Skip to main content
SpringerLink
Log in

Dental Stem Cells for Bone Tissue Engineering

  • Chapter
  • First Online:
Dental Stem Cells

Part of the book series: Stem Cell Biology and Regenerative Medicine ((STEMCELL))

  • 838 Accesses

Abstract

Bone defects and atrophy lead to several clinical problems. Autogenous bone grafts and guided bone regeneration are commonly used to repair bone defects. To promote good outcomes and avoid invasiveness, tissue engineering has been developed as an alternative technique and potential substitute for present therapies. Generally, bone tissue engineering refers to the implantation of an artificial construct in order to regenerate bone tissue. Current artificial structures mainly contain three components: stem cells having differentiation capacity into osteoblasts, scaffold framework, and growth factors regulating various properties of the stem cells. Bone marrow mesenchymal stem cells (BMMSCs), which have been widely investigated, are considered the gold standard for bone tissue engineering. In recent years, investigators have paid more and more attention to dental stem cells (DSCs), mainly dental pulp stem cells (DPSCs), stem cells from human exfoliated deciduous teeth (SHEDs), periodontal ligament stem cells (PDLSCs), stem cells from apical papilla (SCAPs), and dental follicle stem cells (DFSCs). PDLSCs, DFSCs, and SCAPs have osteogenic differentiation potentials based on in vitro studies, and PDLSCs and DFSCs have been confirmed for their osteogenic potentials in in vivo animal studies. In addition, DPSC- and SHED-based bone regeneration strategies have significantly increased bone formation in animal studies. Thus, these DSCs have become candidate sources of seed cells for bone regeneration but further progress is still needed before they can be applied clinically.

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

Access this chapter

Log in via an institution
Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  1. Ito K, Yamada Y, Nagasaka T, Baba S, Ueda M (2005) Osteogenic potential of injectable tissue‐engineered bone: a comparison among autogenous bone, bone substitute (Bio‐Oss®), platelet‐rich plasma, and tissue‐engineered bone with respect to their mechanical properties and histological findings. J Biomed Mater Res A 73(1):63–67

    Article  PubMed  CAS  Google Scholar 

  2. Scheller EL, Krebsbach PH, Kohn DH (2009) Tissue engineering: state of the art in oral rehabilitation. J Oral Rehabil 36(5):368–389. doi:10.1111/j.1365-2842.2009.01939.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Kaigler D, Mooney D (2001) Tissue engineering’s impact on dentistry. J Dent Educ 65(5):456–462

    CAS  PubMed  Google Scholar 

  4. Daltoe FP, Mendonca PP, Mantesso A, Deboni MCZ (2014) Can SHED or DPSCs be used to repair/regenerate non-dental tissues? A systematic review of in vivo studies. Braz Oral Res 28(1):1–7

    Article  Google Scholar 

  5. Rodriguez-Lozano FJ, Bueno C, Insausti CL, Meseguer L, Ramirez MC, Blanquer M, Marin N, Martinez S, Moraleda JM (2011) Mesenchymal stem cells derived from dental tissues. Int Endod J 44(9):800–806. doi:10.1111/j.1365-2591.2011.01877.x

    Article  CAS  PubMed  Google Scholar 

  6. Gronthos S, Mankani M, Brahim J, Robey PG, Shi S (2000) Postnatal human dental pulp stem cells (DPSCs) in vitro and in vivo. Proc Natl Acad Sci U S A 97(25):13625–13630. doi:10.1073/pnas.240309797

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S (2003) SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 100(10):5807–5812. doi:10.1073/pnas.0937635100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S (2004) Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 364(9429):149–155. doi:10.1016/S0140-6736(04)16627-0

    Article  CAS  PubMed  Google Scholar 

  9. Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kuhn U, Mohl C, Sippel C, Hoffmann KH (2005) Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 24(2):155–165. doi:10.1016/j.matbio.2004.12.004

    Article  CAS  PubMed  Google Scholar 

  10. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34(2):166–171. doi:10.1016/j.joen.2007.11.021

    Article  PubMed  PubMed Central  Google Scholar 

  11. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S (2008) Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem cells 26(7):1787–1795. doi:10.1634/stemcells.2007-0979

    Article  CAS  PubMed  Google Scholar 

  12. Cordeiro MM, Dong Z, Kaneko T, Zhang Z, Miyazawa M, Shi S, Smith AJ, Nor JE (2008) Dental pulp tissue engineering with stem cells from exfoliated deciduous teeth. J Endod 34(8):962–969. doi:10.1016/j.joen.2008.04.009

    Article  PubMed  Google Scholar 

  13. d’Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G (2007) Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14(6):1162–1171

    Article  PubMed  CAS  Google Scholar 

  14. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81(8):531–535

    Article  CAS  PubMed  Google Scholar 

  15. Xu J, Wang W, Kapila Y, Lotz J, Kapila S (2009) Multiple differentiation capacity of STRO-1+/CD146+ PDL mesenchymal progenitor cells. Stem Cells Dev 18(3):487–496. doi:10.1089/scd.2008.0113

