Influence of inflammasome NLRP3, and IL1B and IL2 gene polymorphisms in periodontitis susceptibility
Autoři:
Josiane Bazzo de Alencar aff001; Joana Maira Valentini Zacarias aff001; Patrícia Yumeko Tsuneto aff001; Victor Hugo de Souza aff001; Cléverson de Oliveira e Silva aff002; Jeane Eliete Laguila Visentainer aff001; Ana Maria Sell aff001
Působiště autorů:
Department of Clinical Analysis and Biomedicine, Post-Graduation Program in Biosciences and Physiophatology, State University of Maringá, Maringá, Paraná, Brazil
aff001; Department of Dentistry, State University of Maringá, Maringá, Paraná, Brazil
aff002; Department of Basic Health Sciences, State University of Maringá, Maringá, Paraná, Brazil
aff003
Vyšlo v časopise:
PLoS ONE 15(1)
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pone.0227905
Souhrn
The pathogenesis of periodontitis (PD) involves several molecules of the immune system that interact in a network to eliminate the periodontopathogens, yet, they contribute to periodontal tissue destruction. The different mechanisms that lead to periodontal tissue damage are not clear. Despite this, immune response genes have been related to the development of PD previously, such as those involved in inflammasomes which are multiprotein complexes and cytokines including Interleukin-1. The aim of the study was to evaluate the polymorphisms in NLRP3 inflammasome, cytokine and receptor of cytokines genes in the development of periodontitis. This case-control study was conducted in 186 patients with PD (stage II and III and grade B) and 208 controls (localized gingivitis and periodontally healthy individuals). Genotyping was performed using PCR-RFLP for the SNP rs4612666 in NLRP3 and using PCR-SSP for IL1A, IL1B, IL1R, IL1RN, IL4RA, INFG, TGFB1, TNF, IL2, IL4, IL6, and IL10. Cytokine serum levels were measured using Luminex technology. SNPStats and OpenEpi software were used to perform statistical analysis. The higher frequencies of NLRP3 T/C and IL1B -511 T/T genotypes and IL2 (+166, -330) GT haplotype were observed in patients with PD compared to controls. The SNPs in NLRP3, IL1R +1970, IL6–174, TNF -308, IL2 +166 and -330, TGFB1 +869 and +915, IL4RA +1902, IL4–1098 and -590 were associated to PD in men. In conclusion, polymorphisms in NLRP3, IL1B and IL2 genes were associated to PD susceptibility. Men carrying the NLRP3, IL1R, IL6, TNF, IL2, TGFB1, IL4RA and IL4 polymorphisms had greater susceptibility than women for developing PD.
Klíčová slova:
Brazil – Cytokines – Haplotypes – Immune response – Inflammasomes – Periodontitis – Smoking habits – Variant genotypes
Zdroje
1. Nazir MA. Prevalence of periodontal disease, its association with systemic diseases and prevention. Int J Health Sci (Qassim). 2017;11(2): 72–80.
2. Hong M, Kim HY, Seok H, Yeo CD, Kim YS, Song JY, et al. Prevalence and risk factors of periodontitis among adults with or without diabetes mellitus. Korean J Intern Med. 2016;31(5): 910–9. doi: 10.3904/kjim.2016.031 27604799
3. Contreras A, Moreno SM, Jaramillo A, Pelaez M, Duque A, Botero JE, et al. Periodontal microbiology in Latin America. Periodontol 2000. 2015;67(1): 58–86. doi: 10.1111/prd.12074 25494598
4. Honda T, Domon H, Okui T, Kajita K, Amanuma R, Yamazaki K. Balance of inflammatory response in stable gingivitis and progressive periodontitis lesions. Clin Exp Immunol. 2006;144(1): 35–40. doi: 10.1111/j.1365-2249.2006.03028.x 16542362
5. Okui T, Aoki-Nonaka Y, Nakajima T, Yamazaki K. The Role of Distinct T Cell Subsets in Periodontitis-Studies from Humans and Rodent Models. Curr Oral Heal Reports. 2014;1(2): 114–23.
