Abstract
T helper 17 (Th17) cells were first described as a T helper subset involved in the pathogenesis of experimental autoimmune inflammation. Since then, these cells have been described as orchestrators of immunopathology in several human inflammatory conditions including psoriasis, rheumatoid arthritis, and inflammatory bowel disease. More recently, the crucial role of Th17 cells in the regulation of immunity and protection of barrier sites has been unveiled. In the present work, we review the available evidence regarding Th17 cells in health and disease with a focus on the oral mucosa and their role in periodontitis pathogenesis. Recent mechanistic studies in animal models have demonstrated that interleukin-17A (IL-17A) and Th17 cells are critical mediators for alveolar bone destruction during periodontal inflammation. Observations in a cohort of patients with naturally occurring impaired Th17 cell differentiation supported these findings. However, interventional studies are needed to conclusively implicate Th17 cells in the immunopathogenesis of human alveolar bone and tissue destruction that characterize periodontitis.
This is a preview of subscription content, log in via an institution.
Buying options
Tax calculation will be finalised at checkout
Purchases are for personal use only
Learn about institutional subscriptionsReferences
Abusleme, L., & Moutsopoulos, N. M. (2016). IL-17: Overview and role in oral immunity and microbiome. Oral Diseases. https://doi.org/10.1111/odi.12598.
Abusleme, L., Dupuy, A. K., Dutzan, N., Silva, N., Burleson, J. A., Strausbaugh, L. D., et al. (2013). The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. The ISME Journal, 7(5), 1016–1025. https://doi.org/10.1038/ismej.2012.174.
Abusleme, L., Diaz, P. I., Freeman, A. F., Greenwell-Wild, T., Brenchley, L., Desai, J. V., et al. (2018). Human defects in STAT3 promote oral mucosal fungal and bacterial dysbiosis. JCI Insight, 3(17), 122061. https://doi.org/10.1172/jci.insight.122061.
Adibrad, M., Deyhimi, P., Ganjalikhani Hakemi, M., Behfarnia, P., Shahabuei, M., & Rafiee, L. (2012). Signs of the presence of Th17 cells in chronic periodontal disease. Journal of Periodontal Research, 47(4), 525–531. https://doi.org/10.1111/j.1600-0765.2011.01464.x.
Ahern, P. P., Schiering, C., Buonocore, S., McGeachy, M. J., Cua, D. J., Maloy, K. J., et al. (2010). Interleukin-23 drives intestinal inflammation through direct activity on T cells. Immunity, 33(2), 279–288. https://doi.org/10.1016/j.immuni.2010.08.010.
Al-Harthi, L. S., Cullinan, M. P., Leichter, J. W., & Thomson, W. M. (2013). The impact of periodontitis on oral health-related quality of life: A review of the evidence from observational studies. Australian Dental Journal, 58(3), 274–277. https://doi.org/10.1111/adj.12076; quiz 384.
Amatya, N., Garg, A. V., & Gaffen, S. L. (2017). IL-17 signaling: The Yin and the Yang. Trends in Immunology, 38(5), 310–322. https://doi.org/10.1016/j.it.2017.01.006.
Aschenbrenner, D., Foglierini, M., Jarrossay, D., Hu, D., Weiner, H. L., Kuchroo, V. K., et al. (2018). An immunoregulatory and tissue-residency program modulated by c-MAF in human TH17 cells. Nature Immunology, 19(10), 1126–1136. https://doi.org/10.1038/s41590-018-0200-5.
Baer, P. N., & Newton, W. L. (1959). The occurrence of periodontal disease in germfree mice. Journal of Dental Research, 38, 1238. https://doi.org/10.1177/00220345590380062601.
Baker, P. J., Dixon, M., Evans, R. T., Dufour, L., Johnson, E., & Roopenian, D. C. (1999). CD4(+) T cells and the proinflammatory cytokines gamma interferon and interleukin-6 contribute to alveolar bone loss in mice. Infection and Immunity, 67(6), 2804–2809.
Baker, P. J., Garneau, J., Howe, L., & Roopenian, D. C. (2001). T-cell contributions to alveolar bone loss in response to oral infection with Porphyromonas gingivalis. Acta Odontologica Scandinavica, 59(4), 222–225.
Baker, P. J., Howe, L., Garneau, J., & Roopenian, D. C. (2002). T cell knockout mice have diminished alveolar bone loss after oral infection with Porphyromonas gingivalis. FEMS Immunology and Medical Microbiology, 34(1), 45–50.
