Skip to main content
SpringerLink
Log in

Stem Cells for Periodontal Regeneration

  • Chapter
  • First Online:
Dental Stem Cells: Regenerative Potential

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

  • 1000 Accesses

Abstract

Periodontal disease is a very common cluster of diseases affecting the supporting structure of the teeth and eventually leading to tooth loss while also affecting the general health of patients.

Periodontal regeneration has been suggested to reverse damage to the attachment apparatus in selected cases but limitations still exist in the current technology making it not applicable to many situations. Tissue engineering approaches are evaluating novel biomaterials in order to improve the predictability of periodontal regenerative approaches. Dental Stem Cells (DSC) may enhance the regenerative capability of the host during periodontal wound healing. Not all DSCs are the same and periodontal ligament stem cells (PDLSCs) may be the most promising cell source for this application. Other cell types are although been evaluated with promising results.

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

Similar content being viewed by others

References

  1. Dye BA, Tan S, Smith V, Lewis BG, Barker LK, Thornton-Evans G, Eke PI, Beltran-Aguilar ED, Horowitz AM, Li CH (2007) Trends in oral health status: United States, 1988–1994 and 1999–2004. Vital Health Stat 11(248):1–92

    Google Scholar 

  2. Eke PI, Dye BA, Wei L, Thornton-Evans GO, Genco RJ, CDC Periodontal Disease Surveillance Workgroup, Beck J, Douglass G, Page R (2012) Prevalence of periodontitis in adults in the United States: 2009 and 2010. J Dent Res 91(10):914–920

    Article  CAS  PubMed  Google Scholar 

  3. Kassebaum NJ, Bernabe E, Dahiya M, Bhandari B, Murray CJ, Marcenes W (2014) Global burden of severe periodontitis in 1990–2010: a systematic review and meta-regression. J Dent Res 93(11):1045–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Axelsson P, Nystrom B, Lindhe J (2004) The long-term effect of a plaque control program on tooth mortality, caries and periodontal disease in adults. Results after 30 years of maintenance. J Clin Periodontol 31(9):749–757

    Article  CAS  PubMed  Google Scholar 

  5. Phipps KR, Stevens VJ (1995) Relative contribution of caries and periodontal disease in adult tooth loss for an HMO dental population. J Public Health Dent 55(4):250–252

    Article  CAS  PubMed  Google Scholar 

  6. Reich E, Hiller KA (1993) Reasons for tooth extraction in the western states of Germany. Community Dent Oral Epidemiol 21(6):379–383

    Article  CAS  PubMed  Google Scholar 

  7. Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4(1):1–6

    Article  CAS  PubMed  Google Scholar 

  8. Matuliene G, Pjetursson BE, Salvi GE, Schmidlin K, Bragger U, Zwahlen M, Lang NP (2008) Influence of residual pockets on progression of periodontitis and tooth loss: results after 11 years of maintenance. J Clin Periodontol 35(8):685–695

    Article  PubMed  Google Scholar 

  9. Nevins M, Camelo M, De Paoli S, Friedland B, Schenk RK, Parma-Benfenati S, Simion M, Tinti C, Wagenberg B (2006) A study of the fate of the buccal wall of extraction sockets of teeth with prominent roots. Int J Periodontics Restorative Dent 26(1):19–29

    PubMed  Google Scholar 

  10. Waerhaug J (1978) Healing of the dento-epithelial junction following subgingival plaque control. I. As observed in human biopsy material. J Periodontol 49(1):1–8

    Article  CAS  PubMed  Google Scholar 

  11. Waerhaug J (1978) Healing of the dento-epithelial junction following subgingival plaque control. II. As observed on extracted teeth. J Periodontol 49(3):119–134

    Article  CAS  PubMed  Google Scholar 

  12. Caton JG, Zander HA (1979) The attachment between tooth and gingival tissues after periodic root planing and soft tissue curettage. J Periodontol 50(9):462–466

    Article  CAS  PubMed  Google Scholar 

  13. Melcher AH (1976) On the repair potential of periodontal tissues. J Periodontol 47(5):256–260

    Article  CAS  PubMed  Google Scholar 

  14. Nyman S, Lindhe J, Karring T, Rylander H (1982) New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 9(4):290–296

    Article  CAS  PubMed  Google Scholar 

  15. Wikesjo UM, Claffey N, Egelberg J (1991) Periodontal repair in dogs. Effect of heparin treatment of the root surface. J Clin Periodontol 18(1):60–64

    Article  CAS  PubMed  Google Scholar 

  16. Wikesjo UM, Nilveus R (1990) Periodontal repair in dogs: effect of wound stabilization on healing. J Periodontol 61(12):719–724

    Article  CAS  PubMed  Google Scholar 

  17. Takei HH, Han TJ, Carranza FA Jr, Kenney EB, Lekovic V (1985) Flap technique for periodontal bone implants. Papilla preservation technique. J Periodontol 56(4):204–210

    Article  CAS  PubMed  Google Scholar 

  18. Cortellini P, Prato GP, Tonetti MS (1995) The modified papilla preservation technique. A new surgical approach for interproximal regenerative procedures. J Periodontol 66(4):261–266

