Journal of Periodontal and Implant Science

Korean Academy of Periodontology (대한치주과학회)
권호 표지
DOI QR코드

DOI QR Code

Evaluation of the periodontal regenerative properties of patterned human periodontal ligament stem cell sheets

  • Kim, Joong-Hyun (Department of Periodontology, Chonbuk National University School of Dentistry and Institute of Oral Bioscience) ;
  • Ko, Seok-Yeong (Department of Periodontology, Chonbuk National University School of Dentistry and Institute of Oral Bioscience) ;
  • Lee, Justin Ho (Department of Bioengineering, University of Washington) ;
  • Kim, Deok-Ho (Department of Bioengineering, University of Washington) ;
  • Yun, Jeong-Ho (Department of Periodontology, Chonbuk National University School of Dentistry and Institute of Oral Bioscience)
  • Received : 2017.11.15
  • Accepted : 2017.12.23
  • Published : 2017.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Purpose: The aim of this study was to determine the effects of patterned human periodontal ligament stem cell (hPDLSC) sheets fabricated using a thermoresponsive substratum. Methods: In this study, we fabricated patterned hPDLSC sheets using nanotopographical cues to modulate the alignment of the cell sheet. Results: The hPDLSCs showed rapid monolayer formation on various surface pattern widths. Compared to cell sheets grown on flat surfaces, there were no significant differences in cell attachment and growth on the nanopatterned substratum. However, the patterned hPDLSC sheets showed higher periodontal ligamentogenesis-related gene expression in early stages than the unpatterned cell sheets. Conclusions: This experiment confirmed that patterned cell sheets provide flexibility in designing hPDLSC sheets, and that these stem cell sheets may be candidates for application in periodontal regenerative therapy.

