. gingivalis, respectively. The results indicate that linkage disequilibrium of the G2m(n) locus in RPP patients or the Km(1) locus in LJP patients may be associated with high IgG2 antibody responses to the respective bacteria. It was reasoned that the IgG2 antibody responses are associated with the immunoglobulin allotypes. The function of IgG2 antibodies in their reaction to different bacterial antigens may be interpreted as either protective or nonprotective in the two different types of EOP (i.e., LJP and RPP).
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- Ambrosino D. M., Schiffman G., Gotschlich E. C., Schur P. H., Rosenberg G. A., DeLange G. G., van Loghem E., Siber G. R. Correlation between G2m(n) immunoglobulin allotype and human antibody response and susceptibility to polysaccharide encapsulated bacteria. J Clin Invest. 1985 Jun;75(6):1935–1942. doi: 10.1172/JCI111909. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Amir J., Liang X., Granoff D. M. Variability in the functional activity of vaccine-induced antibody to Haemophilus influenzae type b. Pediatr Res. 1990 Apr;27(4 Pt 1):358–364. doi: 10.1203/00006450-199004000-00008. [DOI] [PubMed] [Google Scholar]
- Amir J., Scott M. G., Nahm M. H., Granoff D. M. Bactericidal and opsonic activity of IgG1 and IgG2 anticapsular antibodies to Haemophilus influenzae type b. J Infect Dis. 1990 Jul;162(1):163–171. doi: 10.1093/infdis/162.1.163. [DOI] [PubMed] [Google Scholar]
- Ashley F. P., Gallagher J., Wilson R. F. The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, Bacteroides intermedius and spirochaetes in the subgingival microflora in relation to the early onset of periodontitis in a group of adolescents. Oral Microbiol Immunol. 1989 Dec;4(4):236–238. doi: 10.1111/j.1399-302x.1989.tb00260.x. [DOI] [PubMed] [Google Scholar]
- Burton D. R., Gregory L., Jefferis R. Aspects of the molecular structure of IgG subclasses. Monogr Allergy. 1986;19:7–35. [PubMed] [Google Scholar]
- Chung G. H., Scott M. G., Kim K. H., Kearney J., Siber G. R., Ambrosino D. M., Nahm M. H. Clonal characterization of the human IgG antibody repertoire to Haemophilus influenzae type b polysaccharide. V. In vivo expression of individual antibody clones is dependent on Ig CH haplotypes and the categories of antigen. J Immunol. 1993 Oct 15;151(8):4352–4361. [PubMed] [Google Scholar]
- Ebersole J. L. Systemic humoral immune responses in periodontal disease. Crit Rev Oral Biol Med. 1990;1(4):283–331. doi: 10.1177/10454411900010040601. [DOI] [PubMed] [Google Scholar]
- Farida R., Wilson M., Ivanyi L. Serum IgG antibodies to lipopolysaccharides in various forms of periodontal disease in man. Arch Oral Biol. 1986;31(11):711–715. doi: 10.1016/0003-9969(86)90001-4. [DOI] [PubMed] [Google Scholar]
- Granoff D. M., Pandey J. P., Boies E., Squires J., Munson R. S., Jr, Suarez B. Response to immunization with Haemophilus influenzae type b polysaccharide-pertussis vaccine and risk of Haemophilus meningitis in children with the Km(1) immunoglobulin allotype. J Clin Invest. 1984 Nov;74(5):1708–1714. doi: 10.1172/JCI111588. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Granoff D. M., Shackelford P. G., Pandey J. P., Boies E. G. Antibody responses to Haemophilus influenzae type b polysaccharide vaccine in relation to Km(1) and G2m(23) immunoglobulin allotypes. J Infect Dis. 1986 Aug;154(2):257–264. doi: 10.1093/infdis/154.2.257. [DOI] [PubMed] [Google Scholar]
- Granoff D. M., Suarez B. K., Pandey J. P., Shackelford P. G. Genes associated with the G2m(23) immunoglobulin allotype regulate the IgG subclass responses to Haemophilus influenzae type b polysaccharide vaccine. J Infect Dis. 1988 Jun;157(6):1142–1149. doi: 10.1093/infdis/157.6.1142. [DOI] [PubMed] [Google Scholar]
