Role Of The Epithelial Cell Rests Of Malassez In The Development, Maintenance And Regeneration Of Periodontal Ligament Tissues

Periodontology 2000

Volumn 63, Issue 1, 2013, Pages 217-233

  Xiong, Jimin ^a   Gronthos, Stan ^a   Bartold, P Mark ^a  

^a NONE

Author keywords

[No Author keywords available]

Indexed keywords

ANIMAL; CYTOLOGY; EPITHELIUM CELL; GROWTH, DEVELOPMENT AND AGING; HOMEOSTASIS; HUMAN; MESENCHYMAL STROMA CELL; PERIODONTAL LIGAMENT; PHYSIOLOGY; REGENERATION; TOOTH DEVELOPMENT; TOOTH PAPILLA; TOOTH ROOT; TOOTH SAC;

ANIMALS; CEMENTOGENESIS; DENTAL PAPILLA; DENTAL SAC; DENTINOGENESIS; EPITHELIAL CELLS; HOMEOSTASIS; HUMANS; MESENCHYMAL STROMAL CELLS; ODONTOGENESIS; PERIODONTAL LIGAMENT; REGENERATION; TOOTH ROOT;

EID: 84881500080     PISSN: 09066713     EISSN: 16000757     Source Type: Journal    
DOI: 10.1111/prd.12023     Document Type: Article

References (128)

1. Aasen T, Raya A, Barrero MJ, Garreta E, Consiglio A, Gonzalez F, Vassena R, Bilic J, Pekarik V, Tiscornia G, Edel M, Boue S, Izpisua Belmonte JC. Efficient and rapid generation of induced pluripotent stem cells from human keratinocytes. Nat Biotechnol 2008: 26: 1276-1284.
2. Alatli I, Lundmark C, Hammarstrom L. The localization of epithelial root sheath cells during cementum formation in rat molars. J Periodontal Res 1996: 31: 433-440.
3. Alongi DJ, Yamaza T, Song Y, Fouad AF, Romberg EE, Shi S, Tuan RS, Huang GT. Stem/progenitor cells from inflamed human dental pulp retain tissue regeneration potential. Regen Med 2010: 5: 617-631.
4. Bacigalupo A, Frassoni F, Van Lint MT. Bone marrow or peripheral blood as a source of stem cells for allogeneic transplants. Curr Opin Hematol 2000: 7: 343-347.
5. Bai Y, Matsuzaka K, Hashimoto S, Fukuyama T, Wu L, Miwa T, Liu X, Wang X, Inoue T. Cementum- and periodontal ligament-like tissue formation by dental follicle cell sheets co-cultured with the Hertwig's epithelial root sheath cells. Bone 2011: 48: 1417-1426.
6. Bartold PM, Narayanan AS. Composition of the extracellular matrix. In: Bartold PM, Narayanan AS, editors. Biology of periodontal connective tissues. Carol Stream, IL: Quintessence Publications, Inc., 1998: 151-172.
7. Bartold PM, Shi S, Gronthos S. Stem cells and periodontal regeneration. Periodontol 2000 2006: 40: 164-172.
8. Beck F, Tucci J, Russell A, Senior PV, Ferguson MW. The expression of the gene coding for parathyroid hormone-related protein (PTHrP) during tooth development in the rat. Cell Tissue Res 1995: 280: 283-290.
9. Beertsen W, McCulloch CA, Sodek J. The periodontal ligament: a unique, multifunctional connective tissue. Periodontol 2000 1997: 13: 20-40.
10. Bonewald LF, Harris SE, Rosser J, Dallas MR, Dallas SL, Camacho NP, Boyan B, Boskey A. von Kossa staining alone is not sufficient to confirm that mineralization in vitro represents bone formation. Calcif Tissue Int 2003: 72: 537-547.
11. Bosshardt DD, Schroeder HE. Cementogenesis reviewed: a comparison between human premolars and rodent molars. Anat Rec 1996: 245: 267-292.
