Advanced Search

Journal Navigation

Journal Home

Subscriptions

Archive

Contact Us

Table of Contents

Click here to sign up for SAGE Journal Email Alerts today!

Sign In to gain access to subscriptions and/or personal tools.
Journal of Dental Research
This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Taubman, M.A.
Right arrow Articles by Olson, C.L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Taubman, M.A.
Right arrow Articles by Olson, C.L.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?

Host Response in Experimental Periodontal Disease

M.A. Taubman

Department of Immunology, Forsyth Dental Center, 140 The Fenway, Boston, Massachusetts 02115

H. Yoshie

Department of Immunology, Forsyth Dental Center, 140 The Fenway, Boston, Massachusetts 02115

J.L. Ebersole

Department of Immunology, Forsyth Dental Center, 140 The Fenway, Boston, Massachusetts 02115

D.J. Smith

Department of Immunology, Forsyth Dental Center, 140 The Fenway, Boston, Massachusetts 02115

C.L. Olson

Department of Immunology, Forsyth Dental Center, 140 The Fenway, Boston, Massachusetts 02115

Experiments were performed to determine the role of the immune response in rat periodontal disease. Germ-free rats were fed defined antigen-free liquid diets or a diet containing ovalbumin(OVA) as a prototype antigen. The OVA-fed rats demonstrated increased gingival lymphocytes (mainly T at early times), OVA-sensitized spleen cells, and increased periodontal bone loss. In further studies, rats pre-sensitized with OVA, and receiving OVA in the diet, showed elevated IgG antibody, sensitized spleen cells, and elevated periodontal bone loss scores. The concept that bone loss was due to mixed hypersensitivity reaction is consistent with the periodontal pathology. The effects of pre-immunization with A. actinomycetemcomitans (Aa) on periodontal bone loss in Actinobacillus (Aa) - infected rats was examined. Delayed hypersensitivity (DTH) was present in immunized rats throughout the experimental period. Sham-immunized rats showed DTH after 30 days of infection. In addition, immunized rats showed elevated bone loss scores. These experiments support the contention that a combination of hypersensitivity reactions (i.e., mixed hypersensitivity to Aa) could give rise to the periodontal pathology observed.

Congenitally athymic rats (nude) were shown to have more periodontal bone loss than did normal littermates. However, bone loss in thymus-cell reconstituted nude rats was not different from that in control rats. Normal rats receiving Aa-sensitized T lymphocytes prior to infection with Aa demonstrated increased DTH and periodontal bone loss. These studies support the concept that T-cell functions and thymic regulation of immune responses can exert protective and/or destructive effects in periodontal disease. In order to modify disease, it will be necessary to enhance the protective aspects of the immune response and to minimize the detrimental aspects.

REFERENCES

  • Horton, J.E.; Oppenheim, J.J.; and Mergenhagen, S.E.: A Role for Cell-mediated Immunity in the Pathogenesis of Periodontal Disease, J Periodontol 45:351-360, 1974.[Medline] [Order article via Infotrieve]
  • Horton, J.E.; Raisz, L.G.; Simmons, H.A.; Oppenheim, J.J.; and Mergenhagen, S.E.: Bone Resorbing Activity in Supernatant Fluid from Cultured Human Peripheral Blood Leukocytes, Science 177:793-795, 1972.[Abstract/Free Full Text]
  • WILDE, G.; COOPER, M.; and PAGE, R.C.: Host Tissue Response in Chronic Periodontal Disease. VI. The Role of Cell-mediated Hypersensitivity, J Periodont Res 12:179-196, 1977. 4. TAUBMAN, M.A.; BUCKELEW, J.M.; EBERSOLE, J.L.; and SMITH, D.J.: Periodontal Bone Loss and Immune Response to Ovalbumin in Germfree Rats Fed Antigen-Free Diet with Ovalbumin, Infect Immun 32:145-152, 1981.
  • Ivanyi, L. and Lehner, T.: Stimulation of Lymphocyte Transformation by Bacterial Antigens in Patients with Periodontal Disease, Arch Oral Biol 15:1089-1096, 1970.[CrossRef][Medline] [Order article via Infotrieve]
  • Patters, M.R.; Genco, R.J.; Reed, M.J.; and Mashimo, P.A.: Blastogenic Response of Human Lymphocytes to Oral Bacterial Antigens: Comparison of Individuals with Periodontal Disease to Normal and Edentulous Patients, Infect Immun 14:1213-1220,1976.[Abstract/Free Full Text]
  • Patters, M.R.; Sedransk, N.; and Genco, R.J.: The Lymphoproliferative Response During Human Experimental Gingivitis, J Periodont Res 14:269-278, 1979.[CrossRef][Medline] [Order article via Infotrieve]
  • Ivanyi, L.M.; Wilton, J.M.A.; and Lehner, T.: Cell-mediated Immunity in Periodontal Disease; Cytotoxicity, Migration Inhibition and Lymphocyte Transformation Studies, Immunology 22:141-145, 1972.[Medline] [Order article via Infotrieve]
  • Horton, J.E.; Oppenheim, J.J.; and Mergenhagen, S.E.: Elaboration of Lymphotoxin by Cultured Human Peripheral Blood Leukocytes Stimulated with Dental-Plaque Deposits, Clin Exp Immunol 13:383-393, 1973.[Medline] [Order article via Infotrieve]
  • Wahl, L.M.; Wahl, S.M.; Mergenhagen, S.E.; and
  • Martin, G.R.: Collagenase Production by Lymphokine-activated Macrophages, Science 187:261-263, 1975.[Abstract/Free Full Text]
  • Katz, D.H. and Benacerraf, B.: The Regulatory Influence of Activated T Cells on B Cell Responses to Antigen, Adv Immunol 15:1-94, 1972.[Medline] [Order article via Infotrieve]
  • Gershon, R.K.: T Cell Control of Antibody Production, Contemp Top Immunobiol 3:1-40, 1974.[Medline] [Order article via Infotrieve]
  • Cantor, H. and Weissman, I.: Development and Function of Subpopulations of Thymocytes and T Lymphocytes, Prog Allergy 20:1-64, 1976.[Medline] [Order article via Infotrieve]
  • Katz, D.H.; Hamaoka, T.; and BENACERRAF, B.; Cell Interactions Between Histoincompatible T and B Lymphocytes. II. Failure of Physiologic Cooperative Interactions Between T and B Lymphocytes from Allogenic Donor Strains in Humoral Response to Hapten-Protein Conjugates, J Exp Med 1:1405-1508, 1973.
  • Kindred, B. and Shreffler, D.C.: H-2 Dependence of Co-operation Between T and B Cells in vivo, J Immunol 109: 940-943, 1972.[Abstract/Free Full Text]
  • Germain, R.N. and Benacerraf, B.: Helper and Suppressor T Cell Factors, Springer Semin Immunopathol 3:93-127, 1980.[Medline] [Order article via Infotrieve]
  • Benacerraf, B.; Greene, M.I.; Sy, M.S.; and Dorf, M.E.: Suppressor T Cell Circuits, Ann NY Acad Sci 392:300-308, 1982.[CrossRef][Medline] [Order article via Infotrieve]
  • Blaese, R.M.: T and B Cell Immunodeficiency Diseases. In: Clinical Immunology, Vol. I, Parker, C.W., Ed., Philadelphia: W.B. Saunders, 1980, pp. 314-375.
  • Waldmann, T.A. and Broder, S.: Suppressor Cells on the Regulation of the Immune Response. In: Progress in Clinical Immunology, Vol. 3, Schwartz, R.S., Ed., New York: Grune and Stratton, 1977, pp. 155-199.
  • Mackler, B.F.; Frostad, K.B.; Robertson, P.B.; and Levy, B.M.: Immunoglobulin Bearing Lymphocytes and Plasma Cells in Human Periodontal Disease, J Periodont Res 12:37-45,1977.[CrossRef][Medline] [Order article via Infotrieve]
  • Seymour, G.J. and Greenspan, J.S.: The Phenotypic Characterization of Lymphocyte Subpopulations in Established Human Periodontal Disease, J Periodont Res 14:39-46, 1979.[CrossRef][Medline] [Order article via Infotrieve]
  • Taubman, M.A.; Buckelew, J.M.; Ebersole, J.L.; and Smith, D.J.: Periodontal Bone Loss in Ovalbumin Sensitized Germfree Rats Fed Antigen-Free Diet With Ovalbumin, J Periodont Res 18:324-332, 1983.
  • Lehner, T.: Cellular Aspects of Host Responses. Cellular Immunity in Periodontal Disease: An Overview. In: Host-Parasite Interactions in Periodontal Diseases, Genco, R.J. and Mergenhagen, S.E., Eds., Washington, D.C.: Amer. Soc. for Microbiol., 1982, pp. 202-216.
  • Socransky, S.S.: Microbiology of Periodontal Disease- Present Status and Future Considerations, J Periodontol 48: 497-504,1977.[Medline] [Order article via Infotrieve]
  • FRANK, R.: Bacterial Penetration in the Apical Pocket Wall of Advanced Periodontitis, J Periodont Res 15:563-573, 1980. 26. SAGLIE, F.; CARRANZA, F.; NEWMAN, M.; CHING, L.; and LEWIN, K.: Identification of Tissue Invading Bacteria in Human Periodontal Disease, J Periodont Res 17:452-455, 1982. 27. ALLENSPACH-PETRZILKA, G.E. and GUGGENHEIM, B.: Bacteroides melaninogenicus Subsp. Intermedius Invades Rat Gingival Tissue, J Dent Res 61:259, 1982.
  • Guggenheim, B.G.; Gaegauf-Zollinger, R.; Hefti, A.; and Burckhart, J.J.: The Effect of Cyclosporin A on Periodontal Disease in Rats Monoassociated with Actinomyces viscosus NY1, J Periodont Res 16:26-38, 1981.[CrossRef][Medline] [Order article via Infotrieve]
  • Nobreus, N.; Attstrom, R.; and Egelberg, J.: Effect of Anti-thymocyte Serum on Development of Gingivitis in Dogs, J Periodont Res 9:227-235, 1974.[CrossRef][Medline] [Order article via Infotrieve]
  • Fitzgerald, J.E.; Gebhart, B.M.; and Birdsell, D.C.: Murine Model for Analysis of the Immune Response to Oral Colonization, J Periodont Res 16:564-573, 1981.[CrossRef][Medline] [Order article via Infotrieve]
  • Rocklin, R.E.; Bendtzen, K.; and Greineder, D.: Mediators of Immunity: Lymphokines and Monokines, Adv Immunol 29:55-136, 1980.[Medline] [Order article via Infotrieve]
  • Nobreus, N.; Attstrom, R.; and Egelberg, J.: Effect
  • of Anti-thymocyte Serum on Chronic Gingival Inflammation in Dogs, J Periodont Res 9:236-244, 1974.[CrossRef][Medline] [Order article via Infotrieve]
  • Barefoot, D.H. and Silverman, M.S.: Alveolar Bone Loss in Thymectomized Golden Hamsters, J Periodont Res 48: 699-704, 1977.
  • Rylander, H.; Linde, J.; and Ahlestedt, S.: Experimental Gingivitis in Immunized Dogs, J Periodont Res 11: 339-348, 1976.[CrossRef][Medline] [Order article via Infotrieve]
  • AMSTAD-JOSSI, M. and SCHROEDER, H.E.: Age Related Alterations of Periodontal Structures Around the Cementoenamel Junction and of the Gingival Connective Tissue Composition in Germ-free Rats, J Periodont Res 13:76-90, 1978. 36. LISTGARTEN, M.A.: Similarity of Epithelial Relationships in the Gingiva of Rat and Man, J Periodontol 46:677-680, 1975. 37. IRVING, J.T.; SOCRANSKY, S.S.; and HEELEY, D.J.: Histologic Changes in Experimental Periodontal Disease in Gnotobiotic Rats and Conventional Hamsters, J Periodont Res 9: 73-80, 1974.
  • Irving, J.T.; Newman, M.G.; Socransky, S.S.; and Heeley, J.D.: Histologic Changes in Experimental Periodontal Disease in Rats Monoinfected with a Gram Negative Organism, Arch Oral Biol 20:217-220, 1975.[CrossRef][Medline] [Order article via Infotrieve]
  • Listgarten, M.A.; Johnson, D.; Nowotny, A.; Tanner, A.C.R.; and Socransky, S.S.: Histopathology of Periodontal Disease in Gnotobiotic Rats Monoinfected with Eikenella corrodens, J Periodont Res 13:134-148, 1978.[CrossRef][Medline] [Order article via Infotrieve]
  • Heijl, L.; Wennstrom, J.; and Socransky, S.S.: Periodontal Disease in Gnotobiotic Rats, J Periodont Res 15:405-419, 1980.[CrossRef][Medline] [Order article via Infotrieve]
  • Garant, P.R.: An Electron Microscopic Study of the Periodontal Tissues of Germfree Rats and Rats Monoinfected with Actinomyces naeslundii, J Periodont Res 11 (Suppl 15):9-79, 1976.[CrossRef]
