Effect of Epigallocatechin-3-Gallate on the alveolar bone remodeling and arthritis in collagen-induced arthritis model in mice

콜라겐 유도 관절염 모델에서 동반된 치주염 유발시 EGCG가 치주염 치료에 미치는 효과에 관한 연구

  • Cho, In-Woo (Department of Periodontology,College of Dentistry, Dankook University) ;
  • Yim, Seong-Jun (Department of Periodontology,College of Dentistry, Dankook University) ;
  • Shin, Hyun-Seung (Department of Periodontology,College of Dentistry, Dankook University) ;
  • Park, Jung-Chul (Department of Periodontology,College of Dentistry, Dankook University)
  • 조인우 (단국대학교 치과대학 부속치과병원 치주과학교실) ;
  • 임성준 (단국대학교 치과대학 부속치과병원 치주과학교실) ;
  • 신현승 (단국대학교 치과대학 부속치과병원 치주과학교실) ;
  • 박정철 (단국대학교 치과대학 부속치과병원 치주과학교실)
  • Received : 2015.12.15
  • Accepted : 2016.02.17
  • Published : 2016.04.01

Abstract

The aim of this study was to evaluate the effect of Epigallocatechin-3-Gallate (EGCG) on the alveolar bone metabolism in a collagen-induced arthritis (CIA) model in mice to enhance the understanding of rheumatoid arthritis (RA)-associated alveolar bone loss. Following the induction of CIA in animals (mice, n=16), mandibles were retrieved for micro-computed tomography (micro-CT) and isolation of alveolar bone cells (ABCs). In vitro osteogenic potentials of ABCs were evaluated and the mRNA expression of downstream effector genes was assessed. CIA was successfully induced in all animals, and micro-CT data showed that alveolar bone loss was significantly increased in the CIA group while the treatment of EGCG prevented the alveolar bone resorption. Osteogenesis by ABCs was significantly increased in the CIA+EGCG group in vitro. The analysis of mRNA expressions showed that osteoclastogenesis-associated genes were increased in CIA group while bone protecting genes were upregulated in EGCG treated group. The results demonstrate that EGCG downregulated the alveolar bone resorption in a CIA model in mice, and upregulation of bone protecting genes appear to be involved. Further studies are warranted.

