Dental stem cells and their promising role in neural regeneration: An update

Clinical Oral Investigations

Volumn 17, Issue 9, 2013, Pages 1969-1983

  Martens, W ^a   Bronckaers, A ^a   Politis, C ^a,b   Jacobs, R ^c   Lambrichts, I ^a  

^a HASSELT UNIVERSITY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c DEPARTMENT OF IMAGING AND PATHOLOGY   (Belgium)

Author keywords

Dental stem cells; Neural characteristics; Stem cells; Tooth development

Indexed keywords

ANIMAL; CYTOLOGY; GROWTH, DEVELOPMENT AND AGING; HUMAN; NERVE REGENERATION; STEM CELL; TOOTH;

ANIMALS; HUMANS; NERVE REGENERATION; STEM CELLS; TOOTH;

EID: 84888640496     PISSN: 14326981     EISSN: 14363771     Source Type: Journal    
DOI: 10.1007/s00784-013-1030-3     Document Type: Review

References (132)

1. Ibarretxe G, Crende O, Aurrekoetxea M, Garcia-Murga V, Etxaniz J, Unda F (2012) Neural crest stem cells from dental tissues: a new hope for dental and neural regeneration. Stem Cells Int. doi: 10. 1155/2012/103503, 103503.
2. Rimondini L, Mele S (2009) Stem cell technologies for tissue regeneration in dentistry. Minerva Stomatol 58(10): 483-500.
3. Park HW, Lim MJ, Jung H, Lee SP, Paik KS, Chang MS (2010) Human mesenchymal stem cell-derived Schwann cell-like cells exhibit neurotrophic effects, via distinct growth factor production, in a model of spinal cord injury. Glia 58(9): 1118-1132. doi: 10. 1002/glia. 20992.
4. Sakai K, Yamamoto A, Matsubara K, Nakamura S, Naruse M, Yamagata M, Sakamoto K, Tauchi R, Wakao N, Imagama S, Hibi H, Kadomatsu K, Ishiguro N, Ueda M (2012) Human dental pulp-derived stem cells promote locomotor recovery after complete transection of the rat spinal cord by multiple neuro-regenerative mechanisms. J Clin Investig 122(1): 80-90. doi: 10. 1172/JCI59251.
5. Ross JJ, Verfaillie CM (2008) Evaluation of neural plasticity in adult stem cells. Philos Trans R Soc Lond 363(1489): 199-205.
6. Pittenger MF, Mackay AM, Beck SC, Jaiswal RK, Douglas R, Mosca JD, Moorman MA, Simonetti DW, Craig S, Marshak DR (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284(5411): 143-147.
7. Meirelles Lda S, Fontes AM, Covas DT, Caplan AI (2009) Mechanisms involved in the therapeutic properties of mesenchymal stem cells. Cytokine Growth Factor Rev 20(5-6): 419-427.
8. 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.
9. 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.
10. 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.
11. 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.
12. Sonoyama W, Liu Y, Yamaza T, Tuan RS, Wang S, Shi S, Huang GT (2008) Characterization of the apical papilla and its residing stem cells from human immature permanent teeth: a pilot study. J Endod 34(2): 166-171. doi: 10. 1016/j. joen. 2007. 11. 021.
13. Lakshmipathy U, Verfaillie C (2005) Stem cell plasticity. Blood Rev 19(1): 29-38.
14. Verfaillie CM, Pera MF, Lansdorp PM (2002) Stem cells: hype and reality. Hematology 1: 369-391.
15. Friedenstein AJ, Gorskaja JF, Kulagina NN (1976) Fibroblast precursors in normal and irradiated mouse hematopoietic organs. Exp Hematol 4(5): 267-274.
16. Bianco P, Riminucci M, Gronthos S, Robey PG (2001) Bone marrow stromal stem cells: nature, biology, and potential applications. Stem Cells 19(3): 180-192.
17. Bruder SP, Jaiswal N, Haynesworth SE (1997) Growth kinetics, self-renewal, and the osteogenic potential of purified human mesenchymal stem cells during extensive subcultivation and following cryopreservation. J Cell Biochem 64(2): 278-294.