- Gunsolley J. C., Burmeister J. A., Tew J. G., Best A. M., Ranney R. R. Relationship of serum antibody to attachment level patterns in young adults with juvenile periodontitis or generalized severe periodontitis. J Periodontol. 1987 May;58(5):314–320. doi: 10.1902/jop.1987.58.5.314. [DOI] [PubMed] [Google Scholar]
- Gunsolley J. C., Tew J. G., Gooss C. M., Burmeister J. A., Schenkein H. A. Effects of race and periodontal status on antibody reactive with Actinobacillus actinomycetemcomitans strain Y4. J Periodontal Res. 1988 Sep;23(5):303–307. doi: 10.1111/j.1600-0765.1988.tb01421.x. [DOI] [PubMed] [Google Scholar]
- Hammarström L., Smith C. I. IgG subclasses in bacterial infections. Monogr Allergy. 1986;19:122–133. [PubMed] [Google Scholar]
- Listgarten M. A., Lai C. H., Evian C. I. Comparative antibody titers to Actinobacillus actinomycetemcomitans in juvenile periodontitis, chronic periodontitis and periodontally healthy subjects. J Clin Periodontol. 1981 Jun;8(3):155–164. doi: 10.1111/j.1600-051x.1981.tb02027.x. [DOI] [PubMed] [Google Scholar]
- Lu H., Califano J. V., Schenkein H. A., Tew J. G. Immunoglobulin class and subclass distribution of antibodies reactive with the immunodominant antigen of Actinobacillus actinomycetemcomitans serotype b. Infect Immun. 1993 Jun;61(6):2400–2407. doi: 10.1128/iai.61.6.2400-2407.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- López N. J., Mellado J. C., Leighton G. X. Occurrence of Actinobacillus actinomycetemcomitans, Porphyromonas gingivalis and Prevotella intermedia in juvenile periodontitis. J Clin Periodontol. 1996 Feb;23(2):101–105. doi: 10.1111/j.1600-051x.1996.tb00541.x. [DOI] [PubMed] [Google Scholar]
- Löe H., Brown L. J. Early onset periodontitis in the United States of America. J Periodontol. 1991 Oct;62(10):608–616. doi: 10.1902/jop.1991.62.10.608. [DOI] [PubMed] [Google Scholar]
- Matsumoto H. Characteristics of Mongoloid populations and immunogenetics of various diseases based on the genetic markers of human immunoglobulins. Exp Clin Immunogenet. 1989;6(1):68–87. [PubMed] [Google Scholar]
- Morell A., Skvaril F., Steinberg A. G., Van Loghem E., Terry W. D. Correlations between the concentrations of the four sub-classes of IgG and Gm Allotypes in normal human sera. J Immunol. 1972 Jan;108(1):195–206. [PubMed] [Google Scholar]
- Nahm M. H., Kim K. H., Anderson P., Hetherington S. V., Park M. K. Functional capacities of clonal antibodies to Haemophilus influenzae type b polysaccharide. Infect Immun. 1995 Aug;63(8):2989–2994. doi: 10.1128/iai.63.8.2989-2994.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nakao Y., Matsumoto H., Miyazaki T., Mizuno N., Arima N., Wakisaka A., Okimoto K., Akazawa Y., Tsuji K., Fujita T. IgG heavy-chain (Gm) allotypes and immune response to insulin in insulin-requiring diabetes mellitus. N Engl J Med. 1981 Feb 12;304(7):407–409. doi: 10.1056/NEJM198102123040706. [DOI] [PubMed] [Google Scholar]
- Nishimura F., Nagai A., Kurimoto K., Isoshima O., Takashiba S., Kobayashi M., Akutsu I., Kurihara H., Nomura Y., Murayama Y. A family study of a mother and daughter with increased susceptibility to early-onset periodontitis: microbiological, immunological, host defensive, and genetic analyses. J Periodontol. 1990 Dec;61(12):755–762. doi: 10.1902/jop.1990.61.12.755. [DOI] [PubMed] [Google Scholar]
- Ranney R. R., Yanni N. R., Burmeister J. A., Tew J. G. Relationship between attachment loss and precipitating serum antibody to Actinobacillus actinomycetemcomitans in adolescents and young adults having severe periodontal destruction. J Periodontol. 1982 Jan;53(1):1–7. doi: 10.1902/jop.1982.53.1.1. [DOI] [PubMed] [Google Scholar]
- Schenkein H. A., Van Dyke T. E. Early-onset periodontitis: systemic aspects of etiology and pathogenesis. Periodontol 2000. 1994 Oct;6:7–25. doi: 10.1111/j.1600-0757.1994.tb00023.x. [DOI] [PubMed] [Google Scholar]
- Schur P. H. IgG subclasses--a review. Ann Allergy. 1987 Feb;58(2):89-96, 99. [PubMed] [Google Scholar]