    Article  CAS  PubMed  Google Scholar 

  16. Yalvac ME, Ramazanoglu M, Rizvanov AA, Sahin F, Bayrak OF, Salli U, Kose GT (2010) Isolation and characterization of stem cells derived from human third molar tooth germs of young adults: implications in neo-vascularization, osteo-, adipo-and neurogenesis. Pharmacogenomics J 10(2):105–113. doi:10.1038/tpj.2009.40

    Article  CAS  PubMed  Google Scholar 

  17. Le Blanc K, Ringdén O (2005) Immunobiology of human mesenchymal stem cells and future use in hematopoietic stem cell transplantation. Biol Blood Marrow TR 11(5):321–334

    Article  CAS  Google Scholar 

  18. Tomic S, Djokic J, Vasilijic S, Vucevic D, Todorovic V, Supic G, Colic M (2010) Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells Dev 20(4):695–708. doi:10.1089/scd.2010.0145

    Article  CAS  Google Scholar 

  19. Deskins DL, Bastakoty D, Saraswati S, Shinar A, Holt GE, Young PP (2013) Human mesenchymal stromal cells: identifying assays to predict potency for therapeutic selection. Stem Cells Transl Med 2(2):151–158. doi:10.5966/sctm.2012-0099

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Russell KC, Lacey MR, Gilliam JK, Tucker HA, Phinney DG, O’Connor KC (2011) Clonal analysis of the proliferation potential of human bone marrow mesenchymal stem cells as a function of potency. Biotechnol Bioeng 108(11):2716–2726. doi:10.1002/bit.23193

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Russell KC, Phinney DG, Lacey MR, Barrilleaux BL, Meyertholen KE, O’Connor KC (2010) In vitro high-capacity assay to quantify the clonal heterogeneity in trilineage potential of mesenchymal stem cells reveals a complex hierarchy of lineage commitment. Stem Cells 28(4):788–798. doi:10.1002/stem.312

    Article  CAS  PubMed  Google Scholar 

  22. Galler KM, Cavender AC, Koeklue U, Suggs LJ, Schmalz G, D’Souza RN (2011) Bioengineering of dental stem cells in a PEGylated fibrin gel. Regen Med 6(2):191–200. doi:10.2217/rme.11.3

    Article  CAS  PubMed  Google Scholar 

  23. Huang GT, Yamaza T, Shea LD, Djouad F, Kuhn NZ, Tuan RS, Shi S (2010) Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model. Tissue Eng Part A 16(2):605–615. doi:10.1089/ten.TEA.2009.0518

    Article  CAS  PubMed  Google Scholar 

  24. Hakki SS, Kayis SA, Hakki EE, Bozkurt SB, Duruksu G, Unal ZS, Karaoz E (2015) Comparison of MSCs isolated from pulp and periodontal ligament. J Periodontol 86(2):283–91. doi:10.1902/jop.2014.140257

    Google Scholar 

  25. Chen K, Xiong H, Huang Y, Liu C (2013) Comparative analysis of in vitro periodontal characteristics of stem cells from apical papilla (SCAP) and periodontal ligament stem cells (PDLSCs). Arch Oral Biol 58(8):997–1006. doi:10.1016/j.archoralbio.2013.02.010

    Article  CAS  PubMed  Google Scholar 

  26. Han C, Yang Z, Zhou W, Jin F, Song Y, Wang Y, Huo N, Chen L, Qian H, Hou R, Duan Y, Jin Y (2010) Periapical follicle stem cell: a promising candidate for cementum/periodontal ligament regeneration and bio-root engineering. Stem Cells Dev 19(9):1405–1415. doi:10.1089/scd.2009.0277

    Article  CAS  PubMed  Google Scholar 

  27. Navabazam AR, Sadeghian Nodoshan F, Sheikhha MH, Miresmaeili SM, Soleimani M, Fesahat F (2013) Characterization of mesenchymal stem cells from human dental pulp, preapical follicle and periodontal ligament. Iran J Reprod Med 11(3):235–242

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Carinci F, Papaccio G, Laino G, Palmieri A, Brunelli G, D’Aquino R, Pezzetti F (2008) Comparison between genetic portraits of osteoblasts derived from primary cultures and osteoblasts obtained from human pulpar stem cells. J Craniofac Surg 19(3):616–625. doi:10.1097/SCS.0b013e31816aabc8

    Article  PubMed  Google Scholar 

  29. Graziano A, d’Aquino R, Angelis MGCD, De Francesco F, Giordano A, Laino G, Papaccio G (2008) Scaffold’s surface geometry significantly affects human stem cell bone tissue engineering. J Cell Physiol 214(1):166–172

    Article  CAS  PubMed  Google Scholar 

  30. Laino G, d'Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G (2005) A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20(8):1394–1402. doi:10.1359/JBMR.050325

