Skip to main content

Advertisement

Log in

The Osteogenic Role of Biomaterials Combined with Human-Derived Dental Stem Cells in Bone Tissue Regeneration

  • Review Article
  • Published:
Tissue Engineering and Regenerative Medicine Aims and scope

Abstract

The use of stem cells in regenerative medicine had great potential for clinical applications. However, cell delivery strategies have critical importance in stimulating the differentiation of stem cells and enhancing their potential to regenerate damaged tissues. Different strategies have been used to investigate the osteogenic potential of dental stem cells in conjunction with biomaterials through in vitro and in vivo studies. Osteogenesis has a broad implication in regenerative medicine, particularly for maxillofacial defects. This review summarizes some of the most recent developments in the field of tissue engineering using dental stem cells.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Salgado AJ, Oliveira JM, Martins A, Teixeira FG, Silva NA, Neves NM, et al. Tissue engineering and regenerative medicine: past, present, and future. Int Rev Neurobiol. 2013;108:1–33.

    Article  CAS  PubMed  Google Scholar 

  2. Salgado AJ, Oliveira JT, Pedro AJ, Reis RL. Adult stem cells in bone and cartilage tissue engineering. Curr Stem Cell Res Ther. 2006;1:345–64.

    Article  CAS  PubMed  Google Scholar 

  3. Esposito M, Grusovin MG, Felice P, Karatzopoulos G, Worthington HV, Coulthard P. Interventions for replacing missing teeth: horizontal and vertical bone augmentation techniques for dental implant treatment. Cochrane Database Syst Rev. 2009;2009:CD003607.

  4. Sikavitsas VI, Temenoff JS, Mikos AG. Biomaterials and bone mechanotransduction. Biomaterials. 2001;22:2581–93.

    Article  CAS  PubMed  Google Scholar 

  5. Knothe Tate ML, Adamson JR, Tami AE, Bauer TW. The osteocyte. Int J Biochem Cell Biol. 2004;36:1–8.

  6. Vaananen HK, Zhao H, Mulari M, Halleen JM. The cell biology of osteoclast function. J Cell Sci. 2000;113:377–81.

    Article  CAS  PubMed  Google Scholar 

  7. Cancedda R, Dozin B, Giannoni P, Quarto R. Tissue engineering and cell therapy of cartilage and bone. Matrix Biol. 2003;22:81–91.

    Article  CAS  PubMed  Google Scholar 

  8. Reynolds DL, Chambers LW, Badley EM, Bennett KJ, Goldsmith CH, Jamieson E, et al. Physical disability among Canadians reporting musculoskeletal diseases. J Rheumatol. 1992;19:1020–30.

    CAS  PubMed  Google Scholar 

  9. San Román J, Reis R. Biodegradable systems in medical functions: design, processing, testing and applications. CRC, Boca Ratón. 2004.

  10. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet. 2005;366:1809–20.

    Article  PubMed  Google Scholar 

  11. Hynes K, Menicanin D, Gronthos S, Bartold PM. Clinical utility of stem cells for periodontal regeneration. Periodontol 2000. 2012;59:203–27.

    Article  PubMed  Google Scholar 

  12. Chen FM, Sun HH, Lu H, Yu Q. Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials. 2012;33:6320–44.

    Article  CAS  PubMed  Google Scholar 

  13. Young CS, Abukawa H, Asrican R, Ravens M, Troulis MJ, Kaban LB, et al. Tissue-engineered hybrid tooth and bone. Tissue Eng. 2005;11:1599–610.

    Article  CAS  PubMed  Google Scholar 

  14. Chen FM, Zhang J, Zhang M, An Y, Chen F, Wu ZF. A review on endogenous regenerative technology in periodontal regenerative medicine. Biomaterials. 2010;31:7892–927.

    Article  CAS  PubMed  Google Scholar 

  15. Friedenstein AJ, Chailakhyan RK, Latsinik NV, Panasyuk AF, Keiliss-Borok IV. Stromal cells responsible for transferring the microenvironment of the hemopoietic tissues: cloning in vitro and retransplantation in vivo. Transplantation. 1974;17:331–40.

    Article  CAS  PubMed  Google Scholar 

  16. Kern S, Eichler H, Stoeve J,  Klüter H, Bieback K. Comparative analysis of mesenchymal stem cells from bone marrow, umbilical cord blood, or adipose tissue. Stem cells. 2006;24:1294–301.

    Article  CAS  PubMed  Google Scholar 

  17. Huang GT, Gronthos S, Shi S. Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res. 2009;88:792–806.

  18. Bluteau G, Luder H, De Bari C, Mitsiadis T. Stem cells for tooth engineering. Eur Cell Mater. 2008;16:1–9.

    Article  CAS  PubMed  Google Scholar 

  19. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S. Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A. 2000;97:13625–30.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, et al. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A. 2003;100:5807–12.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Yasui T, Mabuchi Y, Toriumi H, Ebine T, Niibe K, Houlihan DD, et al. Purified human dental pulp stem cells promote osteogenic regeneration. J Dent Res. 2016;95:206–14.