18. Guillot PV, Cui W, Fisk NM, Polak DJ (2007) Stem cell differentiation and expansion for clinical applications of tissue engineering. J Cell Mol Med 11(5): 935-944.
19. Spencer ND, Gimble JM, Lopez MJ (2011) Mesenchymal stromal cells: past, present, and future. Vet Surg 40(2): 129-139.
20. Kopen GC, Prockop DJ, Phinney DG (1999) Marrow stromal cells migrate throughout forebrain and cerebellum, and they differentiate into astrocytes after injection into neonatal mouse brains. Proc Natl Acad Sci U S A 96(19): 10711-10716.
21. Lu D, Li Y, Wang L, Chen J, Mahmood A, Chopp M (2001) Intraarterial administration of marrow stromal cells in a rat model of traumatic brain injury. J Neurotrauma 18(8): 813-819.
22. Chen J, Li Y, Wang L, Lu M, Zhang X, Chopp M (2001) Therapeutic benefit of intracerebral transplantation of bone marrow stromal cells after cerebral ischemia in rats. J Neurol Sci 189(1-2): 49-57.
23. Hofstetter CP, Schwarz EJ, Hess D, Widenfalk J, El Manira A, Prockop DJ, Olson L (2002) Marrow stromal cells form guiding strands in the injured spinal cord and promote recovery. Proc Natl Acad Sci U S A 99(4): 2199-2204.
24. Chen SL, Fang WW, Qian J, Ye F, Liu YH, Shan SJ, Zhang JJ, Lin S, Liao LM, Zhao RC (2004) Improvement of cardiac function after transplantation of autologous bone marrow mesenchymal stem cells in patients with acute myocardial infarction. Chin Med J 117(10): 1443-1448.
25. Horwitz EM, Gordon PL, Koo WK, Marx JC, Neel MD, McNall RY, Muul L, Hofmann T (2002) Isolated allogeneic bone marrow-derived mesenchymal cells engraft and stimulate growth in children with osteogenesis imperfecta: implications for cell therapy of bone. Proc Natl Acad Sci U S A 99(13): 8932-8937.
26. Horwitz EM, Prockop DJ, Gordon PL, Koo WW, Fitzpatrick LA, Neel MD, McCarville ME, Orchard PJ, Pyeritz RE, Brenner MK (2001) Clinical responses to bone marrow transplantation in children with severe osteogenesis imperfecta. Blood 97(5): 1227-1231.
27. Nanci A (2008) Ten Cate's oral histology: development, structure, and function, 6th edn. Mosby Elsevier, Philadelphia.
28. Thesleff I, Jernvall J (1997) The enamel knot: a putative signaling center regulating tooth development. Cold Spring Harb Symp Quant Biol 62: 257-267.
29. 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.
30. 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.
31. Feng J, Mantesso A, De Bari C, Nishiyama A, Sharpe PT (2011) Dual origin of mesenchymal stem cells contributing to organ growth and repair. Proc Natl Acad Sci U S A 108(16): 6503-6508. doi: 10. 1073/pnas. 1015449108.
32. Crisan M, Yap S, Casteilla L, Chen CW, Corselli M, Park TS, Andriolo G, Sun B, Zheng B, Zhang L, Norotte C, Teng PN, Traas J, Schugar R, Deasy BM, Badylak S, Buhring HJ, Giacobino JP, Lazzari L, Huard J, Peault B (2008) A perivascular origin for mesenchymal stem cells in multiple human organs. Cell Stem Cell 3(3): 301-313. doi: 10. 1016/j. stem. 2008. 07. 003.
33. da Silva Meirelles L, Caplan AI, Nardi NB (2008) In search of the in vivo identity of mesenchymal stem cells. Stem Cells 26(9): 2287-2299.
34. 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.
35. Lapthanasupkul P, Feng J, Mantesso A, Takada-Horisawa Y, Vidal M, Koseki H, Wang L, An Z, Miletich I, Sharpe PT (2012) Ring1a/b polycomb proteins regulate the mesenchymal stem cell niche in continuously growing incisors. Dev Biol 367(2): 140-153. doi: 10. 1016/j. ydbio. 2012. 04. 029.