    Article  PubMed  CAS  Google Scholar 

  31. Otabe K, Muneta T, Kawashima N, Suda H, Tsuji K, Sekiya I (2012) Comparison of gingiva, dental pulp, and periodontal ligament cells from the standpoint of mesenchymal stem cell properties. Cell Medicine 4(1):13–21

    Article  PubMed  PubMed Central  Google Scholar 

  32. Zhang QB, Zhang ZQ, Fang SL, Liu YR, Jiang G, Li KF (2014) Effects of hypoxia on proliferation and osteogenic differentiation of periodontal ligament stem cells: an in vitro and in vivo study. Genet Mol Res 13(4):10204–10214. doi:10.4238/2014.December.4.15

    Article  CAS  PubMed  Google Scholar 

  33. Gandia C, Arminan A, Garcia-Verdugo JM, Lledo E, Ruiz A, Minana MD, Sanchez-Torrijos J, Paya R, Mirabet V, Carbonell-Uberos F, Llop M, Montero JA, Sepulveda P (2008) Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction. Stem Cells 26(3):638–645. doi:10.1634/stemcells.2007-0484

    Article  PubMed  Google Scholar 

  34. Liu J, Yu F, Sun Y, Jiang B, Zhang W, Yang J, Liu S (2014) Characteristics and potential applications of human dental tissue‐derived mesenchymal stem cells. Stem Cells 33(3):627–638. doi:10.1002/stem.1909

    Article  CAS  Google Scholar 

  35. Ding G, Liu Y, Wang W, Wei F, Liu D, Fan Z, An Y, Zhang C, Wang S (2010) Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 28(10):1829–1838. doi:10.1002/stem.512

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Liu O, Xu J, Ding G, Liu D, Fan Z, Zhang C, Chen W, Ding Y, Tang Z, Wang S (2013) Periodontal ligament stem cells regulate B lymphocyte function via programmed cell death protein 1. Stem Cells 31(7):1371–1382. doi:10.1002/stem.1387

    Article  CAS  PubMed  Google Scholar 

  37. Riccio M, Maraldi T, Pisciotta A, La Sala GB, Ferrari A, Bruzzesi G, Motta A, Migliaresi C, De Pol A (2012) Fibroin scaffold repairs critical-size bone defects in vivo supported by human amniotic fluid and dental pulp stem cells. Tissue Eng Part A 18(9–10):1006–1013. doi:10.1089/ten.TEA.2011.0542

    Article  CAS  PubMed  Google Scholar 

  38. Seo BM, Sonoyama W, Yamaza T, Coppe C, Kikuiri T, Akiyama K, Lee JS, Shi S (2008) SHED repair critical-size calvarial defects in mice. Oral Dis 14(5):428–434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Yamada Y, Ito K, Nakamura S, Ueda M, Nagasaka T (2011) Promising cell-based therapy for bone regeneration using stem cells from deciduous teeth, dental pulp, and bone marrow. Cell Transplant 20(7):1003–1013. doi:10.3727/096368910X539128

    Article  PubMed  Google Scholar 

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

    PubMed  Google Scholar 

  41. Liu HC, Wang DS, Su F, Wu X, Shi ZP, Lv Y, Wang JZ (2011) Reconstruction of alveolar bone defects using bone morphogenetic protein 2 mediated rabbit dental pulp stem cells seeded on nano-hydroxyapatite/collagen/poly (L-lactide). Tissue Eng Part A 17(19–20):2417–2433. doi:10.1089/ten.TEA.2010.0620

    Article  CAS  PubMed  Google Scholar 

  42. Park SY, Kim KH, Gwak EH, Rhee SH, Lee JC, Shin SY, Seol YJ (2015) Ex vivo bone morphogenetic protein 2 gene delivery using periodontal ligament stem cells for enhanced re‐osseointegration in the regenerative treatment of peri‐implantitis. J Biomed Mater Res A 103(1):38–47. doi:10.1002/jbm.a.35145

    Article  PubMed  CAS  Google Scholar 

  43. Honda MJ, Imaizumi M, Tsuchiya S, Morsczeck C (2010) Dental follicle stem cells and tissue engineering. J Oral Sci 52(4):541–552

    Article  PubMed  Google Scholar 

  44. Abe S, Yamaguchi S, Watanabe A, Hamada K, Amagasa T (2008) Hard tissue regeneration capacity of apical pulp derived cells (APDCs) from human tooth with immature apex. Biochem Biophys Res Commun 371(1):90–93. doi:10.1016/j.bbrc.2008.04.016

    Article  CAS  PubMed  Google Scholar 

  45. Wang S, Mu J, Fan Z, Yu Y, Yan M, Lei G, Zhang G (2012) Insulin-like growth factor 1 can promote the osteogenic differentiation and osteogenesis of stem cells from apical papilla. Stem Cell Res 8(3):346–356. doi:10.1016/j.scr.2011.12.005

    Article  CAS  PubMed  Google Scholar 

  46. Khan Y, Yaszemski MJ, Mikos AG, Laurencin CT (2008) Tissue engineering of bone: material and matrix considerations. J Bone Joint Surg Am 90(Suppl 1):36–42. doi:10.2106/JBJS.G.01260