Bernabe, E., & Marcenes, W. (2010). Periodontal disease and quality of life in British adults. Journal of Clinical Periodontology, 37(11), 968–972. https://doi.org/10.1111/j.1600-051X.2010.01627.x.
Cardoso, C. R., Garlet, G. P., Crippa, G. E., Rosa, A. L., Junior, W. M., Rossi, M. A., et al. (2009). Evidence of the presence of T helper type 17 cells in chronic lesions of human periodontal disease. Oral Microbiology and Immunology, 24(1), 1–6. https://doi.org/10.1111/j.1399-302X.2008.00463.x.
Ciofani, M., Madar, A., Galan, C., Sellars, M., Mace, K., Pauli, F., et al. (2012). A validated regulatory network for Th17 cell specification. Cell, 151(2), 289–303. https://doi.org/10.1016/j.cell.2012.09.016.
Conti, H. R., Baker, O., Freeman, A. F., Jang, W. S., Holland, S. M., Li, R. A., et al. (2011). New mechanism of oral immunity to mucosal candidiasis in hyper-IgE syndrome. Mucosal Immunology, 4(4), 448–455. https://doi.org/10.1038/mi.2011.5.
Correa, J. D., Madeira, M. F., Resende, R. G., Correia-Silva Jde, F., Gomez, R. S., de Souza, D. G., et al. (2012). Association between polymorphisms in interleukin-17A and -17F genes and chronic periodontal disease. Mediators of Inflammation, 2012, 846052. https://doi.org/10.1155/2012/846052.
Cua, D. J., & Tato, C. M. (2010). Innate IL-17-producing cells: The sentinels of the immune system. Nature Reviews. Immunology, 10(7), 479–489. https://doi.org/10.1038/nri2800.
Darveau, R. P. (2010). Periodontitis: A polymicrobial disruption of host homeostasis. Nature Reviews. Microbiology, 8(7), 481–490. https://doi.org/10.1038/nrmicro2337.
Davis Fred, P., Kanno, Y., & O’Shea, J. J. (2015). A metabolic switch for Th17 pathogenicity. Cell, 163(6), 1308–1310. https://doi.org/10.1016/j.cell.2015.11.033.
Dutzan, N., Gamonal, J., Silva, A., Sanz, M., & Vernal, R. (2009). Over-expression 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. Journal of Clinical Periodontology, 36(5), 396–403. https://doi.org/10.1111/j.1600-051X.2009.01390.x.
Dutzan, N., Vernal, R., Vaque, J. P., Garcia-Sesnich, J., Hernandez, M., Abusleme, L., et al. (2012). Interleukin-21 expression and its association with proinflammatory cytokines in untreated chronic periodontitis patients. Journal of Periodontology, 83(7), 948–954. https://doi.org/10.1902/jop.2011.110482.
Dutzan, N., Konkel, J. E., Greenwell-Wild, T., & Moutsopoulos, N. M. (2016). Characterization of the human immune cell network at the gingival barrier. Mucosal Immunology, 9(5), 1163–1172. https://doi.org/10.1038/mi.2015.136.
Dutzan, N., Abusleme, L., Bridgeman, H., Greenwell-Wild, T., Zangerle-Murray, T., Fife, M. E., et al. (2017). On-going mechanical damage from mastication drives homeostatic Th17 cell responses at the oral barrier. Immunity, 46(1), 133–147. https://doi.org/10.1016/j.immuni.2016.12.010.
Dutzan, N., Kajikawa, T., Abusleme, L., Greenwell-Wild, T., Zuazo, C. E., Ikeuchi, T., et al. (2018). A dysbiotic microbiome triggers TH17 cells to mediate oral mucosal immunopathology in mice and humans. Science Translational Medicine, 10(463), eaat0797. https://doi.org/10.1126/scitranslmed.aat0797.
Eke, P. I., Dye, B. A., Wei, L., Thornton-Evans, G. O., Genco, R. J., & CDC Periodontal Disease Surveillance Workgroup: James Beck GDRP. (2012). Prevalence of periodontitis in adults in the United States: 2009 and 2010. Journal of Dental Research, 91(10), 914–920. https://doi.org/10.1177/0022034512457373.
Eke, P. I., Dye, B. A., Wei, L., Slade, G. D., Thornton-Evans, G. O., Borgnakke, W. S., et al. (2015). Update on prevalence of periodontitis in adults in the United States: NHANES 2009 to 2012. Journal of Periodontology, 86(5), 611–622. https://doi.org/10.1902/jop.2015.140520.
