Stem cells and periodontal regeneration

Australian Dental Journal

Volumn 53, Issue 2, 2008, Pages 108-121

  Lin, N H ^a   Gronthos, S ^b   Bartold, P M ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b INSTITUTE OF MEDICAL AND VETERINARY SCIENCE   (Australia)

Author keywords

Mesenchymal stem cells; Periodontal ligament stem cells; Periodontal regeneration

Indexed keywords

ADULT STEM CELL; HUMAN; METHODOLOGY; PERIODONTICS; PERIODONTITIS; PERIODONTIUM; PHYSIOLOGY; REGENERATION; REVIEW; TISSUE ENGINEERING;

ADULT STEM CELLS; GUIDED TISSUE REGENERATION, PERIODONTAL; HUMANS; PERIODONTITIS; PERIODONTIUM; REGENERATION; TISSUE ENGINEERING;

EID: 44249100452     PISSN: 00450421     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1834-7819.2008.00019.x     Document Type: Review

References (134)

1. Pihlstrom BL, Michalowicz BS, Johnson NW. Periodontal diseases. Lancet 2005 366: 1809 1820.
2. Polimeni G, Xiropaidis AV, Wikesjo UM. Biology and principles of periodontal wound healing/regeneration. Periodontol 2000 2006 41: 30 47.
3. Rosling B, Nyman S, Lindhe J, Jern B. The healing potential of the periodontal tissues following different techniques of periodontal surgery in plaque-free dentitions. A 2-year clinical study. J Clin Periodontol 1976 3: 233 250.
4. Caton J, Nyman S, Zander H. Histometric evaluation of periodontal surgery. II. Connective tissue attachment levels after four regenerative procedures. J Clin Periodontol 1980 7: 224 231.
5. Sander L, Karring T. Healing of periodontal lesions in monkeys following the guided tissue regeneration procedure. A histological study. J Clin Periodontol 1995 22: 332 337.
6. Xiao Y, Parry DA, Li H, Arnold R, Jackson WJ, Bartold PM. Expression of extracellular matrix macromolecules around demineralized freeze-dried bone allografts. J Periodontol 1996 67: 1233 1244.
7. Ripamonti U, Reddi AH. Tissue engineering, morphogenesis, and regeneration of the periodontal tissues by bone morphogenetic proteins. Crit Rev Oral Biol Med 1997 8: 154 163.
8. Stavropoulos A, Kostopoulos L, Nyengaard JR, Karring T. Deproteinized bovine bone (Bio-Oss) and bioactive glass (Biogran) arrest bone formation when used as an adjunct to guided tissue regeneration (GTR): an experimental study in the rat. J Clin Periodontol 2003 30: 636 643.
9. Venezia E, Goldstein M, Boyan BD, Schwartz Z. The use of enamel matrix derivative in the treatment of periodontal defects: a literature review and meta-analysis. Crit Rev Oral Biol Med 2004 15: 382 402.
10. Seo BM, Miura M, Gronthos S, et al. Investigation of multipotent postnatal stem cells from human periodontal ligament. Lancet 2004 364: 149 155.
11. Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontol 2000 2006 40: 164 172.
12. Smith A. A glossary for stem-cell biology. Nature 2006 441: 1060.
13. Morrison SJ, Shah NM, Anderson DJ. Regulatory mechanisms in stem cell biology. Cell 1997 88: 287 298.
14. Vats A, Bielby RC, Tolley NS, Nerem R, Polak JM. Stem cells. Lancet 2005 366:592 602.
15. Pera MF, Cooper S, Mills J, Parrington JM. Isolation and characterisation of a multipotent clone of human embryonal carcinoma-cells. Differentiation 1989 42:10 23.
16. Thomson JA, Itskovitz-Eldor J, Shapiro SS, et al. Embryonic stem cell lines derived from human blastocysts. Science 1998 282:1145 1147.
17. Shamblott MJ, Axelman J, Wang S, et al. Derivation of pluripotent stem cells from cultured human primordial germ cells. Proc Natl Acad Sci USA 1998 95:13726 13731.
18. Baum CM, Weissman IL, Tsukamoto AS, Buckle AM, Peault B. Isolation of a candidate human hematopoietic stem-cell population. Proc Natl Acad Sci USA 1992 89:2804 2808.