    Article  PubMed  Google Scholar 

  47. Boeckel DG, Shinkai RSA, Grossi ML, Teixeira ER (2012) culture-based tissue engineering as an alternative to bone grafts in implant dentistry: a literature review. J Oral Implantol 38(s1):538–545. doi:10.1563/AAID-JOI-D-11-00197

    Article  PubMed  Google Scholar 

  48. Annibali S, Cicconetti A, Cristalli MP, Giordano G, Trisi P, Pilloni A, Ottolenghi L (2013) 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 24(3):866–871. doi:10.1097/SCS.0b013e31827ca530

    Article  PubMed  Google Scholar 

  49. Laino G, Graziano A, d’Aquino R, Pirozzi G, Lanza V, Valiante S, De Rosa A, Naro F, Vivarelli E, Papaccio G (2006) An approachable human adult stem cell source for hard-tissue engineering. J Cell Physiol 206(3):693–701. doi:10.1002/jcp.20526

    Article  CAS  PubMed  Google Scholar 

  50. Huang GJ, Gronthos S, Shi S (2009) Mesenchymal stem cells derived from dental tissues vs. those from other sources: their biology and role in regenerative medicine. J Dent Res 88(9):792–806. doi:10.1177/0022034509340867

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Galler KM, D’Souza RN (2011) Tissue engineering approaches for regenerative dentistry. Regen Med 6(1):111–124. doi:10.2217/rme.10.86

    Article  CAS  PubMed  Google Scholar 

  52. Sahdev P, Ochyl LJ, Moon JJ (2014) Biomaterials for nanoparticle vaccine delivery systems. Pharm Res 31(10):2563–2582. doi:10.1007/s11095-014-1419-y

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Tsuchiya S, Ohshima S, Yamakoshi Y, Simmer JP, Honda MJ (2010) Osteogenic differentiation capacity of porcine dental follicle progenitor cells. Connect Tissue Res 51(3):197–207. doi:10.3109/03008200903267542

    Article  CAS  PubMed  Google Scholar 

  54. Coyac BR, Chicatun F, Hoac B, Nelea V, Chaussain C, Nazhat SN, McKee MD (2013) Mineralization of dense collagen hydrogel scaffolds by human pulp cells. J Dent Res 92(7):648–654. doi:10.1177/0022034513488599

    Article  CAS  PubMed  Google Scholar 

  55. Viale-Bouroncle S, Gosau M, Morsczeck C (2014) Laminin regulates the osteogenic differentiation of dental follicle cells via integrin-alpha2/-beta1 and the activation of the FAK/ERK signaling pathway. Cell Tissue Res 357(1):345–354. doi:10.1007/s00441-014-1869-x

    Article  CAS  PubMed  Google Scholar 

  56. Morsczeck C, Schmalz G, Reichert TE, Völlner F, Saugspier M, Viale-Bouroncle S, Driemel O (2009) Gene expression profiles of dental follicle cells before and after osteogenic differentiation in vitro. Clin Oral Investig 13(4):383–391. doi:10.1007/s00784-009-0260-x

    Article  PubMed  Google Scholar 

  57. Chen YJ, Chung MC, Jane Yao CC, Huang CH, Chang HH, Jeng JH, Young TH (2012) The effects of acellular amniotic membrane matrix on osteogenic differentiation and ERK1/2 signaling in human dental apical papilla cells. Biomaterials 33(2):455–463. doi:10.1016/j.biomaterials.2011.09.065

    Article  CAS  PubMed  Google Scholar 

  58. Kanafi MM, Ramesh A, Gupta PK, Bhonde RR (2014) Dental pulp stem cells immobilized in alginate microspheres for applications in bone tissue engineering. Int Endod J 47(7):687–697. doi:10.1111/iej.12205

    Article  CAS  PubMed  Google Scholar 

  59. Dahl M, Jørgensen NR, Hørberg M, Pinholt EM (2014) Carriers in mesenchymal stem cell osteoblast mineralization—state-of-the-art. J Cranio Maxill Surg 42(1):41–47. doi:10.1016/j.jcms.2013.01.047

    Article  Google Scholar 

  60. Lee JS, Yi JK, An SY, Heo JS (2014) Increased osteogenic differentiation of periodontal ligament stem cells on polydopamine film occurs via activation of integrin and PI3K signaling pathways. Cell Physiol Biochem 34(5):1824–1834. doi:10.1159/000366381

    Article  CAS  PubMed  Google Scholar 

  61. Polini A, Pisignano D, Parodi M, Quarto R, Scaglione S (2011) Osteoinduction of human mesenchymal stem cells by bioactive composite scaffolds without supplemental osteogenic growth factors. PloS One 6(10):e26211. doi:10.1371/journal.pone.0026211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Viale-Bouroncle S, Bey B, Reichert TE, Schmalz G, Morsczeck C (2011) beta-tricalcium-phosphate stimulates the differentiation of dental follicle cells. J Mater Sci Mater Med 22(7):1719–1724. doi:10.1007/s10856-011-4345-0

