Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
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Static magnetic fields promote osteoblastic/cementoblastic differentiation in osteoblasts, cementoblasts, and periodontal ligament cells

  • Kim, Eun-Cheol (Department of Oral and Maxillofacial Pathology, Institute of Oral Biology, Kyung Hee University School of Dentistry) ;
  • Park, Jaesuh (Department of Oral and Maxillofacial Pathology, Institute of Oral Biology, Kyung Hee University School of Dentistry) ;
  • Kwon, Il Keun (Department of Dental Materials, Kyung Hee University School of Dentistry) ;
  • Lee, Suk-Won (Department of Biomaterials and Prosthodontics, Kyung Hee University Hospital at Gangdong, Kyung Hee University School of Dentistry) ;
  • Park, Su-Jung (Department of Biomaterials and Prosthodontics, Kyung Hee University Hospital at Gangdong, Kyung Hee University School of Dentistry) ;
  • Ahn, Su-Jin (Department of Biomaterials and Prosthodontics, Kyung Hee University Hospital at Gangdong, Kyung Hee University School of Dentistry)
  • Received : 2017.07.11
  • Accepted : 2017.08.18
  • Published : 2017.10.30
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Abstract

Purpose: Although static magnetic fields (SMFs) have been used in dental prostheses and osseointegrated implants, their biological effects on osteoblastic and cementoblastic differentiation in cells involved in periodontal regeneration remain unknown. This study was undertaken to investigate the effects of SMFs (15 mT) on the osteoblastic and cementoblastic differentiation of human osteoblasts, periodontal ligament cells (PDLCs), and cementoblasts, and to explore the possible mechanisms underlying these effects. Methods: Differentiation was evaluated by measuring alkaline phosphatase (ALP) activity, mineralized nodule formation based on Alizarin red staining, calcium content, and the expression of marker mRNAs assessed by reverse transcription polymerase chain reaction (RT-PCR). Signaling pathways were analyzed by western blotting and immunocytochemistry. Results: The activities of the early marker ALP and the late markers matrix mineralization and calcium content, as well as osteoblast- and cementoblast-specific gene expression in osteoblasts, PDLCs, and cementoblasts were enhanced. SMFs upregulated the expression of Wnt proteins, and increased the phosphorylation of glycogen synthase $kinase-3{\beta}$ ($GSK-3{\beta}$) and total ${\beta}-catenin$ protein expression. Furthermore, p38 and c-Jun N-terminal kinase (JNK) mitogen-activated protein kinase (MAPK), and nuclear $factor-{\kappa}B$ ($NF-{\kappa}B$) pathways were activated. Conclusions: SMF treatment enhanced osteoblastic and/or cementoblastic differentiation in osteoblasts, cementoblasts, and PDLCs. These findings provide a molecular basis for the beneficial osteogenic and/or cementogenic effect of SMFs, which could have potential in stimulating bone or cementum formation during bone regeneration and in patients with periodontal disease.

