Oral administration of all-trans retinoic acid suppresses experimental periodontitis by modulating the Th17/Treg imbalance

Journal of Periodontology

Volumn 85, Issue 5, 2014, Pages 740-750

  Wang, Linyuan ^a,b   Wang, Jinyan ^a   Jin, Ying ^a   Gao, Hong ^c   Lin, Xiaoping ^a  

^a CHINA MEDICAL UNIVERSITY   (China)

^b JINZHOU MEDICAL UNIVERSITY   (China)

^c BEIJING HOSPITAL   (China)

Author keywords

Bone resorption; Periodontitis; RANK ligand; Regulatory; T lymphocytes; Th17 cells; Tretinoin

Indexed keywords

ANTIINFLAMMATORY AGENT; FORKHEAD TRANSCRIPTION FACTOR; FOXP3 PROTEIN, MOUSE; IL10 PROTEIN, MOUSE; IL17A PROTEIN, MOUSE; INTERLEUKIN 10; INTERLEUKIN 17; RETINOIC ACID; RETINOID RELATED ORPHAN RECEPTOR GAMMA; RORC PROTEIN, MOUSE; TRANSFORMING GROWTH FACTOR BETA1;

ALVEOLAR BONE LOSS; ANIMAL; C57BL MOUSE; CD4+ T LYMPHOCYTE; COMPARATIVE STUDY; DISEASE MODEL; DRUG EFFECTS; FEMALE; IMMUNOLOGY; INBRED MOUSE STRAIN; LYMPH NODE; LYMPHOCYTE ACTIVATION; MICROBIOLOGY; MOUSE; ORAL DRUG ADMINISTRATION; PATHOLOGY; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RANDOMIZATION; REGULATORY T LYMPHOCYTE; SPLEEN; TH17 CELL;

ADMINISTRATION, ORAL; ALVEOLAR BONE LOSS; ANIMALS; ANTI-INFLAMMATORY AGENTS; CD4-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; FEMALE; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-10; INTERLEUKIN-17; LYMPH NODES; LYMPHOCYTE ACTIVATION; MICE; MICE, INBRED C57BL; MICE, INBRED STRAINS; NUCLEAR RECEPTOR SUBFAMILY 1, GROUP F, MEMBER 3; PERIODONTITIS; PORPHYROMONAS GINGIVALIS; RANDOM ALLOCATION; SPLEEN; T-LYMPHOCYTES, REGULATORY; TH17 CELLS; TRANSFORMING GROWTH FACTOR BETA1; TRETINOIN;

EID: 84901477903     PISSN: 00223492     EISSN: None     Source Type: Journal    
DOI: 10.1902/jop.2013.130132     Document Type: Article

References (37)