    Article  CAS  PubMed  Google Scholar 

  63. Viale-Bouroncle S, Buergers R, Morsczeck C, Gosau M (2013) beta-Tricalcium phosphate induces apoptosis on dental follicle cells. Calcif Tissue Int 92(5):412–417. doi:10.1007/s00223-012-9694-2

    Article  CAS  PubMed  Google Scholar 

  64. Ning L, Malmstrom H, Ren YF (2015) Porous collagen-hydroxyapatite scaffolds with mesenchymal stem cells for bone regeneration. J Oral Implantol 41(1):45–49. doi:10.1563/AAID-JOI-D-12-00298

    Article  PubMed  Google Scholar 

  65. Guo T, Li Y, Cao G, Zhang Z, Chang S, Czajka-Jakubowska A, Nor JE, Clarkson BH, Liu J (2014) Fluorapatite-modified scaffold on dental pulp stem cell mineralization. J Dent Res 93(12):1290–1295. doi:10.1177/0022034514547914

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Moshaverinia A, Chen C, Xu X, Akiyama K, Ansari S, Zadeh HH, Shi S (2013) Bone regeneration potential of stem cells derived from periodontal ligament or gingival tissue sources encapsulated in RGD-modified alginate scaffold. Tissue Eng Part A 20(3–4):611–621. doi:10.1089/ten.TEA.2013.0229

    PubMed  PubMed Central  Google Scholar 

  67. Viale-Bouroncle S, Gosau M, Küpper K, Möhl C, Brockhoff G, Reichert TE, Morsczeck C (2012) Rigid matrix supports osteogenic differentiation of stem cells from human exfoliated deciduous teeth (SHED). Differentiation 84(5):366–370. doi:10.1016/j.diff.2012.08.005

    Article  CAS  PubMed  Google Scholar 

  68. Lamplot JD, Qin J, Nan G, Wang J, Liu X, Yin L, Tomal J, Li R, Shui W, Zhang H, Kim SH, Zhang W, Zhang J, Kong Y, Denduluri S, Rogers MR, Pratt A, Haydon RC, Luu HH, Angeles J, Shi LL, He TC (2013) BMP9 signaling in stem cell differentiation and osteogenesis. Am J Stem Cells 2(1):1–21

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Wang J, Zhang H, Zhang W, Huang E, Wang N, Wu N, Wen S, Chen X, Liao Z, Deng F, Yin L, Zhang J, Zhang Q, Yan Z, Liu W, Zhang Z, Ye J, Deng Y, Luu HH, Haydon RC, He TC, Deng F (2014) Bone morphogenetic protein-9 effectively induces osteo/odontoblastic differentiation of the reversibly immortalized stem cells of dental apical papilla. Stem Cells Dev 23(12):1405–1416. doi:10.1089/scd.2013.0580

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Ye G, Li C, Xiang X, Chen C, Zhang R, Yang X, Weng Y (2014) Bone morphogenetic Protein-9 induces PDLSCs osteogenic differentiation through the ERK and p38 signal pathways. Int J Med Sci 11(10):1065–1072. doi:10.7150/ijms.8473.eCollection2014

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Saugspier M, Felthaus O, Viale-Bouroncle S, Driemel O, Reichert TE, Schmalz G, Morsczeck C (2010) The differentiation and gene expression profile of human dental follicle cells. Stem Cells Dev 19(5):707–717. doi:10.1089/scd.2009.0027

    Article  CAS  PubMed  Google Scholar 

  72. Silverio KG, Davidson KC, James RG, Adams AM, Foster BL, Nociti FH, Somerman MJ Jr, Moon RT (2012) Wnt/beta-catenin pathway regulates bone morphogenetic protein (BMP2)-mediated differentiation of dental follicle cells. J Periodontal Res 47(3):309–319. doi:10.1111/j.1600-0765.2011.01433.x

    Article  CAS  PubMed  Google Scholar 

  73. Zhang H, Wang J, Deng F, Huang E, Yan Z, Wang Z, Deng Y, Zhang Q, Zhang Z, Ye J, Qiao M, Li R, Wang J, Wei Q, Zhou G, Luu HH, Haydon RC, He TC, Deng F (2015) Canonical Wnt signaling acts synergistically on BMP9-induced osteo/odontoblastic differentiation of stem cells of dental apical papilla (SCAPs). Biomaterials 39:145–154. doi:10.1016/j.biomaterials.2014.11.007

    Article  CAS  PubMed  Google Scholar 

  74. Qu B, Liu O, Fang X, Zhang H, Wang Y, Quan H, Zhang J, Zhou J, Zuo J, Tang J, Tang Z (2014) Distal-less homeobox 2 promotes the osteogenic differentiation potential of stem cells from apical papilla. Cell Tissue Res 357(1):133–143. doi:10.1007/s00441-014-1833-9

