Role of smoking and type 2 diabetes in the immunobalance of advanced chronic periodontitis

Journal of Periodontology

Volumn 82, Issue 3, 2011, Pages 429-438

  Duarte, Poliana M ^a   Santos, Vanessa R ^a   Dos Santos, Fernanda A ^a   De Lima Pereira, Sanivia A ^b   Rodrigues, Denise B R ^b   Napimoga, Marcelo H ^b  

^a GUARULHOS UNIVERSITY   (Brazil)

^b UNIVERSITY OF UBERABA   (Brazil)

Author keywords

Diabetes mellitus; Inflammation; Periodontitis; Plasma cells; Regulatory; Smoking; T lymphocytes

Indexed keywords

FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, HUMAN; INTERLEUKIN 15; INTERLEUKIN 17;

ADULT; ANALYSIS OF VARIANCE; ARTICLE; CASE CONTROL STUDY; CD4+ T LYMPHOCYTE; CHI SQUARE DISTRIBUTION; CHRONIC PERIODONTITIS; FEMALE; GINGIVA; GINGIVA FIBROMATOSIS; HUMAN; IMMUNOLOGY; MALE; MIDDLE AGED; NEUTROPHIL CHEMOTAXIS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONPARAMETRIC TEST; PLASMA CELL; SMOKING; UPREGULATION;

ADULT; ANALYSIS OF VARIANCE; CASE-CONTROL STUDIES; CD4-POSITIVE T-LYMPHOCYTES; CHI-SQUARE DISTRIBUTION; CHRONIC PERIODONTITIS; DIABETES MELLITUS, TYPE 2; FEMALE; FIBROMATOSIS, GINGIVAL; FORKHEAD TRANSCRIPTION FACTORS; GINGIVA; HUMANS; INTERLEUKIN-15; INTERLEUKIN-17; MALE; MIDDLE AGED; NEUTROPHIL INFILTRATION; PLASMA CELLS; SMOKING; STATISTICS, NONPARAMETRIC; UP-REGULATION;

EID: 79952807113     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2010.100215     Document Type: Article

References (50)

