A comparison of the in vitro mineralisation and dentinogenic potential of mesenchymal stem cells derived from adipose tissue, bone marrow and dental pulp

Journal of Bone and Mineral Metabolism

Volumn 33, Issue 4, 2015, Pages 371-382

  Davies, O G ^a   Cooper, P R ^a   Shelton, R M ^a   Smith, A J ^a   Scheven, B A ^a  

^a UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

Dentine; Micro computed tomography; Mineralisation; MSC

Indexed keywords

5' NUCLEOTIDASE; BETA1 INTEGRIN; DENTIN MATRIX PROTEIN 1; ENDOGLIN; THY 1 ANTIGEN; DENTIN SIALOPHOSPHOPROTEIN; PHOSPHOPROTEIN; SCLEROPROTEIN; SIALOGLYCOPROTEIN;

ADIPOGENESIS; ADIPOSE TISSUE DERIVED MESENCHYMAL STEM CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW DERIVED MESENCHYMAL STEM CELL; BONE MINERALIZATION; CELL COMPONENT; CELL DIFFERENTIATION; CELL SELECTION; COMPARATIVE STUDY; CONTROLLED STUDY; DENTINE MATRIX COMPONENT; FLOW CYTOMETRY; FLUORESCENCE ACTIVATED CELL SORTING; GENE EXPRESSION; IN VITRO STUDY; LIMIT OF QUANTITATION; MALE; MESENCHYMAL STEM CELL; MICRO-COMPUTED TOMOGRAPHY; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TISSUE ENGINEERING; TOOTH DEVELOPMENT; TOOTH PULP DERIVED MESENCHYMAL STEM CELL; ADIPOSE TISSUE; ANIMAL; BONE MARROW CELL; CELL CULTURE; CELL CULTURE TECHNIQUE; CELL PROLIFERATION; CELL SEPARATION; CHEMISTRY; CYTOLOGY; GENE EXPRESSION REGULATION; MESENCHYMAL STROMA CELL; PHENOTYPE; PHYSIOLOGY; REGENERATIVE MEDICINE; TOOTH PULP; WISTAR RAT;

ADIPOGENESIS; ADIPOSE TISSUE; ANIMALS; BONE MARROW CELLS; CELL CULTURE TECHNIQUES; CELL DIFFERENTIATION; CELL PROLIFERATION; CELL SEPARATION; CELLS, CULTURED; DENTAL PULP; DENTINOGENESIS; EXTRACELLULAR MATRIX PROTEINS; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; MALE; MESENCHYMAL STROMAL CELLS; PHENOTYPE; PHOSPHOPROTEINS; RATS; RATS, WISTAR; REGENERATIVE MEDICINE; SIALOGLYCOPROTEINS;

EID: 84907966717     PISSN: 09148779     EISSN: 14355604     Source Type: Journal    
DOI: 10.1007/s00774-014-0601-y     Document Type: Article

References (69)

