Generic placeholder image

Current Stem Cell Research & Therapy

Editor-in-Chief

ISSN (Print): 1574-888X
ISSN (Online): 2212-3946

Systematic Review Article

Potential of Mesenchymal Stem Cell Sheets on Periodontal Regeneration: A Systematic Review of Pre-Clinical Studies

Author(s): Aldrin Huamán Mendoza, Danilo Balzarini, Tomaz Alves, Emanuel S. Rovai and Marinella Holzhausen*

Volume 18, Issue 7, 2023

Published on: 27 August, 2022

Page: [958 - 978] Pages: 21

DOI: 10.2174/1574888X17666220706092520

Price: $65

Abstract

Background: Cell sheet technique using mesenchymal stem cells is a high-level strategy in periodontal regenerative medicine. Although recent studies have shown the role of MSCSs in increased dental supporting tissues and bone, there is no systematic review focused specifically on assessing periodontal regeneration in orthotopic animal models.

Objective: To evaluate the potential of mesenchymal stem cell sheets (MSCSs) on periodontal regeneration, compared to control, in experimental animal models

Methods: Pre-clinical studies in periodontal defects of animal models were considered eligible. The electronic search included the MEDLINE, Web of Science, EMBASE and LILACS databases. The review was conducted according to the Preferred Reporting Item for Systematic Reviews and Meta-Analyses statement guidelines.

Results: A total of 17 of the 3989 studies obtained from the electronic database search were included. MSCSs included dental follicle (DF) MSCSs, periodontal ligament (PL) MSCSs, dental pulp (DP) MSCSs, bone marrow (BM) MSCSs, alveolar periosteal (AP) MSCSs and gingival (G) MSCSs. Regarding cell sheet inducing protocol, most of the studies used ascorbic acid (52.94%). Others used culture dishes grafted with a temperature-responsive polymer (47.06%). Adverse effects were not identified in the majority of studies. Meta-analysis was not considered because of methodological heterogeneities. PDL-MSCSs were superior for periodontal regeneration enhancement compared to the control, but in an induced inflammatory microenvironment, DF-MSCSs were better. Moreover, DF-MSCSs, DP-MSCSs, and BM-MSCSs showed improved results compared to the control.

Conclusion: MSCSs can improve periodontal regeneration in animal periodontal defect models.

Keywords: Periodontal regeneration, stem cells, cell sheets, regenerative medicine, tissue engineering, systematic review, animals.