    Article  CAS  PubMed  Google Scholar 

  22. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, et al. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod. 2008;34:166–71.

    Article  PubMed  PubMed Central  Google Scholar 

  23. Morsczeck C, Götz W, Schierholz J, Zeilhofer F, Kühn U, Möhl C, et al. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol. 2005;24:155–65.

    Article  CAS  PubMed  Google Scholar 

  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. The Lancet. 2004;364:149–55.

    Article  CAS  Google Scholar 

  25. Gay IC, Chen S, MacDougall M. Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res. 2007;10:149–60.

    Article  CAS  PubMed  Google Scholar 

  26. Grimm WD, Dannan A, Becher S, Gassmann G, Arnold W, Varga G, et al. The ability of human periodontium-derived stem cells to regenerate periodontal tissues: a preliminary in vivo investigation. Int J Periodontics Restorative Dent. 2011;31:e94–101.

    Google Scholar 

  27. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol. 2009;219:667–76.

    Article  CAS  PubMed  Google Scholar 

  28. Lin NH, Gronthos S, Mark Bartold P. Stem cells and future periodontal regeneration. Periodontol 2000. 2009;51:239–51.

    Article  PubMed  Google Scholar 

  29. Bartold P, Xiao Y, Lyngstaadas S, Paine M, Snead M. Principles and applications of cell delivery systems for periodontal regeneration. Periodontol 2000. 2006;41:123–35.

    Article  PubMed  Google Scholar 

  30. Demirbag B, Huri PY, Kose GT, Buyuksungur A, Hasirci V. Advanced cell therapies with and without scaffolds. Biotechnol J. 2011;6:1437–53.

    Article  CAS  PubMed  Google Scholar 

  31. Kelm JM, Fussenegger M. Scaffold-free cell delivery for use in regenerative medicine. Adv Drug Deliv Rev. 2010;62:753–64.

    Article  CAS  PubMed  Google Scholar 

  32. Izumi Y, Aoki A, Yamada Y, Kobayashi H, Iwata T, Akizuki T, et al. Current and future periodontal tissue engineering. Periodontol 2000. 2011;56:166–87.

    Article  PubMed  Google Scholar 

  33. Kean TJ, Lin P, Caplan AI, Dennis JE. MSCs: Delivery Routes and Engraftment, Cell-Targeting Strategies, and Immune Modulation. Stem Cells Int. 2013;2013:732742.

  34. Lukomska B, Stanaszek L, Zuba-Surma E, Legosz P, Sarzynska S, Drela K. Challenges and controversies in human mesenchymal stem cell therapy. Stem Cells Int. 2019;2019:9628536.

  35. Pouraghaei Sevari S, Ansari S, Chen C, Moshaverinia A. Harnessing dental stem cell immunoregulation using cell-laden biomaterials. J Dent Res. 2021;100:568–75.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Simon CG Jr, Khatri CA, Wight SA, Wang FW. Preliminary report on the biocompatibility of a moldable, resorbable, composite bone graft consisting of calcium phosphate cement and poly (lactide-co-glycolide) microspheres. J Orthop Res. 2002;20:473–82.

    Article  CAS  PubMed  Google Scholar 

  37. Tsai HC, Li YC, Young TH, Chen MH. Novel microinjector for carrying bone substitutes for bone regeneration in periodontal diseases. J Formos Med Assoc. 2016;115:45–50.

    Article  CAS  PubMed  Google Scholar 

  38. Takagi S, Chow LC, Hirayama S, Eichmiller FC. Properties of elastomeric calcium phosphate cement–chitosan composites. Dent Mater. 2003;19:797–804.

    Article  CAS  PubMed  Google Scholar 

  39. Villalona GA, Udelsman B, Duncan DR, McGillicuddy E, Sawh-Martinez RF, Hibino N, et al. Cell-seeding techniques in vascular tissue engineering. Tissue Eng Part B Rev. 2010;16:341–50.

    Article  PubMed  PubMed Central  Google Scholar 

  40. Sevari SP, Ansari S, Moshaverinia A. A narrative overview of utilizing biomaterials to recapitulate the salient regenerative features of dental-derived mesenchymal stem cells. Int J Oral Sci. 2021;13:22.

    Article  Google Scholar 

  41. Granz CL, Gorji A. Dental stem cells: The role of biomaterials and scaffolds in developing novel therapeutic strategies. World J Stem Cells. 2020;12:897.

