Characterization of CD4+CD25+ natural regulatory T cells in the inflammatory infiltrate of human chronic periodontitis

Journal of Leukocyte Biology

Volumn 84, Issue 1, 2008, Pages 311-318

  Cardoso, Cristina Ribeiro ^a   Garlet, Gustavo Pompermaier ^a   Moreira, Ana Paula ^a   Martins Jr , Wálter ^b   Rossi, Marcos Antônio ^a   Silva, João Santana ^a  

^a UNIVERSITY OF SÃO PAULO   (Brazil)

^b UNIVERSITY OF RIBEIRÃO PRETO   (Brazil)

Author keywords

Gingival biopsies; Immune regulation; Inflammation; Periodontal disease; Tregs

Indexed keywords

CD103 ANTIGEN; CD45RO ANTIGEN; CHEMOKINE; CHEMOKINE RECEPTOR CCR4; CYTOTOXIC T LYMPHOCYTE ANTIGEN 4; GLUCOCORTICOID INDUCED TUMOR NECROSIS FACTOR RECEPTOR; INTERLEUKIN 10; MACROPHAGE DERIVED CHEMOKINE; MESSENGER RNA; THYMUS AND ACTIVATION REGULATED CHEMOKINE; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ADULT; ARTICLE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; FEMALE; GENE EXPRESSION; GINGIVAL BIOPSY; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOMODULATION; IMMUNOPATHOGENESIS; INFLAMMATORY INFILTRATE; MALE; PERIODONTITIS; PHENOTYPE; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE;

ADULT; ANTIGENS, CD4; CELL MOVEMENT; CHEMOKINE CCL17; CHEMOKINE CCL22; CHRONIC DISEASE; CYTOKINES; FORKHEAD TRANSCRIPTION FACTORS; GINGIVA; HUMANS; IMMUNOHISTOCHEMISTRY; INFLAMMATION; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; MICROSCOPY, CONFOCAL; PERIODONTITIS; PHENOTYPE; RECEPTORS, CHEMOKINE; T-LYMPHOCYTES, REGULATORY;

EID: 46949090340     PISSN: 07415400     EISSN: None     Source Type: Journal    
DOI: 10.1189/jlb.0108014     Document Type: Article

References (40)