    Article  CAS  PubMed  Google Scholar 

  19. Cortellini P, Prato GP, Tonetti MS (1999) The simplified papilla preservation flap. A novel surgical approach for the management of soft tissues in regenerative procedures. Int J Periodontics Restorative Dent 19(6):589–599

    CAS  PubMed  Google Scholar 

  20. Cortellini P, Tonetti MS (2001) Microsurgical approach to periodontal regeneration. Initial evaluation in a case cohort. J Periodontol 72(4):559–569

    Article  CAS  PubMed  Google Scholar 

  21. Cortellini P, Tonetti MS (2009) Improved wound stability with a modified minimally invasive surgical technique in the regenerative treatment of isolated interdental intrabony defects. J Clin Periodontol 36(2):157–163

    Article  PubMed  Google Scholar 

  22. Trombelli L, Farina R, Franceschetti G (2007) Uso di un solo lembo in chirurgia ricostruttiva. Dent Cadmos 8:19

    Google Scholar 

  23. Trombelli L, Farina R, Franceschetti G, Calura G (2009) Single-flap approach with buccal access in periodontal reconstructive procedures. J Periodontol 80(2):353–360

    Article  PubMed  Google Scholar 

  24. Trombelli L, Farina R, Franceschetti G, Minenna L (2008) Single Flap Approach. Un caso clinico paradigmatico. Dent Clin 2(3):1–7

    Google Scholar 

  25. Rasperini G, Acunzo R, Barnett A, Pagni G (2013) The soft tissue wall technique for the regenerative treatment of non-contained infrabony defects: a case series. Int J Periodontics Restorative Dent 33(3):e79–e87

    Article  PubMed  Google Scholar 

  26. Cortellini P, Tonetti MS (2011) Clinical and radiographic outcomes of the modified minimally invasive surgical technique with and without regenerative materials: a randomized-controlled trial in intra-bony defects. J Clin Periodontol 38(4):365–373

    Article  PubMed  Google Scholar 

  27. Mishra A, Avula H, Pathakota KR, Avula J (2013) Efficacy of modified minimally invasive surgical technique in the treatment of human intrabony defects with or without use of rhPDGF-BB gel: a randomized controlled trial. J Clin Periodontol 40(2):172–179

    Article  CAS  PubMed  Google Scholar 

  28. MacArthur BD, Oreffo RO (2005) Bridging the gap. Nature 433(7021):19

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  30. Lynch SE (2008) Tissue engineering: applications in oral and maxillofacial surgery and periodontics, 2nd edn. Quintessence Publishing Co. Ltd., Chicago

    Google Scholar 

  31. Marx RE, Carlson ER, Eichstaedt RM, Schimmele SR, Strauss JE, Georgeff KR (1998) Platelet-rich plasma: growth factor enhancement for bone grafts. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 85(6):638–646

    Article  CAS  PubMed  Google Scholar 

  32. Anitua E (1999) Plasma rich in growth factors: preliminary results of use in the preparation of future sites for implants. Int J Oral Maxillofac Implants 14(4):529–535

    CAS  PubMed  Google Scholar 

  33. Boyapati L, Wang HL (2006) The role of platelet-rich plasma in sinus augmentation: a critical review. Implant Dent 15(2):160–170

    Article  PubMed  Google Scholar 

  34. Plachokova AS, Nikolidakis D, Mulder J, Jansen JA, Creugers NH (2008) Effect of platelet-rich plasma on bone regeneration in dentistry: a systematic review. Clin Oral Implants Res 19(6):539–545

    Article  PubMed  Google Scholar 

  35. Becker W, Lynch SE, Lekholm U, Becker BE, Caffesse R, Donath K, Sanchez R (1992) A comparison of ePTFE membranes alone or in combination with platelet-derived growth factors and insulin-like growth factor-I or demineralized freeze-dried bone in promoting bone formation around immediate extraction socket implants. J Periodontol 63(11):929–940

    Article  CAS  PubMed  Google Scholar 

  36. Howell TH, Fiorellini J, Jones A, Alder M, Nummikoski P, Lazaro M, Lilly L, Cochran D (1997) A feasibility study evaluating rhBMP-2/absorbable collagen sponge device for local alveolar ridge preservation or augmentation. Int J Periodontics Restorative Dent 17(2):124–139

    CAS  PubMed  Google Scholar 

  37. Howell TH, Fiorellini JP, Paquette DW, Offenbacher S, Giannobile WV, Lynch SE (1997) A phase I/II clinical trial to evaluate a combination of recombinant human platelet-derived growth factor-BB and recombinant human insulin-like growth factor-I in patients with periodontal disease. J Periodontol 68(12):1186–1193

    Article  CAS  PubMed  Google Scholar 

  38. Stefani CM, Machado MA, Sallum EA, Sallum AW, Toledo S, Nociti FH Jr (2000) Platelet-derived growth factor/insulin-like growth factor-1 combination and bone regeneration around implants placed into extraction sockets: a histometric study in dogs. Implant Dent 9(2):126–131