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References

  1. Shimono M, Ishikawa T, Ishikawa H, Matsuzaki H, Hashimoto S, Muramatsu T, et al. Regulatory mechanisms of periodontal regeneration. Microsc Res Tech 2003;60:491-502. https://doi.org/10.1002/jemt.10290
  2. Cook JJ, Summers NJ, Cook EA. Healing in the new millennium: bone stimulators: an overview of where we've been and where we may be heading. Clin Podiatr Med Surg 2015;32:45-59. https://doi.org/10.1016/j.cpm.2014.09.003
  3. Funk RH, Monsees T, Ozkucur N. Electromagnetic effects - from cell biology to medicine. Prog Histochem Cytochem 2009;43:177-264. https://doi.org/10.1016/j.proghi.2008.07.001
  4. Gaetani R, Ledda M, Barile L, Chimenti I, De Carlo F, Forte E, et al. Differentiation of human adult cardiac stem cells exposed to extremely low-frequency electromagnetic fields. Cardiovasc Res 2009;82:411-20. https://doi.org/10.1093/cvr/cvp067
  5. Sakata M, Yamamoto Y, Imamura N, Nakata S, Nakasima A. The effects of a static magnetic field on orthodontic tooth movement. J Orthod 2008;35:249-54. https://doi.org/10.1179/14653120722752
  6. Zhang J, Ding C, Ren L, Zhou Y, Shang P. The effects of static magnetic fields on bone. Prog Biophys Mol Biol 2014;114:146-52. https://doi.org/10.1016/j.pbiomolbio.2014.02.001
  7. Markov MS. Magnetic field therapy: a review. Electromagn Biol Med 2007;26:1-23. https://doi.org/10.1080/15368370600925342
  8. Yang TC, Maeda Y, Gonda T, Wada M. Magnetic attachment for implant overdentures: influence of contact relationship with the denture base on stability and bending strain. Int J Prosthodont 2013;26:563-5. https://doi.org/10.11607/ijp.3481
  9. Aksu AE, Dursun E, Calis M, Ersu B, Safak T, Tozum TF. Intraoral use of extraoral implants for oral rehabilitation of a pediatric patient after resection of ewing sarcoma of the mandible and reconstruction with iliac osteocutaneous free flap. J Craniofac Surg 2014;25:930-3. https://doi.org/10.1097/SCS.0000000000000709
  10. Siadat H, Bassir SH, Alikhasi M, Shayesteh YS, Khojasteh A, Monzavi A. Effect of static magnetic fields on the osseointegration of immediately placed implants: a randomized controlled clinical trial. Implant Dent 2012;21:491-5. https://doi.org/10.1097/ID.0b013e31826dcc2f
  11. Leesungbok R, Ahn SJ, Lee SW, Park GH, Kang JS, Choi JJ. The effects of a static magnetic field on bone formation around a sandblasted, large-grit, acid-etched-treated titanium implant. J Oral Implantol 2013;39:248-55. https://doi.org/10.1563/AAID-JOI-D-11-00101
  12. Yamamoto Y, Ohsaki Y, Goto T, Nakasima A, Iijima T. Effects of static magnetic fields on bone formation in rat osteoblast cultures. J Dent Res 2003;82:962-6. https://doi.org/10.1177/154405910308201205
  13. Denaro V, Papapietro N, Sgambato A, Barnaba SA, Ruzzini L, Paola BD, et al. Periprosthetic electrochemical corrosion of titanium and titanium-based alloys as a cause of spinal fusion failure. Spine 2008;33:8-13. https://doi.org/10.1097/BRS.0b013e31815e3978
  14. Denaro V, Cittadini A, Barnaba SA, Ruzzini L, Denaro L, Rettino A, et al. Static electromagnetic fields generated by corrosion currents inhibit human osteoblast differentiation. Spine 2008;33:955-9. https://doi.org/10.1097/BRS.0b013e31816c90b8
  15. Chiu KH, Ou KL, Lee SY, Lin CT, Chang WJ, Chen CC, et al. Static magnetic fields promote osteoblastlike cells differentiation via increasing the membrane rigidity. Ann Biomed Eng 2007;35:1932-9. https://doi.org/10.1007/s10439-007-9370-2
  16. Hsu SH, Chang JC. The static magnetic field accelerates the osteogenic differentiation and mineralization of dental pulp cells. Cytotechnology 2010;62:143-55. https://doi.org/10.1007/s10616-010-9271-3
  17. Kim EC, Leesungbok R, Lee SW, Lee HW, Park SH, Mah SJ, et al. Effects of moderate intensity static magnetic fields on human bone marrow-derived mesenchymal stem cells. Bioelectromagnetics 2015;36:267-76. https://doi.org/10.1002/bem.21903
  18. Bartold PM, Narayanan AS. Molecular and cell biology of healthy and diseased periodontal tissues. Periodontol 2000 2006;40:29-49. https://doi.org/10.1111/j.1600-0757.2005.00140.x
  19. Miyakoshi J. Effects of static magnetic fields at the cellular level. Prog Biophys Mol Biol 2005;87:213-23. https://doi.org/10.1016/j.pbiomolbio.2004.08.008
  20. Wang Y, Qin QH. A theoretical study of bone remodelling under PEMF at cellular level. Comput Methods Biomech Biomed Engin 2012;15:885-97. https://doi.org/10.1080/10255842.2011.565752
  21. Chung JH, Kim YS, Noh K, Lee YM, Chang SW, Kim EC. Deferoxamine promotes osteoblastic differentiation in human periodontal ligament cells via the nuclear factor erythroid 2-related factormediated antioxidant signaling pathway. J Periodontal Res 2014;49:563-73. https://doi.org/10.1111/jre.12136