1. Garlet, G. P., Avila-Campos, M. J., Milanezi, C. M., Ferreira, B. R., Silva, J. S. (2005) Actinobacillus actinomycetemcomitans-induced periodontal disease in mice: patterns of cytokine, chemokine, and chemokine receptor expression and leukocyte migration. Microbes Infect. 7, 738-747.
2. Madianos, P. N., Bobetsis, Y. A., Kinane, D. F. (2005) Generation of inflammatory stimuli: how bacteria set up inflammatory responses in the gingiva. J. Clin. Periodontol. 32 (Suppl. 6), 57-71.
3. Honda, T., Domon, H., Okui, T., Kajita, K., Amanuma, R., Yamazaki, K. (2006) Balance of inflammatory response in stable gingivitis and progressive periodontitis lesions. Clin. Exp. Immunol. 144, 35-40.
4. Okui, T., Ito, H., Honda, T., Amanuma, R., Yoshie, H., Yamazaki, K. (2008) Characterization of CD4(+) FOXP3(+) T-cell clones established from chronic inflammatory lesions. Oral Microbiol. Immunol. 23, 49-54.
5. Yamazaki, K., Ohsawa, Y., Tabeta, K., Ito, H., Ueki, K., Oda, T., Yoshie, H., Seymour, G. J. (2002) Accumulation of human heat shock protein 60-reactive T cells in the gingival tissues of periodontitis patients. Infect. Immun. 70, 2492-2501.
6. Wassenaar, A., Reinhardus, C., Thepen, T., Abraham-Inpijn, L., Kievits, F. (1995) Cloning, characterization, and antigen specificity of T-lymphocyte subsets extracted from gingival tissue of chronic adult periodontitis patients. Infect. Immun. 63, 2147-2153.
7. Ito, H., Honda, T., Domon, H., Oda, T., Okui, T., Amanuma, R., Nakajima, T., Yamazaki, K. (2005) Gene expression analysis of the CD4+ T-cell clones derived from gingival tissues of periodontitis patients. Oral Microbiol. Immunol. 20, 382-386.
8. Belkaid, Y., Rouse, B. T. (2005) Natural regulatory T cells in infectious disease. Nat. Immunol. 6, 353-360.
9. Campanelli, A. P., Roselino, A. M., Cavassani, K. A., Pereira, M. S., Mortara, R. A., Brodskyn, C. I., Goncalves, H. S., Belkaid, Y., Barral-Netto, M., Barral, A., Silva, J. S. (2006) CD4+CD25+ T cells in skin lesions of patients with cutaneous leishmaniasis exhibit phenotypic and functional characteristics of natural regulatory T cells. J. Infect. Dis. 193, 1313-1322.
10. Cavassani, K. A., Campanelli, A. P., Moreira, A. P., Vancim, J. O., Vitali, L. H., Mamede, R. C., Martinez, R., Silva, J. S. (2006) Systemic and local characterization of regulatory T cells in a chronic fungal infection in humans. J. Immunol. 177, 5811-5818.
11. Fehervari, Z., Sakaguchi, S. (2004) CD4+ Tregs and immune control. J. Clin. Invest. 114, 1209-1217.
12. Sakaguchi, S., Sakaguchi, N., Shimizu, J., Yamazaki, S., Sakihama, T., Itoh, M., Kuniyasu, Y., Nomura, T., Toda, M., Takahashi, T. (2001) Immunologic tolerance maintained by CD25+ CD4+ regulatory T cells: their common role in controlling autoimmunity, tumor immunity, and transplantation tolerance. Immunol. Rev. 182, 18-32.
13. Shevach, E. M. (2002) CD4+ CD25+ suppressor T cells: more questions than answers. Nat. Rev. Immunol. 2, 389-400.
14. Dieckmann, D., Plottner, H., Berchtold, S., Berger, T., Schuler, G. (2001) Ex vivo isolation and characterization of CD4(+)CD25(+) T cells with regulatory properties from human blood. J. Exp. Med. 193, 1303-1310.
15. Nakamura, K., Kitani, A., Fuss, I., Pedersen, A., Harada, N., Nawata, H., Strober, W. (2004) TGF-β 1 plays an important role in the mechanism of CD4+CD25+ regulatory T cell activity in both humans and mice. J. Immunol. 172, 834-842.
16. Fontenot, J. D., Gavin, M. A., Rudensky, A. Y. (2003) Foxp3 programs the development and function of CD4+CD25+ regulatory T cells. Nat. Immunol. 4, 330-336.
17. von Boehmer, H. (2005) Mechanisms of suppression by suppressor T cells. Nat. Immunol. 6, 338-344.
18. Collison, L. W., Workman, C. J., Kuo, T. T., Boyd, K., Wang, Y., Vignali, K. M., Cross, R., Sehy, D., Blumberg, R. S., Vignali, D. A. (2007) The inhibitory cytokine IL-35 contributes to regulatory T-cell function. Nature 450, 566-569.
19. Cao, X., Cai, S. F., Fehniger, T. A., Song, J., Collins, L. I., Piwnica-Worms, D. R., Ley, T. J. (2007) Granzyme B and perforin are important for regulatory T cell-mediated suppression of tumor clearance. Immunity 27, 635-646.
20. Mendez, S., Reckling, S. K., Piccirillo, C. A., Sacks, D., Belkaid, Y. (2004) Role for CD4(+) CD25(+) regulatory T cells in reactivation of persistent leishmaniasis and control of concomitant immunity. J. Exp. Med. 200, 201-210.
21. Guilliams, M., Oldenhove, G., Noel, W., Herin, M., Brys, L., Loi, P., Flamand, V., Moser, M., De Baetselier, P., Beschin, A. (2007) African trypanosomiasis: naturally occurring regulatory T cells favor trypanotolerance by limiting pathology associated with sustained type 1 inflammation. J. Immunol. 179, 2748-2757.