    Article  CAS  PubMed  Google Scholar 

  39. Camelo M, Nevins ML, Schenk RK, Lynch SE, Nevins M (2003) Periodontal regeneration in human Class II furcations using purified recombinant human platelet-derived growth factor-BB (rhPDGF-BB) with bone allograft. Int J Periodontics Restorative Dent 23(3):213–225

    PubMed  Google Scholar 

  40. Nevins M, Camelo M, Nevins ML, Schenk RK, Lynch SE (2003) Periodontal regeneration in humans using recombinant human platelet-derived growth factor-BB (rhPDGF-BB) and allogenic bone. J Periodontol 74(9):1282–1292

    Article  CAS  PubMed  Google Scholar 

  41. McGuire MK, Kao RT, Nevins M, Lynch SE (2006) rhPDGF-BB promotes healing of periodontal defects: 24-month clinical and radiographic observations. Int J Periodontics Restorative Dent 26(3):223–231

    PubMed  Google Scholar 

  42. Nevins M, Giannobile WV, McGuire MK, Kao RT, Mellonig JT, Hinrichs JE, McAllister BS, Murphy KS, McClain PK, Nevins ML, Paquette DW, Han TJ, Reddy MS, Lavin PT, Genco RJ, Lynch SE (2005) Platelet-derived growth factor stimulates bone fill and rate of attachment level gain: results of a large multicenter randomized controlled trial. J Periodontol 76(12):2205–2215

    Article  CAS  PubMed  Google Scholar 

  43. Giannobile WV (1996) Periodontal tissue engineering by growth factors. Bone 19(1 Suppl):23S–37S

    Article  CAS  PubMed  Google Scholar 

  44. Urist MR, Iwata H, Ceccotti PL, Dorfman RL, Boyd SD, McDowell RM, Chien C (1973) Bone morphogenesis in implants of insoluble bone gelatin. Proc Natl Acad Sci U S A 70(12):3511–3515

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Cheng H, Jiang W, Phillips FM, Haydon RC, Peng Y, Zhou L, Luu HH, An N, Breyer B, Vanichakarn P, Szatkowski JP, Park JY, He TC (2003) Osteogenic activity of the fourteen types of human bone morphogenetic proteins (BMPs). J Bone Joint Surg Am 85-A(8):1544–1552

    PubMed  Google Scholar 

  46. Fiorellini JP, Howell TH, Cochran D, Malmquist J, Lilly LC, Spagnoli D, Toljanic J, Jones A, Nevins M (2005) Randomized study evaluating recombinant human bone morphogenetic protein-2 for extraction socket augmentation. J Periodontol 76(4):605–613

    Article  CAS  PubMed  Google Scholar 

  47. Boyne PJ, Marx RE, Nevins M, Triplett G, Lazaro E, Lilly LC, Alder M, Nummikoski P (1997) A feasibility study evaluating rhBMP-2/absorbable collagen sponge for maxillary sinus floor augmentation. Int J Periodontics Restorative Dent 17(1):11–25

    CAS  PubMed  Google Scholar 

  48. Cochran DL, Jones AA, Lilly LC, Fiorellini JP, Howell H (2000) Evaluation of recombinant human bone morphogenetic protein-2 in oral applications including the use of endosseous implants: 3-year results of a pilot study in humans. J Periodontol 71(8):1241–1257

    Article  CAS  PubMed  Google Scholar 

  49. Lee YM, Nam SH, Seol YJ, Kim TI, Lee SJ, Ku Y, Rhyu IC, Chung CP, Han SB, Choi SM (2003) Enhanced bone augmentation by controlled release of recombinant human bone morphogenetic protein-2 from bioabsorbable membranes. J Periodontol 74(6):865–872

    Article  CAS  PubMed  Google Scholar 

  50. Selvig KA, Sorensen RG, Wozney JM, Wikesjo UM (2002) Bone repair following recombinant human bone morphogenetic protein-2 stimulated periodontal regeneration. J Periodontol 73(9):1020–1029

    Article  CAS  PubMed  Google Scholar 

  51. Giannobile WV, Ryan S, Shih MS, Su DL, Kaplan PL, Chan TC (1998) Recombinant human osteogenic protein-1 (OP-1) stimulates periodontal wound healing in class III furcation defects. J Periodontol 69(2):129–137

    Article  CAS  PubMed  Google Scholar 

  52. Rutherford RB, Sampath TK, Rueger DC, Taylor TD (1992) Use of bovine osteogenic protein to promote rapid osseointegration of endosseous dental implants. Int J Oral Maxillofac Implants 7(3):297–301

    CAS  PubMed  Google Scholar 

  53. Dunn CA, Jin Q, Taba M Jr, Franceschi RT, Bruce Rutherford R, Giannobile WV (2005) BMP gene delivery for alveolar bone engineering at dental implant defects. Mol Ther 11(2):294–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. van den Bergh JP, ten Bruggenkate CM, Groeneveld HH, Burger EH, Tuinzing DB (2000) Recombinant human bone morphogenetic protein-7 in maxillary sinus floor elevation surgery in 3 patients compared to autogenous bone grafts. A clinical pilot study. J Clin Periodontol 27(9):627–636