    Article  PubMed  PubMed Central  Google Scholar 

  42. Chimerad M, Barazesh A, Zandi M, Zarkesh I, Moghaddam A, Borjian P, et al. Tissue engineered scaffold fabrication methods for medical applications. Int J Polym Mater. 2022. https://doi.org/10.1080/00914037.2022.2101112.

  43. Akampumuza O, Gao H, Zhang H, Wu D, Qin XH. Raising nanofiber output: the progress, mechanisms, challenges, and reasons for the pursuit. Macromol Mater Eng. 2018;303:1700269.

    Article  Google Scholar 

  44. Uyar T, Kny E. Electrospun materials for tissue engineering and biomedical applications: research, design and commercialization: Woodhead Publishing, 2017.

  45. Bou Chakra E, Hannes B, Dilosquer G, Mansfield CD, Cabrera M. A new instrument for automated microcontact printing with stamp load adjustment. Rev Sci Instrum. 2008;79:064102.

    Article  PubMed  Google Scholar 

  46. Théry M. Micropatterning as a tool to decipher cell morphogenesis and functions. J Cell Sci. 2010;123:4201–13.

    Article  PubMed  Google Scholar 

  47. D’Arcangelo E, McGuigan AP. Micropatterning strategies to engineer controlled cell and tissue architecture in vitro. Biotechniques. 2015;58:13–23.

    Article  CAS  PubMed  Google Scholar 

  48. Skardal A, Atala A. Biomaterials for integration with 3-D bioprinting. Ann Biomed Eng. 2015;43:730–46.

    Article  PubMed  Google Scholar 

  49. Murphy WL, McDevitt TC, Engler AJ. Materials as stem cell regulators. Nat Mater. 2014;13:547–57.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Iaquinta MR, Mazzoni E, Bononi I, Rotondo JC, Mazziotta C, Montesi M, et al. Adult stem cells for bone regeneration and repair. Front Cell Dev Biol. 2019;7:268.

    Article  PubMed  PubMed Central  Google Scholar 

  51. Ma Y, Ji Y, Huang G, Ling K, Zhang X, Xu F. Bioprinting 3D cell-laden hydrogel microarray for screening human periodontal ligament stem cell response to extracellular matrix. Biofabrication. 2015;7:044105.

    Article  PubMed  Google Scholar 

  52. Sorushanova A, Delgado LM, Wu Z, Shologu N, Kshirsagar A, Raghunath R, et al. The collagen suprafamily: from biosynthesis to advanced biomaterial development. Adv Mater. 2019;31:e1801651.

    Article  Google Scholar 

  53. Dong C, Lv Y. Application of collagen scaffold in tissue engineering: recent advances and new perspectives. Polymers (Basel). 2016;8:42.

    Article  PubMed  PubMed Central  Google Scholar 

  54. Ercal P, Pekozer GG. A current overview of scaffold-based bone regeneration strategies with dental stem cells. Cell BiolTransl Med. 2020;9:61–85.

    Google Scholar 

  55. Rahmati M, Pennisi CP, Budd E, Mobasheri A, Mozafari M. Biomaterials for regenerative medicine: historical perspectives and current trends. In: Turksen K, editor. Cell Biology and Translational Medicine, Volume 4. Advances in Experimental Medicine and Biology. Springer, Cham. 2018;1119:1–19.

  56. Reddy MSB, Ponnamma D, Choudhary R, Sadasivuni KK. A comparative review of natural and synthetic biopolymer composite scaffolds. Polymers (Basel). 2021;13:1105.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Denry I, Holloway JA. Ceramics for dental applications: a review. Materials. 2010;3:351–68.

    Article  CAS  PubMed Central  Google Scholar 

  58. Ma Y, Lin M, Huang G, Li Y, Wang S, Bai G, Lu TJ, Xu F. 3D spatiotemporal mechanical microenvironment: a hydrogel-based platform for guiding stem cell fate. Adv Mater. 2018;30:1705911.

    Article  Google Scholar 

  59. Lin H, Yin C, Mo A, Hong G. Applications of hydrogel with special physical properties in bone and cartilage regeneration. Materials. 2021;14:235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Bai X, Gao M, Syed S, Zhuang J, Xu X, Zhang XQ. Bioactive hydrogels for bone regeneration. Bioact Mater. 2018;3:401–17.

    Article  PubMed  PubMed Central  Google Scholar 

  61. Ma Y, Han T, Yang Q, Wang J, Feng B, Jia Y, et al. Viscoelastic cell microenvironment: hydrogel-based strategy for recapitulating dynamic ECM mechanics. Adv Func Mater. 2021;31:2100848.