6. Nibali L, Di Iorio A, Tu Y-K, Vieira AR. Host genetics role in the pathogenesis of periodontal disease and caries. J Clin Periodontol. 2017;44: S52–78. doi: 10.1111/jcpe.12639 27754553
7. Heidari Z, Moudi B, Mahmoudzadeh-Sagheb H. Immunomodulatory factors gene polymorphisms in chronic periodontitis: an overview. BMC Oral Health. 2019;19(1): 29. doi: 10.1186/s12903-019-0715-7 30755190
8. Wang HF, He FQ, Xu CJ, Li DM, Sun XJ, Chi YT, et al. Association between the interleukin-1β C-511T polymorphism and periodontitis: a meta-analysis in the Chinese population. Genet Mol Res. 2017;16(1): 1–9.
9. Nikolopoulos GK, Dimou NL, Hamodrakas SJ, Bagos PG. Cytokine gene polymorphisms in periodontal disease: a meta-analysis of 53 studies including 4178 cases and 4590 controls. J Clin Periodontol. 2008;35(9): 754–67. doi: 10.1111/j.1600-051X.2008.01298.x 18673406
10. Lavu V, Venkatesan V, Venkata Kameswara Subrahmanya Lakka B, Venugopal P, Paul SFD, Rao SR. Polymorphic Regions in the Interleukin-1 Gene and Susceptibility to Chronic Periodontitis: A Genetic Association Study. Genet Test Mol Biomarkers. 2015;19(4): 175–81. doi: 10.1089/gtmb.2014.0275 25710474
11. Scarel-Caminaga RM, Trevilatto PC, Souza AP, Brito RB, Line SRP. Investigation of an IL-2 polymorphism in patients with different levels of chronic periodontitis. J Clin Periodontol. 2002;29(7): 587–91. doi: 10.1034/j.1600-051x.2002.290701.x 12354082
12. Reichert S, Machulla HKG, Klapproth J, Zimmermann U, Reichert Y, Gläser C, et al. Interleukin-2 −330 and 166 gene polymorphisms in relation to aggressive or chronic periodontitis and the presence of periodontopathic bacteria. J Periodontal Res. 2009;44(5): 628–35. doi: 10.1111/j.1600-0765.2008.01173.x 19453859
13. Tsuneto PY, de Souza VH, de Alencar JB, Zacarias JMV, Silva CO, Visentainer JEL, et al. IL18 Polymorphism and Periodontitis Susceptibility, Regardless of IL12B, MMP9, and Smoking Habits. Mediators Inflamm. 2019;2019: 1–9.
14. Ara T, Kurata K, Hirai K, Uchihashi T, Uematsu T, Imamura Y, et al. Human gingival fibroblasts are critical in sustaining inflammation in periodontal disease. J Periodontal Res. 2009;44(1): 21–7. doi: 10.1111/j.1600-0765.2007.01041.x 19515019
15. 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(12): 1349–63. doi: 10.1177/0022034510376402 20739705
16. Sell AM, de Alencar JB, Visentainer JEL, Silva CO. Immunopathogenesis of Chronic Periodontitis. In: Periodontitis—A Useful Reference. InTech. 2017. doi: 10.5772/intechopen.69045
17. Tomás I, Arias-Bujanda N, Alonso-Sampedro M, Casares-De-Cal MA, Sánchez-Sellero C, Suárez-Quintanilla D, et al. Cytokine-based Predictive Models to Estimate the Probability of Chronic Periodontitis: Development of Diagnostic Nomograms. Sci Rep. 2017;7(1): 11580. doi: 10.1038/s41598-017-06674-2 28912468
18. Tâlvan, Chisnoiu D, Rs C. Expression of Interleukin (IL)-1β, IL-8, IL-10 and IL-13 in Chronic Adult Periodontitis Progression. Arch Med. 2017;9. doi: 10.21767/1989-5216.1000219
19. Perozini C, Chibebe PCA, Leao MVP, Queiroz C da S, Pallos D. Gingival crevicular fluid biochemical markers in periodontal disease: a cross-sectional study. Quintessence Int. 2010;41(10): 877–83. 20927426
20. Miller CS, King CP, Langub MC, Kryscio RJ, Thomas MV. Salivary biomarkers of existing periodontal disease: a cross-sectional study. J Am Dent Assoc. 2006;137(3): 322–9. doi: 10.14219/jada.archive.2006.0181 16570465