Eskan, M. A., Jotwani, R., Abe, T., Chmelar, J., Lim, J. H., Liang, S., et al. (2012). The leukocyte integrin antagonist Del-1 inhibits IL-17-mediated inflammatory bone loss. Nature Immunology, 13(5), 465–473. https://doi.org/10.1038/ni.2260.
Fossiez, F., Djossou, O., Chomarat, P., Flores-Romo, L., Ait-Yahia, S., Maat, C., et al. (1996). T cell interleukin-17 induces stromal cells to produce proinflammatory and hematopoietic cytokines. The Journal of Experimental Medicine, 183(6), 2593–2603.
Freeman, A. F., & Holland, S. M. (2010). Clinical manifestations of hyper IgE syndromes. Disease Markers, 29(3–4), 123–130. https://doi.org/10.3233/DMA-2010-0734.
Gaffen, S. L. (2009). Structure and signalling in the IL-17 receptor family. Nature Reviews. Immunology, 9(8), 556–567. https://doi.org/10.1038/nri2586.
Gaffen, S. L. (2011). Recent advances in the IL-17 cytokine family. Current Opinion in Immunology, 23(5), 613–619. https://doi.org/10.1016/j.coi.2011.07.006.
Gaffen, S. L., Jain, R., Garg, A. V., & Cua, D. J. (2014). The IL-23-IL-17 immune axis: From mechanisms to therapeutic testing. Nature Reviews. Immunology, 14(9), 585–600. https://doi.org/10.1038/nri3707.
Ghoreschi, K., Laurence, A., Yang, X. P., Tato, C. M., McGeachy, M. J., Konkel, J. E., et al. (2010). Generation of pathogenic T(H)17 cells in the absence of TGF-beta signalling. Nature, 467(7318), 967–971. https://doi.org/10.1038/nature09447.
Griffen, A. L., Beall, C. J., Campbell, J. H., Firestone, N. D., Kumar, P. S., Yang, Z. K., et al. (2012). Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. The ISME Journal, 6(6), 1176–1185. https://doi.org/10.1038/ismej.2011.191.
Hajishengallis, G. (2014). Immunomicrobial pathogenesis of periodontitis: Keystones, pathobionts, and host response. Trends in Immunology, 35(1), 3–11. https://doi.org/10.1016/j.it.2013.09.001.
Hajishengallis, G. (2015). Periodontitis: From microbial immune subversion to systemic inflammation. Nature Reviews. Immunology, 15(1), 30–44. https://doi.org/10.1038/nri3785.
Hajishengallis, G., Darveau, R. P., & Curtis, M. A. (2012). The keystone-pathogen hypothesis. Nature Reviews. Microbiology, 10(10), 717–725. https://doi.org/10.1038/nrmicro2873.
Harrington, L. E., Hatton, R. D., Mangan, P. R., Turner, H., Murphy, T. L., Murphy, K. M., et al. (2005). Interleukin 17-producing CD4+ effector T cells develop via a lineage distinct from the T helper type 1 and 2 lineages. Nature Immunology, 6(11), 1123–1132. https://doi.org/10.1038/ni1254.
Harris, T. J., Grosso, J. F., Yen, H. R., Xin, H., Kortylewski, M., Albesiano, E., et al. (2007). Cutting edge: An in vivo requirement for STAT3 signaling in TH17 development and TH17-dependent autoimmunity. Journal of Immunology, 179(7), 4313–4317.
Hawkes, J. E., Yan, B. Y., Chan, T. C., & Krueger, J. G. (2018). Discovery of the IL-23/IL-17 signaling pathway and the treatment of psoriasis. Journal of Immunology, 201(6), 1605–1613. https://doi.org/10.4049/jimmunol.1800013.
Heink, S., Yogev, N., Garbers, C., Herwerth, M., Aly, L., Gasperi, C., et al. (2017). Trans-presentation of IL-6 by dendritic cells is required for the priming of pathogenic TH17 cells. Nature Immunology, 18(1), 74–85. https://doi.org/10.1038/ni.3632.
Holland, S. M., DeLeo, F. R., Elloumi, H. Z., Hsu, A. P., Uzel, G., Brodsky, N., et al. (2007). STAT3 mutations in the hyper-IgE syndrome. The New England Journal of Medicine, 357(16), 1608–1619. https://doi.org/10.1056/NEJMoa073687.
Hooper, L. V., Littman, D. R., & Macpherson, A. J. (2012). Interactions between the microbiota and the immune system. Science, 336(6086), 1268–1273. https://doi.org/10.1126/science.1223490.
Hunter, C. A., & Jones, S. A. (2015). IL-6 as a keystone cytokine in health and disease. Nature Immunology, 16(5), 448–457. https://doi.org/10.1038/ni.3153.
Ivanov, I. I., McKenzie, B. S., Zhou, L., Tadokoro, C. E., Lepelley, A., Lafaille, J. J., et al. (2006). The orphan nuclear receptor RORgammat directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell, 126(6), 1121–1133. https://doi.org/10.1016/j.cell.2006.07.035.
Ivanov, I. I., Frutos Rde, L., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., et al. (2008). Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host & Microbe, 4(4), 337–349. https://doi.org/10.1016/j.chom.2008.09.009.
Jin, W., & Dong, C. (2013). IL-17 cytokines in immunity and inflammation. Emerging Microbes & Infections, 2(9), e60. https://doi.org/10.1038/emi.2013.58.
Kassebaum, N. J., Bernabe, E., Dahiya, M., Bhandari, B., Murray, C. J., & Marcenes, W. (2014). Global burden of severe periodontitis in 1990-2010: A systematic review and meta-regression. Journal of Dental Research, 93(11), 1045–1053. https://doi.org/10.1177/0022034514552491.
Kawai, T., Paster, B. J., Komatsuzawa, H., Ernst, C. W., Goncalves, R. B., Sasaki, H., et al. (2007). Cross-reactive adaptive immune response to oral commensal bacteria results in an induction of receptor activator of nuclear factor-kappaB ligand (RANKL)-dependent periodontal bone resorption in a mouse model. Oral Microbiology and Immunology, 22(3), 208–215. https://doi.org/10.1111/j.1399-302X.2007.00348.x.
Komatsu, N., Okamoto, K., Sawa, S., Nakashima, T., Oh-hora, M., Kodama, T., et al. (2014). Pathogenic conversion of Foxp3+ T cells into TH17 cells in autoimmune arthritis. Nature Medicine, 20(1), 62–68. https://doi.org/10.1038/nm.3432.
Kotake, S., Udagawa, N., Takahashi, N., Matsuzaki, K., Itoh, K., Ishiyama, S., et al. (1999). IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. The Journal of Clinical Investigation, 103(9), 1345–1352. https://doi.org/10.1172/JCI5703.
Langrish, C. L., Chen, Y., Blumenschein, W. M., Mattson, J., Basham, B., Sedgwick, J. D., et al. (2005). IL-23 drives a pathogenic T cell population that induces autoimmune inflammation. The Journal of Experimental Medicine, 201(2), 233–240. https://doi.org/10.1084/jem.20041257.
Lee, Y., Awasthi, A., Yosef, N., Quintana, F. J., Xiao, S., Peters, A., et al. (2012). Induction and molecular signature of pathogenic TH17 cells. Nature Immunology, 13(10), 991–999. https://doi.org/10.1038/ni.2416.
Lee, J. S., Tato, C. M., Joyce-Shaikh, B., Gulen, M. F., Cayatte, C., Chen, Y., et al. (2015). Interleukin-23-independent IL-17 production regulates intestinal epithelial permeability. Immunity, 43(4), 727–738. https://doi.org/10.1016/j.immuni.2015.09.003.
Lester, S. R., Bain, J. L., Johnson, R. B., & Serio, F. G. (2007). Gingival concentrations of interleukin-23 and -17 at healthy sites and at sites of clinical attachment loss. Journal of Periodontology, 78(8), 1545–1550. https://doi.org/10.1902/jop.2007.060458.
Mease, P. J. (2015). Inhibition of interleukin-17, interleukin-23 and the TH17 cell pathway in the treatment of psoriatic arthritis and psoriasis. Current Opinion in Rheumatology, 27(2), 127–133. https://doi.org/10.1097/BOR.0000000000000147.
Milner, J. D., Brenchley, J. M., Laurence, A., Freeman, A. F., Hill, B. J., Elias, K. M., et al. (2008). Impaired T(H)17 cell differentiation in subjects with autosomal dominant hyper-IgE syndrome. Nature, 452(7188), 773–776. https://doi.org/10.1038/nature06764.
Miossec, P. (2017). Update on interleukin-17: A role in the pathogenesis of inflammatory arthritis and implication for clinical practice. RMD Open, 3(1), e000284. https://doi.org/10.1136/rmdopen-2016-000284.