36. Janebodin K, Horst OV, Ieronimakis N, Balasundaram G, Reesukumal K, Pratumvinit B, Reyes M (2011) Isolation and characterization of neural crest-derived stem cells from dental pulp of neonatal mice. PLoS One 6(11): e27526. doi: 10. 1371/journal. pone. 0027526.
37. Lovschall H, Tummers M, Thesleff I, Fuchtbauer EM, Poulsen K (2005) Activation of the notch signaling pathway in response to pulp capping of rat molars. Eur J Oral Sci 113(4): 312-317. doi: 10. 1111/j. 1600-0722. 2005. 00221. x.
38. Martens W, Wolfs E, Struys T, Politis C, Bronckaers A, Lambrichts I (2012) Expression pattern of basal markers in human dental pulp stem cells and tissue. Cells Tissues Organs 196(6): 490-500. doi: 10. 1159/000338654.
39. Sloan AJ, Smith AJ (2007) Stem cells and the dental pulp: potential roles in dentine regeneration and repair. Oral Dis 13(2): 151-157.
40. Tecles O, Laurent P, Zygouritsas S, Burger AS, Camps J, Dejou J, About I (2005) Activation of human dental pulp progenitor/stem cells in response to odontoblast injury. Arch Oral Biol 50(2): 103-108.
41. Atari M, Gil-Recio C, Fabregat M, Garcia-Fernandez D, Barajas M, Carrasco MA, Jung HS, Alfaro FH, Casals N, Prosper F, Ferres-Padro E, Giner L (2012) Dental pulp of the third molar: a new source of pluripotent-like stem cells. J Cell Sci 125(Pt 14): 3343-3356. doi: 10. 1242/jcs. 096537.
42. Karbanova J, Soukup T, Suchanek J, Pytlik R, Corbeil D, Mokry J (2011) Characterization of dental pulp stem cells from impacted third molars cultured in low serum-containing medium. Cells Tissues Organs 193(6): 344-365.
43. Thesleff I, Sharpe P (1997) Signalling networks regulating dental development. Mech Dev 67(2): 111-123.
44. Thesleff I, Tummers M (2008) Tooth organogenesis and regeneration. Harvard Stem Cell Institute, Cambridge.
45. Egusa H, Sonoyama W, Nishimura M, Atsuta I, Akiyama K (2012) Stem cells in dentistry-part I: stem cell sources. J Prosthodont Res 56(3): 151-165. doi: 10. 1016/j. jpor. 2012. 06. 001.
46. Chen FM, Sun HH, Lu H, Yu Q (2012) Stem cell-delivery therapeutics for periodontal tissue regeneration. Biomaterials 33(27): 6320-6344. doi: 10. 1016/j. biomaterials. 2012. 05. 048.
47. Smith AJ, Cassidy N, Perry H, Begue-Kirn C, Ruch JV, Lesot H (1995) Reactionary dentinogenesis. Int J Dev Biol 39(1): 273-280.
48. Smith AJ, Lesot H (2001) Induction and regulation of crown dentinogenesis: embryonic events as a template for dental tissue repair? Crit Rev Oral Biol Med 12(5): 425-437.
49. Gronthos S, Brahim J, Li W, Fisher LW, Cherman N, Boyde A, DenBesten P, Robey PG, Shi S (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81(8): 531-535.
50. About I, Bottero MJ, de Denato P, Camps J, Franquin JC, Mitsiadis TA (2000) Human dentin production in vitro. Exp Cell Res 258(1): 33-41.
51. Alge DL, Zhou D, Adams LL, Wyss BK, Shadday MD, Woods EJ, Gabriel Chu TM, Goebel WS (2010) Donor-matched comparison of dental pulp stem cells and bone marrow-derived mesenchymal stem cells in a rat model. J Tissue Eng Regen Med 4(1): 73-81.
52. Shi S, Robey PG, Gronthos S (2001) Comparison of human dental pulp and bone marrow stromal stem cells by cDNA microarray analysis. Bone 29(6): 532-539.