21. Hou LT, Liu CM, Rossomando EF. Crevicular interleukin-1 beta in moderate and severe periodontitis patients and the effect of phase I periodontal treatment. J Clin Periodontol. 1995;22(2): 162–7. doi: 10.1111/j.1600-051x.1995.tb00128.x 7775673
22. Holmlund A, Hanstrom L, Lerner UH. Bone resorbing activity and cytokine levels in gingival crevicular fluid before and after treatment of periodontal disease. J Clin Periodontol. 2004;31(6): 475–82. doi: 10.1111/j.1600-051X.2004.00504.x 15142219
23. Thunell DH, Tymkiw KD, Johnson GK, Joly S, Burnell KK, Cavanaugh JE, et al. A multiplex immunoassay demonstrates reductions in gingival crevicular fluid cytokines following initial periodontal therapy. J Periodontal Res. 2010;45(1): 148–52. doi: 10.1111/j.1600-0765.2009.01204.x 19602112
24. Goutoudi P, Diza E, Arvanitidou M. Effect of periodontal therapy on crevicular fluid interleukin-1β and interleukin-10 levels in chronic periodontitis. J Dent. 2004;32(7): 511–20. doi: 10.1016/j.jdent.2004.04.003 15304296
25. Aral K, Aral CA, Kapila Y. Six-month clinical outcomes of non-surgical periodontal treatment with antibiotics on apoptosis markers in aggressive periodontitis. Oral Dis. 2019;25(3): 839–47. doi: 10.1111/odi.13032 30614174
26. Dagenais M, Skeldon A, Saleh M. The inflammasome: in memory of Dr. Jurg Tschopp. Cell Death Differ. 2012;19(1): 5–12. doi: 10.1038/cdd.2011.159 22075986
27. Abdul-Sater AA, Saïd-Sadier N, Ojcius DM, Yilmaz O, Kelly KA. Inflammasomes bridge signaling between pathogen identification and the immune response. Drugs Today (Barc). 2009;45 Suppl B:105–12.
28. García-Hernández AL, Muñoz-Saavedra ÁE, González-Alva P, Moreno-Fierros L, Llamosas-Hernández FE, Cifuentes-Mendiola SE, et al. Upregulation of proteins of the NLRP3 inflammasome in patients with periodontitis and uncontrolled type 2 diabetes. Oral Dis. 2018;25(2): odi.13003.
29. Zhen Y, Zhang H. NLRP3 inflammasome and inflammatory bowel disease. Vol. 10, Frontiers in Immunology. Front Immunol. 2019;10:276. doi: 10.3389/fimmu.2019.00276 30873162
30. Isaza-Guzmán DM, Medina-Piedrahíta VM, Gutiérrez-Henao C, Tobón-Arroyave SI. Salivary Levels of NLRP3 Inflammasome-Related Proteins as Potential Biomarkers of Periodontal Clinical Status. J Periodontol. 2017;88(12): 1329–38. doi: 10.1902/jop.2017.170244 28691886
31. Aral K, Berdeli E, Cooper PR, Milward MR, Kapila Y, Berdeli A, et al. Differential expression of inflammasome regulatory transcripts in periodontal disease. J Periodontol. 2019. doi: 10.1002/JPER.19-0222 31557327
32. Bostanci N, Emingil G, Saygan B, Turkoglu O, Atilla G, Curtis MA, et al. Expression and regulation of the NALP3 inflammasome complex in periodontal diseases. Clin Exp Immunol. 2009;157(3): 415–22. doi: 10.1111/j.1365-2249.2009.03972.x 19664151
33. Zhou X, Zhang P, Wang Q, Ji N, Xia S, Ding Y, et al. Metformin ameliorates experimental diabetic periodontitis independently of mammalian target of rapamycin (mTOR) inhibition by reducing NIMA-related kinase 7 (Nek7) expression. J Periodontol. 2019;90(9): 1032–42. doi: 10.1002/JPER.18-0528 30945296
34. McAllister MJ, Chemaly M, Eakin AJ, Gibson DS, McGilligan VE. NLRP3 as a potentially novel biomarker for the management of osteoarthritis. Osteoarthr Cartil. 2018;26(5): 612–9. doi: 10.1016/j.joca.2018.02.901 29499288