Graphical Abstract

[1]
Reynolds MA, Kao RT, Camargo PM, et al. Periodontal regeneration - intrabony defects: A consensus report from the AAP Regeneration Workshop. J Periodontol 2015; 86(2) (Suppl.): S105-7.
[http://dx.doi.org/10.1902/jop.2015.140378] [PMID: 25315019]
[2]
Sallum EA, Ribeiro FV, Ruiz KS, Sallum AW. Experimental and clinical studies on regenerative periodontal therapy. Periodontol 2000 2019; 79(1): 22-55.
[http://dx.doi.org/10.1111/prd.12246] [PMID: 30892759]
[3]
Wei F, Qu C, Song T, et al. Vitamin C treatment promotes mesenchymal stem cell sheet formation and tissue regeneration by elevating telomerase activity. J Cell Physiol 2012; 227(9): 3216-24.
[http://dx.doi.org/10.1002/jcp.24012] [PMID: 22105792]
[4]
Okano T, Yamada N, Sakai H, Sakurai Y. A novel recovery system for cultured cells using plasma-treated polystyrene dishes grafted with poly(N-isopropylacrylamide). J Biomed Mater Res 1993; 27(10): 1243-51.
[http://dx.doi.org/10.1002/jbm.820271005] [PMID: 8245039]
[5]
Ito A, Ino K, Kobayashi T, Honda H. The effect of RGD peptide-conjugated magnetite cationic liposomes on cell growth and cell sheet harvesting. Biomaterials 2005; 26(31): 6185-93.
[http://dx.doi.org/10.1016/j.biomaterials.2005.03.039] [PMID: 15899515]
[6]
Chen M, Xu Y, Zhang T, et al. Mesenchymal stem cell sheets: A new cell-based strategy for bone repair and regeneration. Biotechnol Lett 2019; 41(3): 305-18.
[http://dx.doi.org/10.1007/s10529-019-02649-7] [PMID: 30680496]
[7]
Lu Y, Zhang W, Wang J, et al. Recent advances in cell sheet technology for bone and cartilage regeneration: from preparation to application. Int J Oral Sci 2019; 11(2): 17.
[http://dx.doi.org/10.1038/s41368-019-0050-5] [PMID: 31110170]
[8]
Sanz AR, Carrión FS, Chaparro AP. Mesenchymal stem cells from the oral cavity and their potential value in tissue engineering. Periodontol 2000 2015; 67(1): 251-67.
[http://dx.doi.org/10.1111/prd.12070] [PMID: 25494604]
[9]
Bassir SH, Wisitrasameewong W, Raanan J, et al. Potential for stem cell-based periodontal therapy. J Cell Physiol 2016; 231(1): 50-61.
[http://dx.doi.org/10.1002/jcp.25067] [PMID: 26058394]
[10]
Chen FM, Sun HH, Lu H, Yu Q. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials 2012; 33(27): 6320-44.
[http://dx.doi.org/10.1016/j.biomaterials.2012.05.048] [PMID: 22695066]
[11]
Yang J, Yamato M, Shimizu T, et al. Reconstruction of functional tissues with cell sheet engineering. Biomaterials 2007; 28(34): 5033-43.
[http://dx.doi.org/10.1016/j.biomaterials.2007.07.052] [PMID: 17761277]
[12]
Nishida K, Yamato M, Hayashida Y, et al. Corneal reconstruction with tissue-engineered cell sheets composed of autologous oral mucosal epithelium. N Engl J Med 2004; 351(12): 1187-96.
[http://dx.doi.org/10.1056/NEJMoa040455] [PMID: 15371576]
[13]
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(3-4): 469-78.
[http://dx.doi.org/10.1089/ten.2005.11.469] [PMID: 15869425]
[14]
Iwata T, Yamato M, Tsuchioka H, et al. Periodontal regeneration with multi-layered periodontal ligament-derived cell sheets in a canine model. Biomaterials 2009; 30(14): 2716-23.
[http://dx.doi.org/10.1016/j.biomaterials.2009.01.032] [PMID: 19201461]
[15]
Hu J, Cao Y, Xie Y, 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(1): 130.
[http://dx.doi.org/10.1186/s13287-016-0362-8] [PMID: 27613503]
[16]
Magalhães FD, Sarra G, Carvalho GL, et al. Dental tissue-derived stem cell sheet biotechnology for periodontal tissue regeneration: A systematic review. Arch Oral Biol 2021; 129(May): 105182.
[http://dx.doi.org/10.1016/j.archoralbio.2021.105182] [PMID: 34098416]
[17]
Petticrew M, Shekelle P, Stewart LA, Group P. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation. BMJ 2015; 350: g7647.
[18]
Higgins JPT, Thomas J, Chandler J, Cumpston M, Li T, Page MJ, et al. Cochrane handbook for systematic reviews of interventions. Cochrane Handb Syst Rev Interv 2019; 0: 1-694.
[http://dx.doi.org/10.1002/9781119536604]
[19]
Hooijmans CR, Rovers MM, de Vries RBM, Leenaars M, Ritskes-Hoitinga M, Langendam MW. SYRCLE’s risk of bias tool for animal studies. BMC Med Res Methodol 2014; 14(1): 43.
[http://dx.doi.org/10.1186/1471-2288-14-43] [PMID: 24667063]
[20]
Guo S, Kang J, Ji B, et al. Periodontal-derived mesenchymal cell sheets promote periodontal regeneration in inflammatory microenvironment. Tissue Eng Part A 2017; 23(13-14): 585-96.
[http://dx.doi.org/10.1089/ten.tea.2016.0334] [PMID: 28437177]
[21]
