Journal of Ginseng Research

The Korean Society of Ginseng (고려인삼학회)
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Bone remodeling effects of Korean Red Ginseng extracts for dental implant applications

  • Kang, Myong-Hun (Department of Dental Biomaterials and Institute of Biodegradable Materials, Institute of Oral Bioscience and School of Dentistry (Plus BK21 Program), Jeonbuk National University) ;
  • Lee, Sook-Jeong (Department of Bioactive Material Science, Jeonbuk National University) ;
  • Lee, Min-Ho (Department of Dental Biomaterials and Institute of Biodegradable Materials, Institute of Oral Bioscience and School of Dentistry (Plus BK21 Program), Jeonbuk National University)
  • Received : 2019.12.16
  • Accepted : 2020.05.15
  • Published : 2020.11.15
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Abstract

Background: The formation of a nanotube layer on a titanium nanotube (N-Ti) plate facilitates an active reaction between bone cells and the material surface via efficient delivery of the surface materials of the dental implant into the tissues. Studies have reported that Korean Red Ginseng extracts (KRGEs) are involved in a variety of pharmacological activities: we investigated whether implantation with a KRGE-loaded N-Ti miniimplant affects osteogenesis and osseointegration. Methods: KRGE-loaded nanotubes were constructed by fabrication on pure Ti via anodization, and MC3T3-E1 cells were cultured on the N-Ti. N-Ti implants were subsequently placed on a rat's edentulous mandibular site. New bone formation and bone mineral density were measured to analyze osteogenesis and osseointegration. Results: KRGE-loaded N-Ti significantly increased the proliferation and differentiation of MC3T3-E1 cells compared with cells on pure Ti without any KRGE loading. After 1-4 weeks, the periimplant tissue in the edentulous mandibular of the healed rat showed a remarkable increase in new bone formation and bone mineral density. In addition, high levels of the bone morphogenesis protein-2 and bone morphogenesis protein-7, besides collagen, were expressed in the periimplant tissues. Conclusion: Our findings suggest that KRGE-induced osteogenesis and osseointegration around the miniimplant may facilitate the clinical application of dental implants.