12. Bosshardt DD, Selvig KA. Dental cementum: the dynamic tissue covering of the root. Periodontol 2000 1997: 13: 41-75.
13. Bosshardt DD, Nanci A. Immunolocalization of epithelial and mesenchymal matrix constituents in association with inner enamel epithelial cells. J Histochem Cytochem 1998: 46: 135-142.
14. Bosshardt DD, Zalzal S, McKee MD, Nanci A. Developmental appearance and distribution of bone sialoprotein and osteopontin in human and rat cementum. Anat Rec 1998: 250: 13-33.
15. Bosshardt DD, Nanci A. The Hertwig's epithelial root sheath, enamel matrix proteins, and initiation of cementogenesis in porcine teeth. J Clin Periodontol 2004: 31: 184-192.
16. Bosshardt DD. Are cementoblasts a subpopulation of osteoblasts or a unique phenotype? J Dent Res 2005: 84: 390-406.
17. Bosshardt DD. Biological mediators and periodontal regeneration: a review of enamel matrix proteins at the cellular and molecular levels. J Clin Periodontol 2008: 35: 87-105.
18. Brice GL, Sampson WJ, Sims MR. An ultrastructural evaluation of the relationship between epithelial rests of Malassez and orthodontic root resorption and repair in man. Aust Orthod J 1991: 12: 90-94.
19. Bronckers AL, Farach-Carson MC, Van Waveren E, Butler WT. Immunolocalization of osteopontin, osteocalcin, and dentin sialoprotein during dental root formation and early cementogenesis in the rat. J Bone Miner Res 1994: 9: 833-841.
20. Brookes SJ, Robinson C, Kirkham J, Bonass WA. Biochemistry and molecular biology of amelogenin proteins of developing dental enamel. Arch Oral Biol 1995: 40: 1-14.
21. Brunette DM, Melcher AH, Moe HK. Culture and origin of epithelium-like and fibroblast-like cells from porcine periodontal ligament explants and cell suspensions. Arch Oral Biol 1976: 21: 393-400.
22. Buckner CD. Autologous bone marrow transplants to hematopoietic stem cell support with peripheral blood stem cells: a historical perspective. J Hematother 1999: 8: 233-236.
23. Cerri PS, Freymuller E, Katchburian E. Apoptosis in the early developing periodontium of rat molars. Anat Rec 2000: 258: 136-144.
24. Cerri PS, Katchburian E. Apoptosis in the epithelial cells of the rests of Malassez of the periodontium of rat molars. J Periodontal Res 2005: 40: 365-372.
25. Cho MI, Garant PR. Ultrastructural evidence of directed cell migration during initial cementoblast differentiation in root formation. J Periodontal Res 1988: 23: 268-276.
26. Cho MI, Garant PR. Radioautographic study of [3H]mannose utilization during cementoblast differentiation, formation of acellular cementum, and development of periodontal ligament principal fibers. Anat Rec 1989: 223: 209-222.
27. Cho MI, Lin WL, Garant PR. Occurrence of epidermal growth factor-binding sites during differentiation of cementoblasts and periodontal ligament fibroblasts of the young rat: a light and electron microscopic radioautographic study. Anat Rec 1991: 231: 14-24.
28. Cortellini P, Tonetti MS. 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 2011: 38: 365-373.
29. Diekwisch TG. The developmental biology of cementum. Int J Dev Biol 2001: 45: 695-706.
30. Fleischmannova J, Matalova E, Sharpe PT, Misek I, Radlanski RJ. Formation of the tooth-bone interface. J Dent Res 2010: 89: 108-115.
31. Fong CD, Hammarstrom L. Expression of amelin and amelogenin in epithelial root sheath remnants of fully formed rat molars. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2000: 90: 218-223.