  22. Kitagawa M, Tahara H, Kitagawa S, Oka H, Kudo Y, Sato S, et al. Characterization of established cementoblast-like cell lines from human cementum-lining cells in vitro and in vivo. Bone 2006;39:1035-42. https://doi.org/10.1016/j.bone.2006.05.022
  23. Pi SH, Lee SK, Hwang YS, Choi MG, Lee SK, Kim EC. Differential expression of periodontal ligamentspecific markers and osteogenic differentiation in human papilloma virus 16-immortalized human gingival fibroblasts and periodontal ligament cells. J Periodontal Res 2007;42:104-13. https://doi.org/10.1111/j.1600-0765.2006.00921.x
  24. Beertsen W, McCulloch CA, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 1997;13:20-40. https://doi.org/10.1111/j.1600-0757.1997.tb00094.x
  25. Chen FM, Jin Y. Periodontal tissue engineering and regeneration: current approaches and expanding opportunities. Tissue Eng Part B Rev 2010;16:219-55. https://doi.org/10.1089/ten.teb.2009.0562
  26. Kim MB, Song Y, Hwang JK. Kirenol stimulates osteoblast differentiation through activation of the BMP and $Wnt/{\beta}$-catenin signaling pathways in MC3T3-E1 cells. Fitoterapia 2014;98:59-65. https://doi.org/10.1016/j.fitote.2014.07.013
  27. Noth U, Tuli R, Seghatoleslami R, Howard M, Shah A, Hall DJ, et al. Activation of p38 and Smads mediates BMP-2 effects on human trabecular bone-derived osteoblasts. Exp Cell Res 2003;291:201-11. https://doi.org/10.1016/S0014-4827(03)00386-0
  28. Franceschi RT, Xiao G. Regulation of the osteoblast-specific transcription factor, Runx2: responsiveness to multiple signal transduction pathways. J Cell Biochem 2003;88:446-54. https://doi.org/10.1002/jcb.10369
  29. Subramaniam M, Jalal SM, Rickard DJ, Harris SA, Bolander ME, Spelsberg TC. Further characterization of human fetal osteoblastic hFOB 1.19 and hFOB/ER alpha cells: bone formation in vivo and karyotype analysis using multicolor fluorescent in situ hybridization. J Cell Biochem 2002;87:9-15. https://doi.org/10.1002/jcb.10259
  30. Hayami T, Zhang Q, Kapila Y, Kapila S. Dexamethasone's enhancement of osteoblastic markers in human periodontal ligament cells is associated with inhibition of collagenase expression. Bone 2007;40:93-104. https://doi.org/10.1016/j.bone.2006.07.003
  31. Bodine PV, Komm BS. Wnt signaling and osteoblastogenesis. Rev Endocr Metab Disord 2006;7:33-9.
  32. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nature 2005;434:843-50. https://doi.org/10.1038/nature03319
  33. Zhou J, He H, Yang L, Chen S, Guo H, Xia L, et al. Effects of pulsed electromagnetic fields on bone mass and $Wnt/{\beta}$-catenin signaling pathway in ovariectomized rats. Arch Med Res 2012;43:274-82. https://doi.org/10.1016/j.arcmed.2012.06.002
  34. Du L, Fan H, Miao H, Zhao G, Hou Y. Extremely low frequency magnetic fields inhibit adipogenesis of human mesenchymal stem cells. Bioelectromagnetics 2014;35:519-30. https://doi.org/10.1002/bem.21873
  35. Wolf-Goldberg T, Barbul A, Ben-Dov N, Korenstein R. Low electric fields induce ligand-independent activation of EGF receptor and ERK via electrochemical elevation of H(+) and ROS concentrations. Biochim Biophys Acta 2013;1833:1396-408. https://doi.org/10.1016/j.bbamcr.2013.02.011
  36. Ma J, Zhang Z, Su Y, Kang L, Geng D, Wang Y, et al. Magnetic stimulation modulates structural synaptic plasticity and regulates BDNF-TrkB signal pathway in cultured hippocampal neurons. Neurochem Int 2013;62:84-91. https://doi.org/10.1016/j.neuint.2012.11.010
  37. Sun W, Yu Y, Chiang H, Fu Y, Lu D. Exposure to power-frequency magnetic fields can induce activation of P38 mitogen-activated protein kinase. Zhonghua Lao Dong Wei Sheng Zhi Ye Bing Za Zhi 2002;20:252-5.
  38. Soda A, Ikehara T, Kinouchi Y, Yoshizaki K. Effect of exposure to an extremely low frequencyelectromagnetic field on the cellular collagen with respect to signaling pathways in osteoblast-like cells. J Med Invest 2008;55:267-78. https://doi.org/10.2152/jmi.55.267
  39. Vincenzi F, Targa M, Corciulo C, Gessi S, Merighi S, Setti S, et al. Pulsed electromagnetic fields increased the anti-inflammatory effect of $A_{2}A$ and $A_{3}$ adenosine receptors in human T/C-28a2 chondrocytes and hFOB 1.19 osteoblasts. PLoS One 2013;8:e65561. https://doi.org/10.1371/journal.pone.0065561
  40. Sakurai T, Terashima S, Miyakoshi J. Enhanced secretion of prostaglandin E2 from osteoblasts by exposure to a strong static magnetic field. Bioelectromagnetics 2008;29:277-83. https://doi.org/10.1002/bem.20392

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