Clinical associations between IL-17 family cytokines and periodontitis and potential differential roles for IL-17A and IL-17E in periodontal immunity

Inflammation Research

Volumn 63, Issue 12, 2014, Pages 1001-1012

  Azman, Raja ^a   Lappin, David F ^a   MacPherson, Alexandrea ^a   Riggio, Marcello ^a   Robertson, Douglas ^a   Hodge, Penny ^a   Ramage, Gordon ^a   Culshaw, Shauna ^a   Preshaw, Philip M ^b   Taylor, John ^b   Nile, Christopher ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

IL 17; IL 17A; IL 17E; IL 25; IL 8; Periodontitis

Indexed keywords

EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 17; INTERLEUKIN 17 B; INTERLEUKIN 17 C; INTERLEUKIN 17F; INTERLEUKIN 25; INTERLEUKIN 27; INTERLEUKIN 8; TRANSCRIPTION FACTOR RELA; UNCLASSIFIED DRUG; BIOLOGICAL MARKER; CYTOKINE;

ADULT; ARTICLE; BIOFILM; CELL VIABILITY; CONTROLLED STUDY; CYTOKINE RELEASE; ENZYME ASSAY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME PHOSPHORYLATION; FEMALE; GINGIVITIS; HUMAN; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IN VITRO STUDY; KERATINOCYTE; MAJOR CLINICAL STUDY; MALE; PATHOGENESIS; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; PROTEIN BLOOD LEVEL; PROTEIN EXPRESSION; PROTEIN FUNCTION; REAL TIME POLYMERASE CHAIN REACTION; SALIVA ANALYSIS; SALIVA LEVEL; UPREGULATION; BLOOD; CASE CONTROL STUDY; COCULTURE; CYTOLOGY; GENE EXPRESSION REGULATION; IMMUNOLOGY; METABOLISM; MIDDLE AGED;

ADULT; BIOFILMS; BIOLOGICAL MARKERS; CASE-CONTROL STUDIES; COCULTURE TECHNIQUES; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION REGULATION; GINGIVAL CREVICULAR FLUID; HUMANS; INTERLEUKIN-17; KERATINOCYTES; MALE; MIDDLE AGED; PERIODONTITIS; PORPHYROMONAS GINGIVALIS;

EID: 84911989498     PISSN: 10233830     EISSN: 1420908X     Source Type: Journal    
DOI: 10.1007/s00011-014-0776-7     Document Type: Article

References (50)