Miossec, P., & Kolls, J. K. (2012). Targeting IL-17 and TH17 cells in chronic inflammation. Nature Reviews. Drug Discovery, 11(10), 763–776. https://doi.org/10.1038/nrd3794.
Monin, L., & Gaffen, S. L. (2017). Interleukin 17 family cytokines: Signaling mechanisms, biological activities, and therapeutic implications. Cold Spring Harbor Perspectives in Biology. https://doi.org/10.1101/cshperspect.a028522.
Moseley, T. A., Haudenschild, D. R., Rose, L., & Reddi, A. H. (2003). Interleukin-17 family and IL-17 receptors. Cytokine & Growth Factor Reviews, 14(2), 155–174.
Mosmann, T. R., & Coffman, R. L. (1989). TH1 and TH2 cells: Different patterns of lymphokine secretion lead to different functional properties. Annual Review of Immunology, 7, 145–173. https://doi.org/10.1146/annurev.iy.07.040189.001045.
Moutsopoulos, N. M., Kling, H. M., Angelov, N., Jin, W., Palmer, R. J., Nares, S., et al. (2012). Porphyromonas gingivalis promotes Th17 inducing pathways in chronic periodontitis. Journal of Autoimmunity, 39(4), 294–303. https://doi.org/10.1016/j.jaut.2012.03.003.
Moutsopoulos, N. M., Konkel, J., Sarmadi, M., Eskan, M. A., Wild, T., Dutzan, N., et al. (2014). Defective neutrophil recruitment in leukocyte adhesion deficiency type I disease causes local IL-17-driven inflammatory bone loss. Science Translational Medicine, 6(229), 229ra40. https://doi.org/10.1126/scitranslmed.3007696.
Naik, S., Bouladoux, N., Wilhelm, C., Molloy, M. J., Salcedo, R., Kastenmuller, W., et al. (2012). Compartmentalized control of skin immunity by resident commensals. Science, 337(6098), 1115–1119. https://doi.org/10.1126/science.1225152.
O’Shea, J. J., & Paul, W. E. (2010). Mechanisms underlying lineage commitment and plasticity of helper CD4+ T cells. Science, 327(5969), 1098–1102. https://doi.org/10.1126/science.1178334.
Onishi, R. M., & Gaffen, S. L. (2010). Interleukin-17 and its target genes: Mechanisms of interleukin-17 function in disease. Immunology, 129(3), 311–321. https://doi.org/10.1111/j.1365-2567.2009.03240.x.
Patel, D. D., & Kuchroo, V. K. (2015). Th17 cell pathway in human immunity: Lessons from genetics and therapeutic interventions. Immunity, 43(6), 1040–1051. https://doi.org/10.1016/j.immuni.2015.12.003.
Pihlstrom, B. L., Michalowicz, B. S., & Johnson, N. W. (2005). Periodontal diseases. The Lancet, 366(9499), 1809–1820. https://doi.org/10.1016/s0140-6736(05)67728-8.
Rouvier, E., Luciani, M. F., Mattei, M. G., Denizot, F., & Golstein, P. (1993). CTLA-8, cloned from an activated T cell, bearing AU-rich messenger RNA instability sequences, and homologous to a herpesvirus saimiri gene. Journal of Immunology, 150(12), 5445–5456.
Sathaliyawala, T., Kubota, M., Yudanin, N., Turner, D., Camp, P., Thome, J. J., et al. (2013). Distribution and compartmentalization of human circulating and tissue-resident memory T cell subsets. Immunity, 38(1), 187–197. https://doi.org/10.1016/j.immuni.2012.09.020.
Shalom-Barak, T., Quach, J., & Lotz, M. (1998). Interleukin-17-induced gene expression in articular chondrocytes is associated with activation of mitogen-activated protein kinases and NF-kappaB. The Journal of Biological Chemistry, 273(42), 27467–27473.
Shaw, M. H., Kamada, N., Kim, Y. G., & Nunez, G. (2012). Microbiota-induced IL-1beta, but not IL-6, is critical for the development of steady-state TH17 cells in the intestine. The Journal of Experimental Medicine, 209(2), 251–258. https://doi.org/10.1084/jem.20111703.
Taubman, M. A., Buckelew, J. M., Ebersole, J. L., & Smith, D. J. (1981). Periodontal bone loss and immune response to ovalbumin in germfree rats fed antigen-free diet with ovalbumin. Infection and Immunity, 32(1), 145–152.
Taubman, M. A., Valverde, P., Han, X., & Kawai, T. (2005). Immune response: The key to bone resorption in periodontal disease. Journal of Periodontology, 76(11 Suppl), 2033–2041. https://doi.org/10.1902/jop.2005.76.11-S.2033.