32. Fujiyama K, Yamashiro T, Fukunaga T, Balam TA, Zheng L, Takano-Yamamoto T. Denervation resulting in dento-alveolar ankylosis associated with decreased Malassez epithelium. J Dent Res 2004: 83: 625-629.
33. Greenwell H. Position paper: guidelines for periodontal therapy. J Periodontol 2001: 72: 1624-1628.
34. 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.
35. Hamamoto Y, Nakajima T, Ozawa H, Uchida T. Production of amelogenin by enamel epithelium of the Hertwig's root sheath. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 1996: 81: 703-709.
36. Hammarstrom L, Alatli I, Fong CD. Origins of cementum. Oral Dis 1996: 2: 63-69.
37. Hammarstrom L. The role of enamel matrix proteins in the development of cementum and periodontal tissues. Ciba Found Symp 1997: 205: 246-255; discussion 255-260.
38. Hammarstrom L. Enamel matrix, cementum development and regeneration. J Clin Periodontol 1997: 24: 658-668.
39. Hammarstrom L, Heijl L, Gestrelius S. Periodontal regeneration in a buccal dehiscence model in monkeys after application of enamel matrix proteins. J Clin Periodontol 1997: 24: 669-677.
40. Hasegawa N, Kawaguchi H, Ogawa T, Uchida T, Kurihara H. Immunohistochemical characteristics of the epithelial cell rests of Malassez during cementum repair. J Periodontal Res 2003: 38: 51-56.
41. Heijl L. Periodontal regeneration with enamel matrix derivative in one human experimental defect. A case report. J Clin Periodontol 1997: 24: 693-696.
42. Heritier M. Experimental induction of cementogenesis on the enamel of transplanted mouse tooth germs. Arch Oral Biol 1982: 27: 87-97.
43. Heyeraas KJ, Kvinnsland I, Byers MR, Jacobsen EB. Nerve fibers immunoreactive to protein gene product 9.5, calcitonin gene-related peptide, substance P, and neuropeptide Y in the dental pulp, periodontal ligament, and gingiva in cats. Acta Odontol Scand 1993: 51: 207-221.
44. Huang X, Bringas P Jr, Slavkin HC, Chai Y. Fate of HERS during tooth root development. Dev Biol 2009: 334: 22-30.
45. Huang X, Xu X, Bringas P Jr, Hung YP, Chai Y. Smad4-Shh-Nfic signaling cascade-mediated epithelial-mesenchymal interaction is crucial in regulating tooth root development. J Bone Miner Res 2010: 25: 1167-1178.
46. Ikeda E, Morita R, Nakao K, Ishida K, Nakamura T, Takano-Yamamoto T, Ogawa M, Mizuno M, Kasugai S, Tsuji T. Fully functional bioengineered tooth replacement as an organ replacement therapy. Proc Natl Acad Sci USA 2009: 106: 13475-13480.
47. Jiang XY, Fu SL, Nie BM, Li Y, Lin L, Yin L, Wang YX, Lu PH, Xu XM. Methods for isolating highly-enriched embryonic spinal cord neurons: a comparison between enzymatic and mechanical dissociations. J Neurosci Methods 2006: 158: 13-18.
48. Jung HS, Lee DS, Lee JH, Park SJ, Lee G, Seo BM, Ko JS, Park JC. Directing the differentiation of human dental follicle cells into cementoblasts and/or osteoblasts by a combination of HERS and pulp cells. J Mol Histol 2011: 42: 227-235.
49. Kaneko H, Hashimoto S, Enokiya Y, Ogiuchi H, Shimono M. Cell proliferation and death of the Hertwig's epithelial root sheath in the rat. Cell Tissue Res 1999: 298: 95-103.
50. Kat PS, Sampson WJ, Wilson DF, Wiebkin OW. Distribution of the epithelial rests of Malassez and their relationship to blood vessels of the periodontal ligament during rat tooth development. Aust Orthod J 2003: 19: 77-86.
