Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

Inverse behavior of IL-23R and IL-17RA in chronic and aggressive periodontitis

  • Ruiz-Gutierrez, Alondra del Carmen (Specialty in Periodontology, Department of Integral Dental Clinics, University Center of Health Sciences, University of Guadalajara) ;
  • Rodriguez-Montano, Ruth (Institute of Research in Dentistry, Department of Integral Dental Clinics, University Center of Health Sciences, University of Guadalajara) ;
  • Pita-Lopez, Maria Luisa (Research Center in Molecular Biology of Chronic Diseases, Southern University Center, University of Guadalajara) ;
  • Zamora-Perez, Ana Lourdes (Institute of Research in Dentistry, Department of Integral Dental Clinics, University Center of Health Sciences, University of Guadalajara) ;
  • Guerrero-Velazquez, Celia (Institute of Research in Dentistry, Department of Integral Dental Clinics, University Center of Health Sciences, University of Guadalajara)
  • Received : 2020.08.11
  • Accepted : 2021.04.12
  • Published : 2021.08.30
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: Periodontitis is associated with a dysbiosis of periodontopathic bacteria, which stimulate the interleukin (IL)-23/IL-17 axis that plays an essential role in the immunopathogenesis of this disease, leading to alveolar bone destruction through receptor activator of nuclear factor κB ligand (RANKL). IL-23 receptor mRNA (IL-23R) has been identified in periodontitis, and IL-17 receptor A mRNA (IL-17RA) and its protein have not yet been evaluated in patients with periodontitis. In this study was measure IL-23R and IL-17RA in gingival tissue (GT) from patients with generalized chronic periodontitis (GCP) and generalized aggressive periodontitis (GAP) and to explore correlations with clinical parameters. Methods: We included 16 healthy subjects (HS), 18 patients with GCP, and 14 with GAP. GT samples were collected during periodontal surgery. Both IL-23R and IL-17RA were detected by enzyme-linked immunosorbent assay. Results: The results were analyzed with Mann-Whitney U test and Spearman' rank correlation coefficients using SPSS version 25.0. We found lower IL-23R levels in patients with GCP and GAP than in HS. Contrarily, we observed higher IL-17RA levels in GCP and GAP patients than in HS. Moreover, we found negative correlations between IL-23R in GT and probing depth and clinical attachment loss (CAL). Likewise, a positive correlation of IL-17RA in GT with CAL was found. Conclusions: The results of these findings suggest that the reverse behavior between IL-23R and IL-17RA in periodontitis patients may also be involved with the activation of RANKL, which promotes alveolar bone loss.

Keywords

Acknowledgement

This study was carried out with financial support from the University of Guadalajara, and the Mexican Association of Periodontology.