35. He H, Jiang H, Chen Y, Ye J, Wang A, Wang C, et al. Oridonin is a covalent NLRP3 inhibitor with strong anti-inflammasome activity. Nat Commun. 2018;9(1): 2550. doi: 10.1038/s41467-018-04947-6 29959312
36. Zhao D, Wu Y, Zhuang J, Xu C, Zhang F. Activation of NLRP1 and NLRP3 inflammasomes contributed to cyclic stretch-induced pyroptosis and release of IL-1β in human periodontal ligament cells. Oncotarget. 2016;7(42):68292–302. doi: 10.18632/oncotarget.11944 27626170
37. Rocha FRG, Delitto AE, de Souza JAC, Maldonado LAG, Wallet SM, Rossa C. NLRC4 inflammasome has a protective role on inflammatory bone resorption in a murine model of periodontal disease. Immunobiology. 2019. doi: 10.1016/j.imbio.2019.10.004 31848028
38. Park E, Na HS, Song Y-R, Shin SY, Kim Y-M, Chung J. Activation of NLRP3 and AIM2 Inflammasomes by Porphyromonas gingivalis Infection. Bäumler AJ, editor. Infect Immun. 2014;82(1): 112–23. doi: 10.1128/IAI.00862-13 24126516
39. Xue F, Shu R, Xie Y. The expression of NLRP3, NLRP1 and AIM2 in the gingival tissue of periodontitis patients: RT-PCR study and immunohistochemistry. Arch Oral Biol. 2015;60(6): 948–58. doi: 10.1016/j.archoralbio.2015.03.005 25841070
40. Bostanci N, Meier A, Guggenheim B, Belibasakis GN. Regulation of NLRP3 and AIM2 inflammasome gene expression levels in gingival fibroblasts by oral biofilms. Cell Immunol. 2011;270(1): 88–93. doi: 10.1016/j.cellimm.2011.04.002 21550598
41. Ries WL, Seeds MC, Key LL. Interleukin-2 stimulates osteoclastic activity; Increased acid production and radioactive calcium release. J Periodontal Res. 1989;24(4): 242–6. doi: 10.1111/j.1600-0765.1989.tb01788.x 2528623
42. Cerdan C, Martin Y, Courcoul M, Mawas C, Birg F, Olive D. CD28 costimulation up-regulates long-term IL-2R beta expression in human T cells through combined transcriptional and post-transcriptional regulation. J Immunol. 1995;154(3): 1007–13. 7822778
43. Arias-Bujanda N, Regueira-Iglesias A, Alonso-Sampedro M, González-Peteiro MM, Mira A, Balsa-Castro C, et al. Cytokine Thresholds in Gingival Crevicular Fluid with Potential Diagnosis of Chronic Periodontitis Differentiating by Smoking Status. Sci Rep. 2018;8(1):18003. doi: 10.1038/s41598-018-35920-4 30573746
44. Rosenberg NA, Huang L, Jewett EM, Szpiech ZA, Jankovic I, Boehnke M. Genome-wide association studies in diverse populations. Nat Rev Genet. 2010;11(5): 356–66. doi: 10.1038/nrg2760 20395969
45. Armitage GC. Development of a Classification System for Periodontal Diseases and Conditions. Ann Periodontol. 1999;4(1): 1–6. doi: 10.1902/annals.1999.4.1.1 10863370
46. Papapanou PN, Sanz M, Buduneli N, Dietrich T, Feres M, Fine DH, et al. Periodontitis: Consensus report of workgroup 2 of the 2017 World Workshop on the Classification of Periodontal and Peri-Implant Diseases and Conditions. J Periodontol. 2018;89: S173–82. doi: 10.1002/JPER.17-0721 29926951
47. Probst CM, Bompeixe EP, Pereira NF, de O Dalalio MM, Visentainer JE, Tsuneto LT, et al. HLA polymorphism and evaluation of European, African, and Amerindian contribution to the white and mulatto populations from Paraná, Brazil. Hum Biol. 2000;72(4): 597–617. 11048789
48. Reis PG, Ambrosio-Albuquerque EP, Fabreti-Oliveira RA, Moliterno RA, de Souza VH, Sell AM, et al. HLA-A, -B, -DRB1, -DQA1, and -DQB1 profile in a population from southern Brazil. HLA. 2018;92(5): 298–303. doi: 10.1111/tan.13368 30225991
49. Bergström J, Eliasson S, Dock J. A 10-Year Prospective Study of Tobacco Smoking and Periodontal Health. J Periodontol. 2000;71(8): 1338–47. doi: 10.1902/jop.2000.71.8.1338 10972650