22. Iellem, A., Mariani, M., Lang, R., Recalde, H., Panina-Bordignon, P., Sinigaglia, F., D'Ambrosio, D. (2001) Unique chemotactic response profile and specific expression of chemokine receptors CCR4 and CCR8 by CD4(+)CD25(+) regulatory T cells. J. Exp. Med. 194, 847-853.
23. Li, M. O., Wan, Y. Y., Sanjabi, S., Robertson, A. K., Flavell, R. A. (2006) Transforming growth factor-β regulation of immune responses. Annu. Rev. Immunol. 24, 99-146.
24. Seymour, G. J., Gemmell, E., Reinhardt, R. A., Eastcott, J., Taubman, M. A. (1993) Immunopathogenesis of chronic inflammatory periodontal disease: cellular and molecular mechanisms. J. Periodontal Res. 28, 478-486.
25. Gamonal, J., Acevedo, A., Bascones, A., Jorge, O., Silva, A. (2001) Characterization of cellular infiltrate, detection of chemokine receptor CCR5 and interleukin-8 and RANTES chemokines in adult periodontitis. J. Periodontal Res. 36, 194-203.
26. Piccirillo, C. A., Thornton, A. M. (2004) Cornerstone of peripheral tolerance: naturally occurring CD4+CD25+ regulatory T cells. Trends Immunol. 25, 374-380.
27. Read, S., Malmstrom, V., Powrie, F. (2000) Cytotoxic T lymphocyte-associated antigen 4 plays an essential role in the function of CD25(+)CD4(+) regulatory cells that control intestinal inflammation. J. Exp. Med. 192, 295-302.
28. Baecher-Allan, C., Brown, J. A., Freeman, G. J., Hafler, D. A. (2001) CD4+CD25high regulatory cells in human peripheral blood. J. Immunol. 167, 1245-1253.
29. Suffia, I., Reckling, S. K., Salay, G., Belkaid, Y. (2005) A role for CD103 in the retention of CD4+CD25+ Treg and control of Leishmania major infection. J. Immunol. 174, 5444-5455.
30. Ernst, C. W., Lee, J. E., Nakanishi, T., Karimbux, N. Y., Rezende, T. M., Stashenko, P., Seki, M., Taubman, M. A., Kawai, T. (2007) Diminished forkhead box P3/CD25 double-positive T regulatory cells are associated with the increased nuclear factor-κB ligand (RANKL+) T cells in bone resorption lesion of periodontal disease. Clin. Exp. Immunol. 148, 271-280.
31. Garlet, G. P., Martins Jr., W., Fonseca, B. A., Ferreira, B. R., Silva, J. S. (2004) Matrix metalloproteinases, their physiological inhibitors and osteoclast factors are differentially regulated by the cytokine profile in human periodontal disease. J. Clin. Periodontol. 31, 671-679.
32. Pyzik, M., Piccirillo, C. A. (2007) TGF-β1 modulates Foxp3 expression and regulatory activity in distinct CD4+ T cell subsets. J. Leukoc. Biol. 82, 335-346.
33. Walther, M., Tongren, J. E., Andrews, L., Korbel, D., King, E., Fletcher, H., Andersen, R. F., Bejon, P., Thompson, F., Dunachie, S. J., Edele, F., de Souza, J. B., Sinden, R. E., Gilbert, S. C., Riley, E. M., Hill, A. V. (2005) Upregulation of TGF-β, FOXP3, and CD4+CD25+ regulatory T cells correlates with more rapid parasite growth in human malaria infection. Immunity 23, 287-296.
34. Carvalho, E. M., Bacellar, O., Brownell, C., Regis, T., Coffman, R. L., Reed, S. G. (1994) Restoration of IFN-γ production and lymphocyte proliferation in visceral leishmaniasis. J. Immunol. 152, 5949-5956.
35. Mitra, R. S., Judge, T. A., Nestle, F. O., Turka, L. A., Nickoloff, B. J. (1995) Psoriatic skin-derived dendritic cell function is inhibited by exogenous IL-10. Differential modulation of B7-1 (CD80) and B7-2 (CD86) expression. J. Immunol. 154, 2668-2677.
36. Gasim, S., Elhassan, A. M., Khalil, E. A., Ismail, A., Kadaru, A. M., Kharazmi, A., Theander, T. G. (1998) High levels of plasma IL-10 and expression of IL-10 by keratinocytes during visceral leishmaniasis predict subsequent development of post-kala-azar dermal leishmaniasis. Clin. Exp. Immunol. 111, 64-69.
37. Kane, M. M., Mosser, D. M. (2001) The role of IL-10 in promoting disease progression in leishmaniasis. J. Immunol. 166, 1141-1147.
38. Nakajima, T., Ueki-Maruyama, K., Oda, T., Ohsawa, Y., Ito, H., Seymour, G. J., Yamazaki, K. (2005) Regulatory T-cells infiltrate periodontal disease tissues. J. Dent. Res. 84, 639-643.
39. Belkaid, Y., Piccirillo, C. A., Mendez, S., Shevach, E. M., Sacks, D. L. (2002) CD4+CD25+ regulatory T cells control Leishmania major persistence and immunity. Nature 420, 502-507.
40. Cao, D., Malmstrom, V., Baecher-Allan, C., Hafler, D., Klareskog, L., Trollmo, C. (2003) Isolation and functional characterization of regulatory CD25brightCD4+ T cells from the target organ of patients with rheumatoid arthritis. Eur. J. Immunol. 33, 215-223.