Keywords

References

  1. Armitage GC. Development of a classification system for periodontal diseases and conditions. Ann Periodontol 1999;4:1-6. https://doi.org/10.1902/annals.1999.4.1.1
  2. Apicella A, Heunemann P, Dejace L, Marascio M, Plummer CJ, Fischer P. Scaffold requirements for periodontal regeneration with enamel matrix derivative proteins. Colloids Surf B Biointerfaces 2017;156:221-6. https://doi.org/10.1016/j.colsurfb.2017.05.013
  3. Reynolds MA, Kao RT, Camargo PM, Caton JG, Clem DS, Fiorellini JP, et al. Periodontal regeneration - intrabony defects: a consensus report from the AAP Regeneration Workshop. J Periodontol 2015;86:S105-7. https://doi.org/10.1902/jop.2015.140378
  4. Greenwell HCommittee on Research, Science and Therapy. American Academy of Periodontology. Position paper: guidelines for periodontal therapy. J Periodontol 2001;72:1624-8. https://doi.org/10.1902/jop.2001.72.11.1624
  5. Hasegawa M, Yamato M, Kikuchi A, Okano T, Ishikawa I. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng 2005;11:469-78. https://doi.org/10.1089/ten.2005.11.469
  6. Bright R, Hynes K, Gronthos S, Bartold PM. Periodontal ligament-derived cells for periodontal regeneration in animal models: a systematic review. J Periodontal Res 2015;50:160-72. https://doi.org/10.1111/jre.12205
  7. Gay IC, Chen S, MacDougall M. Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 2007;10:149-60. https://doi.org/10.1111/j.1601-6343.2007.00399.x
  8. Ishikawa I, Iwata T, Washio K, Okano T, Nagasawa T, Iwasaki K, et al. Cell sheet engineering and other novel cell-based approaches to periodontal regeneration. Periodontol 2000 2009;51:220-38. https://doi.org/10.1111/j.1600-0757.2009.00312.x
  9. Xu Q, Li B, Yuan L, Dong Z, Zhang H, Wang H, et al. Combination of platelet-rich plasma within periodontal ligament stem cell sheets enhances cell differentiation and matrix production. J Tissue Eng Regen Med 2017;11:627-36. https://doi.org/10.1002/term.1953
  10. Carter SD, Costa PF, Vaquette C, Ivanovski S, Hutmacher DW, Malda J. Additive biomanufacturing: an advanced approach for periodontal tissue regeneration. Ann Biomed Eng 2017;45:12-22. https://doi.org/10.1007/s10439-016-1687-2
  11. Okano T, Bae YH, Jacobs H, Kim SW. Thermally on-off switching polymers for drug permeation and release. J Control Release 1990;11:255-65. https://doi.org/10.1016/0168-3659(90)90138-J
  12. Li M, Feng C, Gu X, He Q, Wei F. Effect of cryopreservation on proliferation and differentiation of periodontal ligament stem cell sheets. Stem Cell Res Ther 2017;8:77. https://doi.org/10.1186/s13287-017-0530-5
  13. Guo S, Kang J, Ji B, Guo W, Ding Y, Wu Y, et al. Periodontal-derived mesenchymal cell sheets promote periodontal regeneration in inflammatory microenvironment. Tissue Eng Part A 2017;23:585-96. https://doi.org/10.1089/ten.tea.2016.0334
  14. Wang Z, Feng Z, Wu G, Bai S, Dong Y, Zhao Y. In vitro studies on human periodontal ligament stem cell sheets enhanced by enamel matrix derivative. Colloids Surf B Biointerfaces 2016;141:102-11. https://doi.org/10.1016/j.colsurfb.2016.01.036
  15. Dalby MJ, Gadegaard N, Tare R, Andar A, Riehle MO, Herzyk P, et al. The control of human mesenchymal cell differentiation using nanoscale symmetry and disorder. Nat Mater 2007;6:997-1003. https://doi.org/10.1038/nmat2013
  16. Kim DH, Provenzano PP, Smith CL, Levchenko A. Matrix nanotopography as a regulator of cell function. J Cell Biol 2012;197:351-60. https://doi.org/10.1083/jcb.201108062
  17. McMurray RJ, Gadegaard N, Tsimbouri PM, Burgess KV, McNamara LE, Tare R, et al. Nanoscale surfaces for the long-term maintenance of mesenchymal stem cell phenotype and multipotency. Nat Mater 2011;10:637-44. https://doi.org/10.1038/nmat3058
  18. Gao H, Li B, Zhao L, Jin Y. Influence of nanotopography on periodontal ligament stem cell functions and cell sheet based periodontal regeneration. Int J Nanomedicine 2015;10:4009-27.
  19. Jiao A, Trosper NE, Yang HS, Kim J, Tsui JH, Frankel SD, et al. Thermoresponsive nanofabricated substratum for the engineering of three-dimensional tissues with layer-by-layer architectural control. ACS Nano 2014;8:4430-9. https://doi.org/10.1021/nn4063962
  20. Kim K, Yi T, Yun JH. Maintained stemness of human periodontal ligament stem cells isolated after prolonged storage of extracted teeth. J Periodontol 2016;87:e148-58. https://doi.org/10.1902/jop.2016.150693
  21. Farag A, Vaquette C, Theodoropoulos C, Hamlet SM, Hutmacher DW, Ivanovski S. Decellularized periodontal ligament cell sheets with recellularization potential. J Dent Res 2014;93:1313-9. https://doi.org/10.1177/0022034514547762
  22. Hu J, Cao Y, Xie Y, Wang H, Fan Z, Wang J, et al. Periodontal regeneration in swine after cell injection and cell sheet transplantation of human dental pulp stem cells following good manufacturing practice. Stem Cell Res Ther 2016;7:130. https://doi.org/10.1186/s13287-016-0362-8