References

  1. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6. https://doi.org/10.1902/annals.1999.4.1.1
  2. Weighardt H, Jusek G, Mages J, Lang R, Hoebe K, Beutler B, et al. Identification of a TLR4- and TRIF-dependent activation program of dendritic cells. Eur J Immunol 2004;34:558-64. https://doi.org/10.1002/eji.200324714
  3. Parham C, Chirica M, Timans J, Vaisberg E, Travis M, Cheung J, et al. A receptor for the heterodimeric cytokine IL-23 is composed of IL-12Rbeta1 and a novel cytokine receptor subunit, IL-23R. J Immunol 2002;168:5699-708. https://doi.org/10.4049/jimmunol.168.11.5699
  4. Floss DM, Klocker T, Schroder J, Lamertz L, Mrotzek S, Strobl B, et al. Defining the functional binding sites of interleukin 12 receptor β1 and interleukin 23 receptor to Janus kinases. Mol Biol Cell 2016;27:2301-16. https://doi.org/10.1091/mbc.E14-12-1645
  5. Song X, Qian Y. IL-17 family cytokines mediated signaling in the pathogenesis of inflammatory diseases. Cell Signal 2013;25:2335-47. https://doi.org/10.1016/j.cellsig.2013.07.021
  6. Kan SH, Mancini G, Gallagher G. Identification and characterization of multiple splice forms of the human interleukin-23 receptor alpha chain in mitogen-activated leukocytes. Genes Immun 2008;9:631-9. https://doi.org/10.1038/gene.2008.64
  7. Franke M, Schroder J, Monhasery N, Ackfeld T, Hummel TM, Rabe B, et al. Human and murine interleukin 23 receptors are novel substrates for a disintegrin and metalloproteases ADAM10 and ADAM17. J Biol Chem 2016;291:10551-61. https://doi.org/10.1074/jbc.M115.710541
  8. Sohda M, Misumi Y, Tashiro K, Yamazaki M, Saku T, Oda K. Identification of a soluble isoform of human IL-17RA generated by alternative splicing. Cytokine 2013;64:642-5. https://doi.org/10.1016/j.cyto.2013.09.012
  9. Hienz SA, Paliwal S, Ivanovski S. Mechanisms of bone resorption in periodontitis. J Immunol Res 2015;2015:615486.
  10. Johnson RB, Wood N, Serio FG. Interleukin-11 and IL-17 and the pathogenesis of periodontal disease. J Periodontol 2004;75:37-43. https://doi.org/10.1902/jop.2004.75.1.37
  11. Takahashi K, Azuma T, Motohira H, Kinane DF, Kitetsu S. The potential role of interleukin-17 in the immunopathology of periodontal disease. J Clin Periodontol 2005;32:369-74. https://doi.org/10.1111/j.1600-051X.2005.00676.x
  12. Vernal R, Dutzan N, Chaparro A, Puente J, Antonieta Valenzuela M, Gamonal J. Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. J Clin Periodontol 2005;32:383-9. https://doi.org/10.1111/j.1600-051X.2005.00684.x
  13. Duarte PM, da Rocha M, Sampaio E, Mestnik MJ, Feres M, Figueiredo LC, et al. Serum levels of cytokines in subjects with generalized chronic and aggressive periodontitis before and after non-surgical periodontal therapy: a pilot study. J Periodontol 2010;81:1056-63. https://doi.org/10.1902/jop.2010.090732
  14. Ozcaka O, Nalbantsoy A, Buduneli N. Interleukin-17 and interleukin-18 levels in saliva and plasma of patients with chronic periodontitis. J Periodontal Res 2011;46:592-8. https://doi.org/10.1111/j.1600-0765.2011.01377.x
  15. Himani GS, Prabhuji ML, Karthikeyan BV. Gingival crevicular fluid and interleukin-23 concentration in systemically healthy subjects: their relationship in periodontal health and disease. J Periodontal Res 2014;49:237-45. https://doi.org/10.1111/jre.12100
  16. Fu QY, Zhang L, Duan L, Qian SY, Pang HX. Correlation of chronic periodontitis in tropical area and IFN-γ, IL-10, IL-17 levels. Asian Pac J Trop Med 2013;6:489-92. https://doi.org/10.1016/S1995-7645(13)60080-2
  17. Ruiz-Gutierrez AC, Herrera-Mora MC, Zamora-Perez AL, Melendez-Ruiz JL, Martinez-Rodriguez VC, Guerrero-Velazquez C. Determinacion de los niveles de IL-17 en el liquido crevicular gingival de pacientes con periodontitis cronica y agresiva. Rev Mex Periodontol 2014;5:46-50.
  18. Mitani A, Niedbala W, Fujimura T, Mogi M, Miyamae S, Higuchi N, et al. Increased expression of interleukin (IL)-35 and IL-17, but not IL-27, in gingival tissues with chronic periodontitis. J Periodontol 2015;86:301-9. https://doi.org/10.1902/jop.2014.140293
  19. Cifcibasi E, Koyuncuoglu C, Ciblak M, Badur S, Kasali K, Firatli E, et al. Evaluation of local and systemic levels of interleukin-17, interleukin-23, and myeloperoxidase in response to periodontal therapy in patients with generalized aggressive periodontitis. Inflammation 2015;38:1959-68. https://doi.org/10.1007/s10753-015-0176-3
  20. Liukkonen J, Gursoy UK, Pussinen PJ, Suominen AL, Kononen E. Salivary concentrations of interleukin (IL)-1β, IL-17A, and IL-23 vary in relation to periodontal status. J Periodontol 2016;87:1484-91. https://doi.org/10.1902/jop.2016.160146
  21. Pena-Echeverria PA, Rodriguez-Montano R, Ruiz-Gutierrez AC, Martinez-Rodriguez VMC, Gomez-Meda BC, Cervantes-Cabrera JJ, et al. Determinacion de la concentracion de IL-23 y el receptor soluble a IL-17 (IL-17RA) en suero y plasma de pacientes con periodontitis cronica y agresiva: un estudio piloto. Rev Mex Periodontol 2017;8:46-53.
