Th2 cells and the IFN-γ R1 subunit in early and advanced experimental periodontitis in rats; an immunohistochemical study


  • Janaína Cavalcante Lemos Lemos Universidade Potiguar – UnP
  • Bruno César de Vasconcelos Gurgel Universidade Federal do Rio Grande do Norte – UFRN



Rats, Periodontal diseases, Th1 cells, Th2 cells, Cytokines, Immunohistochemistry


Aim: To evaluate the involvement of Th2 cells in different periods of the active phase of experimental periodontal disease and expression of the R1 subunit of the receptor for IFN-γ during the early and advanced progression of the disease. Methods: Experimental periodontitis was induced in 30 male Wistar rats by placing cotton ligatures around the mandibular first molars. The rats were then randomly assigned into two groups: G1=15 and G2=15, in group G1, ligatures were maintained for 2 days, a period that corresponds to the initial stage of periodontal disease in rats, in G2 ligatures were left for 15 days, a period that corresponds to the advanced stage of periodontal disease. The contra-lateral teeth served as controls (unligated). An immunohistochemical investigation of the gingival tissue was performed to detect the presence of the Th2 specific transcription factor (GATA3). Results: Light microscopy analysis revealed a decreased expression of GATA-3-positive cells when bone loss progressed. IFN-γ R1 was detected at an early stage during the active phase of disease, but the expression of positive cells remained unaltered during the remaining period of the study. Conclusions: These results indicate that the Th2 response may have a protective role during the pathogenesis of experimental periodontal disease, and that the IFN-γ R1 subunit may not be associated with periodontal disease progression.


Download data is not yet available.


Metrics Loading ...

Author Biographies

Janaína Cavalcante Lemos Lemos, Universidade Potiguar – UnP

Universidade Potiguar - UnP, Faculdade de Odontologia, Departamento / Área de Periodontia

Bruno César de Vasconcelos Gurgel, Universidade Federal do Rio Grande do Norte – UFRN

Faculdade de Odontologia, Departamento / Área de Periodontia


Ianni M, Bruzzesi G, Pugliese D, Porcellini E, Carbone I, Schiavone A, et al. Variations in inflammatory genes are associated with periodontitis. Immun Ageing. 2013; 10:1-8.

Yucel-Lindberg T, Båge T. Inflammatory mediators in the pathogenesis of periodontitis. Expert Rev Mol Med. 2013; 15: e7.

Kayal RA. The role of osteoimmunology in periodontal disease. Biomed Res Int. 2013; 2013: 1-12.

Yamamoto M, Fujihshi K, Hiroi T, McGhee JR, Van Dyke TE, Kiyono H. Molecular and cellular mechanisms for periodontal diseases: role of Th1 and Th2 type cytokines induction of mucosal inflammation. J Periodontal Res. 1997; 32: 115-9.

Di Benedetto A, Gigante I, Colucci S, Grano M. Periodontal disease: linking the primary inflammation to bone loss. Clin Dev Immunol. 2013; 2013: 1-7.

Teng YTA. The role of acquired immunity and periodontal disease progression. Crit Rev Oral Biol Med. 2003; 14: 237-52.

Okoye IS, Wilson MS. CD4+ T helper 2 cells – microbial triggers, differentiation requirements and effector functions. Immunology. 2011; 134: 368-77.

Glowacki AJ, Yoshizawa S, Jhunjhunwala S, Vieira AE, Garlet GP, Sfeir C, et al. Prevention of inflammation-mediated bone loss in murine and canine periodontal disease via recruitment of regulatory lymphocytes. Proc Natl Acad Sci USA. 2013; 12: 18525-30.

Garlet GP. Destructive and protective roles of cytokines in periodontitis: A re-appraisal from host defense and tissue destruction viewpoints. J Dent Res. 2010; 89: 1349-63.

Fu QY, Zhang L, Duan L, Qian SY, Pang HX. Correlation of chronic periodontitis in tropical area and IFN-ã, IL-10, IL-17 levels. Asian Pac J Trop Med. 2013; 6: 489-92.

Baker PJ, Boutaugh NR, Tiffany M, Roopenian DC. B Cell IgD Deletion Prevents Alveolar Bone Loss following murine oral infection. Interdiscip Perspect Infect Dis. 2009; 2009: 1-6.

Chakir H, Wang H, Lefebvre DE, Webb J, Scott FW. T-bet/GATA-3 ratio as a measure of the Th1/Th2 cytokine profile in mixed cell populations: predominant role of GATA-3. J Immunol Methods. 2003; 278: 157-69.

Teng YTA. Mixed Periodontal Th1-Th2 cytokine profile in Actinobacillus actinomycetencomitans – specific osteoprotegerin ligand (or RANK-L) – mediated alveolar bone destruction in vivo. Infect Immun. 2002; 70: 5269-73.

Kuhr A, Popa Wagner A, Schmoll H, Schwahn C, Kocher T. Observations on experimental marginal periodontitis in rats. J Periodontal Res. 2004; 39: 101-6.

Nagasupriya A, Rao DB, Ravikanth M, Kumar NG, Ramachandran CR, Saraswathi TR. Immunohistochemical expression of matrix metalloproteinase 13 in chronic periodontitis. Int J Periodontics Restorative Dent. 2014; 34: 79-84.