51. Kim MY, Reyna J, Chen LS, Zeichner-David M. Role of the transcription factor NFIC in odontoblast gene expression. J Calif Dent Assoc 2009: 37: 875-881.
52. 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.
53. Kvinnsland IH, Tadokoro O, Heyeraas KJ, Kozawa Y, Vandevska-Radunovic V. Neuroendocrine cells in Malassez epithelium and gingiva of the cat. Acta Odontol Scand 2000: 58: 107-112.
54. Lambrichts I, Creemers J, Van Steenberghe D. Periodontal neural endings intimately relate to epithelial rests of Malassez in humans. A light and electron microscope study. J Anat 1993: 182(Pt 2): 153-162.
55. Lee DS, Park JT, Kim HM, Ko JS, Son HH, Gronostajski RM, Cho MI, Choung PH, Park JC. Nuclear factor I-C is essential for odontogenic cell proliferation and odontoblast differentiation during tooth root development. J Biol Chem 2009: 284: 17293-17303.
56. Lee TY, Lee DS, Kim HM, Ko JS, Gronostajski RM, Cho MI, Son HH, Park JC. Disruption of Nfic causes dissociation of odontoblasts by interfering with the formation of intercellular junctions and aberrant odontoblast differentiation. J Histochem Cytochem 2009: 57: 469-476.
57. Lezot F, Davideau JL, Thomas B, Sharpe P, Forest N, Berdal A. Epithelial Dlx-2 homeogene expression and cementogenesis. J Histochem Cytochem 2000: 48: 277-284.
58. Li R, Liang J, Ni S, Zhou T, Qing X, Li H, He W, Chen J, Li F, Zhuang Q, Qin B, Xu J, Li W, Yang J, Gan Y, Qin D, Feng S, Song H, Yang D, Zhang B, Zeng L, Lai L, Esteban MA, Pei D. A mesenchymal-to-epithelial transition initiates and is required for the nuclear reprogramming of mouse fibroblasts. Cell Stem Cell 2010: 7: 51-63.
59. Liao J, Al Shahrani M, Al-Habib M, Tanaka T, Huang GT. Cells isolated from inflamed periapical tissue express mesenchymal stem cell markers and are highly osteogenic. J Endod 2011: 37: 1217-1224.
60. Lin NH, Gronthos S, Bartold PM. Stem cells and periodontal regeneration. Aust Dent J 2008: 53: 108-121.
61. Lindskog S. Formation of intermediate cementum. II: a scanning electron microscopic study of the epithelial root sheath of the Hertwig in monkey. J Craniofac Genet Dev Biol 1982: 2: 161-169.
62. 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.
63. Lindskog S, Hammarstrom L. Formation of intermediate cementum. III: 3H-tryptophan and 3H-proline uptake into the epithelial root sheath of the Hertwig in vitro. J Craniofac Genet Dev Biol 1982: 2: 171-177.
64. Lindskog S, Blomlof L, Hammarstrom L. Evidence for a role of odontogenic epithelium in maintaining the periodontal space. J Clin Periodontol 1988: 15: 371-373.
65. Listl S, Tu YK, Faggion CM Jr. A cost-effectiveness evaluation of enamel matrix derivatives alone or in conjunction with regenerative devices in the treatment of periodontal intra-osseous defects. J Clin Periodontol 2010: 37: 920-927.
66. 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.
67. Loe H, Waerhaug J. Experimental replantation of teeth in dogs and monkeys. Arch Oral Biol 1961: 3: 176-184.
68. Luan X, Ito Y, Diekwisch TG. Evolution and development of the Hertwig's epithelial root sheath. Dev Dyn 2006: 235: 1167-1180.
69. Macneil RL, Sheng N, Strayhorn C, Fisher LW, Somerman MJ. Bone sialoprotein is localized to the root surface during cementogenesis. J Bone Miner Res 1994: 9: 1597-1606.