    Article  CAS  Google Scholar 

  62. Zhu Y, Goh C, Shrestha A. Biomaterial properties modulating bone regeneration. Macromol Biosci. 2021;21:e2000365.

    Article  CAS  Google Scholar 

  63. Aamodt JM, Grainger DW. Extracellular matrix-based biomaterial scaffolds and the host response. Biomaterials. 2016;86:68–82.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Lee YC, Chan YH, Hsieh SC, Lew WZ, Feng SW. Comparing the osteogenic potentials and bone regeneration capacities of bone marrow and dental pulp mesenchymal stem cells in a rabbit calvarial bone defect model. Int J Mol Sci. 2019;20:5015.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Yamada Y, Ito K, Nakamura S, Ueda M, Nagasaka T. Promising cell-based therapy for bone regeneration using stem cells from deciduous teeth, dental pulp, and bone marrow. Cell Transpl. 2011;20:1003–13.

    Article  Google Scholar 

  66. Papaccio G, Graziano A, d’Aquino R, Graziano MF, Pirozzi G, Menditti D, et al. Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair. J Cell Physiol. 2006;208:319–25.

    Article  CAS  PubMed  Google Scholar 

  67. Laino G, Graziano A, d’Aquino R, Pirozzi G, Lanza V, Valiante S, et al. An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol. 2006;206:693–701.

    Article  CAS  PubMed  Google Scholar 

  68. Paino F, La Noce M, Giuliani A, De Rosa A, Mazzoni S, Laino L, et al. Human DPSCs fabricate vascularized woven bone tissue: a new tool in bone tissue engineering. Clin Sci (Lond). 2017;131:699–713.

    Article  CAS  Google Scholar 

  69. Petridis X, Diamanti E, Trigas GC, Kalyvas D, Kitraki E. Bone regeneration in critical-size calvarial defects using human dental pulp cells in an extracellular matrix-based scaffold. J Craniomaxillofac Surg. 2015;43:483–90.

    Article  Google Scholar 

  70. Gutiérrez-Quintero JG, Durán Riveros JY, Martínez Valbuena CA, Pedraza Alonso S, Munévar JC, Viafara-García SM. Critical-sized mandibular defect reconstruction using human dental pulp stem cells in a xenograft model-clinical, radiological, and histological evaluation. Oral Maxillofac Surg. 2020;24:485–93.

    Article  PubMed  Google Scholar 

  71. Zhang W, Saxena S, Fakhrzadeh A, Rudolph S, Young S, Kohn J, et al. Use of human dental pulp and endothelial cell seeded tyrosine-derived polycarbonate scaffolds for robust in vivo alveolar jaw bone regeneration. Front Bioeng Biotechnol. 2020;8:796.

    Article  PubMed  PubMed Central  Google Scholar 

  72. Graziano A, d’Aquino R, Cusella-De Angelis MG, Laino G, Piattelli A, et al. Concave pitcontaining scaffold surfaces improve stem cell-derived osteoblast performance and lead to significant bone tissue formation. PLoS One. 2007;2:e496.

    Article  PubMed  PubMed Central  Google Scholar 

  73. Chan B, Wong R, Rabie B. In vivo production of mineralised tissue pieces for clinical use: a qualitative pilot study using human dental pulp cell. Int J Oral Maxillofac Surg. 2011;40:612–20.

    Article  CAS  PubMed  Google Scholar 

  74. Zhang W, Walboomers XF, van Osch GJ, van den Dolder J, Jansen JA. Hard tissue formation in a porous HA/TCP ceramic scaffold loaded with stromal cells derived from dental pulp and bone marrow. Tissue Eng Part A. 2008;14:285–94.

    Article  PubMed  Google Scholar 

  75. Annibali S, Cicconetti A, Cristalli MP, Giordano G, Trisi P, Pilloni A, et al. A comparative morphometric analysis of biodegradable scaffolds as carriers for dental pulp and periosteal stem cells in a model of bone regeneration. J Craniofac Surg. 2013;24:866–71.

    Article  PubMed  Google Scholar 

  76. El-Gendy R, Yang XB, Newby PJ, Boccaccini AR, Kirkham J. Osteogenic differentiation of human dental pulp stromal cells on 45S5 Bioglass® based scaffolds in vitro and in vivo. Tissue Eng Part A. 2013;19:707–15.

    Article  CAS  PubMed  Google Scholar 

  77. Bakopoulou A, Georgopoulou A, Grivas I, Bekiari C, Prymak O, Loza J, et al. Dental pulp stem cells in chitosan/gelatin scaffolds for enhanced orofacial bone regeneration. Dent Mater. 2019;35:310–27.

    Article  CAS  PubMed  Google Scholar 

  78. Vagropoulou G, Trentsiou M, Georgopoulou A, Papachristou E, Prymak O, Kritis A, et al. Hybrid chitosan/gelatin/nanohydroxyapatite scaffolds promote odontogenic differentiation of dental pulp stem cells and in vitro biomineralization. Dent Mater. 2021;37:e23–36.

    Article  CAS  PubMed  Google Scholar 

  79. 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;19:1846.