50. John SW, Weitzner G, Rozen R, Scriver CR. A rapid procedure for extracting genomic DNA from leukocytes. Nucleic Acids Res. 1991;19(2): 408. doi: 10.1093/nar/19.2.408 2014181
51. Zheng Y, Zhang D, Zhang L, Fu M, Zeng Y, Russell R. Variants of NLRP3 gene are associated with insulin resistance in Chinese Han population with type-2 diabetes. Gene. 2013;530(1): 151–4. doi: 10.1016/j.gene.2013.07.082 23973727
52. Solé X, Guinó E, Valls J, Iniesta R, Moreno V. SNPStats: a web tool for the analysis of association studies. Bioinformatics. 2006;22(15): 1928–9. doi: 10.1093/bioinformatics/btl268 16720584
53. Slatkin M. Linkage disequilibrium—understanding the evolutionary past and mapping the medical future. Nat Rev Genet. 2008;9(6): 477–85. doi: 10.1038/nrg2361 18427557
54. Gauderman WJ. Sample size requirements for matched case-control studies of gene-environment interaction. Stat Med. 2002;21(1): 35–50. doi: 10.1002/sim.973 11782049
55. Isaza-Guzmán DM, Hernández-Viana M, Bonilla-León DM, Hurtado-Cadavid MC, Tobón-Arroyave SI. Determination of NLRP3 (rs4612666) and IL-1B (rs1143634) genetic polymorphisms in periodontally diseased and healthy subjects. Arch Oral Biol. 2016;65: 44–51. doi: 10.1016/j.archoralbio.2016.01.013 26854620
56. Aljehani YA. Risk factors of periodontal disease: Review of the literature. Int J Dent. 2014; 2014: 182513. doi: 10.1155/2014/182513 24963294
57. Albandar JM. Global risk factors and risk indicators for periodontal diseases. Periodontol 2000. 2002;29: 177–206. doi: 10.1034/j.1600-0757.2002.290109.x 12102708
58. Al-Tayeb D. The effects of smoking on the periodontal condition of young adult saudi population. Egypt Dent J. 2008;54: 1–15.
59. Fang Y, Svoboda KKH. Nicotine inhibits human gingival fibroblast migration via modulation of Rac signalling pathways. J Clin Periodontol. 2005;32(12): 1200–7. doi: 10.1111/j.1600-051X.2005.00845.x 16268995
60. Taneja V. Sex Hormones Determine Immune Response. Front Immunol. 2018;9:1931. doi: 10.3389/fimmu.2018.01931 eCollection 2018. 30210492
61. Hitomi Y, Ebisawa M, Tomikawa M, Imai T, Komata T, Hirota T, et al. Associations of functional NLRP3 polymorphisms with susceptibility to food-induced anaphylaxis and aspirin-induced asthma. J Allergy Clin Immunol. 2009;124(4): 779–785. doi: 10.1016/j.jaci.2009.07.044 19767079
62. Yilmaz Ö, Lee KL. The inflammasome and danger molecule signaling: At the crossroads of inflammation and pathogen persistence in the oral cavity. Periodontol 2000. 2015;69(1): 83–95. doi: 10.1111/prd.12084 26252403
63. Belibasakis GN, Johansson A. Aggregatibacter actinomycetemcomitans targets NLRP3 and NLRP6 inflammasome expression in human mononuclear leukocytes. Cytokine. 2012;59(1): 124–30. doi: 10.1016/j.cyto.2012.03.016 22503597
64. Bui FQ, Johnson L, Roberts JA, Hung SC, Lee J, Atanasova KR, et al. Fusobacterium nucleatum infection of gingival epithelial cells leads to NLRP3 inflammasome-dependent secretion of IL-1β and the danger signals ASC and HMGB1. Cell Microbiol. 2016 Jul 1;18(7):970–81. doi: 10.1111/cmi.12560 26687842
65. Guo W, Wang P, Liu Z, Yang P, Ye P. The activation of pyrin domain-containing- 3 inflammasome depends on lipopolysaccharide from Porphyromonas gingivalis and extracellular adenosine triphosphate in cultured oral epithelial cells. BMC Oral Health. 2015 Oct 29;15(1): 133. doi: 10.1186/s12903-015-0115-6 26511096