  23. Dan H, Vaquette C, Fisher AG, Hamlet SM, Xiao Y, Hutmacher DW, et al. The influence of cellular source on periodontal regeneration using calcium phosphate coated polycaprolactone scaffold supported cell sheets. Biomaterials 2014;35:113-22. https://doi.org/10.1016/j.biomaterials.2013.09.074
  24. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004;364:149-55. https://doi.org/10.1016/S0140-6736(04)16627-0
  25. Lemaitre M, Monsarrat P, Blasco-Baque V, Loubieres P, Burcelin R, Casteilla L, et al. Periodontal tissue regeneration using syngeneic adipose-derived stromal cells in a mouse model. Stem Cells Transl Med 2017;6:656-65. https://doi.org/10.5966/sctm.2016-0028
  26. Wang ZS, Feng ZH, Wu GF, Bai SZ, Dong Y, Chen FM, et al. The use of platelet-rich fibrin combined with periodontal ligament and jaw bone mesenchymal stem cell sheets for periodontal tissue engineering. Sci Rep 2016;6:28126. https://doi.org/10.1038/srep28126
  27. Feng R, Lengner C. Application of stem cell technology in dental regenerative medicine. Adv Wound Care (New Rochelle) 2013;2:296-305. https://doi.org/10.1089/wound.2012.0375
  28. Du J, Shan Z, Ma P, Wang S, Fan Z. Allogeneic bone marrow mesenchymal stem cell transplantation for periodontal regeneration. J Dent Res 2014;93:183-8. https://doi.org/10.1177/0022034513513026
  29. Owaki T, Shimizu T, Yamato M, Okano T. Cell sheet engineering for regenerative medicine: current challenges and strategies. Biotechnol J 2014;9:904-14. https://doi.org/10.1002/biot.201300432
  30. Kim JH, Kang MS, Eltohamy M, Kim TH, Kim HW. Dynamic mechanical and nanofibrous topological combinatory cues designed for periodontal ligament engineering. PLoS One 2016;11:e0149967. https://doi.org/10.1371/journal.pone.0149967
  31. Yin Z, Chen X, Chen JL, Shen WL, Hieu Nguyen TM, Gao L, et al. The regulation of tendon stem cell differentiation by the alignment of nanofibers. Biomaterials 2010;31:2163-75. https://doi.org/10.1016/j.biomaterials.2009.11.083
  32. Jiang W, Li L, Zhang D, Huang S, Jing Z, Wu Y, et al. Incorporation of aligned PCL-PEG nanofibers into porous chitosan scaffolds improved the orientation of collagen fibers in regenerated periodontium. Acta Biomater 2015;25:240-52. https://doi.org/10.1016/j.actbio.2015.07.023
  33. Gauvin R, Parenteau-Bareil R, Larouche D, Marcoux H, Bisson F, Bonnet A, et al. Dynamic mechanical stimulations induce anisotropy and improve the tensile properties of engineered tissues produced without exogenous scaffolding. Acta Biomater 2011;7:3294-301. https://doi.org/10.1016/j.actbio.2011.05.034
  34. Yu N, Prodanov L, te Riet J, Yang F, Walboomers XF, Jansen JA. Regulation of periodontal ligament cell behavior by cyclic mechanical loading and substrate nanotexture. J Periodontol 2013;84:1504-13. https://doi.org/10.1902/jop.2012.120513
  35. San Miguel SM, Fatahi MR, Li H, Igwe JC, Aguila HL, Kalajzic I. Defining a visual marker of osteoprogenitor cells within the periodontium. J Periodontal Res 2010;45:60-70. https://doi.org/10.1111/j.1600-0765.2009.01201.x
  36. Kalajzic Z, Li H, Wang LP, Jiang X, Lamothe K, Adams DJ, et al. Use of an alpha-smooth muscle actin GFP reporter to identify an osteoprogenitor population. Bone 2008;43:501-10. https://doi.org/10.1016/j.bone.2008.04.023
  37. Jin H, Choung HW, Lim KT, Jin B, Jin C, Chung JH, et al. Recombinant human plasminogen activator inhibitor-1 promotes cementogenic differentiation of human periodontal ligament stem cells. Tissue Eng Part A 2015;21:2817-28. https://doi.org/10.1089/ten.tea.2014.0399
  38. Zhu B, Liu W, Liu Y, Zhao X, Zhang H, Luo Z, et al. Jawbone microenvironment promotes periodontium regeneration by regulating the function of periodontal ligament stem cells. Sci Rep 2017;7:40088. https://doi.org/10.1038/srep40088
  39. Kadkhoda Z, Safarpour A, Azmoodeh F, Adibi S, Khoshzaban A, Bahrami N. Histopathological comparison between bone marrow- and periodontium-derived stem cells for bone regeneration in rabbit calvaria. Int J Organ Transplant Med 2016;7:9-18.
  40. Scott A, Danielson P, Abraham T, Fong G, Sampaio AV, Underhill TM. Mechanical force modulates scleraxis expression in bioartificial tendons. J Musculoskelet Neuronal Interact 2011;11:124-32.

Cited by

  1. A Study of the Effects of Doxorubicin-Containing Liposomes on Osteogenesis of 3D Stem Cell Spheroids Derived from Gingiva vol.12, pp.17, 2017, https://doi.org/10.3390/ma12172693
  2. Biomaterial-Based Approaches for Regeneration of Periodontal Ligament and Cementum Using 3D Platforms vol.20, pp.18, 2019, https://doi.org/10.3390/ijms20184364
  3. Decellularized matrix could affect the proliferation and differentiation of periodontal ligament stem cells in vitro vol.56, pp.5, 2017, https://doi.org/10.1111/jre.12889
  4. Characterization and evaluation of ascorbic acid-induced cell sheet formation in human periodontal ligament stem cells: An in vitro study vol.63, pp.4, 2021, https://doi.org/10.1016/j.job.2021.10.002