    Article  CAS  PubMed  Google Scholar 

  75. Mimori K, Komaki M, Iwasaki K, Ishikawa I (2007) Extracellular signal-regulated kinase 1/2 is involved in ascorbic acid-induced osteoblastic differentiation in periodontal ligament cells. J Periodontol 78(2):328–334

    Article  PubMed  Google Scholar 

  76. Yu Y, Mu J, Fan Z, Lei G, Yan M, Wang S, Tang C, Wang Z, Yu J, Zhang G (2012) Insulin-like growth factor 1 enhances the proliferation and osteogenic differentiation of human periodontal ligament stem cells via ERK and JNK MAPK pathways. Histochem Cell Biol 137(4):513–525. doi:10.1007/s00418-011-0908-x

    Article  CAS  PubMed  Google Scholar 

  77. Feng X, Huang D, Lu X, Feng G, Xing J, Lu J, Xu K, Xia W, Meng Y, Tao T, Li L, Gu Z (2014) Insulin-like growth factor 1 can promote proliferation and osteogenic differentiation of human dental pulp stem cells via mTOR pathway. Dev Growth Differ 56(9):615–624. doi:10.1111/dgd.12179

    Article  CAS  PubMed  Google Scholar 

  78. Nguyen DV, Li Calzi S, Shaw LC, Kielczewski JL, Korah HE, Grant MB (2013) An ocular view of the IGF-IGFBP system. Growth Horm IGF Res 23(3):45–52. doi:10.1016/j.ghir.2013.03.001

    Article  CAS  PubMed  Google Scholar 

  79. Liu D, Wang Y, Jia Z, Wang LP, Wang J, Yang D, Song J, Wang S, Fan Z (2015) Demethylation of IGFBP5 by histone demethylase KDM6B promotes mesenchymal stem cell-mediated periodontal tissue regeneration by enhancing osteogenic differentiation and anti-inflammation potentials. Stem Cells 33(8):2523–2536. doi:10.1002/stem.2018

    Article  CAS  PubMed  Google Scholar 

  80. Oh SA, Lee HY, Lee JH, Kim TH, Jang JH, Kim HW, Wall I (2012) Collagen three-dimensional hydrogel matrix carrying basic fibroblast growth factor for the cultivation of mesenchymal stem cells and osteogenic differentiation. Tissue Eng Part A 18(9–10):1087–1100. doi:10.1089/ten.TEA.2011.0360

    Article  CAS  PubMed  Google Scholar 

  81. Li B, Qu C, Chen C, Liu Y, Akiyama K, Yang R, Shi S (2012) Basic fibroblast growth factor inhibits osteogenic differentiation of stem cells from human exfoliated deciduous teeth through ERK signaling. Oral Dis 18(3):285–292. doi:10.1111/j.1601-0825.2011.01878.x

    Article  CAS  PubMed  Google Scholar 

  82. Nowwarote N, Pavasant P, Osathanon T (2015) Role of endogenous basic fibroblast growth factor in stem cells isolated from human exfoliated deciduous teeth. Arch Oral Biol 60(3):408–415. doi:10.1016/j.archoralbio.2014.11.017

    Article  CAS  PubMed  Google Scholar 

  83. Osathanon T, Nowwarote N, Manokawinchoke J, Pavasant P (2013) bFGF and JAGGED1 regulate alkaline phosphatase expression and mineralization in dental tissue-derived mesenchymal stem cells. J Cell Biochem 114(11):2551–2561. doi:10.1002/jcb.24602

    Article  CAS  PubMed  Google Scholar 

  84. Wu J, Huang GT, He W, Wang P, Tong Z, Jia Q, Dong L, Niu Z, Ni L (2012) Basic fibroblast growth factor enhances stemness of human stem cells from the apical papilla. J Endod 38(5):614–622. doi:10.1016/j.joen.2012.01.014

    Article  PubMed  PubMed Central  Google Scholar 

  85. Qian J, Jiayuan W, Wenkai J, Peina W, Ansheng Z, Shukai S, Shafei Z, Jun L, Longxing N (2015) Basic fibroblastic growth factor affects the osteogenic differentiation of dental pulp stem cells in a treatment-dependent manner. Int Endod J 48(7):690–700. doi:10.1111/iej.12368

    Article  CAS  PubMed  Google Scholar 

  86. Chang JY, Wang C, Liu J, Huang Y, Jin C, Yang C, Hai B, Liu F, D’Souza RN, McKeehan WL, Wang F (2013) Fibroblast growth factor signaling is essential for self-renewal of dental epithelial stem cells. J Biol Chem 288(40):28952–28961. doi:10.1074/jbc.M113.506873

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Houshmand B, Behnia H, Khoshzaban A, Morad G, Behrouzi G, Dashti SG, Khojasteh A (2013) Osteoblastic differentiation of human stem cells derived from bone marrow and periodontal ligament under the effect of enamel matrix derivative and transforming growth factor-beta. Int J Oral Maxillofac Implants 28(6):e440–e450. doi:10.11607/jomi.te24