19. Slack JM. Stem cells in epithelial tissues. Science 2000 287:1431 1433.
20. Uchida N, Buck DW, He D, et al. Direct isolation of human central nervous system stem cells. Proc Natl Acad Sci USA 2000 97:14720 14725.
21. Becker AJ, McCulloch EA, Till JE. Cytological demonstration of the clonal nature of spleen colonies derived from transplanted mouse marrow cells. Nature 1963 197:452 454.
22. Friedenstein AJ, Petrakova KV, Kurolesova AI, Frolova GP. Heterotopic of bone marrow. Analysis of precursor cells for osteogenic and hematopoietic tissues. Transplantation 1968 6:230 247.
23. Castro-Malaspina H, Gay RE, Resnick G, et al. Characterization of human bone marrow fibroblast colony-forming cells (CFU-F) and their progeny. Blood 1980 56:289 301.
24. Caplan AI. Mesenchymal stem cells. J Orthop Res 1991 9:641 650.
25. Pittenger MF, Mackay AM, Beck SC, et al. Multilineage potential of adult human mesenchymal stem cells. Science 1999 284:143 147.
26. Gronthos S, Zannettino AC, Hay SJ, et al. Molecular and cellular characterisation of highly purified stromal stem cells derived from human bone marrow. J Cell Sci 2003 116:1827 1835.
27. Wexler SA, Donaldson C, Denning-Kendall P, Rice C, Bradley B, Hows JM. Adult bone marrow is a rich source of human mesenchymal 'stem' cells but umbilical cord and mobilized adult blood are not. Br J Haematol 2003 121:368 374.
28. Baroffio A, Hamann M, Bernheim L, Bochaton-Piallat ML, Gabbiani G, Bader CR. Identification of self-renewing myoblasts in the progeny of single human muscle satellite cells. Differentiation 1996 60:47 57.
29. Campagnoli C, Roberts IA, Kumar S, Bennett PR, Bellantuono I, Fisk NM. Identification of mesenchymal stem/progenitor cells in human first-trimester fetal blood, liver, and bone marrow. Blood 2001 98:2396 2402.
30. Zwaka TP. Use of genetically modified stem cells in experimental gene therapies. In: Regenerative medicine 2006. National Institutes of Health. Bethesda:Department of Health and Human Services, 2006:45 52.
31. Hu Y, Liao L, Wang Q, et al. Isolation and identification of mesenchymal stem cells from human fetal pancreas. J Lab Clin Med 2003 141:342 349.
32. Kuznetsov SA, Mankani MH, Gronthos S, Satomura K, Bianco P, Robey PG. Circulating skeletal stem cells. J Cell Biol 2001 153:1133 1140.
33. Zannettino AC, Paton S, Arthur A, et al. Multipotential human adipose-derived stromal stem cells exhibit a perivascular phenotype in vitro and in vivo. J Cell Physiol 2008 214:413 421.
34. 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.
35. Collett GD, Canfield AE. Angiogenesis and pericytes in the initiation of ectopic calcification. Circ Res 2005 96:930 938.
36. Prockop DJ, Sekiya I, Colter DC. Isolation and characterization of rapidly self-renewing stem cells from cultures of human marrow stromal cells. Cytotherapy 2001 3:393 396.
37. Reyes M, Lund T, Lenvik T, Aguiar D, Koodie L, Verfaillie CM. Purification and ex vivo expansion of postnatal human marrow mesodermal progenitor cells. Blood 2001 98:2615 2625.
38. Gronthos S, Simmons PJ. The growth factor requirements of STRO-1-positive human bone marrow stromal precursors under serum-deprived conditions in vitro. Blood 1995 85:929 940.
39. Friedenstein AJ, Ivanov-Smolenski AA, Chajlakjan RK, et al. Origin of bone marrow stromal mechanocytes in radiochimeras and heterotopic transplants. Exp Hematol 1978 6:440 444.
40. Owen ME, Cave J, Joyner CJ. Clonal analysis in vitro of osteogenic differentiation of marrow CFU-F. J Cell Sci 1987 87:731 738.
41. Bennett JH, Joyner CJ, Triffitt JT, Owen ME. Adipocytic cells cultured from marrow have osteogenic potential. J Cell Sci 1999 99:131 139.