    Article  PubMed  Google Scholar 

  55. Wikesjo UM, Sorensen RG, Kinoshita A, Jian Li X, Wozney JM (2004) 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 31(8):662–670

    Article  CAS  PubMed  Google Scholar 

  56. Taba M Jr, Jin Q, Sugai JV, Giannobile WV (2005) Current concepts in periodontal bioengineering. Orthod Craniofac Res 8(4):292–302

    Article  PubMed  PubMed Central  Google Scholar 

  57. Reddi AH (1998) Role of morphogenetic proteins in skeletal tissue engineering and regeneration. Nat Biotechnol 16(3):247–252

    Article  CAS  PubMed  Google Scholar 

  58. Kaigler D, Cirelli JA, Giannobile WV (2006) Growth factor delivery for oral and periodontal tissue engineering. Expert Opin Drug Deliv 3(5):647–662

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Connolly JB (2002) Lentiviruses in gene therapy clinical research. Gene Ther 9(24):1730–1734

    Article  CAS  PubMed  Google Scholar 

  60. Giannobile WV, Lee CS, Tomala MP, Tejeda KM, Zhu Z (2001) Platelet-derived growth factor (PDGF) gene delivery for application in periodontal tissue engineering. J Periodontol 72(6):815–823

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Chen QP, Giannobile WV (2002) Adenoviral gene transfer of PDGF downregulates gas gene product PDGFalphaR and prolongs ERK and Akt/PKB activation. Am J Physiol Cell Physiol 282(3):C538–C544

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Jin QM, Anusaksathien O, Webb SA, Rutherford RB, Giannobile WV (2003) Gene therapy of bone morphogenetic protein for periodontal tissue engineering. J Periodontol 74(2):202–213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Jin Q, Anusaksathien O, Webb SA, Printz MA, Giannobile WV (2004) Engineering of tooth-supporting structures by delivery of PDGF gene therapy vectors. Mol Ther 9(4):519–526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Chang PC, Cirelli JA, Jin Q, Seol YJ, Sugai JV, D’Silva NJ, Danciu TE, Chandler LA, Sosnowski BA, Giannobile WV (2009) Adenovirus encoding human platelet-derived growth factor-B delivered to alveolar bone defects exhibits safety and biodistribution profiles favorable for clinical use. Hum Gene Ther 20(5):486–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Fang J, Zhu YY, Smiley E, Bonadio J, Rouleau JP, Goldstein SA, McCauley LK, Davidson BL, Roessler BJ (1996) Stimulation of new bone formation by direct transfer of osteogenic plasmid genes. Proc Natl Acad Sci U S A 93(12):5753–5758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Dogan A, Ozdemir A, Kubar A, Oygur T (2002) Assessment of periodontal healing by seeding of fibroblast-like cells derived from regenerated periodontal ligament in artificial furcation defects in a dog: a pilot study. Tissue Eng 8(2):273–282

    Article  PubMed  Google Scholar 

  67. McGuire MK, Scheyer ET (2007) A randomized, double-blind, placebo-controlled study to determine the safety and efficacy of cultured and expanded autologous fibroblast injections for the treatment of interdental papillary insufficiency associated with the papilla priming procedure. J Periodontol 78(1):4–17

    Article  PubMed  Google Scholar 

  68. Izumi K, Feinberg SE, Iida A, Yoshizawa M (2003) Intraoral grafting of an ex vivo produced oral mucosa equivalent: a preliminary report. Int J Oral Maxillofac Surg 32(2):188–197

    Article  CAS  PubMed  Google Scholar 

  69. McGuire MK, Scheyer ET, Nunn ME, Lavin PT (2008) A pilot study to evaluate a tissue-engineered bilayered cell therapy as an alternative to tissue from the palate. J Periodontol 79(10):1847–1856

    Article  PubMed  Google Scholar 

  70. Morelli T, Neiva R, Nevins ML, McGuire MK, Scheyer ET, Oh TJ, Braun TM, Nor JE, Bates D, Giannobile WV (2011) Angiogenic biomarkers and healing of living cellular constructs. J Dent Res 90(4):456–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Song J, Izumi K, Lanigan T, Feinberg SE (2004) Development and characterization of a canine oral mucosa equivalent in a serum-free environment. J Biomed Mater Res A 71(1):143–153

    Article  PubMed  CAS  Google Scholar 

  72. 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

    Article  CAS  PubMed  Google Scholar 

  73. Xu Q, Izumi K, Tobita T, Nakanishi Y, Feinberg SE (2009) Constitutive release of cytokines by human oral keratinocytes in an organotypic culture. J Oral Maxillofac Surg 67(6):1256–1264

    Article  PubMed  PubMed Central  Google Scholar 

  74. Somerman MJ, Ouyang HJ, Berry JE, Saygin NE, Strayhorn CL, D’Errico JA, Hullinger T, Giannobile WV (1999) Evolution of periodontal regeneration: from the roots’ point of view. J Periodontal Res 34(7):420–424

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Zhao M, Jin Q, Berry JE, Nociti FH Jr, Giannobile WV, Somerman MJ (2004) Cementoblast delivery for periodontal tissue engineering. J Periodontol 75(1):154–161