1. Gu C, Wu L, Li X. IL-17 family: cytokines, receptors and signaling. Cytokine. 2013;64(2):477–85.
2. Wright JF, Guo Y, Quazi A, et al. Identification of an interleukin 17F/17A heterodimer in activated human CD4 + T cells. J Biol Chem. 2007;282(18):13447–55.
3. Gaffen SL. Structure and signalling in the IL-17 receptor family. Nat Rev Immunol. 2009;9(8):556–67.
4. Yao Z, Painter SL, Fanslow WC, Ulrich D, Macduff BM, Spriggs MK, Armitage RJ. Human IL-17: a novel cytokine derived from T cells. J Immunol. 1995;155(12):5483–6.
5. Cardoso CR, Garlet GP, Crippa GE, Rosa AL, Junior WM, Rossi MA, Silva JS. Evidence of the presence of T helper type 17 cells in chronic lesions of human periodontal disease. Oral Microbiol Immunol. 2009;24(1):1–6.
6. Adibrad M, Deyhimi P. Ganjalikhani Hakemi M, Behfarnia P, Shahabuei M, Rafiee L. Signs of the presence of Th17 cells in chronic periodontal disease. J Periodontal Res. 2012;47(4):525–31.
7. Beklen A, Ainola M, Hukkanen M, Gurgan C, Sorsa T, Konttinen YT. MMPs, IL-1, and TNF are regulated by IL-17 in periodontitis. J Dent Res. 2007;86(4):347–51.
8. Konermann A, Beyer M, Deschner J, Allam JP, Novak N, Winter J, Jepsen S, Jager A. Human periodontal ligament cells facilitate leukocyte recruitment and are influenced in their immunomodulatory function by Th17 cytokine release. Cell Immunol. 2012;272(2):137–43.
9. Allam JP, Duan Y, Heinemann F, et al. IL-23-producing CD68(+) macrophage-like cells predominate within an IL-17-polarized infiltrate in chronic periodontitis lesions. J Clin Periodontol. 2011;38(10):879–86.
10. Honda T, Aoki Y, Takahashi N, et al. Elevated expression of IL-17 and IL-12 genes in chronic inflammatory periodontal disease. Clin Chim Acta. 2008;395(1–2):137–41.
11. Duarte PM, da Rocha M, Sampaio E, Mestnik MJ, Feres M, Figueiredo LC, Bastos MF, Faveri M. 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(7):1056–63.
12. Schenkein HA, Koertge TE, Brooks CN, Sabatini R, Purkall DE, Tew JG. IL-17 in sera from patients with aggressive periodontitis. J Dent Res. 2010;89(9):943–7.
13. 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(5):592–8.
14. 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(4):383–9.
15. Buduneli N, Buduneli E, Kutukculer N. Interleukin-17, RANKL, and osteoprotegerin levels in gingival crevicular fluid from smoking and non-smoking patients with chronic periodontitis during initial periodontal treatment. J Periodontol. 2009;80(8):1274–80.
16. Kadkhodazadeh M, Baghani Z, Ebadian AR, Youssefi N, Mehdizadeh AR, Azimi N. IL-17 gene polymorphism is associated with chronic periodontitis and peri-implantitis in Iranian patients: a cross-sectional study. Immunol Invest. 2013;42(2):156–63.
17. Correa JD, Madeira MF, Resende RG, et al. Association between polymorphisms in interleukin-17A and -17F genes and chronic periodontal disease. Mediators Inflamm. 2012;2012:846052.
18. Saraiva AM. Alves e Silva MR, Correia Silva Jde F, da Costa JE, Gollob KJ, Dutra WO, Moreira PR. Evaluation of IL17A expression and of IL17A, IL17F and IL23R gene polymorphisms in Brazilian individuals with periodontitis. Hum Immunol. 2013;74(2):207–14.
19. Yu JJ, Ruddy MJ, Wong GC, Sfintescu C, Baker PJ, Smith JB, Evans RT, Gaffen SL. An essential role for IL-17 in preventing pathogen-initiated bone destruction: recruitment of neutrophils to inflamed bone requires IL-17 receptor-dependent signals. Blood. 2007;109(9):3794–802.
20. Eskan MA, Jotwani R, Abe T, et al. The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nat Immunol. 2012;13(5):465–73.
21. Koenders MI, Lubberts E, Oppers-Walgreen B, et al. Blocking of interleukin-17 during reactivation of experimental arthritis prevents joint inflammation and bone erosion by decreasing RANKL and interleukin-1. Am J Pathol. 2005;167(1):141–9.
22. Koenders MI, Marijnissen RJ, Devesa I, et al. Tumor necrosis factor-interleukin-17 interplay induces S100A8, interleukin-1beta, and matrix metalloproteinases, and drives irreversible cartilage destruction in murine arthritis: rationale for combination treatment during arthritis. Arthritis Rheum. 2011;63(8):2329–39.
23. Iyoda M, Shibata T, Kawaguchi M, Hizawa N, Yamaoka T, Kokubu F, Akizawa T. IL-17A and IL-17F stimulate chemokines via MAPK pathways (ERK1/2 and p38 but not JNK) in mouse cultured mesangial cells: synergy with TNF-alpha and IL-1beta. Am J Physiol Renal Physiol. 2010;298(3):F779–87.
24. Kotake S, Yago T, Kawamoto M, Nanke Y. Role of osteoclasts and interleukin-17 in the pathogenesis of rheumatoid arthritis: crucial ‘human osteoclastology’. J Bone Miner Metab. 2012;30(2):125–35.
25. Konermann A, Winter J, Novak N, Allam JP, Jager A. Verification of IL-17A and IL-17F in oral tissues and modulation of their expression pattern by steroid hormones. Cell Immunol. 2013;285(1–2):133–40.