  22. Chitrapriya MN, Rao SR, Lavu V. Interleukin-17 and interleukin-18 levels in different stages of inflammatory periodontal disease. J Indian Soc Periodontol 2015;19:14-7. https://doi.org/10.4103/0972-124X.145798
  23. Batool H, Nadeem A, Kashif M, Shahzad F, Tahir R, Afzal N. Salivary levels of IL-6 and IL-17 could be an indicator of disease severity in patients with calculus associated chronic periodontitis. Biomed Res Int 2018;2018:8531961.
  24. Sadeghi R, Sattari M, Dehghan F, Akbari S. Interleukin-17 and interleukin-23 levels in gingival crevicular fluid of patients with chronic and aggressive periodontitis. Cent Eur J Immunol 2018;43:76-80. https://doi.org/10.5114/ceji.2018.74876
  25. Thorbert-Mros S, Larsson L, Kalm J, Berglundh T. Interleukin-17 producing T cells and interleukin-17 mRNA expression in periodontitis and longstanding gingivitis lesions. J Periodontol 2019;90:516-21. https://doi.org/10.1002/JPER.18-0326
  26. Rivadeneyra-Burgos C, Rodriguez-Montan o R, Ruiz-Gutierrez AC, Martinez-Rodriguez VC, MelendezRuiz JL, Pita-Lopez ML, et al. Determinacion de los niveles del receptor soluble de IL-23 en suero y plasma de pacientes con periodontitis cronica y agresiva. Rev Mex Periodontol 2017;8:5-10.
  27. Ohyama H, Kato-Kogoe N, Kuhara A, Nishimura F, Nakasho K, Yamanegi K, et al. The involvement of IL-23 and the Th17 pathway in periodontitis. J Dent Res 2009;88:633-8. https://doi.org/10.1177/0022034509339889
  28. Hillyer P, Larche MJ, Bowman EP, McClanahan TK, de Waal Malefyt R, Schewitz LP, et al. Investigating the role of the interleukin-23/-17A axis in rheumatoid arthritis. Rheumatology (Oxford) 2009;48:1581-9. https://doi.org/10.1093/rheumatology/kep293
  29. van Baarsen LG, Lebre MC, van der Coelen D, Aarrass S, Tang MW, Ramwadhdoebe TH, et al. Heterogeneous expression pattern of interleukin 17A (IL-17A), IL-17F and their receptors in synovium of rheumatoid arthritis, psoriatic arthritis and osteoarthritis: possible explanation for nonresponse to anti-IL-17 therapy? Arthritis Res Ther 2014;16:426. https://doi.org/10.1186/s13075-014-0426-z
  30. Sanchez-Hernandez PE, Zamora-Perez AL, Fuentes-Lerma M, Robles-Gomez C, Mariaud-Schmidt RP, Guerrero-Velazquez C. IL-12 and IL-18 levels in serum and gingival tissue in aggressive and chronic periodontitis. Oral Dis 2011;17:522-9. https://doi.org/10.1111/j.1601-0825.2011.01798.x
  31. Franco-Topete R, Zepeda-Nuno JS, Zamora-Perez AL, Fuentes-Lerma MG, Gomez-Meda BC, Guerrero-Velazquez C. IFN-γR2 is strongly expressed on endothelial cells of gingival tissues from patients with chronic periodontitis. J Appl Oral Sci 2018;26:e20170291. https://doi.org/10.1590/1678-7757-2017-0291
  32. Sato K, Suematsu A, Okamoto K, Yamaguchi A, Morishita Y, Kadono Y, et al. Th17 functions as an osteoclastogenic helper T cell subset that links T cell activation and bone destruction. J Exp Med 2006;203:2673-82. https://doi.org/10.1084/jem.20061775
  33. Bostanci N, Emingil G, Afacan B, Han B, Ilgenli T, Atilla G, et al. Tumor necrosis factor-alpha-converting enzyme (TACE) levels in periodontal diseases. J Dent Res 2008;87:273-7. https://doi.org/10.1177/154405910808700311
  34. Ghoreschi K, Laurence A, Yang XP, Tato CM, McGeachy MJ, Konkel JE, et al. Generation of pathogenic TH17 cells in the absence of TGF-β signalling. Nature 2010;467:967-71. https://doi.org/10.1038/nature09447
  35. Liu S, Desharnais J, Sahasrabudhe PV, Jin P, Li W, Oates BD, et al. Inhibiting complex IL-17A and IL-17RA interactions with a linear peptide. Sci Rep 2016;6:26071. https://doi.org/10.1038/srep26071
  36. Lin D, Li L, Sun Y, Wang W, Wang X, Ye Y, et al. IL-17 regulates the expressions of RANKL and OPG in human periodontal ligament cells via TRAF6/TBK1-JNK/NF-κB pathways. Immunology 2014;144:472-85. https://doi.org/10.1111/imm.12395
  37. Caton JG, Armitage G, Berglundh T, Chapple IL, Jepsen S, Kornman KS, et al. A new classification scheme for periodontal and peri-implant diseases and conditions - Introduction and key changes from the 1999 classification. J Clin Periodontol 2018;45 Suppl 20:S1-8.
  38. Zaki AA. The new classification of periodontal diseases. BDJ Team 2020;7:32-3. https://doi.org/10.1038/s41407-020-0435-5
  39. Gaur S, Agnihotri R. Alzheimer's disease and chronic periodontitis: Is there an association? Geriatr Gerontol Int 2015;15:391-404. https://doi.org/10.1111/ggi.12425
  40. Ballerini P, Diomede F, Petragnani N, Cicchitti S, Merciaro I, Cavalcanti MF, et al. Conditioned medium from relapsing-remitting multiple sclerosis patients reduces the expression and release of inflammatory cytokines induced by LPS-gingivalis in THP-1 and MO3.13 cell lines. Cytokine 2017;96:261-72. https://doi.org/10.1016/j.cyto.2017.04.022