    Article  PubMed  PubMed Central  Google Scholar 

  80. Itoh Y, Sasaki J, Hashimoto M, Katata C, Hayashi M, Imazato S. Pulp regeneration by 3-dimensional dental pulp stem cell constructs. J Dent Res. 2018;97:1137–43.

    Article  CAS  PubMed  Google Scholar 

  81. Djagny KB, Wang Z, Xu S. Gelatin: a valuable protein for food and pharmaceutical industries. Crit Rev Food Sci Nutr. 2001;41:481–92.

    Article  CAS  PubMed  Google Scholar 

  82. Elzoghby AO. Gelatin-based nanoparticles as drug and gene delivery systems: reviewing three decades of research. J Control Release. 2013;172:1075–91.

    Article  CAS  PubMed  Google Scholar 

  83. Gu Y, Bai Y, Zhang D. Osteogenic stimulation of human dental pulp stem cells with a novel gelatin-hydroxyapatite-tricalcium phosphate scaffold. J Biomed Mater Res A. 2018;106:1851–61.

    Article  CAS  Google Scholar 

  84. Khayat A, Monteiro N, Smith E, Pagni S, Zhang W, Khademhosseini A, et al. GelMA-encapsulated hDPSCs and HUVECs for dental pulp regeneration. J Dent Res. 2017;96:192–9.

    Article  CAS  PubMed  Google Scholar 

  85. Goodarzi H, Hashemi-Najafabadi S, Baheiraei N, Bagheri F. Preparation and characterization of nanocomposite scaffolds (collagen/b-TCP/SrO) for bone tissue engineering. Tissue Eng Regen Med. 2019;16:237–51.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Akkouch A, Zhang Z, Rouabhia M. Engineering bone tissue using human dental pulp stem cells and an osteogenic collagen-hydroxyapatite-poly (l-lactide-co-e-caprolactone) scaffold. J Biomater Appl. 2014;28:922–36.

    Article  PubMed  Google Scholar 

  87. Ferroni L, Gardin C, Sivolella S, Brunello G, Berengo M, Piattelli A, et al. A hyaluronan-based scaffold for the in vitro construction of dental pulp-like tissue. Int J Mol Sci. 2015;16:4666–81.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  88. Schmidt J, Pilbauerova N, Soukup T, Suchankova-Kleplova T, Suchanek J. Low molecular weight hyaluronic acid effect on dental pulp stem cells in vitro. Biomolecules. 2020;11:22.

    Article  PubMed  PubMed Central  Google Scholar 

  89. Xia K, Chen Z, Chen J, Xu H, Xu Y, Yang T, et al. RGD- and VEGF-mimetic peptide epitope-functionalized self-assembling peptide hydrogels promote dentin-pulp complex regeneration. Int J Nanomedicine. 2020;15:6631–47.

    Article  CAS  Google Scholar 

  90. Zhang W, Walboomers XF, Shi S, Fan M, Jansen JA. Multi-lineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng. 2006;12:2813–23.

    Article  CAS  PubMed  Google Scholar 

  91. Hagar MN, Yazid F, Luchman NA, Ariffin SHZ, Wahab RMA. Comparative evaluation of osteogenic differentiation potential of stem cells derived from dental pulp and exfoliated deciduous teeth cultured over granular hydroxyapatite based scaffold. BMC Oral Health. 2021;21:263.

    Article  Google Scholar 

  92. Yamada Y, Nakamura S, Ito K, Sugito T, Yoshimi R, Nagasaka T, et al. A feasibility of useful cell-based therapy by bone regeneration with deciduous tooth stem cells, dental pulp stem cells, or bone-marrow-derived mesenchymal stem cells for clinical study using tissue engineering technology. Tissue Eng Part A. 2010;16:1891–900.

    Article  CAS  PubMed  Google Scholar 

  93. Ito K, Yamada Y, Nakamura S, Ueda M. Osteogenic potential of effective bone engineering using dental pulp stem cells, bone marrow stem cells, and periosteal cells for osseointegration of dental implants. Int J Oral Maxillofac Implants. 2011;26:947–54.

  94. Abdal Dayem A, Lee SB, Cho SG. The impact of metallic nanoparticles on stem cell proliferation and differentiation. Nanomaterials (Basel). 2018;8:761.

    Article  PubMed  PubMed Central  Google Scholar 

  95. Yamakawa D, Kawase-Koga Y, Fujii Y, Kanno Y, Sato M, Ohba S, et al. Effects of helioxanthin derivative-treated human dental pulp stem cells on fracture healing. Int J Mol Sci. 2020;21:9158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Fujii Y, Kawase-Koga Y, Hojo H, Yano F, Sato M, Chung UI, et al. Bone regeneration by human dental pulp stem cells using a helioxanthin derivative and cell-sheet technology. Stem Cell Res Ther. 2018;9:24.