42. Kuznetsov SA, Krebsbach PH, Satomura K, et al. Single-colony derived strains of human marrow stromal fibroblasts form bone after transplantation in vivo. J Bone Miner Res 1997 12:1335 1347.
43. Muraglia A, Cancedda R, Quarto R. Clonal mesenchymal progenitors from human bone marrow differentiate in vitro according to a hierarchical model. J Cell Sci 2000 113:1161 1166.
44. Prockop DJ. Marrow stromal cells as stem cells for nonhematopoietic tissues. Science 1997 276:71 74.
45. Narayanan AS, Bartold PM. Biochemistry of periodontal connective tissues and their regeneration: a current perspective. Connect Tissue Res 1996 34:191 201.
46. MacNeil RL, Somerman MJ. Development and regeneration of the periodontium: parallels and contrasts. Periodontol 2000 1999 19:8 20.
47. Lindskog S. Formation of intermediate cementum. I: early mineralization of aprismatic enamel and intermediate cementum in monkey. J Craniofac Genet Dev Biol 1982 2:147 160.
48. Slavkin HC, Bringas P Jr., Bessem C, et al. Hertwig's epithelial root sheath differentiation and initial cementum and bone formation during long-term organ culture of mouse mandibular first molars using serumless, chemically-defined medium. J Periodont Res 1989 24:28 40.
49. MacNeil RL, Thomas HF. Development of the murine periodontium. II. Role of the epithelial root sheath in formation of the periodontal attachment. J Periodontol 1993 64:285 291.
50. Hammarstrom L, Alatli I, Fong CD. Origins of cementum. Oral Dis 1996 2:63 69.
51. Yamamoto T, Hinrichsen KV. The development of cellular cementum in rat molars, with special reference to the fiber arrangement. Anat Embryol (Berl) 1993 188:537 549.
52. Yamamoto T, Domon T, Takahashi S, Wakita M. Comparative study of the initial genesis of acellular and cellular cementum in rat molars. Anat Embryol (Berl) 1994 190:521 527.
53. Ten Cate A. Formation of supporting bone in association with periodontal ligament organisation in the mouse. Arch Oral Biol 1975 20:137 138.
54. Ten Cate AR. The role of epithelium in the development, structure and function of the tissues of tooth support. Oral Dis 1996 2:55 62.
55. Clark R. The molecular and cellular biology of wound repair. 2nd edn. New York:Plenum, 1996.
56. Wikesjo UM, Crigger M, Nilveus R, Selvig KA. Early healing events at the dentin-connective tissue interface. Light and transmission electron microscopy observations. J Periodontol 1991 62:5 14.
57. Wang HL, Greenwell H, Fiorellini J, et al. Periodontal regeneration (American Academy of Periodontology Position Paper). J Periodontol 2005 76:1601 1622.
58. 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.
59. Aukhil I. Biology of wound healing. Periodontol 2000 2000 22:44 50.
60. Thesleff I, Nieminen P. Tooth morphogenesis and cell differentiation. Curr Opin Cell Biol 1996 8:844 850.
61. Gould TR, Melcher AH, Brunette DM. Migration and division of progenitor cell populations in periodontal ligament after wounding. J Periodont Res 1980 15:20 42.
62. Gould TR. Ultrastructural characteristics of progenitor cell populations in the periodontal ligament. J Dent Res 1983 62:873 876.
63. Lin WL, McCulloch CA, Cho MI. Differentiation of periodontal ligament fibroblasts into osteoblasts during socket healing after tooth extraction in the rat. Anat Rec 1994 240:492 506.
64. McCulloch CA, Melcher AH. Cell migration in the periodontal ligament of mice. J Periodont Res 1983 18:339 352.
65. Chen SC, Marino V, Gronthos S, Bartold PM. Location of putative stem cells in human periodontal ligament. J Periodont Res 2006 41:547 553.
66. Melcher AH, Cheong T, Cox J, Nemeth E, Shiga A. Synthesis of cementum-like tissue in vitro by cells cultured from bone: a light and electron microscope study. J Periodont Res 1986 21:592 612.
67. 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.
68. Seo BM, Miura M, Sonoyama W, Coppe C, Stanyon R, Shi S. Recovery of stem cells from cryopreserved periodontal ligament. J Dent Res 2005 84:907 912.
69. Nagatomo K, Komaki M, Sekiya I, et al. Stem cell properties of human periodontal ligament cells. J Periodontal Res 2006 41:303 310.
70. 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.
71. Jo YY, Lee HJ, Kook SY, et al. Isolation and characterization of postnatal stem cells from human dental tissues. Tissue Eng 2007 13:767 773.
72. Smith B, Cafesse R, Nasjleti C, Kon S, Castelli W. Effects of citric acid, and fibronectin and laminin application in treating periodontitis. J Clin Periodontol 1987 14:396 402.
73. Dreyer WP, van Heerden JD. The effect of citric acid on the healing of periodontal ligament-free, healthy roots, horizontally implanted against bone and gingival connective tissue. J Periodont Res 1986 21:210 220.
74. 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.
75. Karring T, Nyman S, Lindhe J. Healing following implantation of periodontitis affected roots into bone tissue. J Clin Periodontol 1980 7:96 105.
76. Nyman S, Karring T, Lindhe J, Planten S. Healing following implantation of periodontitis-affected roots into gingival connective tissue. J Clin Periodontol 1980 7:394 401.
77. Nyman S, Gottlow J, Karring T, Lindhe J. The regenerative potential of the periodontal ligament. An experimental study in the monkey. J Clin Periodontol 1982 9:257 265.
78. Nyman S, Lindhe J, Karring T, Rylander H. New attachment following surgical treatment of human periodontal disease. J Clin Periodontol 1982 9:290 296.
79. Gottlow J. Guided tissue regeneration using bioresorbable and non-resorbable devices: initial healing and long-term results. J Periodontol 1993 64:1157 1165.
80. Scantlebury TV. 1982-1992: a decade of technology development for guided tissue regeneration. J Periodontol 1993 64:1129 1137.
81. Lundgren D, Laurell L, Gottlow J, et al. The influence of the design of two different bioresorbable barriers on the results of guided tissue regeneration therapy. An intra-individual comparative study in the monkey. J Periodontol 1995 66:605 612.
82. Magnusson I, Batich C, Collins BR. New attachment formation following controlled tissue regeneration using biodegradable membranes. J Periodontol 1988 59:1 6.
83. Kwan SK, Lekovic V, Camargo PM, et al. The use of autogenous periosteal grafts as barriers for the treatment of intrabony defects in humans. J Periodontol 1998 69:1203 1209.
84. Haney JM, Nilveus RE, McMillan PJ, Wikesjo UM. Periodontal repair in dogs: expanded polytetrafluoroethylene barrier membranes support wound stabilization and enhance bone regeneration. J Periodontol 1993 64:883 890.
85. Karring T, Cortellini P. Regenerative therapy: furcation defects. Periodontol 2000 1999 19:115 137.
86. Needleman IG, Worthington HV, Giedrys-Leeper E, Tucker RJ. Guided tissue regeneration for periodontal infra-bony defects. Cochrane Database Syst Rev CD001724. 2006.
87. Lynch SE, de Castilla GR, Williams RC, et al. The effects of short-term application of a combination of platelet-derived and insulin-like growth factors on periodontal wound healing. J Periodontol 1991 62:458 467.
88. Rutherford RB, Ryan ME, Kennedy JE, Tucker MM, Charette MF. Platelet-derived growth factor and dexamethasone combined with a collagen matrix induce regeneration of the periodontium in monkeys. J Clin Periodontol 1993 20:537 544.