    Article  PubMed  PubMed Central  Google Scholar 

  76. Kaigler D, Pagni G, Park CH, Tarle SA, Bartel RL, Giannobile WV (2010) Angiogenic and osteogenic potential of bone repair cells for craniofacial regeneration. Tissue Eng A 16(9):2809–2820

    Article  CAS  Google Scholar 

  77. Pagni G, Kaigler D, Rasperini G, Avila-Ortiz G, Barte R, Giannobile WV (2012) Bone repair cells for craniofacial regeneration. Adv Drug Deliv Rev 64(12):1310–1319

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Grande DA, Southerland SS, Manji R, Pate DW, Schwartz RE, Lucas PA (1995) Repair of articular cartilage defects using mesenchymal stem cells. Tissue Eng 1(4):345–353

    Article  CAS  PubMed  Google Scholar 

  79. Owen P, Connaghan DG, Holland HK, Steis RG (1998) Bone marrow transplantation: cancer therapy comes of age. J Med Assoc Ga 87(2):145–146, 148

    CAS  PubMed  Google Scholar 

  80. Prockop DJ (1997) Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 276(5309):71–74

    Article  CAS  PubMed  Google Scholar 

  81. Park SR, Oreffo RO, Triffitt JT (1999) Interconversion potential of cloned human marrow adipocytes in vitro. Bone 24(6):549–554

    Article  CAS  PubMed  Google Scholar 

  82. 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

    Article  CAS  PubMed  Google Scholar 

  83. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Shi S, Le AD (2009) Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 183(12):7787–7798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. 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

    Article  CAS  PubMed  Google Scholar 

  85. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. 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

    Article  PubMed  PubMed Central  Google Scholar 

  87. Hynes K, Menicanin D, Gronthos S, Bartold PM (2012) Clinical utility of stem cells for periodontal regeneration. Periodontol 2000 59(1):203–227

    Article  PubMed  Google Scholar 

  88. Park JY, Jeon SH, Choung PH (2011) Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant 20(2):271–285

    Article  PubMed  Google Scholar 

  89. Gay IC, Chen S, MacDougall M (2007) Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 10(3):149–160

    Article  CAS  PubMed  Google Scholar 

  90. Huang GT, 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, Gronthos S, Shi S, Wang S (2008) Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 26(4):1065–1073

    Article  PubMed  PubMed Central  Google Scholar 

  92. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Shi S, Gronthos S (2003) Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 18(4):696–704

    Article  PubMed  Google Scholar 

  94. Treves-Manusevitz S, Hoz L, Rachima H, Montoya G, Tzur E, Vardimon A, Narayanan AS, Amar S, Arzate H, Pitaru S (2013) Stem cells of the lamina propria of human oral mucosa and gingiva develop into mineralized tissues in vivo. J Clin Periodontol 40(1):73–81

    Article  CAS  PubMed  Google Scholar 

  95. Wang F, Yu M, Yan X, Wen Y, Zeng Q, Yue W, Yang P, Pei X (2011) Gingiva-derived mesenchymal stem cell-mediated therapeutic approach for bone tissue regeneration. Stem Cells Dev 20(12):2093–2102

    Article  CAS  PubMed  Google Scholar 

  96. Wang L, Shen H, Zheng W, Tang L, Yang Z, Gao Y, Yang Q, Wang C, Duan Y, Jin Y (2011) Characterization of stem cells from alveolar periodontal ligament. Tissue Eng A 17(7–8):1015–1026

    Article  CAS  Google Scholar 

  97. Kaku M, Komatsu Y, Mochida Y, Yamauchi M, Mishina Y, Ko CC (2012) Identification and characterization of neural crest-derived cells in adult periodontal ligament of mice. Arch Oral Biol 57(12):1668–1675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Jo YY, Lee HJ, Kook SY, Choung HW, Park JY, Chung JH, Choung YH, Kim ES, Yang HC, Choung PH (2007) Isolation and characterization of postnatal stem cells from human dental tissues. Tissue Eng 13(4):767–773

    Article  CAS  PubMed  Google Scholar 

  99. Ikeda E, Yagi K, Kojima M, Yagyuu T, Ohshima A, Sobajima S, Tadokoro M, Katsube Y, Isoda K, Kondoh M, Kawase M, Go MJ, Adachi H, Yokota Y, Kirita T, Ohgushi H (2007) Multipotent cells from the human third molar: feasibility of cell-based therapy for liver disease. Differentiation 75(5):495–505

    Google Scholar 

  100. Iohara K, Zheng L, Ito M, Tomokiyo A, Matsushita K, Nakashima M (2006) Side population cells isolated from porcine dental pulp tissue with self-renewal and multipotency for dentinogenesis, chondrogenesis, adipogenesis, and neurogenesis. Stem Cells 24(11):2493–2503

    Article  CAS  PubMed  Google Scholar 

  101. 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

    Article  PubMed  Google Scholar 

  102. 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

    Article  CAS  PubMed  Google Scholar 

  103. Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, Liu H, Gronthos S, Wang CY, Wang S, Shi S (2006) Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS One 1, e79