    Article  Google Scholar 

  97. Camacho-Alonso F, Tudela-Mulero M, Buend´ıa A, Navarro J, Pérez-Sayáns M, Mercado-Díaz A. Bone regeneration in critical-sized mandibular symphysis defects using bioceramics with or without bone marrow mesenchymal stem cells in healthy, diabetic, osteoporotic, and diabetic-osteoporotic rats. Dent Mater. 2022;38:1283.

    Article  CAS  PubMed  Google Scholar 

  98. Zhang W, Zhang Z, Chen S, Macri L, Kohn J, Yelick PC. Mandibular jaw bone regeneration using human dental cell-seeded tyrosine-derived polycarbonate scaffolds. Tissue Eng Part A. 2016;22:985–93.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Lee SH, Shin H. Matrices and scaffolds for delivery of bioactive molecules in bone and cartilage tissue engineering. Adv Drug Deliv Rev. 2007;59:339–59.

    Article  CAS  PubMed  Google Scholar 

  100. Nakajima K, Kunimatsu R, Ando K, Ando T, Hayashi Y, Kihara T, et al. Comparison of the bone regeneration ability between stem cells from human exfoliated deciduous teeth, human dental pulp stem cells and human bone marrow mesenchymal stem cells. Biochem Biophys Res Commun. 2018;497:876–82.

    Article  CAS  PubMed  Google Scholar 

  101. Cao S, Han J, Sharma N, Msallem B, Jeong W, Son J, et al. In vitro mechanical and biological properties of 3D printed polymer composite and b-tricalcium phosphate scaffold on human dental pulp stem cells. Materials (Basel). 2020;13:3057.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Seo BM, Sonoyama W, Yamaza T, Coppe C, Kikuiri T, Akiyama K, Lee JS, Shi S. SHED repair critical-size calvarial defects in mice. Oral Dis. 2008;14:428–34.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Yamaza T, Kentaro A, Chen C, Liu Y, Shi Y, Gronthos S, et al. Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res Ther. 2010;1:5.

    Article  Google Scholar 

  104. Zheng Y, Liu Y, Zhang CM, Zhang HY, Li WH, Shi S, et al. Stem cells from deciduous tooth repairmandibular defect in swine. J Dent Res. 2009;88:249–54.

    Article  PubMed  PubMed Central  Google Scholar 

  105. Kunwong N, Tangjit N, Rattanapinyopituk K, Dechkunakorn S, Anuwongnukroh N, Arayapisit T, et al. Optimization of poly (lactic-co-glycolic acid)-bioactive glass composite scaffold for bone tissue engineering using stem cells from human exfoliated deciduous teeth. Arch Oral Biol. 2021;123:105041.

    Article  CAS  PubMed  Google Scholar 

  106. Wang X, Sha XJ, Li GH, Yang FS, Ji K, Wen LY, et al. Comparative characterization of stem cells from human exfoliated deciduous teeth and dental pulp stem cells. Arch Oral Biol. 2012;57:1231–40.

    Article  CAS  PubMed  Google Scholar 

  107. Prahasanti C, Subrata LH, Saskianti T, Suardita K, Ernawati DS. Combined hydroxyapatite scaffold and stem cell from human exfoliated deciduous teeth modulating alveolar bone regeneration via regulating receptor activator of nuclear factor-Κb and osteoprotegerin system. Iran J Med Sci. 2019;44:415–21.

    Google Scholar 

  108. Kang YH, Lee HJ, Jang SJ, Byun JH, Lee JS, Lee HC, et al. Immunomodulatory properties and in vivo osteogenesis of human dental stem cells from fresh and cryopreserved dental follicles. Differentiation. 2015;90:48–58.

    Article  CAS  PubMed  Google Scholar 

  109. Tsuchiya S, Ohshima S, Yamakoshi Y, Simmer JP, Honda MJ. Osteogenic differentiation capacity of porcine dental follicle progenitor cells. Connect Tissue Res. 2010;51:197–207.

    Article  CAS  PubMed  Google Scholar 

  110. Rezai-Rad M, Bova JF, Orooji M, Pepping J, Qureshi A, Del Piero F, et al. Evaluation of bone regeneration potential of dental follicle stem cells for treatment of craniofacial defects. Cytotherapy. 2015;17:1572–81.

    Article  CAS  PubMed  Google Scholar 

  111. Lucaciu O, Soriţău O, Gheban D, Ciuca DR, Virtic O, Vulpoi A, et al. Dental follicle stem cells in bone regeneration on titanium implants. BMC Biotechnol. 2015;15:114.

    Article  Google Scholar 

  112. Hu L, Zhao B, Gao Z, Xu J, Fan Z, Zhang C, et al. Regeneration characteristics of different dental derived stem cell sheets. J Oral Rehabil. 2020;47:66–72.