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References

  1. Oshida Y, Tuna EB, Aktoren O, Gencay K. Dental implant systems. Int J Mol Sci 2010;11:1580-678. https://doi.org/10.3390/ijms11041580
  2. Adell R. Tissue integrated prostheses in clinical dentistry. Int Dent J 1985;35:259-65.
  3. Miao X, Wang D, Xu L, Wang J, Zeng D, Lin S, Huang C, Liu X, Jiang X. The response of human osteoblasts, epithelial cells, fibroblasts, macrophages and oral bacteria to nanostructured titanium surfaces: a systematic study. Int J Nanomedicine 2017;12:1415-30. https://doi.org/10.2147/IJN.S126760
  4. Park J, Bauer S, von der Mark K, Schmuki P. Nanosize and vitality: TiO2 nanotube diameter directs cell fate. Nano Lett 2007;7:1686-91. https://doi.org/10.1021/nl070678d
  5. Das K, Bose S, Bandyopadhyay A. TiO2 nanotubes on Ti: influence of nanoscale morphology on bone cell-materials interaction. J Biomed Mater Res A 2009;90:225-37.
  6. Lee YH, Bhattarai G, Park IS, Kim GR, Kim GE, Lee MH, Yi HK. Bone regeneration around N-acetyl cysteine-loaded nanotube titanium dental implant in rat mandible. Biomaterials 2013;34:10199-208. https://doi.org/10.1016/j.biomaterials.2013.08.080
  7. Brekhman II, Dardymov IV. New substances of plant origin which increase nonspecific resistance. Annu Rev Pharmacol 1969;9:419-30. https://doi.org/10.1146/annurev.pa.09.040169.002223
  8. Shibata S, Ando T, Tanaka O. Chemical studies on the oriental plant drugs. XVII. The prosapogenin of the ginseng saponins (ginsenosides-Rb1, -Rb2, and -Rc). Chem Pharm Bull (Tokyo) 1966;14:1157-61. https://doi.org/10.1248/cpb.14.1157
  9. Attele AS, Wu JA, Yuan CS. Ginseng pharmacology: multiple constituents and multiple actions. Biochem Pharmacol 1999;58:1685-93. https://doi.org/10.1016/S0006-2952(99)00212-9
  10. Gonzalez-Burgos E, Fernandez-Moriano C, Gomez-Serranillos MP. Potential neuroprotective activity of Ginseng in Parkinson's disease: a review. J Neuroimmune Pharmacol 2015;10:14-29. https://doi.org/10.1007/s11481-014-9569-6
  11. Jung JH, Kang IG, Kim DY, Hwang YJ, Kim ST. The effect of Korean red ginseng on allergic inflammation in a murine model of allergic rhinitis. J Ginseng Res 2013;37:167-75. https://doi.org/10.5142/jgr.2013.37.167
  12. Wong AS, Che CM, Leung KW. Recent advances in ginseng as cancer therapeutics: a functional and mechanistic overview. Nat Prod Rep 2015;32:256-72. https://doi.org/10.1039/C4NP00080C
  13. Bei J, Zhang X, Wu J, Hu Z, Xu B, Lin S, Cui L, Wu T, Zou L. Ginsenoside Rb1 does not halt osteoporotic bone loss in ovariectomized rats. PLoS One 2018;13:e0202885. https://doi.org/10.1371/journal.pone.0202885
  14. He F, Yu C, Liu T, Jia H. Ginsenoside Rg1 as an effective regulator of mesenchymal stem cells. Front Pharmacol 2019;10:1565. https://doi.org/10.3389/fphar.2019.01565
  15. Park CM, Kim HM, Kim DH, Han HJ, Noh H, Jang JH, Park SH, Chae HJ, Chae SW, Ryu EK, et al. Ginsenoside Re inhibits osteoclast differentiation in mouse bone marrow-derived macrophages and Zebrafish scale model. Mol Cells 2016;39:855-61. https://doi.org/10.14348/molcells.2016.0111
  16. Park IS, Lee MH, Bae TS, Seol KW. Effects of anodic oxidation parameters on a modified titanium surface. J Biomed Mater Res B Appl Biomater 2008;84:422-9.
  17. Jacinto A, Wolpert L. Filopodia. Curr Biol 2001;11:R634. https://doi.org/10.1016/S0960-9822(01)00378-5
  18. Britland S, Clark P, Connolly P, Moores G. Micropatterned substratum adhesiveness: a model for morphogenetic cues controlling cell behavior. Exp Cell Res 1992;198:124-9. https://doi.org/10.1016/0014-4827(92)90157-4
  19. Georger Jr JHSD, Rudolph AS, Hickman JJ. Coplanar patterns of self-assembled monolayers for selective cell adhesion and outgrowth, thin solid films. Thin Solid Films 1992;210-211:716-9. https://doi.org/10.1016/0040-6090(92)90383-M
  20. Stenger DAGJ, Dulcey CS, Hickman JJ, Rudolph AS, Nielsen TB, McCort SM, Calvert JM. Coplanar molecular assemblies of amino and perfluorinated alkylsilanes: characterization and geometric definition of mammalian cell adhesion and growth. Journal of American Chemical Society 1992;114:8435-42. https://doi.org/10.1021/ja00048a013
  21. Moon SH, Lee SJ, Park IS, Lee MH, Soh YJ, Bae TS, Kim HS. Bioactivity of Ti-6Al-4V alloy implants treated with ibandronate after the formation of the nanotube TiO2 layer. J Biomed Mater Res B Appl Biomater 2012;100:2053-9.
  22. Popat KC, Eltgroth M, Latempa TJ, Grimes CA, Desai TA. Decreased Staphylococcus epidermis adhesion and increased osteoblast functionality on antibiotic-loaded titania nanotubes. Biomaterials 2007;28:4880-8. https://doi.org/10.1016/j.biomaterials.2007.07.037