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  104. Isaka J, Ohazama A, Kobayashi M, Nagashima C, Takiguchi T, Kawasaki H, Tachikawa T, Hasegawa K (2001) Participation of periodontal ligament cells with regeneration of alveolar bone. J Periodontol 72(3):314–323

    Article  CAS  PubMed  Google Scholar 

  105. McCulloch CA, Bordin S (1991) Role of fibroblast subpopulations in periodontal physiology and pathology. J Periodontal Res 26(3 Pt 1):144–154

    Article  CAS  PubMed  Google Scholar 

  106. Lindroos B, Maenpaa K, Ylikomi T, Oja H, Suuronen R, Miettinen S (2008) Characterisation of human dental stem cells and buccal mucosa fibroblasts. Biochem Biophys Res Commun 368(2):329–335

    Article  CAS  PubMed  Google Scholar 

  107. Seo BM, Miura M, Sonoyama W, Coppe C, Stanyon R, Shi S (2005) Recovery of stem cells from cryopreserved periodontal ligament. J Dent Res 84(10):907–912

    Article  PubMed  Google Scholar 

  108. Lian JB, Javed A, Zaidi SK, Lengner C, Montecino M, van Wijnen AJ, Stein JL, Stein GS (2004) Regulatory controls for osteoblast growth and differentiation: role of Runx/Cbfa/AML factors. Crit Rev Eukaryot Gene Expr 14(1–2):1–41

    Article  CAS  PubMed  Google Scholar 

  109. Gay I, Cavender A, Peto D, Sun Z, Speer A, Cao H, Amendt BA (2014) Differentiation of human dental stem cells reveals a role for microRNA-218. J Periodontal Res 49(1):110–120

    Article  CAS  PubMed  Google Scholar 

  110. Sharpe PT (2001) Neural crest and tooth morphogenesis. Adv Dent Res 15:4–7

    Article  CAS  PubMed  Google Scholar 

  111. Barboza EP, Duarte ME, Geolas L, Sorensen RG, Riedel GE, Wikesjo UM (2000) Ridge augmentation following implantation of recombinant human bone morphogenetic protein-2 in the dog. J Periodontol 71(3):488–496

    Article  CAS  PubMed  Google Scholar 

  112. Mizuno N, Ozeki Y, Shiba H, Kajiya M, Nagahara T, Takeda K, Kawaguchi H, Abiko Y, Kurihara H (2008) Humoral factors released from human periodontal ligament cells influence calcification and proliferation in human bone marrow mesenchymal stem cells. J Periodontol 79(12):2361–2370

    Article  CAS  PubMed  Google Scholar 

  113. Tomoeda M, Yamada S, Shirai H, Ozawa Y, Yanagita M, Murakami S (2008) PLAP-1/asporin inhibits activation of BMP receptor via its leucine-rich repeat motif. Biochem Biophys Res Commun 371(2):191–196

    Article  CAS  PubMed  Google Scholar 

  114. Yamada S, Ozawa Y, Tomoeda M, Matoba R, Matsubara K, Murakami S (2006) Regulation of PLAP-1 expression in periodontal ligament cells. J Dent Res 85(5):447–451

    Article  CAS  PubMed  Google Scholar 

  115. Yamada Y, Ueda M, Hibi H, Baba S (2006) A novel approach to periodontal tissue regeneration with mesenchymal stem cells and platelet-rich plasma using tissue engineering technology: a clinical case report. Int J Periodontics Restorative Dent 26(4):363–369

    PubMed  Google Scholar 

  116. Karring T, Nyman S, Lindhe J, Sirirat M (1984) Potentials for root resorption during periodontal wound healing. J Clin Periodontol 11(1):41–52

    Article  CAS  PubMed  Google Scholar 

  117. Kémoun P, Laurencin-Dalicieux S, Rue J, Farges JC, Gennero I, Conte-Auriol F, Briand-Mesange F, Gadelorge M, Arzate H, Narayanan AS, Brunel G, Salles JP (2007) Human dental follicle cells acquire cementoblast features under stimulation by BMP-2/-7 and enamel matrix derivatives (EMD) in vitro. Cell Tissue Res 329(2):283–294

    Article  PubMed  CAS  Google Scholar 

  118. Ji K, Liu Y, Lu W, Yang F, Yu J, Wang X, Ma Q, Yang Z, Wen L, Xuan K (2013) Periodontal tissue engineering with stem cells from the periodontal ligament of human retained deciduous teeth. J Periodontal Res 48(1):105–116

    Article  CAS  PubMed  Google Scholar 

  119. Silverio KG, Rodrigues TL, Coletta RD, Benevides L, Da Silva JS, Casati MZ, Sallum EA, Nociti FH Jr (2010) Mesenchymal stem cell properties of periodontal ligament cells from deciduous and permanent teeth. J Periodontol 81(8):1207–1215

    Article  CAS  PubMed  Google Scholar 

  120. Song JS, Kim SO, Kim SH, Choi HJ, Son HK, Jung HS, Kim CS, Lee JH (2012) In vitro and in vivo characteristics of stem cells derived from the periodontal ligament of human deciduous and permanent teeth. Tissue Eng A 18(19–20):2040–2051