    Article  CAS  PubMed  Google Scholar 

  113. He H, Yu J, Cao J, E L, Wang D, Zhang H, et al. Biocompatibility and osteogenic capacity of periodontal ligament stem cells on nHAC/PLA and HA/TCP scaffolds. J Biomater Sci Polym Ed. 2011;22:179–94.

    Article  CAS  PubMed  Google Scholar 

  114. Ge S, Zhao N, Wang L, Yu M, Liu H, Song A, et al. Bone repair by periodontal ligament stem cellseeded nanohydroxyapatite-chitosan scaffold. Int J Nanomedicine. 2012;7:5405.

    Article  CAS  Google Scholar 

  115. Diomede F, Zini N, Gatta V, Fulle S, Merciaro I, D’Aurora M, et al. Human periodontal ligament stem cells cultured onto corticocancellous scaffold drive bone regenerative process. Eur Cell Mater. 2016;32:181–201.

    Article  CAS  PubMed  Google Scholar 

  116. Han J, Menicanin D, Marino V, Ge S, Mrozik K, Gronthos S, et al. Assessment of the regenerative potential of allogeneic in a rodent periodontal defect model. J Periodontal Res. 2014;49:333–45.

    Article  CAS  PubMed  Google Scholar 

  117. Nagy K, Láng O, Láng J, Perczel-Kovách K, Gyulai-Gaál S, Kádár K, et al. A novel hydrogel scaffold for. Interv Med Appl Sci. 2018;10:162–70.

    PubMed  PubMed Central  Google Scholar 

  118. LS S, Kasmieh R, Wakimoto H, Hingtgen S, van deWater JA, Mohapatra G, Figueiredo JL, Martuza RL, Weissleder R, Shah K. Assessment of therapeutic efficacy and fate of engineered human mesenchymal stem cells for cancer therapy. Proc Natl Acad Sci U S A. 2009;106:4822–7.

    Article  Google Scholar 

  119. E LL, Xu WH, Feng L, Liu Y, Cai DQ, Wen N, et al. Estrogen enhances the bone regeneration potential of derived from osteoporotic rats and seeded on nano-hydroxyapatite/collagen/poly (L-lactide). Int J Mol Med. 2016;37:1475–86.

    Article  PubMed  PubMed Central  Google Scholar 

  120. Ma Y, Ji Y, Zhong T, Wan W, Yang Q, Li A, et al. Bioprinting-based PDLSC-ECM screening for in vivo repair of alveolar bone defect using cell-laden, injectable and photocrosslinkable hydrogels. ACS Biomater Sci Eng. 2017;3:3534–45.

    Article  CAS  PubMed  Google Scholar 

  121. Kim IH, Jeon M, Cheon K, Kim SH, Jung HS, Shin Y, et al. In vivo evaluation of decellularized human tooth scaffold for dental tissue regeneration. Appl Sci (Basel). 2021;11:8472.

    Article  CAS  PubMed  Google Scholar 

  122. Ferrarotti F, Romano F, Gamba MN, Quirico A, Giraudi M, Audagna M, et al. Human intrabony defect regeneration with micrografts containing dental pulp stem cells: a randomized controlled clinical trial. J Clin Periodontol. 2018;45:841–50.

    Article  CAS  PubMed  Google Scholar 

  123. Chen FM, Gao LN, Tian BM, Zhang XY, Zhang YJ, Dong GY, et al. Treatment of periodontal intrabony defects using autologous periodontal ligament stem cells: a randomized clinical trial. Stem Cell Res Ther. 2016;7:33.

  124. Hernández-Monjaraz B, Santiago-Osorio E, Ledesma-Martínez E, Alcauter-Zavala A, Mendoza-Núñez VM. Retrieval of a periodontally compromised tooth by allogeneic grafting of mesenchymal stem cells from dental pulp: a case report. J Int Med Res. 2018;46:2983–93.

    Article  PubMed  PubMed Central  Google Scholar 

  125. Zeng N, Ayyub M, Sun H, Wen X, Xiang P, Gao Z. Effects of physical activity on motor skills and cognitive development in early childhood: a systematic review. BioMed Res Int. 2017;2017:2760716.

  126. Xuan K, Li B, Guo H, Sun W, Kou X, He X, Zhang Y, Sun J, Liu A, Liao L, Liu S. Deciduous autologous tooth stem cells regenerate dental pulp after implantation into injured teeth. Sci Transl Med. 2018;10:eaaf3227.

    Article  PubMed  Google Scholar 

  127. d’Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, et al. Human mandible bone defect repair by the grafting of dental pulp stem/progenitor cells and collagen sponge biocomplexes. Eur Cell Mater. 2009;18:75–83.