Liang Y, Wen L, Shang F, Wu J, Sui K, Ding Y. Endothelial progenitors enhanced the osteogenic capacities of mesenchymal stem cells in vitro and in a rat alveolar bone defect model. Arch Oral Biol 2016; 68: 123-30.
[http://dx.doi.org/10.1016/j.archoralbio.2016.04.007] [PMID: 27131592]
[22]
Sun J, Dong Z, Zhang Y, et al. Osthole improves function of periodontitis periodontal ligament stem cells via epigenetic modification in cell sheets engineering. Sci Rep 2017; 7(1): 5254.
[http://dx.doi.org/10.1038/s41598-017-05762-7] [PMID: 28701802]
[23]
Takewaki M, Kajiya M, Takeda K, et al. MSC/ECM cellular complexes induce periodontal tissue regeneration. J Dent Res 2017; 96(9): 984-91.
[http://dx.doi.org/10.1177/0022034517708770] [PMID: 28521114]
[24]
Takizawa S, Yamamoto T, Honjo KI, et al. Transplantation of dental pulp-derived cell sheets cultured on human amniotic membrane induced to differentiate into bone. Oral Dis 2019; 25(5): 1352-62.
[http://dx.doi.org/10.1111/odi.13096] [PMID: 30912198]
[25]
Tsumanuma Y, Iwata T, Kinoshita A, et al. Allogeneic transplantation of periodontal ligament-derived multipotent mesenchymal stromal cell sheets in canine critical-size supra-alveolar periodontal defect model Biores Open Access. 2016; 5(1): 22-36.
[26]
Tsumanuma Y, Iwata T, Washio K, et al. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 2011; 32(25): 5819-25.
[http://dx.doi.org/10.1016/j.biomaterials.2011.04.071] [PMID: 21605900]
[27]
Vaquette C, Saifzadeh S, Farag A, Hutmacher DW, Ivanovski S. Periodontal tissue engineering with a multiphasic construct and cell sheets. J Dent Res 2019; 98(6): 673-81.
[http://dx.doi.org/10.1177/0022034519837967] [PMID: 30971166]
[28]
Yang H, Li J, Hu Y, et al. Treated dentin matrix particles combined with dental follicle cell sheet stimulate periodontal regeneration. Dent Mater 2019; 35(9): 1238-53.
[http://dx.doi.org/10.1016/j.dental.2019.05.016] [PMID: 31201017]
[29]
Zhu B, Liu W, Liu Y, et al. Jawbone microenvironment promotes periodontium regeneration by regulating the function of periodontal ligament stem cells. Sci Rep 2017; 7(January): 40088.
[http://dx.doi.org/10.1038/srep40088] [PMID: 28053317]
[30]
Tatsuhiro F, Seiko T, Yusuke T, Reiko TT, Kazuhito S. Dental pulp stem cell-derived, scaffold-free constructs for bone regeneration. Int J Mol Sci 2018; 19(7): E1846.
[http://dx.doi.org/10.3390/ijms19071846] [PMID: 29932167]
[31]
Zhang H, Liu S, Zhu B, Xu Q, Ding Y, Jin Y. Composite cell sheet for periodontal regeneration: Crosstalk between different types of MSCs in cell sheet facilitates complex periodontal-like tissue regeneration. Stem Cell Res Ther 2016; 7(1): 168.
[http://dx.doi.org/10.1186/s13287-016-0417-x] [PMID: 27842561]
[32]
Panduwawala CP, Zhan X, Dissanayaka WL, Samaranayake LP, Jin L, Zhang C. In vivo periodontal tissue regeneration by periodontal ligament stem cells and endothelial cells in three-dimensional cell sheet constructs. J Periodontal Res 2017; 52(3): 408-18.
[http://dx.doi.org/10.1111/jre.12405] [PMID: 27495271]
[33]
Wang ZS, Feng ZH, Wu GF, Bai SZ, Dong Y, Chen FM. The use of platelet-rich fibrin combined with periodontal ligament and jaw bone mesenchymal stem cell sheets for periodontal tissue engineering. Sci Rep 2015; 2016(6): 1-15.
[http://dx.doi.org/10.1038/srep28126] [PMID: 27324079]
[34]
Yu Y, Bi CS, Wu RX, et al. Effects of short-term inflammatory and/or hypoxic pretreatments on periodontal ligament stem cells: In vitro and in vivo studies. Cell Tissue Res 2016; 366(2): 311-28.
[http://dx.doi.org/10.1007/s00441-016-2437-3] [PMID: 27301447]
[35]
Liu J, Wang L, Liu W, Li Q, Jin Z, Jin Y. Dental follicle cells rescue the regenerative capacity of periodontal ligament stem cells in an inflammatory microenvironment. PLoS One 2014; 9(9): e108752.
[http://dx.doi.org/10.1371/journal.pone.0108752] [PMID: 25275580]
[36]
Guo W, He Y, Tang X, et al. Scaffold-free cell pellet transplantations can be applied to periodontal regeneration. Cell Transplant 2014; 23(2): 181-94.
[http://dx.doi.org/10.3727/096368912X662426] [PMID: 23363564]
[37]
Farag A, Hashimi SM, Vaquette C, Bartold PM, Hutmacher DW, Ivanovski S. The effect of decellularized tissue engineered constructs on periodontal regeneration. J Clin Periodontol 2018; 45(5): 586-96.
[http://dx.doi.org/10.1111/jcpe.12886] [PMID: 29500836]
[38]
Flores MG, Yashiro R, Washio K, Yamato M, Okano T, Ishikawa I. Periodontal ligament cell sheet promotes periodontal regeneration in athymic rats. J Clin Periodontol 2008; 35(12): 1066-72.