  • Van Der Hoeven, J.S.; Mikx, F.H.; Plasschaert, A.J.; and Maltha, J.C.: Experimental Periodontal Disease in Rats Induced by Plaque Forming Microorganisms, J Periodont Res 10:143-147, 1975.[CrossRef][Medline] [Order article via Infotrieve]
  • Yoshie, H.; Taubman, M.A.; Ebersole, J.L.; Olson, C.L.; Smith, D.J.; and Pappo, J.: Actinobacillus actinomycetemcomitans is a B Cell Mitogen in Rats, Submitted for publication, 1984.
  • Chen, P.; Nair, B.C.; and Genco, R.J.: Lymphocyte Activation by Actinobacillus actinomycetemcomitans and its LPS, J Dent Res 60:524, 1981.
  • Smith, S.; Bick, P.H.; Miller, G.A.; Ranney, R.R.; Rice, P.L.; Lalor, J., II; and Tew, J.G.: Polyclonal B-cell Activation: Severe Periodontal Disease in Young Adults, Clin Immunol Immunopathol 16:354-366, 1980.[CrossRef][Medline] [Order article via Infotrieve]
  • Garant, P.R. and Cho, M.I.: Histopathogenesis of Spontaneous Periodontal Disease in Conventional Rats. III. The Mononuclear Cell Infiltrate and Cytoplasmic Changes in Associated Fibroblasts, J Periodont Res 15:165-176, 1980.[CrossRef][Medline] [Order article via Infotrieve]
  • Hay, J.B.: Delayed (Cellular) Hypersensitivity. In: Inflamma
  • tion, Immunity and Hypersensitivity, H.Z. Movat, Ed., Hagerstown, MD: Harper and Row, 1979, pp. 271-318.
  • Taubman, M.A.; Yoshie, H.; Wetherell, J.R., Jr.; Ebersole, J.L.; and Smith, D.J.: Immune Response and Periodontal Bone Loss in Germfree Rats Immunized and Infected with Actinobacillus actinomycetemcomitans, J Periodont Res 18:393-401, 1983.[CrossRef][Medline] [Order article via Infotrieve]
  • Festing, M.F.W.; May, D.; Connors, T.A.; Lovell, D.; and Sparrow, S.: An Athymic Nude Mutation in the Rat, Nature 274:356-366, 1978.
  • TAUBMAN, M.A.; EBERSOLE, J.L.; SMITH, D.J.; and SPRINGS, L.V.: The Nude Rat: Potential Model for Periodontal Disease Studies, IADR Progr & Abst 60:No. 459, 1981. 51. CRAWFORD, J.M.; TAUBMAN, M.A.; and SMITH, D.J.: The Natural History of Periodontal Bone Loss in Germ Free and Gnotobiotic Rats Infected with Periodontopathic Microorganisms, J Periodont Res 13:316-325, 1978.
  • Yoshie, H.; Taubman, M.A.; Olson, C.L.; Ebersole, J.L.; and Smith, D.J.: Periodontal Bone Loss and Immune Characteristics of Congenitally Athymic and Thymus Cell Reconstituted Athymic Rats, J Dent Res 62:273, 1983.
  • YOSHIE, H.; TAUBMAN, M.A.; OLSON, C.L.; EBERSOLE, J.L.; SMITH, D.J.; and HARA, K.: Effect of Transfer of Actinobacillus-Sensitized T Lymphocytes on Periodontal Bone in Infected Rats, AADR Progr & Abst 62:No. 663, 1983. 54. SALLAY, K.; SANAVI, F.; RING, I.; PHAM, P.; BEHLING, U.H.; and NOWOTNY, A.: Alveolar Bone Destruction in the Immunosuppressed Rat, J Periodont Res 17:263-274, 1982. 55. MACKLER, B.F.; ALTMAN, L.C.; WAHL, S.; ROSEN-STREICH, J.J.; OPPENHEIM, J.J.; and MERGENHAGEN, S.E.: Blastogenesis and Lymphokine Synthesis by T and B Lymphocytes from Patients with Periodontal Disease, Infect Immun 10:844-850, 1974.
  • Rocklin, E.W.; MacDermott, R.P.; Chess, L.; Schloss-Man, S.F.; and David, J.R.: Studies on Mediator Production by Highly Purified Human T and B Lymphocytes, J Exp Med 140:1303-1316, 1974.[Abstract/Free Full Text]
  • Chen, P.; Trummel, C.; Horton, J.; Baker, J.J.; and Oppenheim, J.J.: Production of Osteoclast Activating Factor by Normal Human Peripheral Blood Rosetting and Nonrosetting Lymphocytes, Eur J Immunol 6:732-736.
  • Mangan, D.R. and Lopatin, D.E.: In vitro Stimulation of Immunoglobulin Production from Human Peripheral Blood Lymphocytes by a Soluble Preparation of Actinomyces viscosus, Infect Immun 31:236-244, 1981.[Abstract/Free Full Text]
  • Clagett, J.; Engel, D.; and Chi, E.: In vitro Expression of Immunoglobulin M and G Subclasses by Murine B Lymphocytes in Response to a Polyclonal Activator from Actinomyces, Infect Immun 29:234-243, 1980.[Abstract/Free Full Text]
  • Hoffman, M.M. and Schour, I.: Quantitative Studies in the Development of the Rat Molar. II. Alveolar Bone, Cementum, and Eruption, Am J Orthod 26:854-874, 1940.