53. Chai Y, Jiang X, Ito Y, Bringas P Jr, Han J, Rowitch DH, Soriano P, McMahon AP, Sucov HM (2000) Fate of the mammalian cranial neural crest during tooth and mandibular morphogenesis. Development 127(8): 1671-1679.
54. Graham A, Begbie J, McGonnell I (2004) Significance of the cranial neural crest. Dev Dyn 229(1): 5-13.
55. Thesleff I, Aberg T (1999) Molecular regulation of tooth development. Bone 25(1): 123-125.
56. Miletich I, Sharpe PT (2004) Neural crest contribution to mammalian tooth formation. Birth Defects Res C Embryo Today 72(2): 200-212.
57. d'Aquino R, Graziano A, Sampaolesi M, Laino G, Pirozzi G, De Rosa A, Papaccio G (2007) Human postnatal dental pulp cells co-differentiate into osteoblasts and endotheliocytes: a pivotal synergy leading to adult bone tissue formation. Cell Death Differ 14(6): 1162-1171.
58. Kiraly M, Kadar K, Horvathy DB, Nardai P, Racz GZ, Lacza Z, Varga G, Gerber G (2011) Integration of neuronally predifferentiated human dental pulp stem cells into rat brain in vivo. Neurochem Int 59(3): 371-381.
59. Kiraly M, Porcsalmy B, Pataki A, Kadar K, Jelitai M, Molnar B, Hermann P, Gera I, Grimm WD, Ganss B, Zsembery A, Varga G (2009) Simultaneous PKC and cAMP activation induces differentiation of human dental pulp stem cells into functionally active neurons. Neurochem Int 55(5): 323-332.
60. Laino G, d'Aquino R, Graziano A, Lanza V, Carinci F, Naro F, Pirozzi G, Papaccio G (2005) A new population of human adult dental pulp stem cells: a useful source of living autologous fibrous bone tissue (LAB). J Bone Miner Res 20(8): 1394-1402.
61. Paino F, Ricci G, De Rosa A, D'Aquino R, Laino L, Pirozzi G, Tirino V, Papaccio G (2010) Ecto-mesenchymal stem cells from dental pulp are committed to differentiate into active melanocytes. Eur Cell Mater 20: 295-305.
62. Stevens A, Zuliani T, Olejnik C, LeRoy H, Obriot H, Kerr-Conte J, Formstecher P, Bailliez Y, Polakowska RR (2008) Human dental pulp stem cells differentiate into neural crest-derived melanocytes and have label-retaining and sphere-forming abilities. Stem Cells Dev 17(6): 1175-1184.
63. Struys T, Moreels M, Martens W, Donders R, Wolfs E, Lambrichts I (2010) Ultrastructural and immunocytochemical analysis of multilineage differentiated human dental pulp- and umbilical cord-derived mesenchymal stem cells. Cells Tissues Organs 193(6): 366-378.
64. Batouli S, Miura M, Brahim J, Tsutsui TW, Fisher LW, Gronthos S, Robey PG, Shi S (2003) Comparison of stem-cell-mediated osteogenesis and dentinogenesis. J Dent Res 82(12): 976-981.
65. Huang GT, Yamaza T, Shea LD, Djouad F, Kuhn NZ, Tuan RS, Shi S (2010) Stem/progenitor cell-mediated de novo regeneration of dental pulp with newly deposited continuous layer of dentin in an in vivo model. Tissue Eng 16(2): 605-615.
66. Marchionni C, Bonsi L, Alviano F, Lanzoni G, Di Tullio A, Costa R, Montanari M, Tazzari PL, Ricci F, Pasquinelli G, Orrico C, Grossi A, Prati C, Bagnara GP (2009) Angiogenic potential of human dental pulp stromal (stem) cells. Int J Immunopathol Pharmacol 22(3): 699-706.