89. Ripamonti U, Reddi AH. Periodontal regeneration: potential role of bone morphogenetic proteins. J Periodont Res 1994 29:225 235.
90. Ten Cate AR. The role of epithelium in the development, structure and function of the tissues of tooth support. Oral Diseases 1996 2:55 62.
91. Hammarström L. Enamel matrix, cementum development and regeneration. J Clin Periodontol 1997 24:658 668.
92. Venezia E, Goldstein M, Boyan BD, Schwartz Z. The use of enamel matrix derivative in the treatment of periodontal defects: a literature review and meta-analysis. Crit Rev Oral Biol Med 2004 15:382 402.
93. Gestrelius S, Andersson C, Lidstrom D, Hammarstrom L, Somerman M. In vitro studies on periodontal ligament cells and enamel matrix derivative. J Clin Periodontol 1997 24:685 692.
94. Van der Pauw MT, Van den Bos T, Everts V, Beertsen W. Enamel matrix-derived protein stimulates attachment of periodontal ligament fibroblasts and enhances alkaline phosphate actvity and transforming growth factor beta1 release of periodontal ligament and gingival fibroblasts. J Periodontol 2000 71:31 43.
95. Haase HR, Bartold PM. Enamel matrix derivative induces matrix synthesis by cultured human periodontal fibroblast cells. J Periodontol 2001 72:341 348.
96. Melcher AH. Cells of the periodontium: their role in the healing of wounds. Ann R Coll Surg Engl 1985 67:130 131.
97. Pitaru S, McCulloch CA, Narayanan SA. Cellular origins and differentiation control mechanisms during periodontal development and wound healing. J Periodont Res 1994 29:81 94.
98. McCulloch CA. Progenitor cell populations in the periodontal ligament of mice. Anat Rec 1985 211:258 262.
99. Lekic P, McCulloch CA. Periodontal ligament cell population: the central role of fibroblasts in creating a unique tissue. Anat Rec 1996 245:327 341.
100. 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.
101. 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 USA 2000 97:13625 13630.
102. Trubiani O, Di Primio R, Traini T, et al. Morphological and cytofluorimetric analysis of adult mesenchymal stem cells expanded ex vivo from periodontal ligament. Int J Immunopathol Pharmacol 2005 18:213 221.
103. Ivanovski S, Haase HR, Bartold PM. Isolation and characterisation of fibroblasts derived from regenerating human periodontal defects. Arch Oral Biol 2001 46:679 688.
104. Luan X, Ito Y, Dangaria S, Diekwisch TG. Dental follicle progenitor cell heterogeneity in the developing mouse periodontium. Stem Cells Dev 2006 15:595 608.
105. Techawattanawisal W, Nakahama K, Komaki M, Abe M, Takagi Y, Morita I. Isolation of multipotent stem cells from adult rat periodontal ligament by neurosphere-forming culture system. Biochem Biophys Res Commun 2007 357:917 923.
106. Vacanti CA, Langer R, Schloo B, Vacanti JP. Synthetic polymers seeded with chondrocytes provide a template for new cartilage formation. Plast Reconstr Surg 1991 88:753 759.
107. Narem R, Sambanis A. Tissue engineering: from biology to biological structures. Tissue Eng 1995 1:3 13.
108. Brekke JH, Toth JM. Principles of tissue engineering applied to programmable osteogenesis. J Biomed Mater Res 1998 43:380 398.
109. Whang K, Healy KE, Elenz DR, et al. Engineering bone regeneration with bioabsorbable scaffolds with novel microarchitecture. Tissue Eng 1999 5:35 51.
110. Vanheusden AJ, Goffinet G, Zahedi S, Nusgens B, Lapiere CM, Rompen EH. In vitro stimulation of human gingival epithelial cell attachment to dentin by surface conditioning. J Periodontol 1999 70:594 603.
111. van Dijk LJ, Schakenraad JM, van der Voort HM, Herkstroter FM, Busscher HJ. Cell-seeding of periodontal ligament fibroblasts. A novel technique to create new attachment. A pilot study. J Clin Periodontol 1991 18:196 199.