66. Liu Y-CG, Lerner UH, Teng Y-TA. Cytokine responses against periodontal infection: protective and destructive roles. Periodontol 2000. 2010;52(1): 163–206. doi: 10.1111/j.1600-0757.2009.00321.x 20017801
67. Chen H, Wilkins LM, Aziz N, Cannings C, Wyllie DH, Bingle C, et al. Single nucleotide polymorphisms in the human interleukin-1B gene affect transcription according to haplotype context. Hum Mol Genet. 2006;15(4): 519–29. doi: 10.1093/hmg/ddi469 16399797
68. Trevilatto PC, de Souza Pardo AP, Scarel-Caminaga RM, de Brito RB, Alvim-Pereira F, Alvim-Pereira CC, et al. Association of IL1 gene polymorphisms with chronic periodontitis in Brazilians. Arch Oral Biol. 2011;56(1): 54–62. doi: 10.1016/j.archoralbio.2010.09.004 20934174
69. Tanaka K, Miyake Y, Hanioka T, Arakawa M. Relationship Between IL1 Gene Polymorphisms and Periodontal Disease in Japanese Women. DNA Cell Biol. 2014;33(4): 227–33. doi: 10.1089/dna.2013.2202 24460370
70. Ribeiro MM, Pacheco RA, Fischer R, Macedo JB. Interaction of IL1B and IL1RN polymorphisms, smoking habit, gender, and ethnicity with aggressive and chronic periodontitis susceptibility. Contemp Clin Dent. 2016;7(3):349–56. doi: 10.4103/0976-237X.188560 27630500
71. Li G, Yue Y, Tian Y, Li J, Wang M, Liang H, et al. Association of matrix metalloproteinase (MMP)-1, 3, 9, interleukin (IL)-2, 8 and cyclooxygenase (COX)-2 gene polymorphisms with chronic periodontitis in a Chinese population. Cytokine. 2012;60(2): 552–60. doi: 10.1016/j.cyto.2012.06.239 22819245
72. Hoffmann SC, Stanley EM, Darrin Cox E, Craighead N, DiMercurio BS, Koziol DE, et al. Association of cytokine polymorphic inheritance and in vitro cytokine production in anti-CD3/CD28-stimulated peripheral blood lymphocytes. Transplantation. 2001;72(8): 1444–50. doi: 10.1097/00007890-200110270-00019 11685118
73. Vahabi S, Nazemisalman B, Hosseinpour S, Salavitabar S, Aziz A. Interleukin-2, -16, and -17 gene polymorphisms in Iranian patients with chronic periodontitis. J Investig Clin Dent. 2018;9(2): e12319. doi: 10.1111/jicd.12319 29400002
74. Kimura S, Fujimoto N, Okada H. Impaired Autologous Mixed-Lymphocyte Reaction of Peripheral Blood Lymphocytes in Adult Periodontitis. Infect Immun.1991; 59(12): 4418–4424. 1834575
75. Shenker BJ, Datar S. Fusobacterium nucleatum inhibits human T-cell activation by arresting cells in the mid-G1 phase of the cell cycle. Infect Immun. 1995;63(12): 4830–6. 7591143
76. Shenker BJ, McArthur WP, Tsai CC. Immune suppression induced by Actinobacillus actinomycetemcomitans. I. Effects on human peripheral blood lymphocyte responses to mitogens and antigens. J Immunol. 1982;128(1): 148–54. 7054277
77. Kavrikova D, Borilova Linhartova P, Lucanova S, Poskerova H, Fassmann A, Izakovicova Holla L. Chemokine Receptor 2 (CXCR2) Gene Variants and Their Association with Periodontal Bacteria in Patients with Chronic Periodontitis. Mediators Inflamm. 2019;2019: 1–8.
78. Naito M, Miyaki K, Naito T, Zhang L, Hoshi K, Hara A, et al. Association between vitamin D receptor gene haplotypes and chronic periodontitis among Japanese men. Int J Med Sci. 2007;4(4): 216–22. doi: 10.7150/ijms.4.216 17848979
79. Zacarias JMV, de Alencar JB, Tsuneto PY, de Souza VH, Silva CO, Visentainer JEL, et al. The Influence of TLR4, CD14, OPG, and RANKL Polymorphisms in Periodontitis: A Case-Control Study. Mediators Inflamm. 2019;2019: 1–10.