[http://dx.doi.org/10.1111/j.1600-051X.2008.01326.x] [PMID: 19040584]
[39]
Jiang Y, Liu JM, Huang JP, et al. Regeneration potential of decellularized periodontal ligament cell sheets combined with 15-Deoxy-Δ 12,14-prostaglandin J 2 nanoparticles in a rat periodontal defect. Biomed Mater 2021; 16(4): 045008.
[http://dx.doi.org/10.1088/1748-605X/abee61]
[40]
Akizuki T, Oda S, Komaki M, et al. Application of periodontal ligament cell sheet for periodontal regeneration: A pilot study in beagle dogs. J Periodontal Res 2005; 40(3): 245-51.
[http://dx.doi.org/10.1111/j.1600-0765.2005.00799.x] [PMID: 15853971]
[41]
Dan H, Vaquette C, Fisher AG, et al. The influence of cellular source on periodontal regeneration using calcium phosphate coated polycaprolactone scaffold supported cell sheets. Biomaterials 2014; 35(1): 113-22.
[http://dx.doi.org/10.1016/j.biomaterials.2013.09.074] [PMID: 24120045]
[42]
Ding G, Liu Y, Wang W, et al. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 2010; 28(10): 1829-38.
[http://dx.doi.org/10.1002/stem.512] [PMID: 20979138]
[43]
Raju R, Oshima M, Inoue M, et al. Three-dimensional periodontal tissue regeneration using a bone-ligament complex cell sheet. Sci Rep 2020; 10(1): 1656.
[http://dx.doi.org/10.1038/s41598-020-58222-0] [PMID: 32015383]
[44]
Wikesjö UME, Sorensen RG, Kinoshita A, Jian Li X, Wozney JM. Periodontal repair in dogs: Effect of recombinant human bone morphogenetic protein-12 (rhBMP-12) on regeneration of alveolar bone and periodontal attachment. J Clin Periodontol 2004; 31(8): 662-70.
[http://dx.doi.org/10.1111/j.1600-051X.2004.00541.x] [PMID: 15257745]
[45]
Kondo M, Kameishi S, Grainger DW, Okano T. Novel therapies using cell sheets engineered from allogeneic mesenchymal stem/stromal cells. Emerg Top Life Sci 2020; 4(6): 677-89.
[http://dx.doi.org/10.1042/ETLS20200151] [PMID: 33231260]
[46]
Silva FS, Ramos RN, de Almeida DC, et al. Mesenchymal stem cells derived from human exfoliated deciduous teeth (SHEDs) induce immune modulatory profile in monocyte-derived dendritic cells. PLoS One 2014; 9(5): e98050.
[http://dx.doi.org/10.1371/journal.pone.0098050] [PMID: 24846008]
[47]
Pierdomenico L, Bonsi L, Calvitti M, et al. Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 2005; 80(6): 836-42.
[http://dx.doi.org/10.1097/01.tp.0000173794.72151.88] [PMID: 16210973]
[48]
Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009; 219(3): 667-76.
[http://dx.doi.org/10.1002/jcp.21710] [PMID: 19160415]
[49]
Yang Z, Jin F, Zhang X, et al. Tissue engineering of cementum/periodontal-ligament complex using a novel three-dimensional pellet cultivation system for human periodontal ligament stem cells. Tissue Eng Part C Methods 2009; 15(4): 571-81.
[http://dx.doi.org/10.1089/ten.tec.2008.0561] [PMID: 19534606]
[50]
Wada N, Gronthos S, Bartold PM. Immunomodulatory effects of stem cells. Periodontol 2000 2013; 63(1): 198-216.
[http://dx.doi.org/10.1111/prd.12024] [PMID: 23931061]
[51]
Avinash K, Malaippan S, Dooraiswamy JN. Methods of isolation and characterization of stem cells from different regions of oral cavity using markers: A systematic review. Int J Stem Cells 2017; 10(1): 12-20.
[http://dx.doi.org/10.15283/ijsc17010] [PMID: 28531913]
[52]
Tassi SA, Sergio NZ, Misawa MYO, Villar CC. Efficacy of stem cells on periodontal regeneration: Systematic review of pre-clinical studies. J Periodontal Res 2017; 52(5): 793-812.
[http://dx.doi.org/10.1111/jre.12455] [PMID: 28394043]
[53]
Amghar-Maach S, Gay-Escoda C, Sánchez-Garcés MÁ. Regeneration of periodontal bone defects with dental pulp stem cells grafting: Systematic Review. J Clin Exp Dent 2019; 11(4): e373-81.
[http://dx.doi.org/10.4317/jced.55574] [PMID: 31110618]
[54]
Marchesan J, Girnary MS, Jing L, et al. An experimental murine model to study periodontitis. Nat Protoc 2018; 13(10): 2247-67.
[http://dx.doi.org/10.1038/s41596-018-0035-4] [PMID: 30218100]
[55]
Li D, Feng Y, Tang H, et al. A simplified and effective method for generation of experimental murine periodontitis model. Front Bioeng Biotechnol 2020; 8(May): 444.
[http://dx.doi.org/10.3389/fbioe.2020.00444] [PMID: 32523937]
[56]
Pellegrini G, Seol YJ, Gruber R, Giannobile WV. Pre-clinical models for oral and periodontal reconstructive therapies. J Dent Res 2009; 88(12): 1065-76.
[http://dx.doi.org/10.1177/0022034509349748] [PMID: 19887682]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy