Clinical utility of stem cells for periodontal regeneration

Periodontology 2000

Volumn 59, Issue 1, 2012, Pages 203-227

  Hynes, Kim ^a   Menicanin, Danijela ^a   Gronthos, Stan ^a   Bartold, P Mark ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CLASSIFICATION; CYTOLOGY; DECIDUOUS TOOTH; HUMAN; MESENCHYMAL STEM CELL; METHODOLOGY; PERIODONTAL DISEASE; PERIODONTAL LIGAMENT; PERIODONTICS; PHYSIOLOGY; STEM CELL; TISSUE ENGINEERING; TOOTH PULP; TOOTH SAC;

DENTAL PULP; DENTAL SAC; GUIDED TISSUE REGENERATION, PERIODONTAL; HUMANS; MESENCHYMAL STEM CELLS; PERIODONTAL DISEASES; PERIODONTAL LIGAMENT; STEM CELLS; TISSUE ENGINEERING; TOOTH, DECIDUOUS;

EID: 84859838125     PISSN: 09066713     EISSN: 16000757     Source Type: Journal    
DOI: 10.1111/j.1600-0757.2012.00443.x     Document Type: Article

References (182)

1. Abe S, Yamaguchi S, Amagasa T. Multilineage cells from apical pulp of human tooth with immature apex. Oral Science International 2007: 4: 45-58.
2. Akizuki T, Oda S, Komaki M, Tsuchioka H, Kawakatsu N, Kikuchi A, Yamato M, Okano T, Ishikawa I. Application of periodontal ligament cell sheet for periodontal regeneration: a pilot study in beagle dogs. J Periodontal Res 2005: 40: 245-251.
3. Arinzeh TL, Peter SJ, Archambault MP, van den Bos C, Gordon S, Kraus K, Smith A, Kadiyala S. Allogeneic mesenchymal stem cells regenerate bone in a critical-sized canine segmental defect. J Bone Joint Surg Am 2003: 85-A: 1927-1935.
4. Arthur A, Shi S, Zannettino AC, Fujii N, Gronthos S, Koblar SA. Implanted adult human dental pulp stem cells induce endogenous axon guidance. Stem Cells 2009: 27: 2229-2237.
5. Arthur A, Zannettino A, Gronthos S. The therapeutic applications of multipotential mesenchymal/stromal stem cells in skeletal tissue repair. J Cell Physiol 2009: 218: 237-245.
6. Barberi T, Willis LM, Socci ND, Studer L. Derivation of multipotent mesenchymal precursors from human embryonic stem cells. PLoS Med 2005: 2: e161.
7. Bartold PM, Marshall RI, Haynes DR. Periodontitis and rheumatoid arthritis: a review. J Periodontol 2005: 76: 2066-2074.
8. Bartold PM, McCulloch CA, Narayanan AS, Pitaru S. Tissue engineering: a new paradigm for periodontal regeneration based on molecular and cell biology. Periodontol 2000 2000: 24: 253-269.
9. Bartold PM, Narayanan AS. Periodontal regeneration: biology of the periodontal connective tissues. Chicago: Quintessence Publishing, 1998.
10. Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontol 2000 2006: 40: 164-172.
11. Bartold PM, Xiao Y, Lyngstaadas SP, Paine ML, Snead ML. Principles and applications of cell delivery systems for periodontal regeneration. Periodontol 2000 2006: 41: 123-135.
12. Beertsen W, McCulloch CA, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 1997: 13: 20-40.
13. Beltrao-Braga PI, Pignatari GC, Maiorka PC, Oliveira NA, Lizier NF, Wenceslau CV, Miglino MA, Muotri AR, Kerkis I. Feeder-free derivation of induced pluripotent stem cells from human immature dental pulp stem cells. Cell Transplant 2011: [Epub ahead of print].
14. Bensaid W, Oudina K, Viateau V, Potier E, Bousson V, Blanchat C, Sedel L, Guillemin G, Petite H. De novo reconstruction of functional bone by tissue engineering in the metatarsal sheep model. Tissue Eng 2005: 11: 814-824.
15. Bergenholtz G. Inflammatory response of the dental pulp to bacterial irritation. J Endod 1981: 7: 100-104.
16. Berkovitz BK. The structure of the periodontal ligament: an update. Eur J Orthod 1990: 12: 51-76.
17. Bianco P, Kuznetsov SA, Riminucci M, Gehron Robey P. Postnatal skeletal stem cells. Methods Enzymol 2006: 419: 117-148.
18. Bianco P, Riminucci M, Gronthos S, Robey PG. Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 2001: 19: 180-192.
19. Boyko GA, Melcher AH, Brunette DM. Formation of new periodontal ligament by periodontal ligament cells implanted in vivo after culture in vitro. A preliminary study of transplanted roots in the dog. J Periodontal Res 1981: 16: 73-88.
20. Bratthall G, Soderholm G, Neiderud AM, Kullendorff B, Edwardsson S, Attstrom R. Guided tissue regeneration in the treatment of human infrabony defects. Clinical, radiographical and microbiological results: a pilot study. J Clin Periodontol 1998: 25: 908-914.
21. Brodke D, Pedrozo HA, Kapur TA, Attawia M, Kraus KH, Holy CE, Kadiyala S, Bruder SP. Bone grafts prepared with selective cell retention technology heal canine segmental defects as effectively as autograft. J Orthop Res 2006: 24: 857-866.
22. Bruder SP, Jaiswal N, Ricalton NS, Mosca JD, Kraus KH, Kadiyala S. Mesenchymal stem cells in osteobiology and applied bone regeneration. Clin Orthop Relat Res 1998: 355S: S247-S256.
23. Bruder SP, Kraus KH, Goldberg VM, Kadiyala S. The effect of implants loaded with autologous mesenchymal stem cells on the healing of canine segmental bone defects. J Bone Joint Surg Am 1998: 80: 985-996.
24. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991: 9: 641-650.
25. Caplan AI. Review: mesenchymal stem cells: cell-based reconstructive therapy in orthopedics. Tissue Eng 2005: 11: 1198-1211.
26. Caplan AI. Adult mesenchymal stem cells for tissue engineering versus regenerative medicine. J Cell Physiol 2007: 213: 341-347.
27. Cate T. Ten Cate's oral histology: development, structure and function. St. Louis, MO: CV Mosby, 2003.
28. 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: 7892-7927.
29. Chen YL, Chen PK, Jeng LB, Huang CS, Yang LC, Chung HY, Chang SC. Periodontal regeneration using ex vivo autologous stem cells engineered to express the BMP-2 gene: an alternative to alveolaplasty. Gene Ther 2008: 15: 1469-1477.
30. Chung VH, Chen AY, Kwan CC, Chen PK, Chang SC. Mandibular alveolar bony defect repair using bone morphogenetic protein 2-expressing autologous mesenchymal stem cells. J Craniofac Surg 2011: 22: 450-454.
31. Cordeiro MM, Dong Z, Kaneko T, Zhang Z, Miyazawa M, Shi S, Smith AJ, Nor JE. Dental pulp tissue engineering with stem cells from exfoliated deciduous teeth. J Endod 2008: 34: 962-969.
32. Covas DT, Panepucci RA, Fontes AM, Silva WA Jr, Orellana MD, Freitas MC, Neder L, Santos AR, Peres LC, Jamur MC, Zago MA. Multipotent mesenchymal stromal cells obtained from diverse human tissues share functional properties and gene-expression profile with CD146+ perivascular cells and fibroblasts. Exp Hematol 2008: 36: 642-654.
33. d'Aquino R, De Rosa A, Lanza V, Tirino V, Laino L, Graziano A, Desiderio V, Laino G, Papaccio G. 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.
34. da Silva Meirelles L, Chagastelles PC, Nardi NB. Mesenchymal stem cells reside in virtually all post-natal organs and tissues. J Cell Sci 2006: 119: 2204-2213.
35. Dai KR, Xu XL, Tang TT, Zhu ZA, Yu CF, Lou JR, Zhang XL. Repairing of goat tibial bone defects with BMP-2 gene-modified tissue-engineered bone. Calcif Tissue Int 2005: 77: 55-61.
36. Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 2000: 28: 875-884.
37. Derubeis AR, Cancedda R. Bone marrow stromal cells (BMSCs) in bone engineering: limitations and recent advances. Ann Biomed Eng 2004: 32: 160-165.
38. Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, Jacobs DR Jr, Papapanou PN, Sacco RL. Relationship between periodontal disease, tooth loss, and carotid artery plaque: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Stroke 2003: 34: 2120-2125.
39. Desvarieux M, Demmer RT, Rundek T, Boden-Albala B, Jacobs DR Jr, Sacco RL, Papapanou PN. Periodontal microbiota and carotid intima-media thickness: the Oral Infections and Vascular Disease Epidemiology Study (INVEST). Circulation 2005: 111: 576-582.
40. Ding G, Liu Y, Wang W, Wei F, Liu D, Fan Z, An Y, Zhang C, Wang S. Allogeneic periodontal ligament stem cell therapy for periodontitis in swine. Stem Cells 2010: 28: 1829-1838.
41. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D, Deans R, Keating A, Prockop D, Horwitz E. Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 2006: 8: 315-317.
42. Dorotka R, Windberger U, Macfelda K, Bindreiter U, Toma C, Nehrer S. Repair of articular cartilage defects treated by microfracture and a three-dimensional collagen matrix. Biomaterials 2005: 26: 3617-3629.
43. Duailibi SE, Duailibi MT, Vacanti JP, Yelick PC. Prospects for tooth regeneration. Periodontol 2000 2006: 41: 177-187.
44. Duan X, Tu Q, Zhang J, Ye J, Sommer C, Mostoslavsky G, Kaplan D, Yang P, Chen J. Application of induced pluripotent stem (iPS) cells in periodontal tissue regeneration. J Cell Physiol 2011: 226: 150-157.
45. Egusa H, Okita K, Kayashima H, Yu G, Fukuyasu S, Saeki M, Matsumoto T, Yamanaka S, Yatani H. Gingival fibroblasts as a promising source of induced pluripotent stem cells. PLoS ONE 2010: 5: e12743.
46. Erices A, Conget P, Minguell JJ. Mesenchymal progenitor cells in human umbilical cord blood. Br J Haematol 2000: 109: 235-242.
47. Evans MJ, Kaufman MH. Establishment in culture of pluripotential cells from mouse embryos. Nature 1981: 292: 154-156.
48. Feng F, Akiyama K, Liu Y, Yamaza T, Wang TM, Chen JH, Wang BB, Huang GT, Wang S, Shi S. Utility of PDL progenitors for in vivo tissue regeneration: a report of 3 cases. Oral Dis 2010: 16: 20-28.
49. Field JR, McGee M, Stanley R, Ruthenbeck G, Papadimitrakis T, Zannettino A, Gronthos S, Itescu S. The efficacy of allogeneic mesenchymal precursor cells for the repair of an ovine tibial segmental defect. Vet Comp Orthop Traumatol 2011: 24: 113-121.
50. Frank RM. Ultrastructural relationship between the odontoblast, its process and the nerve fibre. Edinburgh, UK: Churchill Livingstone, 1968.
51. Friedenstein AJ, Chailakhjan RK, Lalykina KS. The development of fibroblast colonies in monolayer cultures of guinea-pig bone marrow and spleen cells. Cell Tissue Kinet 1970: 3: 393-403.
52. Friedenstein AJ, Gorskaja JF, Kulagina NN. Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 1976: 4: 267-274.
53. Friedenstein AJ, Piatetzky S II, Petrakova KV. Osteogenesis in transplants of bone marrow cells. J Embryol Exp Morphol 1966: 16: 381-390.
54. Garraway R, Young WG, Daley T, Harbrow D, Bartold PM. An assessment of the osteoinductive potential of commercial demineralized freeze-dried bone in the murine thigh muscle implantation model. J Periodontol 1998: 69: 1325-1336.
55. Gould TR, Melcher AH, Brunette DM. Migration and division of progenitor cell populations in periodontal ligament after wounding. J Periodontal Res 1980: 15: 20-42.
56. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S. Stem cell properties of human dental pulp stem cells. J Dent Res 2002: 81: 531-535.
57. Gronthos S, Chen S, Wang CY, Robey PG, Shi S. Telomerase accelerates osteogenesis of bone marrow stromal stem cells by upregulation of CBFA1, osterix, and osteocalcin. J Bone Miner Res 2003: 18: 716-722.
58. 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: 13625-13630.
59. Gronthos S, Mrozik K, Shi S, Bartold PM. Ovine periodontal ligament stem cells: isolation, characterization, and differentiation potential. Calcif Tissue Int 2006: 79: 310-317.
60. Gronthos S, Zannettino AC, Hay SJ, Shi S, Graves SE, Kortesidis A, Simmons PJ. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003: 116: 1827-1835.
61. Guo W, Gong K, Shi H, Zhu G, He Y, Ding B, Wen L, Jin Y. Dental follicle cells and treated dentin matrix scaffold for tissue engineering the tooth root. Biomaterials 2012: 33: 1291-1302.
62. Guo W, He Y, Zhang X, Lu W, Wang C, Yu H, Liu Y, Li Y, Zhou Y, Zhou J, Zhang M, Deng Z, Jin Y. The use of dentin matrix scaffold and dental follicle cells for dentin regeneration. Biomaterials 2009: 30: 6708-6723.
63. Handa K, Saito M, Tsunoda A, Yamauchi M, Hattori S, Sato S, Toyoda M, Teranaka T, Narayanan AS. Progenitor cells from dental follicle are able to form cementum matrix in vivo. Connect Tissue Res 2002: 43: 406-408.
64. Handa K, Saito M, Yamauchi M, Kiyono T, Sato S, Teranaka T, Sampath Narayanan A. Cementum matrix formation in vivo by cultured dental follicle cells. Bone 2002: 31: 606-611.
65. Harris R, Griffin CJ. The fine structure of the mature odontoblasts and cell rich zone of the human dental pulp. Aust Dent J 1969: 14: 168-177.
66. Hasegawa M, Yamato M, Kikuchi A, Okano T, Ishikawa I. Human periodontal ligament cell sheets can regenerate periodontal ligament tissue in an athymic rat model. Tissue Eng 2005: 11: 469-478.
67. Hasegawa N, Kawaguchi H, Hirachi A, Takeda K, Mizuno N, Nishimura M, Koike C, Tsuji K, Iba H, Kato Y, Kurihara H. Behavior of transplanted bone marrow-derived mesenchymal stem cells in periodontal defects. J Periodontol 2006: 77: 1003-1007.
68. Hirooka H. The biologic concept for the use of enamel matrix protein: true periodontal regeneration. Quintessence Int 1998: 29: 621-630.
69. Hoffman RL. Bone formation and resorption around developing teeth transplanted into the femur. Am J Anat 1966: 118: 91-102.
70. Horwitz EM, Le Blanc K, Dominici M, Mueller I, Slaper-Cortenbach I, Marini FC, Deans RJ, Krause DS, Keating A. Clarification of the nomenclature for MSC: the International Society for Cellular Therapy position statement. Cytotherapy 2005: 7: 393-395.
71. Horwitz EM, Prockop DJ, Fitzpatrick LA, Koo WW, Gordon PL, Neel M, Sussman M, Orchard P, Marx JC, Pyeritz RE, Brenner MK. Transplantability and therapeutic effects of bone marrow-derived mesenchymal cells in children with osteogenesis imperfecta. Nat Med 1999: 5: 309-313.
72. in't Anker PS, Noort WA, Scherjon SA, Kleijburg-van der Keur C, Kruisselbrink AB, van Bezooijen RL, Beekhuizen W, Willemze R, Kanhai HH, Fibbe WE. Mesenchymal stem cells in human second-trimester bone marrow, liver, lung, and spleen exhibit a similar immunophenotype but a heterogeneous multilineage differentiation potential. Haematologica 2003: 88: 845-852.
73. In't Anker PS, Scherjon SA, Kleijburg-van der Keur C, de Groot-Swings GM, Claas FH, Fibbe WE, Kanhai HH. Isolation of mesenchymal stem cells of fetal or maternal origin from human placenta. Stem Cells 2004: 22: 1338-1345.
74. Isaka J, Ohazama A, Kobayashi M, Nagashima C, Takiguchi T, Kawasaki H, Tachikawa T, Hasegawa K. Participation of periodontal ligament cells with regeneration of alveolar bone. J Periodontol 2001: 72: 314-323.
75. Iwata T, Yamato M, Zhang Z, Mukobata S, Washio K, Ando T, Feijen J, Okano T, Ishikawa I. Validation of human periodontal ligament-derived cells as a reliable source for cytotherapeutic use. J Clin Periodontol 2010: 37: 1088-1099.
76. Ji YM, Jeon SH, Park JY, Chung JH, Choung YH, Choung PH. Dental stem cell therapy with calcium hydroxide in dental pulp capping. Tissue Eng Part A 2010: 16: 1823-1833.
77. Jiang Y, Jahagirdar BN, Reinhardt RL, Schwartz RE, Keene CD, Ortiz-Gonzalez XR, Reyes M, Lenvik T, Lund T, Blackstad M, Du J, Aldrich S, Lisberg A, Low WC, Largaespada DA, Verfaillie CM. Pluripotency of mesenchymal stem cells derived from adult marrow. Nature 2002: 418: 41-49.
78. Jo YY, Lee HJ, Kook SY, Choung HW, Park JY, Chung JH, Choung YH, Kim ES, Yang HC, Choung PH. Isolation and characterization of postnatal stem cells from human dental tissues. Tissue Eng 2007: 13: 767-773.
79. Karring T, Nyman S, Gottlow J, Laurell L. Development of the biological concept of guided tissue regeneration - animal and human studies. Periodontol 2000 1993: 1: 26-35.
80. Kawaguchi H, Hirachi A, Hasegawa N, Iwata T, Hamaguchi H, Shiba H, Takata T, Kato Y, Kurihara H. Enhancement of periodontal tissue regeneration by transplantation of bone marrow mesenchymal stem cells. J Periodontol 2004: 75: 1281-1287.
81. Kemoun 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. Human dental follicle cells acquire cementoblast features under stimulation by BMP-2/-7 and enamel matrix derivatives (EMD) in vitro. Cell Tissue Res 2007: 329: 283-294.
82. Kim SH, Kim KH, Seo BM, Koo KT, Kim TI, Seol YJ, Ku Y, Rhyu IC, Chung CP, Lee YM. Alveolar bone regeneration by transplantation of periodontal ligament stem cells and bone marrow stem cells in a canine peri-implant defect model: a pilot study. J Periodontol 2009: 80: 1815-1823.
83. Kode JA, Mukherjee S, Joglekar MV, Hardikar AA. Mesenchymal stem cells: immunobiology and role in immunomodulation and tissue regeneration. Cytotherapy 2009: 11: 377-391.
84. Kon E, Muraglia A, Corsi A, Bianco P, Marcacci M, Martin I, Boyde A, Ruspantini I, Chistolini P, Rocca M, Giardino R, Cancedda R, Quarto R. Autologous bone marrow stromal cells loaded onto porous hydroxyapatite ceramic accelerate bone repair in critical-size defects of sheep long bones. J Biomed Mater Res 2000: 49: 328-337.
85. Krampera M, Pizzolo G, Aprili G, Franchini M. Mesenchymal stem cells for bone, cartilage, tendon and skeletal muscle repair. Bone 2006: 39: 678-683.
86. Kuo TF, Lin HC, Yang KC, Lin FH, Chen MH, Wu CC, Chang HH. Bone marrow combined with dental bud cells promotes tooth regeneration in miniature pig model. Artif Organs 2011: 35: 113-121.
87. Kuznetsov SA, Krebsbach PH, Satomura K, Kerr J, Riminucci M, Benayahu D, Robey PG. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997: 12: 1335-1347.
88. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG. Circulating skeletal stem cells. J Cell Biol 2001: 153: 1133-1140.
89. Laino G, d'Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G. A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 2005: 20: 1394-1402.
90. Lang H, Schuler N, Arnhold S, Nolden R, Mertens T. Formation of differentiated tissues in vivo by periodontal cell populations cultured in vitro. J Dent Res 1995: 74: 1219-1225.
91. Lang H, Schuler N, Nolden R. Attachment formation following replantation of cultured cells into periodontal defects - a study in minipigs. J Dent Res 1998: 77: 393-405.
92. Langeland K. Tissue response to dental caries. Endod Dent Traumatol 1987: 3: 149-171.
93. Larmas M. Response of pulpo-dentinal complex to caries attack. Proc Finn Dent Soc 1986: 82: 298-304.
94. Lekic PC, Rajshankar D, Chen H, Tenenbaum H, McCulloch CA. Transplantation of labeled periodontal ligament cells promotes regeneration of alveolar bone. Anat Rec 2001: 262: 193-202.
95. Li H, Yan F, Lei L, Li Y, Xiao Y. Application of autologous cryopreserved bone marrow mesenchymal stem cells for periodontal regeneration in dogs. Cells Tissues Organs 2009: 190: 94-101.
96. Li R, Guo W, Yang B, Guo L, Sheng L, Chen G, Li Y, Zou Q, Xie D, An X, Chen Y, Tian W. Human treated dentin matrix as a natural scaffold for complete human dentin tissue regeneration. Biomaterials 2011: 32: 4525-4538.
97. Lian Q, Lye E, Suan Yeo K, Khia Way Tan E, Salto-Tellez M, Liu TM, Palanisamy N, El Oakley RM, Lee EH, Lim B, Lim SK. Derivation of clinically compliant MSCs from CD105+, CD24- differentiated human ESCs. Stem Cells 2007: 25: 425-436.
98. Lian Q, Zhang Y, Zhang J, Zhang HK, Wu X, Lam FF, Kang S, Xia JC, Lai WH, Au KW, Chow YY, Siu CW, Lee CN, Tse HF. Functional mesenchymal stem cells derived from human induced pluripotent stem cells attenuate limb ischemia in mice. Circulation 2010: 121: 1113-1123.
99. Liu G, Zhao L, Zhang W, Cui L, Liu W, Cao Y. Repair of goat tibial defects with bone marrow stromal cells and beta-tricalcium phosphate. J Mater Sci Mater Med 2008: 19: 2367-2376.
100. Liu HW, Yacobi R, Savion N, Narayanan AS, Pitaru S. A collagenous cementum-derived attachment protein is a marker for progenitors of the mineralized tissue-forming cell lineage of the periodontal ligament. J Bone Miner Res 1997: 12: 1691-1699.
101. Liu X, Li X, Fan Y, Zhang G, Li D, Dong W, Sha Z, Yu X, Feng Q, Cui F, Watari F. Repairing goat tibia segmental bone defect using scaffold cultured with mesenchymal stem cells. J Biomed Mater Res B Appl Biomater 2010: 94: 44-52.
102. Liu Y, Zheng Y, Ding G, Fang D, Zhang C, Bartold PM, Gronthos S, Shi S, Wang S. Periodontal ligament stem cell-mediated treatment for periodontitis in miniature swine. Stem Cells 2008: 26: 1065-1073.
103. Marcacci M, Kon E, Zaffagnini S, Giardino R, Rocca M, Corsi A, Benvenuti A, Bianco P, Quarto R, Martin I, Muraglia A, Cancedda R. Reconstruction of extensive long-bone defects in sheep using porous hydroxyapatite sponges. Calcif Tissue Int 1999: 64: 83-90.
104. Martin GR. Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 1981: 78: 7634-7638.
105. McCulloch CA, Lekic P, McKee MD. Role of physical forces in regulating the form and function of the periodontal ligament. Periodontol 2000 2000: 24: 56-72.
106. McCulloch CA, Nemeth E, Lowenberg B, Melcher AH. Paravascular cells in endosteal spaces of alveolar bone contribute to periodontal ligament cell populations. Anat Rec 1987: 219: 233-242.
107. Menicanin D, Bartold PM, Zannettino AC, Gronthos S. Identification of a common gene expression signature associated with immature clonal mesenchymal cell populations derived from bone marrow and dental tissues. Stem Cells Dev 2010: 19: 1501-1510.
108. Miura M, Gronthos S, Zhao M, Lu B, Fisher LW, Robey PG, Shi S. SHED: stem cells from human exfoliated deciduous teeth. Proc Natl Acad Sci U S A 2003: 100: 5807-5812.
109. Miyoshi K, Tsuji D, Kudoh K, Satomura K, Muto T, Itoh K, Noma T. Generation of human induced pluripotent stem cells from oral mucosa. J Biosci Bioeng 2010: 110: 345-350.
110. Mjor IA, Fejerskov O. Human oral embryology and histology. Copenhagen: Munksgaard, 1986.
111. Modino SA, Sharpe PT. Tissue engineering of teeth using adult stem cells. Arch Oral Biol 2005: 50: 255-258.
112. Morsczeck C, Gotz W, Schierholz J, Zeilhofer F, Kuhn U, Mohl C, Sippel C, Hoffmann KH. Isolation of precursor cells (PCs) from human dental follicle of wisdom teeth. Matrix Biol 2005: 24: 155-165.
113. Mrugala D, Bony C, Neves N, Caillot L, Fabre S, Moukoko D, Jorgensen C, Noel D. Phenotypic and functional characterisation of ovine mesenchymal stem cells: application to a cartilage defect model. Ann Rheum Dis 2008: 67: 288-295.
114. Muraglia A, Martin I, Cancedda R, Quarto R. A nude mouse model for human bone formation in unloaded conditions. Bone 1998: 22: 131S-134S.
115. Murphy JM, Fink DJ, Hunziker EB, Barry FP. Stem cell therapy in a caprine model of osteoarthritis. Arthritis Rheum 2003: 48: 3464-3474.
116. Murphy WL, Mooney DJ. Controlled delivery of inductive proteins, plasmid DNA and cells from tissue engineering matrices. J Periodontal Res 1999: 34: 413-419.
117. Nakae H, Narayanan AS, Raines E, Page RC. Isolation and partial characterization of mitogenic factors from cementum. Biochemistry 1991: 30: 7047-7052.
118. Nakahara T, Nakamura T, Kobayashi E, Inoue M, Shigeno K, Tabata Y, Eto K, Shimizu Y. Novel approach to regeneration of periodontal tissues based on in situ tissue engineering: effects of controlled release of basic fibroblast growth factor from a sandwich membrane. Tissue Eng 2003: 9: 153-162.
119. Nakano T, Kodama H, Honjo T. Generation of lymphohematopoietic cells from embryonic stem cells in culture. Science 1994: 265: 1098-1101.
120. Nakashima M. Bone morphogenetic proteins in dentin regeneration for potential use in endodontic therapy. Cytokine Growth Factor Rev 2005: 16: 369-376.
121. Nakashima M, Akamine A. The application of tissue engineering to regeneration of pulp and dentin in endodontics. J Endod 2005: 31: 711-718.
122. Nakashima M, Reddi AH. The application of bone morphogenetic proteins to dental tissue engineering. Nat Biotechnol 2003: 21: 1025-1032.
123. Narayanan AS, Bartold PM. Biochemistry of periodontal connective tissues and their regeneration: a current perspective. Connect Tissue Res 1996: 34: 191-201.
124. Nishimura F, Iwamoto Y, Soga Y. The periodontal host response with diabetes. Periodontol 2000 2007: 43: 245-253.
125. Oda Y, Yoshimura Y, Ohnishi H, Tadokoro M, Katsube Y, Sasao M, Kubo Y, Hattori K, Saito S, Horimoto K, Yuba S, Ohgushi H. Induction of pluripotent stem cells from human third molar mesenchymal stromal cells. J Biol Chem 2010: 285: 29270-29278.
126. Olivier EN, Rybicki AC, Bouhassira EE. Differentiation of human embryonic stem cells into bipotent mesenchymal stem cells. Stem Cells 2006: 24: 1914-1922.
127. Owen GR, Jackson J, Chehroudi B, Burt H, Brunette DM. A PLGA membrane controlling cell behaviour for promoting tissue regeneration. Biomaterials 2005: 26: 7447-7456.
128. Park JY, Jeon SH, Choung PH. Efficacy of periodontal stem cell transplantation in the treatment of advanced periodontitis. Cell Transplant 2011: 20: 271-285.
129. Pereira RF, Halford KW, O'Hara MD, Leeper DB, Sokolov BP, Pollard MD, Bagasra O, Prockop DJ. Cultured adherent cells from marrow can serve as long-lasting precursor cells for bone, cartilage, and lung in irradiated mice. Proc Natl Acad Sci U S A 1995: 92: 4857-4861.
130. Petersen BE, Bowen WC, Patrene KD, Mars WM, Sullivan AK, Murase N, Boggs SS, Greenberger JS, Goff JP. Bone marrow as a potential source of hepatic oval cells. Science 1999: 284: 1168-1170.
131. Petite H, Viateau V, Bensaid W, Meunier A, de Pollak C, Bourguignon M, Oudina K, Sedel L, Guillemin G. Tissue-engineered bone regeneration. Nat Biotechnol 2000: 18: 959-963.
132. Pieri F, Lucarelli E, Corinaldesi G, Fini M, Aldini NN, Giardino R, Donati D, Marchetti C. Effect of mesenchymal stem cells and platelet-rich plasma on the healing of standardized bone defects in the alveolar ridge: a comparative histomorphometric study in minipigs. J Oral Maxillofac Surg 2009: 67: 265-272.
133. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005: 366: 1809-1820.
134. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR. Multilineage potential of adult human mesenchymal stem cells. Science 1999: 284: 143-147.
135. Pontoriero R, Lindhe J. Guided tissue regeneration in the treatment of degree III furcation defects in maxillary molars. J Clin Periodontol 1995: 22: 810-812.
136. Portmann-Lanz CB, Schoeberlein A, Huber A, Sager R, Malek A, Holzgreve W, Surbek DV. Placental mesenchymal stem cells as potential autologous graft for pre- and perinatal neuroregeneration. Am J Obstet Gynecol 2006: 194: 664-673.
137. Quarto R, Mastrogiacomo M, Cancedda R, Kutepov SM, Mukhachev V, Lavroukov A, Kon E, Marcacci M. Repair of large bone defects with the use of autologous bone marrow stromal cells. N Engl J Med 2001: 344: 385-386.
138. Sacchetti B, Funari A, Michienzi S, Di Cesare S, Piersanti S, Saggio I, Tagliafico E, Ferrari S, Robey PG, Riminucci M, Bianco P. Self-renewing osteoprogenitors in bone marrow sinusoids can organize a hematopoietic microenvironment. Cell 2007: 131: 324-336.
139. Sakai VT, Zhang Z, Dong Z, Neiva KG, Machado MA, Shi S, Santos CF, Nor JE. SHED differentiate into functional odontoblasts and endothelium. J Dent Res 2010: 89: 791-796.
140. Schroeder HE. Handbook of microscopic anatomy. Berlin: Springer-Verlag, 1986.
141. Seo BM, Miura M, Gronthos S, Bartold PM, Batouli S, Brahim J, Young M, Robey PG, Wang CY, Shi S. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004: 364: 149-155.
142. Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S. The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 2005: 8: 191-199.
143. Shi S, Gronthos S. Perivascular niche of postnatal mesenchymal stem cells in human bone marrow and dental pulp. J Bone Miner Res 2003: 18: 696-704.
144. Simsek SB, Keles GC, Baris S, Cetinkaya BO. Comparison of mesenchymal stem cells and autogenous cortical bone graft in the treatment of class II furcation defects in dogs. Clin Oral Investig 2012: 16: 251-258.
145. Smith JR, Pochampally R, Perry A, Hsu SC, Prockop DJ. Isolation of a highly clonogenic and multipotential subfraction of adult stem cells from bone marrow stroma. Stem Cells 2004: 22: 823-831.
146. Soncini M, Vertua E, Gibelli L, Zorzi F, Denegri M, Albertini A, Wengler GS, Parolini O. Isolation and characterization of mesenchymal cells from human fetal membranes. J Tissue Eng Regen Med 2007: 1: 296-305.
147. Sonoyama W, Liu Y, Fang D, Yamaza T, Seo BM, Zhang C, Liu H, Gronthos S, Wang CY, Wang S, Shi S. Mesenchymal stem cell-mediated functional tooth regeneration in swine. PLoS ONE 2006: 1: e79.
148. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT. Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 2008: 34: 166-171.
149. Srisuwan T, Tilkorn DJ, Wilson JL, Morrison WA, Messer HM, Thompson EW, Abberton KM. Molecular aspects of tissue engineering in the dental field. Periodontol 2000 2006: 41: 88-108.
150. Stanley HR. Human pulp response to restorative dental procedures. Gainesville: Storter Printing Company, 1981.
151. Suchanek J, Visek B, Soukup T, El-Din Mohamed SK, Ivancakova R, Mokry J, Aboul-Ezz EH, Omran A. Stem cells from human exfoliated deciduous teeth - isolation, long term cultivation and phenotypical analysis. Acta Medica (Hradec Kralove) 2010: 53: 93-99.
152. Takahashi K, Tanabe K, Ohnuki M, Narita M, Ichisaka T, Tomoda K, Yamanaka S. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell 2007: 131: 861-872.
153. Takahashi K, Yamanaka S. Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 2006: 126: 663-676.
154. Tamaoki N, Takahashi K, Tanaka T, Ichisaka T, Aoki H, Takeda-Kawaguchi T, Iida K, Kunisada T, Shibata T, Yamanaka S, Tezuka K. Dental pulp cells for induced pluripotent stem cell banking. J Dent Res 2010: 89: 773-778.
155. Tan Z, Zhao Q, Gong P, Wu Y, Wei N, Yuan Q, Wang C, Liao D, Tang H. Research on promoting periodontal regeneration with human basic fibroblast growth factor-modified bone marrow mesenchymal stromal cell gene therapy. Cytotherapy 2009: 11: 317-325.
156. Ten Cate Ar. Oral histology, development, structure and function. Toronto, ON: C.V. Mosby Company, 1989.
157. Thomson JA, Itskovitz-Eldor J, Shapiro SS, Waknitz MA, Swiergiel JJ, Marshall VS, Jones JM. Embryonic stem cell lines derived from human blastocysts. Science 1998: 282: 1145-1147.
158. Trowbridge HO. Pathogenesis of pulpitis resulting from dental caries. J Endod 1981: 7: 52-60.
159. Tsumanuma Y, Iwata T, Washio K, Yoshida T, Yamada A, Takagi R, Ohno T, Lin K, Yamato M, Ishikawa I, Okano T, Izumi Y. Comparison of different tissue-derived stem cell sheets for periodontal regeneration in a canine 1-wall defect model. Biomaterials 2011: 32: 5819-5825.
160. Viateau V, Guillemin G, Bousson V, Oudina K, Hannouche D, Sedel L, Logeart-Avramoglou D, Petite H. Long-bone critical-size defects treated with tissue-engineered grafts: a study on sheep. J Orthop Res 2007: 25: 741-749.
161. Vollner F, Ernst W, Driemel O, Morsczeck C. A two-step strategy for neuronal differentiation in vitro of human dental follicle cells. Differentiation 2009: 77: 433-441.
162. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S. Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 2009: 219: 667-676.
163. Wada N, Wang B, Lin NH, Laslett AL, Gronthos S, Bartold PM. Induced pluripotent stem cell lines derived from human gingival fibroblasts and periodontal ligament fibroblasts. J Periodontal Res 2011: 46: 438-447.
164. Wagner W, Wein F, Seckinger A, Frankhauser M, Wirkner U, Krause U, Blake J, Schwager C, Eckstein V, Ansorge W, Ho AD. Comparative characteristics of mesenchymal stem cells from human bone marrow, adipose tissue, and umbilical cord blood. Exp Hematol 2005: 33: 1402-1416.
165. Wallace SC, Gellin RG, Miller MC, Mishkin DJ. Guided tissue regeneration with and without decalcified freeze-dried bone in mandibular Class II furcation invasions. J Periodontol 1994: 65: 244-254.
166. Wang J, Wang X, Sun Z, Yang H, Shi S, Wang S. Stem cells from human-exfoliated deciduous teeth can differentiate into dopaminergic neuron-like cells. Stem Cells Dev 2010: 19: 1375-1383.
167. Wei N, Gong P, Liao D, Yang X, Li X, Liu Y, Yuan Q, Tan Z. Auto-transplanted mesenchymal stromal cell fate in periodontal tissue of beagle dogs. Cytotherapy 2010: 12: 514-521.
168. Woodbury D, Schwarz EJ, Prockop DJ, Black IB. Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 2000: 61: 364-370.
169. Xiong X, Buekens P, Fraser WD, Beck J, Offenbacher S. Periodontal disease and adverse pregnancy outcomes: a systematic review. BJOG 2006: 113: 135-143.
170. 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 Transplant 2011: 20: 1003-1013.
171. Yamada Y, Ueda M, Naiki T, Takahashi M, Hata K, Nagasaka T. Autogenous injectable bone for regeneration with mesenchymal stem cells and platelet-rich plasma: tissue-engineered bone regeneration. Tissue Eng 2004: 10: 955-964.
172. Yan X, Qin H, Qu C, Tuan RS, Shi S, Huang GT. iPS cells reprogrammed from human mesenchymal-like stem/progenitor cells of dental tissue origin. Stem Cells Dev 2010: 19: 469-480.
173. Yang Y, Rossi FM, Putnins EE. Periodontal regeneration using engineered bone marrow mesenchymal stromal cells. Biomaterials 2010: 31: 8574-8582.
174. Yao S, Pan F, Prpic V, Wise GE. Differentiation of stem cells in the dental follicle. J Dent Res 2008: 87: 767-771.
175. Yokoi T, Saito M, Kiyono T, Iseki S, Kosaka K, Nishida E, Tsubakimoto T, Harada H, Eto K, Noguchi T, Teranaka T. Establishment of immortalized dental follicle cells for generating periodontal ligament in vivo. Cell Tissue Res 2007: 327: 301-311.
176. Young HE, Steele TA, Bray RA, Hudson J, Floyd JA, Hawkins K, Thomas K, Austin T, Edwards C, Cuzzourt J, Duenzl M, Lucas PA, Black AC Jr. Human reserve pluripotent mesenchymal stem cells are present in the connective tissues of skeletal muscle and dermis derived from fetal, adult, and geriatric donors. Anat Rec 2001: 264: 51-62.
177. 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. Induced pluripotent stem cell lines derived from human somatic cells. Science 2007: 318: 1917-1920.
178. Yuan J, Cui L, Zhang WJ, Liu W, Cao Y. Repair of canine mandibular bone defects with bone marrow stromal cells and porous beta-tricalcium phosphate. Biomaterials 2007: 28: 1005-1013.
179. Zannettino AC, Paton S, Arthur A, Khor F, Itescu S, Gimble JM, Gronthos S. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008: 214: 413-421.
180. Zhang W, Walboomers XF, Van Kuppevelt TH, Daamen WF, Van Damme PA, Bian Z, Jansen JA. In vivo evaluation of human dental pulp stem cells differentiated towards multiple lineages. J Tissue Eng Regen Med 2008: 2: 117-125.
181. Zheng Y, Liu Y, Zhang CM, Zhang HY, Li WH, Shi S, Le AD, Wang SL. Stem cells from deciduous tooth repair mandibular defect in swine. J Dent Res 2009: 88: 249-254.
182. Zhu L, Liu W, Cui L, Cao Y. Tissue-engineered bone repair of goat-femur defects with osteogenically induced bone marrow stromal cells. Tissue Eng 2006: 12: 423-433.