1. Nunn ME. Understanding the etiology of periodontitis: An overview of periodontal risk factors. Periodontol 2000 2003;32:11-23. (Pubitemid 37487567)
2. Kinane DF, Mark Bartold P. Clinical relevance of the host responses of periodontitis. Periodontol 2000 2007; 43:278-293.
3. Emrich LJ, Shlossman M, Genco RJ. Periodontal disease in non-insulin-dependent diabetes mellitus. J Periodontol 1991;62:123-131.
4. Novak MJ, Potter RM, Blodgett J, Ebersole JL. Periodontal disease in Hispanic Americans with type 2 diabetes. J Periodontol 2008;79:629-636.
5. Stoltenberg JL, Osborn JB, Pihlstrom BL, et al. Association between cigarette smoking, bacterial pathogens, and periodontal status. J Periodontol 1993;64:1225-1230.
6. Haffajee AD, Socransky SS. Relationship of cigarette smoking to attachment level profiles. J Clin Periodontol 2001;28:283-295. (Pubitemid 33761337)
7. Gemmell E, Seymour GJ. Immunoregulatory control of Th1/Th2 cytokine profiles in periodontal disease. Periodontol 2000 2004;35:21-41. (Pubitemid 41742817)
8. Tesmer LA, Lundy SK, Sarkar S, Fox DA. Th17 cells in human disease. Immunol Rev 2008;223:87-113. (Pubitemid 351986173)
9. Cardoso CR, Garlet GP, Crippa GE, et al. Evidence of the presence of T helper type 17 cells in chronic lesions of human periodontal disease. Oral Microbiol Immunol 2009;24:1-6.
10. Dutzan N, Gamonal J, Silva A, Sanz M, Vernal R. Overexpression of forkhead box P3 and its association with receptor activator of nuclear factor-kappa B ligand, interleukin (IL)-17, IL-10 and transforming growth factor-beta during the progression of chronic periodontitis. J Clin Periodontol 2009; 36:396-403.
11. Fietta P, Delsante G. The effector T helper cell triade. Riv Biol 2009;102:61-74.
12. Kim HR, Hwang KA, Park SH, Kang I. IL-7 and IL-15: Biology and roles in T-cell immunity in health and disease. Crit Rev Immunol 2008;28:325-339.
13. McInnes IB, Gracie JA. Interleukin-15: A new cytokine target for the treatment of inflammatory diseases. Curr Opin Pharmacol 2004;4:392-397. (Pubitemid 38987067)
14. McInnes IB, Leung BP, Sturrock RD, Field M, Liew FY. Interleukin-15 mediates T cell-dependent regulation of tumor necrosis factor-alpha production in rheumatoid arthritis. Nat Med 1997;3:189-195. (Pubitemid 27064704)
15. Chen X, Jensen PE. The role of B lymphocytes as antigen-presenting cells. Arch Immunol Ther Exp (Warsz) 2008;56:77-83. (Pubitemid 351556111)
16. Ohlrich EJ, Cullinan MP, Seymour GJ. The immunopathogenesis of periodontal disease. Aust Dent J 2009; 54(Suppl. 1):S2-S10.
17. Seymour GJ, Gemmell E, Reinhardt RA, Eastcott J, Taubman MA. Immunopathogenesis of chronic inflammatory periodontal disease: Cellular and molecular mechanisms. J Periodontal Res 1993;28:478-486.
18. Ebersole JL, Taubman MA. The protective nature of host responses in periodontal diseases. Periodontol 2000 1994;5:112-141.
19. Berglundh T, Donati M, Zitzmann N. B cells in periodontitis - Friends or enemies? Periodontol 2000 2008;45:51-66.
20. Houri-Haddad Y, Wilensky A, Shapira L. T-cell phenotype as a risk factor for periodontal disease. Periodontol 2000 2007;45:67-75.
21. César-Neto JB, Duarte PM, de Oliveira MC, Tambeli CH, Sallum EA, Nociti FH Jr. Smoking modulates interleukin-6:interleukin-10 and RANKL:osteoprotegerin ratios in the periodontal tissues. J Periodontal Res 2007;42:184-191.
22. Duarte PM, de Oliveira MC, Tambeli CH, Parada CA, Casati MZ, Nociti FH Jr. Overexpression of interleukin- 1beta and interleukin-6 may play an important role in periodontal breakdown in type 2 diabetic patients. J Periodontal Res 2007;42:377-381.
23. Ryder MI, Wu TC, Kallaos SS, Hyun W. Alterations of neutrophil f-actin kinetics by tobacco smoke: Implications for periodontal diseases. J Periodontal Res 2002;37:286-292.
24. Araujo MW, Hovey KM, Benedek JR, et al. Reproducibility of probing depth measurement using a constant- force electronic probe: Analysis of inter- and intraexaminer variability. J Periodontol 2003;74:1736-1740. (Pubitemid 38181214)
25. Ainamo J, Bay I. Problems and proposals for recording gingivitis and plaque. Int Dent J 1975;25:229-235.
26. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6.