70. Mahmoud Torabinejad REW. Endodontics: principles and practice. 4th Ed. St louis, MO: Saunders Elsevier Inc, 2008: 3-4.
71. McDermott SP, Eppert K, Lechman ER, Doedens M, Dick JE. Comparison of human cord blood engraftment between immunocompromised mouse strains. Blood 2010: 116: 193-200.
72. Meyle J, Hoffmann T, Topoll H, Heinz B, Al-Machot E, Jervoe-Storm PM, Meiss C, Eickholz P, Jepsen S. A multi-centre randomized controlled clinical trial on the treatment of intra-bony defects with enamel matrix derivatives/synthetic bone graft or enamel matrix derivatives alone: results after 12 months. J Clin Periodontol 2011: 38: 652-660.
73. 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 USA 2003: 100: 5807-5812.
74. Mizuno N, Shiba H, Mouri Y, Xu W, Kudoh S, Kawaguchi H, Kurihara H. Characterization of epithelial cells derived from periodontal ligament by gene expression patterns of bone-related and enamel proteins. Cell Biol Int 2005: 29: 111-117.
75. 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.
76. Mouri Y, Shiba H, Mizuno N, Noguchi T, Ogawa T, Kurihara H. Differential gene expression of bone-related proteins in epithelial and fibroblastic cells derived from human periodontal ligament. Cell Biol Int 2003: 27: 519-524.
77. Moxham BJ, Webb PP, Benjamin M, Ralphs JR. Changes in the cytoskeleton of cells within the periodontal ligament and dental pulp of the rat first molar tooth during ageing. Eur J Oral Sci 1998: 106(Suppl. 1): 376-383.
78. Nakao K, Morita R, Saji Y, Ishida K, Tomita Y, Ogawa M, Saitoh M, Tomooka Y, Tsuji T. The development of a bioengineered organ germ method. Nat Methods 2007: 4: 227-230.
79. Nam H, Kim J, Park J, Park JC, Kim JW, Seo BM, Lee JC, Lee G. Expression profile of the stem cell markers in human the Hertwig's epithelial root sheath/Epithelial rests of Malassez cells. Mol Cells 2011: 31: 355-360.
80. Nokhbehsaim M, Winter J, Rath B, Jager A, Jepsen S, Deschner J. Effects of enamel matrix derivative on periodontal wound healing in an inflammatory environment in vitro. J Clin Periodontol 2011: 38: 479-490.
81. Ocana OH, Nieto MA. Epithelial plasticity, stemness and pluripotency. Cell Res 2010: 20: 1086-1088.
82. Oshima M, Mizuno M, Imamura A, Ogawa M, Yasukawa M, Yamazaki H, Morita R, Ikeda E, Nakao K, Takano-Yamamoto T, Kasugai S, Saito M, Tsuji T. Functional tooth regeneration using a bioengineered tooth unit as a mature organ replacement regenerative therapy. PLoS ONE 2011: 6: e21531.
83. Owens PD. The root surface in human teeth: a microradiographic study. J Anat 1976: 122: 389-401.
84. Owens PD. Ultrastructure of the Hertwig's epithelial root sheath during early root development in premolar teeth in dogs. Arch Oral Biol 1978: 23: 91-104.
85. Park JC, Herr Y, Kim HJ, Gronostajski RM, Cho MI. Nfic gene disruption inhibits differentiation of odontoblasts responsible for root formation and results in formation of short and abnormal roots in mice. J Periodontol 2007: 78: 1795-1802.
86. Park JC, Kim JM, Jung IH, Kim JC, Choi SH, Cho KS, Kim CS. Isolation and characterization of human periodontal ligament (PDL) stem cells (PDLSCs) from the inflamed PDL tissue: in vitro and in vivo evaluations. J Clin Periodontol 2011: 38: 721-731.
87. Paynter KJ, Pudy G. A study of the structure, chemical nature, and development of cementum in the rat. Anat Rec 1958: 131: 233-251.