Keywords

Acknowledgement

Supported by : 한국연구재단

References

  1. Tonetti MS, Claffey N, European Workshop in Periodontology group C. Advances in the progression of periodontitis and proposal of definitions of a periodontitis case and disease progression for use in risk factor research. Group C consensus report of the 5th European Workshop in Periodontology. J Clin Periodontol 2005;32 Suppl 6:210-213. https://doi.org/10.1111/j.1600-051X.2005.00822.x
  2. Graves D. Cytokines that promote periodontal tissue destruction. J Periodontol 2008;79:1585-1591. https://doi.org/10.1902/jop.2008.080183
  3. Mercado F, Marshall R, Klestov A, Bartold P. Relationship between rheumatoid arthritis and periodontitis. Journal of periodontology 2001;72:779-787. https://doi.org/10.1902/jop.2001.72.6.779
  4. Pons-Fuster A, Rodriguez Agudo C, Galvez Munoz P, Saiz Cuenca E, Pina Perez FM, Lopez-Jornet P. Clinical evaluation of periodontal disease in patients with rheumatoid arthritis: A cross-sectional study. Quintessence Int 2015;46:817-822.
  5. Bingham CO, 3rd, Moni M. Periodontal disease and rheumatoid arthritis: the evidence accumulates for complex pathobiologic interactions. Curr Opin Rheumatol 2013;25:345-353. https://doi.org/10.1097/BOR.0b013e32835fb8ec
  6. Mercado F, Marshall RI, Klestov AC, Bartold PM. Is there a relationship between rheumatoid arthritis and periodontal disease? J Clin Periodontol 2000;27:267-272. https://doi.org/10.1034/j.1600-051x.2000.027004267.x
  7. Park JC, Su C, Jung IH, et al. Mechanism of alveolar bone loss in a collagen-induced arthritis model in mice. J Clin Periodontol 2011;38:122-130. https://doi.org/10.1111/j.1600-051X.2010.01645.x
  8. Kornman KS, Page RC, Tonetti MS. The host response to the microbial challenge in periodontitis: assembling the players. Periodontology 2000 1997;14:33-53. https://doi.org/10.1111/j.1600-0757.1997.tb00191.x
  9. Graves DT, Oates T, Garlet GP. Review of osteoimmunology and the host response in endodontic and periodontal lesions. Journal of oral microbiology 2011;3.
  10. Siegel J. Comparative effectiveness of treatments for rheumatoid arthritis. Annals of internal medicine 2008;148:162-163. https://doi.org/10.7326/0003-4819-148-2-200801150-00012
  11. Donahue KE, Jonas DE, Hansen RA, et al. Drug therapy for rheumatoid arthritis in adults: An update. 2012.
  12. Donahue KE, Gartlehner G, Jonas DE, et al. Systematic review: comparative effectiveness and harms of disease-modifying medications for rheumatoid arthritis. Annals of Internal Medicine 2008;148:124-134.
  13. Ahmed S, Anuntiyo J, Malemud CJ, Haqqi TM. Biological basis for the use of botanicals in osteoarthritis and rheumatoid arthritis: a review. Evid Based Complement Alternat Med 2005;2:301-308. https://doi.org/10.1093/ecam/neh117
  14. Siddiqui IA, Afaq F, Adhami VM, Ahmad N, Mukhtar H. Antioxidants of the beverage tea in promotion of human health. Antioxid Redox Signal 2004;6:571-582. https://doi.org/10.1089/152308604773934323
  15. Takai S, Matsushima-Nishiwaki R, Adachi S, et al. (-)-Epigallocatechin gallate reduces platelet-derived growth factor-BB-stimulated interleukin-6 synthesis in osteoblasts: suppression of SAPK/JNK. Mediators Inflamm 2008;2008:291808.
  16. Yun JH, Kim CS, Cho KS, Chai JK, Kim CK, Choi SH. (-)-Epigallocatechin gallate induces apoptosis, via caspase activation, in osteoclasts differentiated from RAW 264.7 cells. J Periodontal Res 2007;42:212-218. https://doi.org/10.1111/j.1600-0765.2006.00935.x
  17. Corps AN, Curry VA, Buttle DJ, Hazleman BL, Riley GP. Inhibition of interleukin-1beta-stimulated collagenase and stromelysin expression in human tendon fibroblasts by epigallocatechin gallate ester. Matrix Biol 2004;23:163-169. https://doi.org/10.1016/j.matbio.2004.05.001
  18. Riegsecker S, Wiczynski D, Kaplan MJ, Ahmed S. Potential benefits of green tea polyphenol EGCG in the prevention and treatment of vascular inflammation in rheumatoid arthritis. Life Sci 2013;93:307-312. https://doi.org/10.1016/j.lfs.2013.07.006
  19. Yang EJ, Lee J, Lee SY, et al. EGCG attenuates autoimmune arthritis by inhibition of STAT3 and HIF-1alpha with Th17/Treg control. PLoS One 2014;9:e86062. https://doi.org/10.1371/journal.pone.0086062
  20. Asahi Y, Noiri Y, Miura J, et al. Effects of the tea catechin epigallocatechin gallate on Porphyromonas gingivalis biofilms. J Appl Microbiol 2014;116:1164-1171. https://doi.org/10.1111/jam.12458
  21. Jung IH, Lee DE, Yun JH, et al. Anti-inflammatory effect of (-)-epigallocatechin-3-gallate on Porphyromonas gingivalis lipopolysaccharidestimulated fibroblasts and stem cells derived from human periodontal ligament. J Periodontal Implant Sci 2012;42:185-195. https://doi.org/10.5051/jpis.2012.42.6.185
  22. Cho AR, Kim JH, Lee DE, et al. The effect of orally administered epigallocatechin-3-gallate on ligatureinduced periodontitis in rats. J Periodontal Res 2013;48:781-789.
  23. Tominari T, Matsumoto C, Watanabe K, et al. Epigallocatechin gallate (EGCG) suppresses lipopolysaccharide-induced inflammatory bone resorption, and protects against alveolar bone loss in mice. FEBS Open Bio 2015;5:522-527. https://doi.org/10.1016/j.fob.2015.06.003
  24. Lee SW, Kim JH, Park YB, Lee SK. Bortezomib attenuates murine collagen-induced arthritis. Ann Rheum Dis 2009;68:1761-1767. https://doi.org/10.1136/ard.2008.097709