112. 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.
113. Kawaguchi H, Hirachi A, Hasegawa N, et al. Enhancement of periodontal tissue regeneration by transplantation of bone marrow mesenchymal stem cells. J Periodontol 2004 75:1281 1287.
114. Sonoyama W, Liu Y, Fang D, et al. Mesenchymal stem cell-mediated functional tooth regeneration in Swine. PLoS ONE. 2006 1:e79.
115. Ramseier CA, Abramson ZR, Jin Q, Giannobile WV. Gene therapeutics for periodontal regenerative medicine. Dent Clin North Am 2006 50:245 263.
116. Anusaksathien O, Webb SA, Jin QM, Giannobile WV. Platelet-derived growth factor gene delivery stimulates ex vivo gingival repair. Tissue Eng 2003 9:745 756.
117. Jin QM, Anusaksathien O, Webb SA, Rutherford RB, Giannobile WV. Gene therapy of bone morphogenetic protein for periodontal tissue engineering. J Periodontol 2003 74:202 213.
118. Jin Q, Anusaksathien O, Webb SA, Printz MA, Giannobile WV. Engineering of tooth-supporting structures by delivery of PDGF gene therapy vectors. Mol Ther 2004 9:519 526.
119. Dunn CA, Jin Q, Taba M. Jr., Franceschi RT, Rutherford RB, Giannobile WV. BMP gene delivery for alveolar bone engineering at dental implant defects. Mol Ther 2005 11:294 299.
120. Imperiale MJ, Kochanek S. Adenovirus vectors: biology, design, and production. Curr Top Microbiol Immunol 2004 273:335 357.
121. Brivanlou AH, Gage FH, Jaenisch R, Jessell T, Melton D, Rossant J. Stem cells. Setting standards for human embryonic stem cells. Science 2003 300:913 916.
122. King GN, King N, Cruchley AT, Wozney JM, Hughes FJ. Recombinant human bone morphogenetic protein-2 promotes wound healing in rat periodontal fenestration defects. J Dent Res 1997 76:1460 1470.
123. Bhatnagar RS, Qian JJ, Wedrychowska A, Sadeghi M, Wu YM, Smith N. Design of biomimetic habitats for tissue engineering with P-15, a synthetic peptide analogue of collagen. Tissue Eng 1999 5:53 65.
124. Jin QM, Zhao M, Webb SA, Berry JE, Somerman MJ, Giannobile WV. Cementum engineering with three-dimensional polymer scaffolds. J Biomed Mater Res A 2003 67:54 60.
125. Zhao M, Jin Q, Berry JE, Nociti FH Jr., Giannobile WV, Somerman MJ. Cementoblast delivery for periodontal tissue engineering. J Periodontol 2004 75:154 161.
126. Ripamonti U, Crooks J, Petit JC, Rueger DC. Periodontal tissue regeneration by combined applications of recombinant human osteogenic protein-1 and bone morphogenetic protein-2. A pilot study in Chacma baboons (Papio ursinus). Eur J Oral Sci 2001 109:241 248.
127. Maitra A, Arking DE, Shivapurkar N, et al. Genomic alterations in cultured human embryonic stem cells. Nat Genet 2005 37:1099 1103.
128. Martin MJ, Muotri A, Gage FH, Varki A. Human embryonic stem cells express an immunogenic nonhuman sialic acid. Nat Med 2005 11:228 232.
129. Draper JS, Pigott C, Thomson JA, Andrews PW. Surface antigens of human embryonic stem cells: changes upon differentiation in culture. J Anat 2002 200:249 258.
130. Bradley JA, Bolton EM, Pedersen RA. Stem cell medicine encounters the immune system. Nat Rev Immunol 2002 2:859 871.
131. Ivanovski S, Gronthos S, Shi S, Bartold PM. Stem cells in the periodontal ligament. Oral Dis 2006 12:358 363.
132. Nasef A, Mathieu N, Chapel A, et al. Immunosuppressive effects of mesenchymal stem cells: involvement of HLA-G. Transplantation 2007 84:231 237.
133. Yu J, Thomson JA. Embryonic stem cells. In: Regenerative medicine 2006. National Institutes of Health. Bethesda:Department of Health and Human Services, 2006:1 12.
134. Deans RJ, Moseley AB. Mesenchymal stem cells: biology and potential clinical uses. Exp Hematol 2000 28:875 884.