88. Reitan K. Behavior of Malassez' epithelial rests during orthodontic tooth movement. Acta Odontol Scand 1961: 19: 443-468.
89. Rincon JC, Xiao Y, Young WG, Bartold PM. Production of osteopontin by cultured porcine the epithelial cell rests of Malassez. J Periodontal Res 2005: 40: 417-426.
90. Rincon JC, Xiao Y, Young WG, Bartold PM. Enhanced proliferation, attachment and osteopontin expression by porcine periodontal cells exposed to Emdogain. Arch Oral Biol 2005: 50: 1047-1054.
91. Rincon JC, Young WG, Bartold PM. The the epithelial cell rests of Malassez-a role in periodontal regeneration? J Periodontal Res 2006: 41: 245-252.
92. 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.
93. Saygin NE, Giannobile WV, Somerman MJ. Molecular and cell biology of cementum. Periodontol 2000 2000: 24: 73-98.
94. Schroeder HE. Development, structure and function of periodontal tissues. In: Oksche A, Vollrath L, editors. Handbook of microscopic anatomy. Berlin: Springer-Verlag, 1985: 23-228.
95. Schroeder HE. Biological problems of regenerative cementogenesis: synthesis and attachment of collagenous matrices on growing and established root surfaces. Int Rev Cytol 1992: 142: 1-59.
96. 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.
97. Shimono M, Ishikawa T, Ishikawa H, Matsuzaki H, Hashimoto S, Muramatsu T, Shima K, Matsuzaka K, Inoue T. Regulatory mechanisms of periodontal regeneration. Microsc Res Tech 2003: 60: 491-502.
98. Shinmura Y, Tsuchiya S, Hata K, Honda MJ. Quiescent the epithelial cell rests of Malassez can differentiate into ameloblast-like cells. J Cell Physiol 2008: 217: 728-738.
99. Shore RC, Berkovitz BK, Moxham BJ. Intercellular contacts between fibroblasts in the periodontal connective tissues of the rat. J Anat 1981: 133: 67-76.
100. Slavkin HC. Towards a cellular and molecular understanding of periodontics. Cementogenesis revisited. J Periodontol 1976: 47: 249-255.
101. Slavkin HC, Bessem C, Fincham AG, Bringas P Jr, Santos V, Snead ML, Zeichner-David M. Human and mouse cementum proteins immunologically related to enamel proteins. Biochim Biophys Acta 1989: 991: 12-18.
102. Slavkin HC, Bringas P Jr, Bessem C, Santos V, Nakamura M, Hsu MY, Snead ML, Zeichner-David M, Fincham AG. The 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 Periodontal Res 1989: 24: 28-40.
103. 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.
104. Sonoyama W, Seo BM, Yamaza T, Shi S. Human the Hertwig's epithelial root sheath cells play crucial roles in cementum formation. J Dent Res 2007: 86: 594-599.
105. 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.
106. Steele-Perkins G, Butz KG, Lyons GE, Zeichner-David M, Kim HJ, Cho MI, Gronostajski RM. Essential role for NFI-C/CTF transcription-replication factor in tooth root development. Mol Cell Biol 2003: 23: 1075-1084.
107. Tadokoro O, Maeda T, Heyeraas KJ, Vandevska-Radunovic V, Kozawa Y, Hals Kvinnsland I. Merkel-like cells in Malassez epithelium in the periodontal ligament of cats: an immunohistochemical, confocal-laser scanning and immuno electron-microscopic investigation. J Periodontal Res 2002: 37: 456-463.
108. Tadokoro O, Vandevska-Randunovic V, Inoue K. Epithelial cell rests of Malassez and OX6-immunopositive cells in the periodontal ligament of rat molars: a light and transmission electron microscope study. Anat Rec (Hoboken) 2008: 291: 242-253.
109. Talic NF, Evans CA, Daniel JC, Zaki AE. Proliferation of epithelial rests of Malassez during experimental tooth movement. Am J Orthod Dentofacial Orthop 2003: 123: 527-533.