67. Gandia C, Arminan A, Garcia-Verdugo JM, Lledo E, Ruiz A, Minana MD, Sanchez-Torrijos J, Paya R, Mirabet V, Carbonell-Uberos F, Llop M, Montero JA, Sepulveda P (2008) Human dental pulp stem cells improve left ventricular function, induce angiogenesis, and reduce infarct size in rats with acute myocardial infarction. Stem Cells 26(3): 638-645.
68. Nakashima M, Iohara K, Sugiyama M (2009) Human dental pulp stem cells with highly angiogenic and neurogenic potential for possible use in pulp regeneration. Cytokine Growth Factor Rev 20(5-6): 435-440.
69. Arthur A, Rychkov G, Shi S, Koblar SA, Gronthos S (2008) Adult human dental pulp stem cells differentiate toward functionally active neurons under appropriate environmental cues. Stem Cells 26(7): 1787-1795.
70. Arthur A, Shi S, Zannettino AC, Fujii N, Gronthos S, Koblar SA (2009) Implanted adult human dental pulp stem cells induce endogenous axon guidance. Stem Cells 27(9): 2229-2237.
71. Nosrat IV, Smith CA, Mullally P, Olson L, Nosrat CA (2004) Dental pulp cells provide neurotrophic support for dopaminergic neurons and differentiate into neurons in vitro; implications for tissue engineering and repair in the nervous system. Eur J Neurosci 19(9): 2388-2398.
72. Nosrat IV, Widenfalk J, Olson L, Nosrat CA (2001) Dental pulp cells produce neurotrophic factors, interact with trigeminal neurons in vitro, and rescue motoneurons after spinal cord injury. Dev Biol 238(1): 120-132.
73. Yalvac ME, Rizvanov AA, Kilic E, Sahin F, Mukhamedyarov MA, Islamov RR, Palotas A (2009) Potential role of dental stem cells in the cellular therapy of cerebral ischemia. Curr Pharm Des 15(33): 3908-3916.
74. Papaccio G, Graziano A, d'Aquino R, Graziano MF, Pirozzi G, Menditti D, De Rosa A, Carinci F, Laino G (2006) Long-term cryopreservation of dental pulp stem cells (SBP-DPSCs) and their differentiated osteoblasts: a cell source for tissue repair. J Cell Physiol 208(2): 319-325.
75. 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 Part C Methods 14(2): 149-156.
76. Zhang W, Walboomers XF, Shi S, Fan M, Jansen JA (2006) Multilineage differentiation potential of stem cells derived from human dental pulp after cryopreservation. Tissue Eng 12(10): 2813-2823.
77. Bakopoulou A, Leyhausen G, Volk J, Tsiftsoglou A, Garefis P, Koidis P, Geurtsen W (2011) Assessment of the impact of two different isolation methods on the osteo/odontogenic differentiation potential of human dental stem cells derived from deciduous teeth. Calcif Tissue Int 88(2): 130-141.
78. Kerkis I, Kerkis A, Dozortsev D, Stukart-Parsons GC, Gomes Massironi SM, Pereira LV, Caplan AI, Cerruti HF (2006) Isolation and characterization of a population of immature dental pulp stem cells expressing OCT-4 and other embryonic stem cell markers. Cells Tissues Organs 184(3-4): 105-116.
79. Wang J, Wang X, Sun Z, Wang X, Yang H, Shi S, Wang S (2010) Stem cells from human-exfoliated deciduous teeth can differentiate into dopaminergic neuron-like cells. Stem Cells Dev 19(9): 1375-1383.
80. Sakai VT, Zhang Z, Dong Z, Neiva KG, Machado MA, Shi S, Santos CF, Nor JE (2010) SHED differentiate into functional odontoblasts and endothelium. J Dent Res 89(8): 791-796.
81. Gay IC, Chen S, MacDougall M (2007) Isolation and characterization of multipotent human periodontal ligament stem cells. Orthod Craniofac Res 10(3): 149-160.
82. 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.
83. Techawattanawisal W, Nakahama K, Komaki M, Abe M, Takagi Y, Morita I (2007) Isolation of multipotent stem cells from adult rat periodontal ligament by neurosphere-forming culture system. Biochem Biophys Res Commun 357(4): 917-923.
84. 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.