  25. Kim JS, Kim JM, O JJ, Jeon BS. Inhibition of inducible nitric oxide synthase expression and cell death by (-)-epigallocatechin-3-gallate, a green tea catechin, in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson's disease. J Clin Neurosci 2010;17:1165-1168. https://doi.org/10.1016/j.jocn.2010.01.042
  26. Lee YK, Kim JS, Lim SC. Effects of atractylodis rhizoma pharmacopuncture on an acute gastric mucosal lesion induced by compound 48/80 in rats. J Pharmacopuncture 2012;15:12-17. https://doi.org/10.3831/KPI.2012.15.1.012
  27. Park CH, Abramson ZR, Taba M, Jr., et al. Threedimensional micro-computed tomographic imaging of alveolar bone in experimental bone loss or repair. J Periodontol 2007;78:273-281. https://doi.org/10.1902/jop.2007.060252
  28. Kim CS, Choi SH, Cho KS, Chai JK, Wikesjo UM, Kim CK. Periodontal healing in one-wall intra-bony defects in dogs following implantation of autogenous bone or a coral-derived biomaterial. J Clin Periodontol 2005;32:583-589. https://doi.org/10.1111/j.1600-051X.2005.00729.x
  29. Shi S, Gronthos S, Chen S, et al. Bone formation by human postnatal bone marrow stromal stem cells is enhanced by telomerase expression. Nat Biotechnol 2002;20:587-591.
  30. Belibasakis GN, Bostanci N, Hashim A, et al. Regulation of RANKL and OPG gene expression in human gingival fibroblasts and periodontal ligament cells by Porphyromonas gingivalis: a putative role of the Arg-gingipains. Microb Pathog 2007;43:46-53. https://doi.org/10.1016/j.micpath.2007.03.001
  31. Kanzaki H, Chiba M, Shimizu Y, Mitani H. Dual regulation of osteoclast differentiation by periodontal ligament cells through RANKL stimulation and OPG inhibition. Journal of dental research 2001;80:887-891. https://doi.org/10.1177/00220345010800030801
  32. Yun JH, Kim CS, Cho KS, Chai JK, Kim CK, Choi SH. (-)-Epigallocatechin gallate induces apoptosis, via caspase activation, in osteoclasts differentiated from RAW 264.7 cells. Journal of periodontal research 2007;42:212-218. https://doi.org/10.1111/j.1600-0765.2006.00935.x
  33. Park JC, Kim JM, Jung IH, et al. Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: in vitro and in vivo evaluations. Journal of clinical periodontology 2011;38:721-731. https://doi.org/10.1111/j.1600-051X.2011.01716.x
  34. Hirayama T, Danks L, Sabokbar A, Athanasou NA. Osteoclast formation and activity in the pathogenesis of osteoporosis in rheumatoid arthritis. Rheumatology (Oxford) 2002;41:1232-1239. https://doi.org/10.1093/rheumatology/41.11.1232
  35. Bucay N, Sarosi I, Dunstan CR, et al. Osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes & development 1998;12:1260-1268. https://doi.org/10.1101/gad.12.9.1260
  36. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, Riggs BL. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. Journal of Bone and Mineral Research 2000;15:2-12. https://doi.org/10.1359/jbmr.2000.15.1.2
  37. Kong Y-Y, Feige U, Sarosi I, et al. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature 1999;402:43-47. https://doi.org/10.1038/35005552
  38. Huang H, Kang L, Chen S, et al. (-)-Epigallocatechin-3-Gallate (EGCG) decreases osteoclastogeneis via opg/rankl modulation. Bone 2009;44:S329-S330.
  39. Chen C, Kang L, Hung S, Ho M, Chang J, Wang G. (-)-epigallocatechin-3-gallate (EGCG) modulate OPG/RANKL/RANK in murine bone marrow mesenchymal stem cell and osteoblast. In: CALCIFIED TISSUE INTERNATIONAL. vol. 80: SPRINGER 233 SPRING STREET, NEW YORK, NY 10013 USA, 2007:S74-S74.
  40. Huang P, Chen C, Kang L, Hung S, Wang G, Chang J. (-)-epigallocatechin-3-gallate (EGCG) increases OPG/RANKL expression in osteoclast feeder cell, ST2. In: CALCIFIED TISSUE INTERNATIONAL. vol. 82: SPRINGER 233 SPRING ST, NEW YORK, NY 10013 USA, 2008:S99-S100.
  41. Shen CL, Yeh JK, Cao JJ, Chyu MC, Wang JS. Green tea and bone health: Evidence from laboratory studies. Pharmacol Res 2011;64:155-161.
  42. Chen L, Lee M-J, Li H, Yang CS. Absorption, distribution, and elimination of tea polyphenols in rats. Drug Metabolism and Disposition 1997;25:1045-1050.
  43. Kim JS, Kim J-M, Jeong-Ja O, Jeon BS. Inhibition of inducible nitric oxide synthase expression and cell death by (-)-epigallocatechin-3-gallate, a green tea catechin, in the 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine mouse model of Parkinson's disease. Journal of Clinical Neuroscience 2010;17:1165-1168. https://doi.org/10.1016/j.jocn.2010.01.042
  44. Nakagawa K, Okuda S, Miyazawa T. Dosedependent incorporation of tea catechins,(-)-epigallocatechin-3-gallate and (-)-epigallocatechin, into human plasma. Bioscience, biotechnology, and biochemistry 1997;61:1981-1985. https://doi.org/10.1271/bbb.61.1981
  45. Ullmann, Haller, Decourt, Girault, Spitzer, Weber. Plasma-kinetic characteristics of purified and isolated green tea catechin epigallocatechin gallate (EGCG) after 10 days repeated dosing in healthy volunteers. International journal for vitamin and nutrition research 2004;74:269-278. https://doi.org/10.1024/0300-9831.74.4.269
  46. Chow HS, Cai Y, Hakim IA, et al. Pharmacokinetics and safety of green tea polyphenols after multipledose administration of epigallocatechin gallate and polyphenon E in healthy individuals. Clinical Cancer Research 2003;9:3312-3319.