Journal of Dental Research, Vol. 63, No. 3, 455-460 (1984)
DOI: 10.1177/00220345840630031801


Add to CiteULike CiteULike   Add to Complore Complore   Add to Connotea Connotea   Add to Del.icio.us Del.icio.us   Add to Digg Digg   Add to Reddit Reddit   Add to Technorati Technorati   Add to Twitter Twitter    What's this?


This article has been cited by other articles:


Home page
Infect. Immun.Home page
M. Miyamoto, K. Ishihara, and K. Okuda
The Treponema denticola Surface Protease Dentilisin Degrades Interleukin-1{beta} (IL-1{beta}), IL-6, and Tumor Necrosis Factor Alpha
Infect. Immun., April 1, 2006; 74(4): 2462 - 2467.
[Abstract] [Full Text] [PDF]


Home page
J. Immunol.Home page
X. Han, T. Kawai, J. W. Eastcott, and M. A. Taubman
Bacterial-Responsive B Lymphocytes Induce Periodontal Bone Resorption
J. Immunol., January 1, 2006; 176(1): 625 - 631.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
H. C. Schreiner, K. Sinatra, J. B. Kaplan, D. Furgang, S. C. Kachlany, P. J. Planet, B. A. Perez, D. H. Figurski, and D. H. Fine
Tight-adherence genes of Actinobacillus actinomycetemcomitans are required for virulence in a rat model
PNAS, June 10, 2003; 100(12): 7295 - 7300.
[Abstract] [Full Text] [PDF]


Home page
CROBMHome page
E. Gemmell, K. Yamazaki, and G.J. Seymour
DESTRUCTIVE PERIODONTITIS LESIONS ARE DETERMINED BY THE NATURE OF THE LYMPHOCYTIC RESPONSE
Critical Reviews in Oral Biology & Medicine, January 1, 2002; 13(1): 17 - 34.
[Abstract] [Full Text] [PDF]


Home page
The Diabetes EducatorHome page
W. W. Hallmon and B. L. Mealey
Implications of Diabetes Mellitus and Periodontal Disease
The Diabetes Educator, January 1, 1992; 18(4): 310 - 315.
[PDF]


Home page
CROBMHome page
J. L. Ebersole
Systemic Humoral Immune Responses in Periodontal Disease
Critical Reviews in Oral Biology & Medicine, January 1, 1990; 1(4): 283 - 331.
[Full Text] [PDF]


Home page
ADRHome page
M.A. Taubman, E.D. Stoufi, G.J. Seymour, D.J. Smith, and J.L. Ebersole
Immunoregulatory Aspects of Periodontal Disease
Advances in Dental Research, November 1, 1988; 2(2): 328 - 333.
[Abstract] [PDF]


Home page
JDRHome page
G.J. Seymour
Invited Review: Possible Mechanisms Involved in the Immunoregulation of Chronic Inflammatory Periodontal Disease
Journal of Dental Research, January 1, 1987; 66(1): 2 - 9.
[Abstract] [PDF]


This Article
Right arrow Abstract Freely available
Right arrow Full Text (PDF)
Right arrow Alert me when this article is cited
Right arrow Alert me if a correction is posted
Right arrow Citation Map
Services
Right arrow Email this article to a friend
Right arrow Similar articles in this journal
Right arrow Similar articles in PubMed
Right arrow Alert me to new issues of the journal
Right arrow Add to Saved Citations
Right arrow Download to citation manager
Right arrowRequest Permissions
Right arrow Request Reprints
Right arrow Add to My Marked Citations
Citing Articles
Right arrow Citing Articles via HighWire
Right arrow Citing Articles via Google Scholar
Right arrow Citing Articles via Scopus
Google Scholar
Right arrow Articles by Taubman, M.A.
Right arrow Articles by Olson, C.L.
Right arrow Search for Related Content
PubMed
Right arrow PubMed Citation
Right arrow Articles by Taubman, M.A.
Right arrow Articles by Olson, C.L.
Social Bookmarking
 Add to CiteULike   Add to Complore   Add to Connotea   Add to Del.icio.us   Add to Digg   Add to Reddit   Add to Technorati   Add to Twitter  
What's this?