80. Boström EA, Kindstedt E, Sulniute R, Palmqvist P, Majster M, Holm CK, et al. Increased Eotaxin and MCP-1 Levels in Serum from Individuals with Periodontitis and in Human Gingival Fibroblasts Exposed to Pro-Inflammatory Cytokines. Ojcius DM, editor. PLoS One. 2015;10(8): e0134608. doi: 10.1371/journal.pone.0134608 26241961
81. Yamazaki K, Honda T, Oda T, Ueki-Maruyama K, Nakajima T, Yoshie H, et al. Effect of periodontal treatment on the C-reactive protein and proinflammatory cytokine levels in Japanese periodontitis patients. J Periodontal Res. 2005;40(1): 53–8. doi: 10.1111/j.1600-0765.2004.00772.x 15613080
82. Becerik S, Öztürk VÖ, Atmaca H, Atilla G, Emingil G. Gingival Crevicular Fluid and Plasma Acute-Phase Cytokine Levels in Different Periodontal Diseases. J Periodontol. 2012;83(10): 1304–13. doi: 10.1902/jop.2012.110616 22248224
83. Al-Rassam ZT, Taha MYM. Serum Cytokines Profiles and Some Salivary Parameters in Chronic Periodontitis Patients in Mosul-Iraq. Int J Sci Basic Appl Res. 2014;16(1): 339–50.
84. Andrukhov O, Ulm C, Reischl H, Nguyen PQ, Matejka M, Rausch-Fan X. Serum Cytokine Levels in Periodontitis Patients in Relation to the Bacterial Load. J Periodontol. 2011;82(6): 885–92. doi: 10.1902/jop.2010.100425 21138356
85. Fiorillo L, Cervino G, Herford AS, Lauritano F, D’Amico C, Lo Giudice R, et al. Interferon Crevicular Fluid Profile and Correlation with Periodontal Disease and Wound Healing: A Systemic Review of Recent Data. Int J Mol Sci. 2018; 19(7). doi: 10.3390/ijms19071908 29966238
86. Garlet GP, Cardoso CRB, Campanelli AP, Garlet TP, Avila-Campos MJ, Cunha FQ, et al. The essential role of IFN-γ in the control of lethal Aggregatibacter actinomycetemcomitans infection in mice. Microbes Infect. 2008;10(5): 489–96. doi: 10.1016/j.micinf.2008.01.010 18403243
87. Schroder K, Hertzog PJ, Ravasi T, Hume DA. Interferon-γ: an overview of signals, mechanisms and functions. J Leukoc Biol. 2004;75(2):163–89. doi: 10.1189/jlb.0603252 14525967
88. Takayanagi H, Ogasawara K, Hida S, Chiba T, Murata S, Sato K, et al. T-cell-mediated regulation of osteoclastogenesis by signalling cross-talk between RANKL and IFN-γ. Nature. 2000;408(6812):600–5. doi: 10.1038/35046102 11117749
89. Kitaura H, Kimura K, Ishida M, Sugisawa H, Kohara H, Yoshimatsu M, et al. Effect of cytokines on osteoclast formation and bone resorption during mechanical force loading of the periodontal membrane. Sci World J. 2014;2014: 617032. doi: 10.1155/2014/617032 24574904
90. Cetinkaya B, Guzeldemir E, Ogus E, Bulut S. Proinflammatory and Anti-Inflammatory Cytokines in Gingival Crevicular Fluid and Serum of Patients With Rheumatoid Arthritis and Patients With Chronic Periodontitis. J Periodontol. 2013;84(1): 84–93. doi: 10.1902/jop.2012.110467 22414257
91. Miranda TS, Heluy SL, Cruz DF, da Silva HDP, Feres M, Figueiredo LC, et al. The ratios of pro-inflammatory to anti-inflammatory cytokines in the serum of chronic periodontitis patients with and without type 2 diabetes and/or smoking habit. Clin Oral Investig. 2019;23(2): 641–50. doi: 10.1007/s00784-018-2471-5 29737428
92. Bluestone JA, Mackay CR, O’Shea JJ, Stockinger B. The functional plasticity of T cell subsets. Nat Rev Immunol. 2009;9(11): 811–6. doi: 10.1038/nri2654 19809471
93. Silva N, Abusleme L, Bravo D, Dutzan N, Garcia-Sesnich J, Vernal R, et al. Host response mechanisms in periodontal diseases. J Appl Oral Sci. 2015;23(3): 329–55. doi: 10.1590/1678-775720140259 26221929
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