  23. Stadlinger B, Korn P, Todtmann N, Eckelt U, Range U, Burki A, Ferguson SJ, Kramer I, Kautz A, Schnabelrauch M, et al. Osseointegration of biochemically modified implants in an osteoporosis rodent model. Eur Cell Mater 2013;25:326-40. discussion 39-40. https://doi.org/10.22203/eCM.v025a23
  24. Stein GS, Lian JB, Owen TA. Relationship of cell growth to the regulation of tissue-specific gene expression during osteoblast differentiation. FASEB J 1990;4:3111-23. https://doi.org/10.1096/fasebj.4.13.2210157
  25. Golub EE, B-BK. The role of alkaline phosphatase in mineralization. Curr. Opin. Orthopaed. 2007;18:444-8. https://doi.org/10.1097/BCO.0b013e3282630851
  26. Mathews S, Bhonde R, Gupta PK, Totey S. A novel tripolymer coating demonstrating the synergistic effect of chitosan, collagen type 1 and hyaluronic acid on osteogenic differentiation of human bone marrow derived mesenchymal stem cells. Biochem Biophys Res Commun 2011;414:270-6. https://doi.org/10.1016/j.bbrc.2011.09.071
  27. Siddiqi MH, Siddiqi MZ, Ahn S, Kang S, Kim YJ, Sathishkumar N, Yang DU, Yang DC. Ginseng saponins and the treatment of osteoporosis: mini literature review. J Ginseng Res 2013;37:261-8. https://doi.org/10.5142/jgr.2013.37.261
  28. Balloni S, Calvi EM, Damiani F, Bistoni G, Calvitti M, Locci P, Becchetti E, Marinucci L. Effects of titanium surface roughness on mesenchymal stem cell commitment and differentiation signaling. Int J Oral Maxillofac Implants 2009;24:627-35.
  29. Derynck R, Zhang Y. Intracellular signalling: the mad way to do it. Curr Biol 1996;6:1226-9. https://doi.org/10.1016/S0960-9822(96)00702-6
  30. Reddi AH. Bone and cartilage differentiation. Curr Opin Genet Dev 1994;4:737-44. https://doi.org/10.1016/0959-437X(94)90141-O
  31. Kawai M, Bessho K, Maruyama H, Miyazaki J, Yamamoto T. Simultaneous gene transfer of bone morphogenetic protein (BMP) -2 and BMP-7 by in vivo electroporation induces rapid bone formation and BMP-4 expression. BMC Musculoskelet Disord 2006;7:62. https://doi.org/10.1186/1471-2474-7-62
  32. Mundy G, Garrett R, Harris S, Chan J, Chen D, Rossini G, Boyce B, Zhao M, Gutierrez G. Stimulation of bone formation in vitro and in rodents by statins. Science 1999;286:1946-9. https://doi.org/10.1126/science.286.5446.1946
  33. Lu JM, Yao Q, Chen C. Ginseng compounds: an update on their molecular mechanisms and medical applications. Curr Vasc Pharmacol 2009;7:293-302. https://doi.org/10.2174/157016109788340767
  34. Polan ML, Hochberg RB, Trant AS, Wuh HC. Estrogen bioassay of ginseng extract and ArginMax, a nutritional supplement for the enhancement of female sexual function. J Womens Health (Larchmt) 2004;13:427-30. https://doi.org/10.1089/154099904323087114
  35. Shin HY, Jeong HJ, Hyo Jin A, Hong SH, Um JY, Shin TY, Kwon SJ, Jee SY, Seo BI, Shin SS, et al. The effect of Panax ginseng on forced immobility time & immune function in mice. Indian J Med Res 2006;124:199-206.
  36. Wang W, Zhao Y, Rayburn ER, Hill DL, Wang H, Zhang R. In vitro anticancer activity and structure-activity relationships of natural products isolated from fruits of Panax ginseng. Cancer Chemother Pharmacol 2007;59:589-601. https://doi.org/10.1007/s00280-006-0300-z
  37. Kim HR, Cui Y, Hong SJ, Shin SJ, Kim DS, Kim NM, So SH, Lee SK, Kim EC, Chae SW, et al. Effect of ginseng mixture on osteoporosis in ovariectomized rats. Immunopharmacol Immunotoxicol 2008;30:333-45. https://doi.org/10.1080/08923970801949125
  38. Kim J, Lee H, Kang KS, Chun KH, Hwang GS. Protective effect of Korean Red Ginseng against glucocorticoid-induced osteoporosis in vitro and in vivo. J Ginseng Res 2015;39:46-53. https://doi.org/10.1016/j.jgr.2014.06.001
  39. Gu Y, Zhou J, Wang Q, Fan W, Yin G. Ginsenoside Rg1 promotes osteogenic differentiation of rBMSCs and healing of rat tibial fractures through regulation of GR-dependent BMP-2/SMAD signaling. Sci Rep 2016;6:25282. https://doi.org/10.1038/srep25282
  40. Li J, Wang Q, Yang R, Zhang J, Li X, Zhou X, Miao D. BMI-1 mediates estrogendeficiency-induced bone loss by inhibiting reactive oxygen species accumulation and T cell activation. J Bone Miner Res 2017;32:962-73. https://doi.org/10.1002/jbmr.3059
  41. Siddiqi MZ, Siddiqi MH, Kim YJ, Jin Y, Huq MA, Yang DC. Effect of fermented red ginseng extract enriched in ginsenoside Rg3 on the differentiation and mineralization of preosteoblastic MC3T3-E1 cells. J Med Food 2015;18:542-8. https://doi.org/10.1089/jmf.2014.3251
  42. Kim DY, Jung MS, Park YG, Yuan HD, Quan HY, Chung SH. Ginsenoside Rh2(S) induces the differentiation and mineralization of osteoblastic MC3T3-E1 cells through activation of PKD and p38 MAPK pathways. BMB Rep 2011;44:659-64. https://doi.org/10.5483/BMBRep.2011.44.10.659

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