Noh MK, Jung M, Kim SH, Lee SR, Park KH, Kim DH, et al. Assessment of IL-6, IL-8 and TNF-á levels in the gingival tissue of patients with periodontitis. Exp Ther Med. 2013; 6: 847-51.

O’Garra A. Cytokines induce the development of functionally heterogeneous T helper cell subsets. Immunity. 1998; 8: 275-83.

Gemmell E, Seymour GJ. Immunoregulatory control of Th1/Th2 cytokine profiles in peridontal disease. Periodontology 2000. 2004; 35: 21-41.

Sasaki H, Okamatsu Y, Kawai T, Taubman M, Stashenko P. The interleukin- 10 knockout mouse is highly susceptible to Porphyromonas gingivalisinduced alveolar bone loss. J Periodontal Res. 2004; 39: 432-41.

Zhao L, Zhou Y, Xu Y, Sun Y, Li L, Chen W. Effect of non-surgical periodontal therapy on the levels of Th17/Th1/Th2 cytokines and their transcription factors in Chinese chronic periodontitis patients. J Clin Periodontol. 2011; 38: 509-16.

Graves DT, Fine D, Teng YT, Van Dyke TE, Hajishengallis G. The use of rodent models to investigate host-bacteria interactions related to periodontal diseases. J Clin Periodontol. 2008; 35: 89-105.

Cavagni J, Soletti AC, Gaio EJ, Rösing CK. The effect of dexamethasone in the pathogenesis of ligature-induced periodontal disease in Wistar rats. Braz Oral Res. 2005; 19: 290-4.

Gurgel BC, Duarte PM, Nociti FH JR, Sallum EA, Casat MZ, Sallum AW, et al. Impact of an anti-inflammatory therapy and its withdrawal on the progression of experimental periodontitis in rats. J Periodontol. 2004; 75: 1613-8.

Galvão MP, Chapper A, Rösing CK, Ferreira MB, De Souza MA. Methodological considerations on descriptive studies of induced periodontal disease in rats. Pesq Odontol Bras. 2003; 17: 56-62.

Souza DM; Ricardo LH; Rocha RF. Effects of alcohol intake in periodontitis progression in female rats: a histometric study. Braz J Oral Sci. 2013; 13: 229-34.

Oz HS, Puleo DA. Animal models for periodontal diseases. J Biomed Biotechnol. 2011; 1- 8.

Lins RD, Figueiredo CR, Queiroz LM, Da Silveira EJ, Freitas RA. Immunohistoquemical evaluation of the inflammatory response in periodontal disease. Braz Dent J. 2008; 19: 9-14.

Oliver-Bell J, Butcher JP, Malcolm J, MacLeod MK, Adrados Planell A, Campbell L, et al. Periodontitis in the absence of B cells and specific antibacterial antibody. Mol Oral Microbiol. 2015; 30: 160-9.

Yamazaki K, Nakajima T, Hara K. Immunohistological analysis of T cell functional subsets in chronic inflammatory periodontal disease. Clin Exp Immunol. 1995; 99: 384-91.

Nyman S, Schroeder HE, Lindhe J. Supression of inflammation and bone resorption by indomethacin durin experimental periodontitis in dogs. J Periodontol. 1979; 50: 450-61.

Arun KV, Talwar A, Kumar TS. T-helper cells in the etiopathogenesis of periodontal disease: A mini review. J Indian Soc Periodontol. 2011; 15: 4-10.

Pradeep AR, Roopa Y, Swati PP. Interleukin-4, a T-helper 2 cell cytokine, is associated with the remission of periodontal disease. J Periodontal Res. 2008; 43: 712-6.

Berker E, Kantarci A, Hasturk H, Van Dyke TE. Blocking proinflammatory cytokine release modulates peripheral blood mononuclear cell response to Porphyromonas gingivalis. J Periodontol. 2013; 84: 1337-45.

Behfarnia P, Birang R, Pishva SS, Hakemi MG, Khorasani MM. Expression levels of th-2 and th-17 characteristic genes in healthy tissue versus periodontitis. J Dent (Tehran). 2013; 10: 23-31.

Ukai T, Mori Y, Onoyama M, Hara Y. Immunohistological study of interferon-gamma- and interleukin-4-bearing cells in human periodontitis gingiva. Arch Oral Biol. 2001; 46: 901-8.

Talwar A, Arun KV, Kumar TSS, Clements J. Plasticity of T helper cell subsets: Implications in periodontal disease. J Indian Soc Periodontol. 2013; 17: 288-91.

Bach EA, Aguet M, Schreiber RD. The IFN gamma receptor: a paradigm for cytokine receptor signaling. Ann Rev Immunol. 1997; 15: 563-91.

Skarenta H, Yang Y, Pestka S, Fathman CG. Ligand-independent downregulation of IFN-? Receptor 1 following TCR engagement. J Immunol. 2000; 164: 3506-11.

Alayan J, Ivanovski S, Farah CS. Alveolar bone loss in T helper 1/T helper 2 cytokine-deficient mice. J Periodontal Res. 2007; 42: 97-103.



How to Cite

Lemos JCL, Gurgel BC de V. Th2 cells and the IFN-γ R1 subunit in early and advanced experimental periodontitis in rats; an immunohistochemical study. Braz. J. Oral Sci. [Internet]. 2015 May 28 [cited 2022 Dec. 8];14(2):106-11. Available from:




Most read articles by the same author(s)