Teng, Y. T., Nguyen, H., Gao, X., Kong, Y. Y., Gorczynski, R. M., Singh, B., et al. (2000). Functional human T-cell immunity and osteoprotegerin ligand control alveolar bone destruction in periodontal infection. The Journal of Clinical Investigation, 106(6), R59–R67.
Tonetti, M. S., Jepsen, S., Jin, L., & Otomo-Corgel, J. (2017). Impact of the global burden of periodontal diseases on health, nutrition and wellbeing of mankind: A call for global action. Journal of Clinical Periodontology, 44(5), 456–462. https://doi.org/10.1111/jcpe.12732.
Tsukasaki, M., Komatsu, N., Nagashima, K., Nitta, T., Pluemsakunthai, W., Shukunami, C., et al. (2018). Host defense against oral microbiota by bone-damaging T cells. Nature Communications, 9(1), 701. https://doi.org/10.1038/s41467-018-03147-6.
Veldhoen, M. (2017). Interleukin 17 is a chief orchestrator of immunity. Nature Immunology, 18(6), 612–621. https://doi.org/10.1038/ni.3742.
Vernal, R., Dutzan, N., Chaparro, A., Puente, J., Antonieta Valenzuela, M., & Gamonal, J. (2005). Levels of interleukin-17 in gingival crevicular fluid and in supernatants of cellular cultures of gingival tissue from patients with chronic periodontitis. Journal of Clinical Periodontology, 32(4), 383–389. https://doi.org/10.1111/j.1600-051X.2005.00684.x.
Vernal, R., Dutzan, N., Hernandez, M., Chandia, S., Puente, J., Leon, R., et al. (2006). High expression levels of receptor activator of nuclear factor-kappa B ligand associated with human chronic periodontitis are mainly secreted by CD4+ T lymphocytes. Journal of Periodontology, 77(10), 1772–1780. https://doi.org/10.1902/jop.2006.050376.
Xiao, E., Mattos, M., Vieira, G. H. A., Chen, S., Correa, J. D., Wu, Y., et al. (2017). Diabetes enhances IL-17 expression and alters the oral microbiome to increase its pathogenicity. Cell Host & Microbe, 22(1), 120–8.e4. https://doi.org/10.1016/j.chom.2017.06.014.
Xu, M., Pokrovskii, M., Ding, Y., Yi, R., Au, C., Harrison, O. J., et al. (2018). c-MAF-dependent regulatory T cells mediate immunological tolerance to a gut pathobiont. Nature, 554, 373. https://doi.org/10.1038/nature25500. Retrieved from https://www.nature.com/articles/nature25500#supplementary-information.
Yamane, H., & Paul, W. E. (2013). Early signaling events that underlie fate decisions of naive CD4(+) T cells toward distinct T-helper cell subsets. Immunological Reviews, 252(1), 12–23. https://doi.org/10.1111/imr.12032.
Yang, J., Sundrud, M. S., Skepner, J., & Yamagata, T. (2014). Targeting Th17 cells in autoimmune diseases. Trends in Pharmacological Sciences, 35(10), 493–500. https://doi.org/10.1016/j.tips.2014.07.006.
Zappa, U., Reinking-Zappa, M., Graf, H., & Case, D. (1992). Cell populations associated with active probing attachment loss. Journal of Periodontology, 63(9), 748–752. https://doi.org/10.1902/jop.1992.63.9.748.
Zenobia, C., & Hajishengallis, G. (2015). Basic biology and role of interleukin-17 in immunity and inflammation. Periodontology 2000, 69(1), 142–159. https://doi.org/10.1111/prd.12083.
Acknowledgments
This work was partly funded by the Chilean government through FONDECYT # 11180389 (to N.D) and FONDECYT # 11180505 (to L.A).
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2019 Springer Nature Switzerland AG
About this paper
Cite this paper
Dutzan, N., Abusleme, L. (2019). T Helper 17 Cells as Pathogenic Drivers of Periodontitis. In: Belibasakis, G.N., Hajishengallis, G., Bostanci, N., Curtis, M.A. (eds) Oral Mucosal Immunity and Microbiome. Advances in Experimental Medicine and Biology, vol 1197. Springer, Cham. https://doi.org/10.1007/978-3-030-28524-1_9
Download citation
DOI: https://doi.org/10.1007/978-3-030-28524-1_9
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-28523-4
Online ISBN: 978-3-030-28524-1
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)