85. Morsczeck C, Vollner F, Saugspier M, Brandl C, Reichert TE, Driemel O, Schmalz G (2010) Comparison of human dental follicle cells (DFCs) and stem cells from human exfoliated deciduous teeth (SHED) after neural differentiation in vitro. Clin Oral Investig 14(4): 433-440.
86. Yao S, Pan F, Prpic V, Wise GE (2008) Differentiation of stem cells in the dental follicle. J Dent Res 87(8): 767-771.
87. Yokoi T, Saito M, Kiyono T, Iseki S, Kosaka K, Nishida E, Tsubakimoto T, Harada H, Eto K, Noguchi T, Teranaka T (2007) Establishment of immortalized dental follicle cells for generating periodontal ligament in vivo. Cell Tissue Res 327(2): 301-311.
88. D'Souza R (2002) Development of the pulpodentin complex. In: Kenneth M, Hargreaves HEG (eds) Seltzer and Bender's dental pulp. Quintessence, Carol Stream.
89. Bakopoulou A, Leyhausen G, Volk J, Tsiftsoglou A, Garefis P, Koidis P, Geurtsen W (2011) Comparative analysis of in vitro osteo/odontogenic differentiation potential of human dental pulp stem cells (DPSCs) and stem cells from the apical papilla (SCAP). Arch Oral Biol 56(7): 709-721. doi: 10. 1016/j. archoralbio. 2010. 12. 008.
90. Abe S, Yamaguchi S, Amagasa T (2007) Multilineage cells from apical pulp of human tooth with immature apex. Oral Sci Int 4: 45-58.
91. Chueh LH, Huang GT (2006) Immature teeth with periradicular periodontitis or abscess undergoing apexogenesis: a paradigm shift. J Endod 32(12): 1205-1213.
92. Huang GT, Sonoyama W, Liu Y, Liu H, Wang S, Shi S (2008) The hidden treasure in apical papilla: the potential role in pulp/dentin regeneration and bioroot engineering. J Endod 34(6): 645-651.
93. Wislet-Gendebien S, Hans G, Leprince P, Rigo JM, Moonen G, Rogister B (2005) Plasticity of cultured mesenchymal stem cells: switch from nestin-positive to excitable neuron-like phenotype. Stem Cells 23(3): 392-402.
94. Wislet-Gendebien S, Leprince P, Moonen G, Rogister B (2003) Regulation of neural markers nestin and GFAP expression by cultivated bone marrow stromal cells. J Cell Sci 116(Pt 16): 3295-3302.
95. Woodbury D, Schwarz EJ, Prockop DJ, Black IB (2000) Adult rat and human bone marrow stromal cells differentiate into neurons. J Neurosci Res 61(4): 364-370.
96. Ma K, Fox L, Shi G, Shen J, Liu Q, Pappas JD, Cheng J, Qu T (2011) Generation of neural stem cell-like cells from bone marrow-derived human mesenchymal stem cells. Neurol Res 33(10): 1083-1093. doi: 10. 1179/1743132811Y. 0000000053.
97. Kitada M (2012) Mesenchymal cell populations: development of the induction systems for Schwann cells and neuronal cells and finding the unique stem cell population. Anat Sci Int 87(1): 24-44. doi: 10. 1007/s12565-011-0128-4.
98. Maltman DJ, Hardy SA, Przyborski SA (2011) Role of mesenchymal stem cells in neurogenesis and nervous system repair. Neurochem Int 59(3): 347-356. doi: 10. 1016/j. neuint. 2011. 06. 008.
99. Struys T, Moreels M, Martens W, Donders R, Wolfs E, Lambrichts I (2011) Ultrastructural and immunocytochemical analysis of multilineage differentiated human dental pulp- and umbilical cord-derived mesenchymal stem cells. Cells Tissues Organs 193(6): 366-378. doi: 10. 1159/000321400.
100. De Miguel MP, Fuentes-Julian S, Blazquez-Martinez A, Pascual CY, Aller MA, Arias J, Arnalich-Montiel F (2012) Immunosuppressive properties of mesenchymal stem cells: advances and applications. Curr Mol Med 12(5): 574-591.