110. 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.
111. Ten Cate AR. The development of the periodontium-a largely ectomesenchymally derived unit. Periodontol 2000 1997: 13: 9-19.
112. Tenorio D, Cruchley A, Hughes FJ. Immunocytochemical investigation of the rat cementoblast phenotype. J Periodontal Res 1993: 28: 411-419.
113. Terling C, Heymann R, Rozell B, Obrink B, Wroblewski J. Dynamic expression of E-cadherin in ameloblasts and cementoblasts in mice. Eur J Oral Sci 1998: 106(Suppl. 1): 137-142.
114. Thomas HF, Kollar EJ. Tissue interactions in normal murine root development. In: Davidovitch Z, editor. The biological mechanisms of tooth eruption and root resorption. Birmingham, AL: EBSCO Medi, 1988: 145-151.
115. Thomas HF. Root formation. Int J Dev Biol 1995: 39: 231-237.
116. Tomazela-Herndl SA, Arana-Chavez VE. Ultrastructure of early mineral deposition during hyaline layer formation in rat molars. Arch Oral Biol 2001: 46: 305-311.
117. Tummers M, Thesleff I. Root or crown: a developmental choice orchestrated by the differential regulation of the epithelial stem cell niche in the tooth of two rodent species. Development 2003: 130: 1049-1057.
118. Von BA. Über die Ausdehnung des Schmelzorganes and seine Bedeutung fur die Zahnbildung. Arch mikrosk Anat EntwMech 1887: 29: 367-395.
119. Wallace JA, Vergona K. Epithelial rests' function in replantation: is splinting necessary in replantation? Oral Surg Oral Med Oral Pathol 1990: 70: 644-649.
120. Webb PP, Moxham BJ, Benjamin M, Ralphs JR. Changing expression of intermediate filaments in fibroblasts and cementoblasts of the developing periodontal ligament of the rat molar tooth. J Anat 1996: 188(Pt 3): 529-539.
121. Wesselink PR, Beertsen W. The prevalence and distribution of rests of Malassez in the mouse molar and their possible role in repair and maintenance of the periodontal ligament. Arch Oral Biol 1993: 38: 399-403.
122. Xiong J, Mrozik KM, Gronthos S, Bartold PM. Epithelial cell rests of Malassez contain unique stem cell populations capable of undergoing epithelial-mesenchymal transition. Stem Cells Dev 2012: 21: 2012-2025.
123. Yamamoto T, Takahashi S. The Hertwig's epithelial root sheath cells do not transform into cementoblasts in rat molar cementogenesis. Ann Anat 2009: 191: 547-555.
124. Yamaoka Y, Sawa Y, Ebata N, Yoshida S, Kawasaki T. Desmosomal proteins in cultured and intact human periodontal ligament fibroblasts. Tissue Cell 1999: 31: 605-609.
125. Yamashiro T, Fujiyama K, Fukunaga T, Wang Y, Takano-Yamamoto T. Epithelial rests of Malassez express immunoreactivity of TrkA and its distribution is regulated by sensory nerve innervation. J Histochem Cytochem 2000: 48: 979-984.
126. Yukna RA, Mellonig JT. Histologic evaluation of periodontal healing in humans following regenerative therapy with enamel matrix derivative. A 10-case series. J Periodontol 2000: 71: 752-759.
127. Zeichner-David M, Oishi K, Su Z, Zakartchenko V, Chen LS, Arzate H, Bringas P Jr. Role of the Hertwig's epithelial root sheath cells in tooth root development. Dev Dyn 2003: 228: 651-663.
128. Zhang Q, Shi S, Liu Y, Uyanne J, Shi Y, Le AD. Mesenchymal stem cells derived from human gingiva are capable of immunomodulatory functions and ameliorate inflammation-related tissue destruction in experimental colitis. J Immunol 2009: 183: 7787-7798.