    Article  CAS  Google Scholar 

  121. Hung TY, Lin HC, Chan YJ, Yuan K (2012) Isolating stromal stem cells from periodontal granulation tissues. Clin Oral Investig 16(4):1171–1180

    Article  PubMed  Google Scholar 

  122. Ronay V, Belibasakis GN, Attin T, Schmidlin PR, Bostanci N (2014) Expression of embryonic stem cell markers and osteogenic differentiation potential in cells derived from periodontal granulation tissue. Cell Biol Int 38(2):179–186

    Article  CAS  PubMed  Google Scholar 

  123. Zhu W, Liang M (2015) Periodontal ligament stem cells: current status, concerns, and future prospects. Stem Cells Int 2015:972313

    PubMed  PubMed Central  Google Scholar 

  124. Trofin EA, Monsarrat P, Kémoun P (2013) Cell therapy of periodontium: from animal to human? Front Physiol 4:325

    Article  PubMed  PubMed Central  Google Scholar 

  125. Zheng W, Wang S, Ma D, Tang L, Duan Y, Jin Y (2009) Loss of proliferation and differentiation capacity of aged human periodontal ligament stem cells and rejuvenation by exposure to the young extrinsic environment. Tissue Eng A 15(9):2363–2371

    Article  CAS  Google Scholar 

  126. Pierdomenico L, Bonsi L, Calvitti M, Rondelli D, Arpinati M, Chirumbolo G, Becchetti E, Marchionni C, Alviano F, Fossati V, Staffolani N, Franchina M, Grossi A, Bagnara GP (2005) Multipotent mesenchymal stem cells with immunosuppressive activity can be easily isolated from dental pulp. Transplantation 80(6):836–842

    Article  PubMed  Google Scholar 

  127. 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Mrozik KM, Wada N, Marino V, Richter W, Shi S, Wheeler DL, Gronthos S, Bartold PM (2013) Regeneration of periodontal tissues using allogeneic periodontal ligament stem cells in an ovine model. Regen Med 8(6):711–723

    Article  CAS  PubMed  Google Scholar 

  129. Marei MK, Nouh SR, Saad MM, Ismail NS (2005) Preservation and regeneration of alveolar bone by tissue-engineered implants. Tissue Eng 11(5–6):751–767

    Article  CAS  PubMed  Google Scholar 

  130. Perry BC, Zhou D, Wu X, Yang FC, Byers MA, Chu TM, Hockema JJ, Woods EJ, Goebel WS (2008) Collection, cryopreservation, and characterization of human dental pulp-derived mesenchymal stem cells for banking and clinical use. Tissue Eng C Methods 14(2):149–156

    Article  CAS  Google Scholar 

  131. Fujii S, Maeda H, Wada N, Kano Y, Akamine A (2006) Establishing and characterizing human periodontal ligament fibroblasts immortalized by SV40T-antigen and hTERT gene transfer. Cell Tissue Res 324(1):117–125

    Article  CAS  PubMed  Google Scholar 

  132. Philippe B, Luc S, Valerie PB, Jerome R, Alessandra BR, Louis C (2010) Culture and use of mesenchymal stromal cells in phase I and II clinical trials. Stem Cells Int 2010:503593

    Article  PubMed  PubMed Central  Google Scholar 

  133. Akita D, Morokuma M, Saito Y, Yamanaka K, Akiyama Y, Sato M, Mashimo T, Toriumi T, Arai Y, Kaneko T, Tsukimura N, Isokawa K, Ishigami T, Honda MJ (2014) Periodontal tissue regeneration by transplantation of rat adipose-derived stromal cells in combination with PLGA-based solid scaffolds. Biomed Res 35(2):91–103

    Article  CAS  PubMed  Google Scholar 

  134. Tobita M, Uysal AC, Ogawa R, Hyakusoku H, Mizuno H (2007) Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng 14(6):945–953

    Article  CAS  Google Scholar 

  135. Tobita M, Uysal AC, Ogawa R, Hyakusoku H, Mizuno H (2008) Periodontal tissue regeneration with adipose-derived stem cells. Tissue Eng A 14(6):945–953

    Article  CAS  Google Scholar 

  136. Tobita M, Uysal CA, Guo X, Hyakusoku H, Mizuno H (2013) Periodontal tissue regeneration by combined implantation of adipose tissue-derived stem cells and platelet-rich plasma in a canine model. Cytotherapy 15(12):1517–1526

    Article  CAS  PubMed  Google Scholar 

  137. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126(4):663–676

    Article  CAS  PubMed  Google Scholar 

  138. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S (2007) Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 131(5):861–872

    Article  CAS  PubMed  Google Scholar 

  139. Park IH, Zhao R, West JA, Yabuuchi A, Huo H, Ince TA, Lerou PH, Lensch MW, Daley GQ (2008) Reprogramming of human somatic cells to pluripotency with defined factors. Nature 451(7175):141–146

    Article  CAS  PubMed  Google Scholar 

  140. Yu J, Vodyanik MA, Smuga-Otto K, Antosiewicz-Bourget J, Frane JL, Tian S, Nie J, Jonsdottir GA, Ruotti V, Stewart R, Slukvin II, Thomson JA (2007) Induced pluripotent stem cell lines derived from human somatic cells. Science 318(5858):1917–1920