    Article  PubMed  Google Scholar 

  88. He W, Zhang J, Niu Z, Yu Q, Wang Z, Zhang R, Su L, Fu L, Smith AJ, Cooper PR (2014) Regulatory interplay between NFIC and TGF-β1 in apical papilla-derived stem cells. J Dent Res 93(5):496–501. doi:10.1177/0022034514525200

    Article  CAS  PubMed  Google Scholar 

  89. Chang HH, Chang MC, Wu IH, Huang GF, Huang WL, Wang YL, Lee SY, Yeh CY, Guo MK, Chan CP, Hsien HC, Jeng JH (2015) Role of ALK5/Smad2/3 and MEK1/ERK signaling in transforming growth factor beta 1-modulated growth, collagen turnover, and differentiation of stem cells from apical papilla of human tooth. J Endod 41(8):1272–1280. doi:10.1016/j.joen.2015.03.022

    Article  PubMed  Google Scholar 

  90. Ochiai H, Yamamoto Y, Yokoyama A, Yamashita H, Matsuzaka K, Abe S, Azuma T (2010) Dual nature of TGF-β1 in osteoblastic differentiation of human periodontal ligament cells. J Hard Tissue Biol 19(3):187–194

    Article  CAS  Google Scholar 

  91. Ochiai H, Okada S, Saito A, Hoshi K, Yamashita H, Takato T, Azuma T (2012) Inhibition of insulin-like growth factor-1 (IGF-1) expression by prolonged transforming growth factor-β1 (TGF-β1) administration suppresses osteoblast differentiation. J Biol Chem 287(27):22654–22661. doi:10.1074/jbc.M111.279091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Felthaus O, Gosau M, Ettl T, Prantl L, Morsczeck C (2014) Migration of human dental follicle cells in vitro. J Periodontal Res 49(2):205–212. doi:10.1111/jre.12096

    Article  CAS  PubMed  Google Scholar 

  93. Yuda A, Maeda H, Fujii S, Monnouchi S, Yamamoto N, Wada N, Koori K, Tomokiyo A, Hamano S, Hasegawa D, Akamine A (2015) Effect of CTGF/CCN2 on osteo/cementoblastic and fibroblastic differentiation of a human periodontal ligament stem/progenitor cell line. J Cell Physiol 230(1):150–159. doi:10.1002/jcp.24693

    Article  CAS  PubMed  Google Scholar 

  94. Lee UL, Jeon SH, Park JY, Choung PH (2011) Effect of platelet-rich plasma on dental stem cells derived from human impacted third molars. Regen Med 6(1):67–79. doi:10.2217/rme.10.9610.2217/rme.11.63

    Article  CAS  PubMed  Google Scholar 

  95. Lee JY, Nam H, Park YJ, Lee SJ, Chung CP, Han SB, Lee G (2011) The effects of platelet-rich plasma derived from human umbilical cord blood on the osteogenic differentiation of human dental stem cells. Vitro Cell Dev Biol Anim 47(2):157–164. doi:10.1007/s11626-010-9364-5

    Article  Google Scholar 

  96. Zhao SN, Liu WF, Zhang ZT (2013) Effect of platelet-rich plasma on cell proliferation and osteogenic activity of pulp stem cells. Zhonghua Kou Qiang Yi Xue Za Zhi 48(3):177–182

    PubMed  Google Scholar 

  97. Manimaran K, Sankaranarayanan S, Ravi VR, Elangovan S, Chandramohan M, Perumal SM (2014) Treatment of osteoradionecrosis of mandible with bone marrow concentrate and with dental pulp stem cells. Ann Maxillofac Surg 4(2):189–192. doi:10.4103/2231-0746.147130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Monnouchi S, Maeda H, Yuda A, Hamano S, Wada N, Tomokiyo A, Koori K, Sugii H, Serita S, Akamine A (2015) Mechanical induction of interleukin-11 regulates osteoblastic/cementoblastic differentiation of human periodontal ligament stem/progenitor cells. J Periodontal Res 50(2):231–239. doi:10.1111/jre.12200

    Article  CAS  PubMed  Google Scholar 

  99. Liu W, Konermann A, Guo T, Jager A, Zhang L, Jin Y (2014) Canonical Wnt signaling differently modulates osteogenic differentiation of mesenchymal stem cells derived from bone marrow and from periodontal ligament under inflammatory conditions. Biochim Biophys Acta 1840(3):1125–1134. doi:10.1016/j.bbagen.2013.11.003

    Article  CAS  PubMed  Google Scholar 

  100. Yin LH, Cheng WX, Qin ZS, Sun KM, Zhong M, Wang JK, Gao WY, Yu ZH (2014) Effects of ginsenoside Rg-1 on the proliferation and osteogenic differentiation of human periodontal ligament stem cells. Chin J Integr Med [Epub ahead of print]. doi:10.1007/s11655-014-1856-9