- Shackelford P. G., Granoff D. M., Nahm M. H., Scott M. G., Suarez B., Pandey J. P., Nelson S. J. Relation of age, race, and allotype to immunoglobulin subclass concentrations. Pediatr Res. 1985 Aug;19(8):846–849. doi: 10.1203/00006450-198508000-00014. [DOI] [PubMed] [Google Scholar]
- Shapira L., Smidt A., Van Dyke T. E., Barak V., Soskolne A. W., Brautbar C., Sela M. N., Bimstein E. Sequential manifestation of different forms of early-onset periodontitis. A case report. J Periodontol. 1994 Jun;65(6):631–635. doi: 10.1902/jop.1994.65.6.631. [DOI] [PubMed] [Google Scholar]
- Slack J. H. Strain-dependent IgG subclass response patterns. J Immunol. 1987 Dec 1;139(11):3734–3738. [PubMed] [Google Scholar]
- Spektor M. D., Vandesteen G. E., Page R. C. Clinical studies of one family manifesting rapidly progressive, juvenile and prepubertal periodontitis. J Periodontol. 1985 Feb;56(2):93–101. doi: 10.1902/jop.1985.56.2.93. [DOI] [PubMed] [Google Scholar]
- Steinberg A. G., Morell A., Skvaril F., van Loghem E. The effect of Gm(23) on the concentration of IgG2 and IgG4 in normal human serum. J Immunol. 1973 Jun;110(6):1642–1645. [PubMed] [Google Scholar]
- 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]
- Vandesteen G. E., Williams B. L., Ebersole J. L., Altman L. C., Page R. C. Clinical, microbiological and immunological studies of a family with a high prevalence of early-onset periodontitis. J Periodontol. 1984 Mar;55(3):159–169. doi: 10.1902/jop.1984.55.3.159. [DOI] [PubMed] [Google Scholar]
- Vincent J. W., Suzuki J. B., Falkler W. A., Jr, Cornett W. C. Reaction of human sera from juvenile periodontitis, rapidly progressive periodontitis, and adult periodontitis patients with selected periodontopathogens. J Periodontol. 1985 Aug;56(8):464–469. doi: 10.1902/jop.1985.56.8.464. [DOI] [PubMed] [Google Scholar]
- Whitney C., Ant J., Moncla B., Johnson B., Page R. C., Engel D. Serum immunoglobulin G antibody to Porphyromonas gingivalis in rapidly progressive periodontitis: titer, avidity, and subclass distribution. Infect Immun. 1992 Jun;60(6):2194–2200. doi: 10.1128/iai.60.6.2194-2200.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Williams B. L., Ebersole J. L., Spektor M. D., Page R. C. Assessment of serum antibody patterns and analysis of subgingival microflora of members of a family with a high prevalence of early-onset periodontitis. Infect Immun. 1985 Sep;49(3):742–750. doi: 10.1128/iai.49.3.742-750.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wilson M. E., Hamilton R. G. Immunoglobulin G subclass response of juvenile periodontitis subjects to principal outer membrane proteins of Actinobacillus actinomycetemcomitans. Infect Immun. 1995 Mar;63(3):1062–1069. doi: 10.1128/iai.63.3.1062-1069.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 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]
- Yount W. J., Dorner M. M., Kunkel H. G., Kabat E. A. Studies on human antibodies. VI. Selective variations in subgroup composition and genetic markers. J Exp Med. 1968 Mar 1;127(3):633–646. doi: 10.1084/jem.127.3.633. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Zambon J. J. Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol. 1985 Jan;12(1):1–20. doi: 10.1111/j.1600-051x.1985.tb01348.x. [DOI] [PubMed] [Google Scholar]
- van der Giessen M., Freyee W., Rossouw E., van Loghem E. Qualitative and quantitative studies on IgG2 globulins in individual human sera with an antiserum capable of differentiating between Gm(n+) and Gm(n-) proteins. Clin Exp Immunol. 1973 May;14(1):127–139. [PMC free article] [PubMed] [Google Scholar]
- van der Giessen M., Rossouw E., van Veen T. A., van Loghem E., Zegers B. J., Sander P. C. Quantification of IgG subclasses in sera of normal adults and healthy children between 4 and 12 years of age. Clin Exp Immunol. 1975 Sep;21(3):501–509. [PMC free article] [PubMed] [Google Scholar]