1. Hernández M, Dutzan N, García-Sesnich J, et al. Host-pathogen interactions in progressive chronic periodontitis. J Dent Res 2011;90:1164-1170.
2. Teng YT. The role of acquired immunity and periodontal disease progression. Crit Rev Oral Biol Med 2003;14:237-252.
3. Gemmell E, Yamazaki K, Seymour GJ. The role of T cells in periodontal disease: Homeostasis and autoimmunity. Periodontol 2000 2007;43:14-40.
4. Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol 2008;79(Suppl. 8): 1585-1591.
5. Peters A, Lee Y, Kuchroo VK. The many faces of Th17 cells. Curr Opin Immunol 2011;23:702-706.
6. Woltman AM, de Haij S, Boonstra JG, Gobin SJ, Daha MR, van Kooten C. Interleukin-17 and CD40-ligand synergistically enhance cytokine and chemokine production by renal epithelial cells. J Am Soc Nephrol 2000;11:2044-2055.
7. Hirata T, Osuga Y, Hamasaki K, et al. Interleukin (IL)-17A stimulates IL-8 secretion, cyclooxygensase-2 expression, and cell proliferation of endometriotic stromal cells. Endocrinology 2008;149:1260-1267. (Pubitemid 351397970)
8. Kotake S, Udagawa N, Takahashi N, et al. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 1999;103:1345-1352. (Pubitemid 29218305)
9. Miossec P, Kolls JK. Targeting IL-17 and TH17 cells in chronic inflammation. Nat Rev Drug Discov 2012; 11:763-776.
10. + regulatory t cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol 2004;22:531-562. (Pubitemid 38680433)
11. 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;47:525-531.
12. Zhao L, Zhou Y, Xu Y, Sun Y, Li L, Chen W. Effect of non-surgical periodontal therapy on the levels of Th17/Th1/Th2 cytokines and their transcription factors in Chinese chronic periodontitis patients. J Clin Periodontol 2011;38:509-516.
13. Ernst CW, Lee JE, Nakanishi T, et al. Diminished forkhead box P3/CD25 double-positive T regulatory cells are associated with the increased nuclear factor kappaB ligand (RANKL+) T cells in bone resorption lesion of periodontal disease. Clin Exp Immunol 2007; 148:271-280. (Pubitemid 46587581)
14. Garlet GP, Cardoso CR, Mariano FS, et al. Regulatory T cells attenuate experimental periodontitis progression in mice. J Clin Periodontol 2010;37:591-600.
15. Bettelli E, Carrier Y, Gao W, et al. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature 2006;441:235-238.
16. Valmori D, Raffin C, Raimbaud I, Ayyoub M. Human RORγτ+ TH17 cells preferentially differentiate from naive FOXP3+Treg in the presence of lineagespecific polarizing factors. Proc Natl Acad Sci USA 2010;107:19402-19407.
17. Wang W, Shao S, Jiao Z, Guo M, Xu H, Wang S. The Th17/Treg imbalance and cytokine environment in peripheral blood of patients with rheumatoid arthritis. Rheumatol Int 2012;32:887-893.
18. Zhao L, Yang J, Wang HP, Liu RY. Imbalance in the Th17/Treg and cytokine environment in peripheral blood of patients with adenocarcinoma and squamous cell carcinoma. Med Oncol 2013;30:461.
19. Dutzan N, Vernal R, Vaque JP, et al. Interleukin-21 expression and its association with proinflammatory cytokines in untreated chronic periodontitis patients. J Periodontol 2012;83:948-954.
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: 465-473.
21. Boyle WJ, Simonet WS, Lacey DL. Osteoclast differentiation and activation. Nature 2003;423: 337-342. (Pubitemid 40852708)
22. Kawai T, Matsuyama T, Hosokawa Y, et al. B and T lymphocytes are the primary sources of RANKL in the bone resorptive lesion of periodontal disease. Am J Pathol 2006;169:987-998. (Pubitemid 44411961)
23. Lin X, Han X, Kawai T, Taubman MA. Antibody to receptor activator of NF-κB ligand ameliorates T cell-mediated periodontal bone resorption. Infect Immun 2011;79:911-917.
24. 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.
25. Dutzan N, Gamonal J, Silva A, Sanz M, Vernal R. 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. J Clin Periodontol 2009;36: 396-403.
26. Pino-Lagos K, Benson MJ, Noelle RJ. Retinoic acid in the immune system. Ann N Y Acad Sci 2008; 1143:170-187.
27. Kwok SK, Park MK, Cho ML, et al. Retinoic acid attenuates rheumatoid inflammation in mice. J Immunol 2012;189:1062-1071.
28. Keino H, Watanabe T, Sato Y, Okada AA. Antiinflammatory effect of retinoic acid on experimental autoimmune uveoretinitis. Br J Ophthalmol 2010; 94:802-807.
29. Yamashita K, Eastcott JW, Taubman MA, Smith DJ, Cox DS. Effect of adoptive transfer of cloned Actinobacillus actinomycetemcomitans-specific T helper cells on periodontal disease. Infect Immun 1991;59:1529-1534.
30. Eick S, Pfister W, Stürzebecher U, Jarema S, Stürzebecher J. Inhibitors of benzamidine type influence the virulence properties of Porphyromonas gingivalis strains. Acta Biochim Pol 2003;50: 725-734. (Pubitemid 38623804)
31. Alayan J, Gemmell E, Ford P, et al. The role of cytokines in a Porphyromonas gingivalis-induced murine abscess model. Oral Microbiol Immunol 2007;22: 304-312. (Pubitemid 47351230)
32. Okui T, Aoki Y, Ito H, Honda T, Yamazaki K. The presence of IL-17+/FOXP3+ double-positive cells in periodontitis. J Dent Res 2012;91:574-579.
33. Yu JJ, Ruddy MJ, Wong GC, et al. 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;109:3794-3802. (Pubitemid 46641730)
34. Ishii H, Tanabe S, Ueno M, et al. ifn-γ-dependent secretion of IL-10 from Th1 cells and microglia/macrophages contributes to functional recovery after spinal cord injury. Cell Death Dis 2013;4:e710.
35. Geissmann F, Revy P, Brousse N, et al. Retinoids regulate survival and antigen presentation by immature dendritic cells. J Exp Med 2003;198:623-634. (Pubitemid 37040396)
36. Theill LE, Boyle WJ, Penninger JM. RANK-L and RANK: T cells, bone loss, and mammalian evolution. Annu Rev Immunol 2002;20:795-823. (Pubitemid 34293440)
37. Yao Z, Fanslow WC, Seldin MF, et al. Herpesvirus saimiri encodes a new cytokine, IL-17, which binds to a novel cytokine receptor. J Immunol 2011;187: 4392-4402.