    Article  CAS  PubMed  Google Scholar 

  141. Tamaoki N, Takahashi K, Tanaka T, Ichisaka T, Aoki H, Takeda-Kawaguchi T, Iida K, Kunisada T, Shibata T, Yamanaka S, Tezuka K (2010) Dental pulp cells for induced pluripotent stem cell banking. J Dent Res 89(8):773–778

    Article  CAS  PubMed  Google Scholar 

  142. Trubiani O, Piattelli A, Gatta V, Marchisio M, Diomede F, D’Aurora M, Merciaro I, Pierdomenico L, Maraldi NM, Zini N (2015) Assessment of an efficient xeno-free culture system of human periodontal ligament stem cells. Tissue Eng C Methods 21(1):52–64

    Article  CAS  Google Scholar 

  143. Li H, Yan F, Lei L, Li Y, Xiao Y (2009) Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs 190(2):94–101

    Article  PubMed  Google Scholar 

  144. Okuda K, Yamamiya K, Kawase T, Mizuno H, Ueda M, Yoshie H (2009) Treatment of human infrabony periodontal defects by grafting human cultured periosteum sheets combined with platelet-rich plasma and porous hydroxyapatite granules: case series. J Int Acad Periodontol 11(3):206–213

    PubMed  Google Scholar 

  145. Su F, Liu SS, Ma JL, Wang DS, E LL, Liu HC (2015) Enhancement of periodontal tissue regeneration by transplantation of osteoprotegerin-engineered periodontal ligament stem cells. Stem Cell Res Ther 6:22

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  146. Mordenfeld A, Hallman M, Johansson CB, Albrektsson T (2010) Histological and histomorphometrical analyses of biopsies harvested 11 years after maxillary sinus floor augmentation with deproteinized bovine and autogenous bone. Clin Oral Implants Res 21(9):961–970

    PubMed  Google Scholar 

  147. De Kok IJ, Drapeau SJ, Young R, Cooper LF (2005) Evaluation of mesenchymal stem cells following implantation in alveolar sockets: a canine safety study. Int J Oral Maxillofac Implants 20(4):511–518

    PubMed  Google Scholar 

  148. Pelegrine AA, da Costa CE, Correa ME, Marques JF Jr (2010) Clinical and histomorphometric evaluation of extraction sockets treated with an autologous bone marrow graft. Clin Oral Implants Res 21(5):535–542

    Article  PubMed  Google Scholar 

  149. Dennis JE, Esterly K, Awadallah A, Parrish CR, Poynter GM, Goltry KL (2007) Clinical-scale expansion of a mixed population of bone-marrow-derived stem and progenitor cells for potential use in bone-tissue regeneration. Stem Cells 25(10):2575–2582

    Article  PubMed  Google Scholar 

  150. Kaigler D, Pagni G, Park CH, Braun TM, Holman LA, Yi E, Tarle SA, Bartel RL, Giannobile WV (2013) Stem cell therapy for craniofacial bone regeneration: a randomized, controlled feasibility trial. Cell Transplant 22(5):767–777

    Article  PubMed  PubMed Central  Google Scholar 

  151. Kaigler D, Avila-Ortiz G, Travan S, Taut AD, Padial-Molina M, Rudek I, Wang F, Lanis A, Giannobile WV (2015) Bone engineering of maxillary sinus bone deficiencies using enriched CD90+ stem cell therapy: a randomized clinical trial. J Bone Miner Res 30(7):1206–1216

    Article  CAS  PubMed  Google Scholar 

  152. Chen JS, Wong VW, Gurtner GC (2012) Therapeutic potential of bone marrow-derived mesenchymal stem cells for cutaneous wound healing. Front Immunol 3:192

    Article  PubMed  PubMed Central  Google Scholar 

  153. Hoogduijn MJ, Dor FJ (2013) Mesenchymal stem cells: are we ready for clinical application in transplantation and tissue regeneration? Front Immunol 4:144

    Article  PubMed  PubMed Central  Google Scholar 

  154. Chen FM, Jin Y (2010) Periodontal tissue engineering and regeneration: current approaches and expanding opportunities. Tissue Eng B Rev 16(2):219–255

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Private Practice, Via Lamarmora 29, 50121, Florence, Italy

    Giorgio Pagni

  2. University of Milan, Milan, Italy

    Giorgio Pagni

Authors
  1. Giorgio Pagni
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Giorgio Pagni .

Editor information

Editors and Affiliations

  1. Department of Biomedical Sciences, University of Padova, Padova, Italy

    Barbara Zavan

  2. Department of Neurosciences, University of Padova, Padova, Italy

    Eriberto Bressan

Rights and permissions

Reprints and permissions

Copyright information

© 2016 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Pagni, G. (2016). Stem Cells for Periodontal Regeneration. In: Zavan, B., Bressan, E. (eds) Dental Stem Cells: Regenerative Potential. Stem Cell Biology and Regenerative Medicine. Humana Press, Cham. https://doi.org/10.1007/978-3-319-33299-4_9

Download citation

Publish with us

Policies and ethics

Search

Navigation