101. Nauta AJ, Fibbe WE (2007) Immunomodulatory properties of mesenchymal stromal cells. Blood 110(10): 3499-3506. doi: 10. 1182/blood-2007-02-069716.
102. Ding G, Liu Y, An Y, Zhang C, Shi S, Wang W, Wang S (2010) Suppression of T cell proliferation by root apical papilla stem cells in vitro. Cells Tissues Organs 191(5): 357-364. doi: 10. 1159/000276589.
103. 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.
104. Tomic S, Djokic J, Vasilijic S, Vucevic D, Todorovic V, Supic G, Colic M (2011) Immunomodulatory properties of mesenchymal stem cells derived from dental pulp and dental follicle are susceptible to activation by toll-like receptor agonists. Stem Cells Dev 20(4): 695-708. doi: 10. 1089/scd. 2010. 0145.
105. Wada N, Menicanin D, Shi S, Bartold PM, Gronthos S (2009) Immunomodulatory properties of human periodontal ligament stem cells. J Cell Physiol 219(3): 667-676. doi: 10. 1002/jcp. 21710.
106. Yamaza T, Kentaro A, Chen C, Liu Y, Shi Y, Gronthos S, Wang S, Shi S (2010) Immunomodulatory properties of stem cells from human exfoliated deciduous teeth. Stem Cell Res Ther 1(1): 5. doi: 10. 1186/scrt5.
107. Karaoz E, Dogan BN, Aksoy A, Gacar G, Akyuz S, Ayhan S, Genc ZS, Yuruker S, Duruksu G, Demircan PC, Sariboyaci AE (2010) Isolation and in vitro characterisation of dental pulp stem cells from natal teeth. Histochem Cell Biol 133(1): 95-112.
108. Huang AH, Snyder BR, Cheng PH, Chan AW (2008) Putative dental pulp-derived stem/stromal cells promote proliferation and differentiation of endogenous neural cells in the hippocampus of mice. Stem Cells 26(10): 2654-2663.
109. Sasaki R, Aoki S, Yamato M, Uchiyama H, Wada K, Okano T, Ogiuchi H (2008) Neurosphere generation from dental pulp of adult rat incisor. Eur J Neurosci 27(3): 538-548.
110. Kadar K, Kiraly M, Porcsalmy B, Molnar B, Racz GZ, Blazsek J, Kallo K, Szabo EL, Gera I, Gerber G, Varga G (2009) Differentiation potential of stem cells from human dental origin-promise for tissue engineering. J Physiol Pharmacol 60(Suppl 7): 167-175.
111. Osathanon T, Nowwarote N, Pavasant P (2011) Basic fibroblast growth factor inhibits mineralization but induces neuronal differentiation by human dental pulp stem cells through a FGFR and PLCgamma signaling pathway. J Cell Biochem 112(7): 1807-1816.
112. Apel C, Forlenza OV, de Paula VJ, Talib LL, Denecke B, Eduardo CP, Gattaz WF (2009) The neuroprotective effect of dental pulp cells in models of Alzheimer's and Parkinson's disease. J Neural Transm 116(1): 71-78.
113. de Almeida FM, Marques SA, Ramalho Bdos S, Rodrigues RF, Cadilhe DV, Furtado D, Kerkis I, Pereira LV, Rehen SK, Martinez AM (2011) Human dental pulp cells: a new source of cell therapy in a mouse model of compressive spinal cord injury. J Neurotrauma 28(9): 1939-1949. doi: 10. 1089/neu. 2010. 1317.
114. Struys T, Ketkar-Atre A, Gervois P, Leten C, Hilkens P, Martens W, Bronckaers A, Dresselaers T, Politis C, Lambrichts I, Himmelreich U (2012) Magnetic resonance imaging of human dental pulp stem cells in vitro and in vivo. Cell Transplant. doi: 10. 3727/096368912X657774.
115. Sasaki R, Aoki S, Yamato M, Uchiyama H, Wada K, Ogiuchi H, Okano T, Ando T (2011) PLGA artificial nerve conduits with dental pulp cells promote facial nerve regeneration. J Tissue Eng Regen Med. doi: 10. 1002/term. 387.