    Article  PubMed  Google Scholar 

  128. Giuliani A, Manescu A, Langer M, Rustichelli F, Desiderio V, Paino F, et al. Three years after transplants in human mandibles, histological and in-line holotomography revealed that stem cells regenerated a compact rather than a spongy bone: biological and clinical implications. Stem Cells Transl Med. 2013;2:316–24.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  129. Barbier L, Ramos E, Mendiola J, Rodriguez O, Santamaria G, Santamaria J, et al. Autologous dental pulp mesenchymal stem cells for inferior third molar post-extraction socket healing: a split-mouth randomised clinical trial. Med Oral Patol Oral Cir Bucal. 2018;23:e469.

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Graziano A, Carinci F, Scolaro S, d’Aquino R. Periodontal tissue generation using autologous dental ligament micro-grafts: case report with 6 months follow-up. Ann Oral Maxillofac Surg. 2013;1:20.

    Article  Google Scholar 

  131. Brunelli G, Motroni A, Graziano A, D’Aquino R, Zollino I, Carinci F. Sinus lift tissue engineering using autologous pulp micro-grafts: a case report of bone density evaluation. J Indian Soc Periodontol. 2013;17:644.

    Article  PubMed  PubMed Central  Google Scholar 

  132. Tanikawa DYS, Pinheiro CCG, Almeida MCA, Oliveira CRGCM, Coudry RA, Rocha DL, et al. Deciduous dental pulp stem cells for maxillary alveolar reconstruction in cleft lip and palate patients. Stem Cells Int. 2020;2020:6234167.

  133. Shiu ST, Lee WF, Chen SM, Hao LT, Hung YT, Lai PC, et al. Effect of different bone grafting materials and mesenchymal stem cells on bone regeneration: a micro-computed tomography and histomorphometric study in a rabbit calvarial defect model. Int J Mol Sci. 2021;22:8101.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  134. Li J, Chen M, Wei X, Hao Y, Wang J. Evaluation of 3D-printed polycaprolactone scaffolds coated with freeze-dried platelet-rich plasma for bone regeneration. Materials (Basel). 2017;10:831

    Article  PubMed  PubMed Central  Google Scholar 

  135. Campos JM, Sousa AC, Caseiro AR, Pedrosa SS, Pinto PO, Branquinho MV, et al. Dental pulp stem cells and Bonelike® for bone regeneration in ovine model. Regen Biomater. 2019;6:49–59.

    Article  CAS  PubMed  Google Scholar 

  136. Huang K, Ou Q, Xie Y, Chen X, Fang Y, Huang C, et al. Halloysite nanotube based scaffold for enhanced bone regeneration. ACS Biomater Sci Eng. 2019;5:4037–47.

    Article  CAS  PubMed  Google Scholar 

  137. Farea M, Husein A, Halim AS, Abdullah NA, Mokhtar KI, Lim CK, et al. Synergistic effects of chitosan scaffold and TGFβ1 on the proliferation and osteogenic differentiation of dental pulp stem cells derived from human exfoliated deciduous teeth. Arch Oral Biol. 2014;59:1400–11.

    Article  CAS  PubMed  Google Scholar 

  138. Chen FM, Gao LN, Tian BM, Zhang XY, Zhang YJ, Dong GY, et al. Treatment of periodontal intrabony defects using autologous : a randomized clinical trial. Stem Cell Res Ther. 2016;7:33.

    Article  Google Scholar 

  139. Hernández-Monjaraz B, Santiago-Osorio E, Ledesma-Martínez E, Aguiñiga-Sánchez I, Sosa-Hernández NA, Mendoza-Núñez VM. Dental pulp mesenchymal stem cells as a treatment for periodontal disease in older adults. Stem Cells Int. 2020;2020:8890873.

Download references

Acknowledgement

This work was supported by the deanship of scientific research-University of Petra (16/4/2022) and Cell Therapy Center-The university of Jordan. This work was supported by the deanship of scientific research-University of Petra (16/4/2022) and Cell Therapy Center-The university of Jordan.

Author information

Authors and Affiliations

Authors

Contributions

DA: who had the idea for the article. LST, MBO, YIH, JAA, Nazneen Aslam, who performed the literature search and DA, NA, HJ and AA who drafted and/or critically revised the work.

Corresponding authors

Correspondence to Duaa Abuarqoub or Abdalla Awidi.

Ethics declarations

Conflict of interest

The authors have no conflict of interest to declare.

Ethical statement

There are no experiments carried out for this article.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Abuarqoub, D., Theeb, L.S., Omari, M.B. et al. The Osteogenic Role of Biomaterials Combined with Human-Derived Dental Stem Cells in Bone Tissue Regeneration. Tissue Eng Regen Med 20, 251–270 (2023). https://doi.org/10.1007/s13770-022-00514-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13770-022-00514-9

Keywords

Navigation