26. Gumus P, Buduneli E, Biyikoglu B, Aksu K, Sarac F, Nile C, Lappin D, Buduneli N. Gingival crevicular fluid, serum levels of receptor activator of nuclear factor-kappa B ligand, osteoprotegerin, interleukin-17 in rheumatoid arthritis and osteoporosis patients with periodontal disease. J Periodontol. 2013;84(11):1627–37.
27. Ozcaka O, Buduneli N, Ceyhan BO, Akcali A, Hannah V, Nile C, Lappin DF. Is IL-17 involved in the interaction between polycystic ovary syndrome and gingival inflammation? J Periodontol. 2013;83(12):1529–37.
28. Monteleone G, Pallone F, Macdonald TT. Interleukin-25: a two-edged sword in the control of immune-inflammatory responses. Cytokine Growth Factor Rev. 2010;21(6):471–5.
29. Tamachi T, Maezawa Y, Ikeda K, et al. IL-25 enhances allergic airway inflammation by amplifying a TH2 cell-dependent pathway in mice. J Allergy Clin Immunol. 2006;118(3):606–14.
30. Angkasekwinai P, Chang SH, Thapa M, Watarai H, Dong C. Regulation of IL-9 expression by IL-25 signaling. Nat Immunol. 2010;11(3):250–6.
31. Saenz SA, Noti M, Artis D. Innate immune cell populations function as initiators and effectors in Th2 cytokine responses. Trends Immunol. 2010;31(11):407–13.
32. Owyang AM, Zaph C, Wilson EH, et al. Interleukin 25 regulates type 2 cytokine-dependent immunity and limits chronic inflammation in the gastrointestinal tract. J Exp Med. 2006;203(4):843–9.
33. Kleinschek MA, Owyang AM, Joyce-Shaikh B, et al. IL-25 regulates Th17 function in autoimmune inflammation. J Exp Med. 2007;204(1):161–70.
34. Caruso R, Sarra M, Stolfi C, et al. Interleukin-25 inhibits interleukin-12 production and Th1 cell-driven inflammation in the gut. Gastroenterology. 2009;136(7):2270–9.
35. Caruso R, Stolfi C, Sarra M, Rizzo A, Fantini MC, Pallone F, MacDonald TT, Monteleone G. Inhibition of monocyte-derived inflammatory cytokines by IL-25 occurs via p38 Map kinase-dependent induction of Socs-3. Blood. 2009;113(15):3512–9.
36. Navazesh M. Methods for collecting saliva. Ann N Y Acad Sci. 1993;694:72–7.
37. Pratten J, Smith AW, Wilson M. Response of single species biofilms and microcosm dental plaques to pulsing with chlorhexidine. J Antimicrob Chemother. 1998;42(4):453–9.
38. Ramage G, Jose A, Coco B, Rajendran R, Rautemaa R, Murray C, Lappin DF, Bagg J. Commercial mouthwashes are more effective than azole antifungals against Candida albicans biofilms in vitro. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 2011;111(4):456–60.
39. Sherry L, Millhouse E, Lappin DF, Murray C, Culshaw S, Nile CJ, Ramage G. Investigating the biological properties of carbohydrate derived fulvic acid (CHD-FA) as a potential novel therapy for the management of oral biofilm infections. BMC Oral Health. 2013;13:47.
40. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–8.
41. Buduneli N, Kinane DF. Host-derived diagnostic markers related to soft tissue destruction and bone degradation in periodontitis. J Clin Periodontol. 2011;38(Suppl 11):85–105.
42. Yamada H. Current perspectives on the role of IL-17 in autoimmune disease. J Inflamm Res. 2010;3:33–44.
43. Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontology. 2000;1997(14):33–53.
44. Hata K, Andoh A, Shimada M, et al. IL-17 stimulates inflammatory responses via NF-kappaB and MAP kinase pathways in human colonic myofibroblasts. Am J Physiol Gastrointest Liver Physiol. 2002;282(6):G1035–44.
45. Buss H, Dorrie A, Schmitz ML, Hoffmann E, Resch K, Kracht M. Constitutive and interleukin-1-inducible phosphorylation of p65 NF-{kappa}B at serine 536 is mediated by multiple protein kinases including I{kappa}B kinase (IKK)-{alpha}, IKK{beta}, IKK{epsilon}, TRAF family member-associated (TANK)-binding kinase 1 (TBK1), and an unknown kinase and couples p65 to TATA-binding protein-associated factor II31-mediated interleukin-8 transcription. J Biol Chem. 2004;279(53):55633–43.
46. Geng H, Wittwer T, Dittrich-Breiholz O, Kracht M, Schmitz ML. Phosphorylation of NF-kappaB p65 at Ser468 controls its COMMD1-dependent ubiquitination and target gene-specific proteasomal elimination. EMBO Rep. 2009;10(4):381–6.
47. Mattioli I, Sebald A, Bucher C, Charles RP, Nakano HT, Kracht M, Schmitz ML. Transient and selective NF-kappa B p65 serine 536 phosphorylation induced by T cell costimulation is mediated by I kappa B kinase beta and controls the kinetics of p65 nuclear import. J Immunol. 2004;172(10):6336–44.
48. Yoshimura A, Naka T, Kubo M. SOCS proteins, cytokine signalling and immune regulation. Nat Rev Immunol. 2007;7(6):454–65.
49. Liang SC, Long AJ, Bennett F, et al. An IL-17F/A heterodimer protein is produced by mouse Th17 cells and induces airway neutrophil recruitment. J Immunol. 2007;179(11):7791–9.
50. Kuestner RE, Taft DW, Haran A, et al. Identification of the IL-17 receptor related molecule IL-17RC as the receptor for IL-17F. J Immunol. 2007;179(8):5462–73.