116. Kress B, Gottschalk A, Anders L, Stippich C, Palm F, Bahren W, Sartor K (2004) High-resolution dental magnetic resonance imaging of inferior alveolar nerve responses to the extraction of third molars. Eur Radiol 14(8): 1416-1420.
117. Valmaseda-Castellon E, Berini-Aytes L, Gay-Escoda C (2001) Inferior alveolar nerve damage after lower third molar surgical extraction: a prospective study of 1117 surgical extractions. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 92(4): 377-383.
118. Alhassani AA, AlGhamdi AS (2010) Inferior alveolar nerve injury in implant dentistry: diagnosis, causes, prevention, and management. J Oral Implantol 36(5): 401-407.
119. Erbay SH, Bhadelia RA, O'Callaghan M, Gupta P, Riesenburger R, Krackov W, Polak JF (2006) Nerve atrophy in severe trigeminal neuralgia: noninvasive confirmation at MR imaging-initial experience. Radiology 238(2): 689-692.
120. Smith MH, Lung KE (2006) Nerve injuries after dental injection: a review of the literature. J Can Dent Assoc 72(6): 559-564.
121. Jones RH (2010) The use of vein grafts in the repair of the inferior alveolar nerve following surgery. Aust Dent J 55(2): 207-213.
122. Satar B, Karahatay S, Kurt B, Ural AU, Safali M, Avcu F, Oztas E, Kucuktag Z (2009) Repair of transected facial nerve with mesenchymal stromal cells: histopathologic evidence of superior outcome. Laryngoscope 119(11): 2221-2225.
123. Atsumi Y, Imai T, Matsumoto K, Sakuda M, Maeda T, Kurisu K, Wakisaka S (2000) Effects of different types of injury to the inferior alveolar nerve on the behavior of Schwann cells during the regeneration of periodontal nerve fibers of rat incisor. Arch Histol Cytol 63(1): 43-54.
124. Tohill M, Mantovani C, Wiberg M, Terenghi G (2004) Rat bone marrow mesenchymal stem cells express glial markers and stimulate nerve regeneration. Neurosci Lett 362(3): 200-203.
125. Walsh S, Midha R (2009) Practical considerations concerning the use of stem cells for peripheral nerve repair. Neurosurg Focus 26(2): E2.
126. Brohlin M, Mahay D, Novikov LN, Terenghi G, Wiberg M, Shawcross SG, Novikova LN (2009) Characterisation of human mesenchymal stem cells following differentiation into Schwann cell-like cells. Neurosci Res 64(1): 41-49.
127. Caddick J, Kingham PJ, Gardiner NJ, Wiberg M, Terenghi G (2006) Phenotypic and functional characteristics of mesenchymal stem cells differentiated along a Schwann cell lineage. Glia 54(8): 840-849.
128. Dezawa M, Takahashi I, Esaki M, Takano M, Sawada H (2001) Sciatic nerve regeneration in rats induced by transplantation of in vitro differentiated bone-marrow stromal cells. Eur J Neurosci 14(11): 1771-1776.
129. Keilhoff G, Goihl A, Langnase K, Fansa H, Wolf G (2006) Transdifferentiation of mesenchymal stem cells into Schwann cell-like myelinating cells. Eur J Cell Biol 85(1): 11-24.
130. Ladak A, Olson J, Tredget EE, Gordon T (2011) Differentiation of mesenchymal stem cells to support peripheral nerve regeneration in a rat model. Exp Neurol 228(2): 242-252.
131. Lin W, Chen X, Wang X, Liu J, Gu X (2008) Adult rat bone marrow stromal cells differentiate into Schwann cell-like cells in vitro. In Vitro Cell Dev Biol 44(1-2): 31-40.
132. Mimura T, Dezawa M, Kanno H, Sawada H, Yamamoto I (2004) Peripheral nerve regeneration by transplantation of bone marrow stromal cell-derived Schwann cells in adult rats. J Neurosurg 101(5): 806-812.