    Google Scholar 

  101. Kim SY, An SY, Lee JS, Heo JS (2015) Zanthoxylum schinifolium enhances the osteogenic potential of periodontal ligament stem cells. Vitro Cell Dev Biol Anim 51(2):165–173. doi:10.1007/s11626-014-9824-4

    Article  CAS  Google Scholar 

  102. Kim SY, Lee JY, Park YD, Kang KL, Lee JC, Heo JS (2013) Hesperetin alleviates the inhibitory effects of high glucose on the osteoblastic differentiation of periodontal ligament stem cells. PloS One 8(6):e67504. doi:10.1371/journal.pone.0067504

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Drees J, Felthaus O, Gosau M, Morsczeck C (2014) Butyrate stimulates the early process of the osteogenic differentiation but inhibits the biomineralization in dental follicle cells (DFCs). Odontology 102(2):154–159. doi:10.1007/s10266-013-0117-2

    Article  CAS  PubMed  Google Scholar 

  104. Brighton CT, Krebs AG (1972) Oxygen tension of healing fractures in the rabbit. J Bone Joint Surg Am 54(2):323–332

    CAS  PubMed  Google Scholar 

  105. Heppenstall RB, Grislis G, Hunt TK (1975) Tissue gas tensions and oxygen consumption in healing bone defects. Clin Orthop Relat Res 106:357–365

    Article  PubMed  Google Scholar 

  106. Vanacker J, Viswanath A, De Berdt P, Everard A, Cani PD, Bouzin C, Feron O, Diogenes A, Leprince JG, des Rieux A (2014) Hypoxia modulates the differentiation potential of stem cells of the apical papilla. J Endod 40(9):1410–1418. doi:10.1016/j.joen.2014.04.008

    Article  PubMed  Google Scholar 

  107. Iida K, Takeda-Kawaguchi T, Tezuka Y, Kunisada T, Shibata T, Tezuka K (2010) Hypoxia enhances colony formation and proliferation but inhibits differentiation of human dental pulp cells. Arch Oral Biol 55(9):648–654. doi:10.1016/j.archoralbio.2010.06.005

    Article  CAS  PubMed  Google Scholar 

  108. Sakdee JB, White RR, Pagonis TC, Hauschka PV (2009) Hypoxia-amplified proliferation of human dental pulp cells. J Endod 35(6):818–823. doi:10.1016/j.joen.2009.03.001

    Article  PubMed  Google Scholar 

  109. Osathanon T, Vivatbutsiri P, Sukarawan W, Sriarj W, Pavasant P, Sooampon S (2015) Cobalt chloride supplementation induces stem-cell marker expression and inhibits osteoblastic differentiation in human periodontal ligament cells. Arch Oral Biol 60(1):29–36. doi:10.1016/j.archoralbio.2014.08.018

    Article  CAS  PubMed  Google Scholar 

  110. Mu C, Lv T, Wang Z, Ma S, Ma J, Liu J, Yu J, Mu J (2014) Mechanical stress stimulates the osteo/odontoblastic differentiation of human stem cells from apical papilla via erk 1/2 and JNK MAPK pathways. Biomed Res Int 2014:494378. doi:10.1155/2014/494378

    Article  PubMed  PubMed Central  Google Scholar 

  111. Filho Cerruti H, Kerkis I, Kerkis A, Tatsui NH, da Costa NA, Bueno DF, da Silva MC (2007) Allogenous bone grafts improved by bone marrow stem cells and platelet growth factors: clinical case reports. Artif Organs 31(4):268–273. doi:10.1111/j.1525-1594.2007.00374.x

    Article  PubMed  CAS  Google Scholar 

  112. Rickert D, Sauerbier S, Nagursky H, Menne D, Vissink A, Raghoebar G (2011) Maxillary sinus floor elevation with bovine bone mineral combined with either autogenous bone or autogenous stem cells: a prospective randomized clinical trial. Clin Oral Implants Res 22(3):251–258. doi:10.1111/j.1600-0501.2010.01981.x

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Capital Medical University School of Stomatology, Tian Tan Xi Li No.4, Beijing, 100050, China

    Zhipeng Fan & Xiao Lin

Authors
  1. Zhipeng Fan
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiao Lin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Zhipeng Fan .

Editor information

Editors and Affiliations

  1. Yeditepe University, Genetics and Bioengineering Department, Istanbul, Turkey

    Fikrettin Şahin

  2. Yeditepe University, Genetics and Bioengineering Department, Istanbul, Turkey

    Ayşegül Doğan

  3. Yeditepe University, Genetics and Bioengineering Department, ISTANBUL, Turkey

    Selami Demirci

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Fan, Z., Lin, X. (2016). Dental Stem Cells for Bone Tissue Engineering. In: Şahin, F., Doğan, A., Demirci, S. (eds) Dental Stem Cells. Stem Cell Biology and Regenerative Medicine. Springer, Cham. https://doi.org/10.1007/978-3-319-28947-2_10

Download citation

Publish with us

Policies and ethics

Search

Navigation