27. Magalhães ME, Cavalcanti BA, Cavalcanti S, Giannella- Neto D. Could pre-diabetes be considered a clinical condition? Opinions from an endocrinologist and a cardiologist. Diabetol Metab Syndr 2010;2:2.
28. Liang S, Hosur KB, Domon H, Hajishengallis G. Periodontal inflammation and bone loss in aged mice. J Periodontal Res 2010;45:574-578.
29. Benatti BB, Silvério KG, Casati MZ, Sallum EA, Nociti FH Jr. Inflammatory and bone-related genes are modulated by aging in human periodontal ligament cells. Cytokine 2009;46:176-181.
30. Bradshaw EM, Raddassi K, Elyaman W, et al. Monocytes from patients with type 1 diabetes spontaneously secrete proinflammatory cytokines inducing Th17 cells. J Immunol 2009;183:4432-4439.
31. Arababadi MK, Nosratabadi R, Hassanshahi G, et al. Nephropathic complication of type-2 diabetes is following pattern of autoimmune diseases? Diabetes Res Clin Pract 2010;87:33-37.
32. Sakaguchi S, Yamaguchi T, Nomura T, Ono M. Regulatory T cells and immune tolerance. Cell 2008;133: 775-787. (Pubitemid 351707693)
33. Majlessi L, Lo-Man R, Leclerc C. Regulatory B and T cells in infections. Microbes Infect 2008;10:1030-1035.
34. Nakajima T, Ueki-Maruyama K, Oda T, et al. Regulatory T-cells infiltrate periodontal disease tissues. J Dent Res 2005;84:639-643. (Pubitemid 43827846)
35. Koenen HJ, Fasse E, Joosten I. IL-15 and cognate antigen successfully expand de novo-induced human antigen-specific regulatory CD4+ T cells that require antigen-specific activation for suppression. J Immunol 2003;171:6431-6441. (Pubitemid 37532071)
36. Ruprecht CR, Gattorno M, Ferlito F, et al. Coexpression of CD25 and CD27 identifies FoxP3+ regulatory T cells in inflamed synovia. J Exp Med 2005;201:1793-1803. (Pubitemid 41002898)
37. Benito-Miguel M, García-Carmona Y, Balsa A, et al. A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+ CD25+ regulatory T cells and CD4+CD25- responder T cells. J Immunol 2009;183:8268-8279.
38. Kuczyński S, Winiarska H, Abramczyk M, Szczawińska K, Wierusz-Wysocka B, Dworacka M. IL-15 is elevated in serum patients with type 1 diabetes mellitus. Diabetes Res Clin Pract 2005;69:231-236. (Pubitemid 41140101)
39. Ferrari-Lacraz S, Zanelli E, Neuberg M, et al. Targeting IL-15 receptor-bearing cells with an antagonist mutant IL-15/Fc protein prevents disease development and progression in murine collagen-induced arthritis. JImmunol 2004;173:5818-5826. (Pubitemid 39392172)
40. Lappin DF, MacLeod CP, Kerr A, Mitchell T, Kinane DF. Anti-inflammatory cytokine IL-10 and T cell cytokine profile in periodontitis granulation tissue. Clin Exp Immunol 2001;123:294-300. (Pubitemid 32174782)
41. Johnson RB, Serio FG. The contribution of interleukin- 13 and -15 to the cytokine network within normal and diseased gingiva. J Periodontol 2007;78:691-695.
42. Xia J, Liu W, Hu B, Tian Z, Yang Y. IL-15 promotes regulatory T cell function and protects against diabetes development in NK-depleted NOD mice. Clin Immunol 2010;134:130-139.
43. Berglundh T, Donati M. Aspects of adaptive host response in periodontitis. J Clin Periodontol 2005; 32(Suppl. 6):87-107. (Pubitemid 41391059)
44. Hu CY, Rodriguez-Pinto D, Du W, et al. Treatment with CD20-specific antibody prevents and reverses autoimmunediabetes in mice. J Clin Invest 2007;117: 3857-3867. (Pubitemid 350224095)
45. Mariño E, Villanueva J, Walters S, Liuwantara D, Mackay F, Grey ST. CD4(+)CD25(+) T-cells control autoimmunity in the absence of B-cells. Diabetes 2009;58:1568-1577.
46. Fiorina P, Vergani A, Dada S, et al. Targeting CD22 reprograms B-cells and reverses autoimmune diabetes. Diabetes 2008;57:3013-3024.
47. Hein GE. Glycation endproducts in osteoporosis - Is there a pathophysiologic importance? Clin Chim Acta 2006;371:32-36. (Pubitemid 44164644)
48. Lalla E, Lamster IB, Drury S, Fu C, Schmidt AM. Hyperglycemia, glycoxidation and receptor for advanced glycation endproducts: Potential mechanisms underlying diabetic complications, including diabetesassociated periodontitis. Periodontol 2000 2000;23: 50-62.
49. King GL. The role of inflammatory cytokines in diabetes and its complications. J Periodontol 2008; 79(Suppl. 8):1527-1534.
50. Goh SY, Cooper ME. Clinical review: The role of advanced glycation end products in progression and complications of diabetes. J Clin Endocrinol Metab 2008;93:1143-1152. (Pubitemid 351519698)