1. Shi S, Bartold PM, Miura M, Seo BM, Robey PG, Gronthos S (2005) The efficacy of mesenchymal stem cells to regenerate and repair dental structures. Orthod Craniofac Res 8:191–199
2. Alfotawei R, Naudi KB, Lappin D, Barbenel J, Di Silvio L, Hunter K, McMahon J, Avoub A (2014) The use of TriCalcium phosphate (TCP) and stem cells for the regeneration of osteoperiosteal critical-size mandibular bony defects, an in vitro and preclinical study. J Craniomaxillofac Surg. doi:10.1016/j.jcms.2013.12.006
3. Lin Y, Luo E, Chen X, Liu L, Qiao J, Yan Z, Li Z, Tang W, Zheng X, Tian W (2005) Molecular and cellular characterization during chondrogenic differentiation of adipose tissue-derived stromal cells in vitro and cartilage formation in vivo. J Cell Mol Med 9:929–939
4. Liu TM, Martina M, Hutmacher DW, Hui JH, Lee EH, Lim B (2007) Identification of common pathways mediating differentiation of bone marrow- and adipose tissue-derived human mesenchymal stem cells into three mesenchymal lineages. Stem Cells 25:750–760
5. Zuk PA, Zhu M, Mizuno H, Huang J, Futrell JW, Katz AJ (2001) Multilineage cells from human adipose tissue: implications for cell-based therapies. Tissue Eng 7:211–228
6. Owen M, Friedenstein AJ (1988) Stromal stem cells: marrow-derived osteogenic precursors. Ciba Found Symp 136:42–60
7. 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 USA 97:13625–13630
8. Nakashima M, Mizunuma K, Murakami T, Akamine A (2002) Induction of dental pulp stem cell differentiation into odontoblasts by electroporation-mediated gene delivery of growth/differentiation factor 11 (GDF11). Gene Ther 9:814–818
9. Wu L, Zhu F, Wu Y, Lin Y, Nie X, Jing W, Qiao J, Liu L, Tang W, Zheng X, Tian W (2008) Dentin sialophosphoprotein-promoted mineralisation and expression of odontogenic genes in adipose-derived stromal cells. Cells Tissues Organs 187:103–112
10. Prescott RS, Alsanea R, Fayad MI, Johnson BR, Wenckus CS, Hao J, John AS, George A (2008) In vivo generation of dental pulp-like tissue by using dental pulp stem cells, a collagen scaffold and dentine matrix protein 1 after subcutaneous transplantation in mice. J Endod 34:4216
11. Lei G, Yu Y, Jiang Y, Wang S, Yan M, Smith AJ (2013) Differentiation of BMMSCs into odontoblast-like cells induced by natural dentine matrix. Arch Oral Biol 58:862–870
12. Smith AJ, Tobias RS, Plant CG, Browne RM, Lesot H, Ruch JV (1990) In vivo morphogenetic activity of dentine matrix proteins. J Biol Buccale 18:123–129
13. Smith AJ, Tobias RS, Cassidy N, Plant CG, Browne RM, Begue-Kirn C, Ruch JV, Lesot H (1994) Odontoblast stimulation in ferrets by dentine matrix components. Arch Oral Biol 39:13–22
14. Smith AJ, Scheven BA, Takahashi Y, Ferracane JL, Shelton RM, Cooper PR (2012) Dentine as a bioactive extracellular matrix. Arch Oral Biol 57:109–121
15. Liu J, Jin T, Ritchie H, Smith AJ, Clarkson BH (2005) In vitro differentiation and mineralisation of human dental pulp cells induced by dentin extract. In Vitro Cell Dev Biol Anim 41:232–238
16. Chun SY, Lee HJ, Choi YA, Kim KM, Baek SH, Park HS, Kim JY, Ahn JM, Cho JY, Cho DW, Shin HI, Park EK (2011) Analysis of the soluble human tooth proteome and its ability to induce dentin/tooth regeneration. Tissue Eng Part A 17:181–191
17. Yu Y, Wang L, Yu J, Lei G, Yan M, Smith G, Cooper PR, Tang C, Zhang G, Smith AJ (2014) Dentin matrix proteins (DMPs) enhance differentiation of BMMSCs via ERK and p38 MAPK pathways. Cell Tissue Res 356(1):171–182. doi:10.1007/s00441-013-1790-8
18. Schaffler A, Buchler C (2007) Concise review: adipose tissue-derived stromal cells–basic and clinical implications for novel cell-based therapies. Stem Cells 25:818–827
19. Patel M, Smith AJ, Sloan AJ, Smith G, Cooper PR (2009) Phenotype and behaviour of dental pulp cells during expansion culture. Arch Oral Biol 54:898–908
20. Clarke PR, Williams HI (1975) Ossification of extradural fat in Paget’s disease of the spine. Br J Surg 62:571–572
21. Shackelford GD, Barton LL, Mcalister WH (1975) Calcified subcutaneous fat necrosis in infancy. J Can Assoc Radiol 26:203–207
22. Zaminy A, Ragerdi Kashani I, Barbarestani M, Hedayatpour A, Mahmoudi R, Farzaneh NEJADA (2008) Osteogenic differentiation of rat mesenchymal stem cells from adipose tissue in comparison with bone marrow mesenchymal stem cells: melatonin as a differentiation factor. Iran Biomed J 12:133–141
23. Hayashi O, Katsubi Y, Hirose M, Ohgushi H, Ito H (2008) Comparison of osteogenic ability of rat mesenchymal stem cells from bone marrow, periosteum, and adipose tissue. Calcif Tissue Int 82:238–247
24. De Ugarte DA, Morizono K, Elbarbary A, Alfonso Z, Zuk PA, Zhu M (2003) Comparison of multi-lineage cells from human adipose tissue and bone marrow. Cells Tissues Organs 174:101–109
25. Izadpanah R, Trygg C, Patel B, Kriedt C, Dufour J, Gimble JM, Bunnell BA (2006) Biologic properties of mesenchymal stem cells derived from bone marrow and adipose tissue. J Cell Biochem 99:1285–1297
26. Ferro F, Spelat R, Falini G, Gallelli A, D’Aurizio F, Puppato E, Ambesi-Impiombato FS, Curcio F (2011) Adipose tissue-derived stem cell in vitro differentiation in a three-dimensional dental bud structure. Am J Pathol 178:2299–2310
27. Hung CN, Mar K, Chang HC, Chiang YL, Hu HY, Lai CC, Chu RM, Ma CM (2011) A comparison between adipose tissue and dental pulp as sources of MCSs for tooth regeneration. Biomaterials 32:6995–7005
28. Zuk PA, Zhu M, Ashjian P, De Ugarte DA, Huang JI, Mizuno H (2002) Human adipose tissue is a source of multipotent stem cells. Mol Biol Cell 13:4279–4295
29. Soleimani M, Nadri S (2009) A protocol for isolation and culture of mesenchymal stem cells from mouse bone marrow. Nat Protoc 4:102–106
30. Gronthos S, Li W, Fisher LW, Cherman N, Boyde A (2002) Stem cell properties of human dental pulp stem cells. J Dent Res 81:531–535
31. Chung MT, Liu C, Hyun JS, Lo DD, Montoro DT, Hasegawa M, Li S, Sorkin M, Rennert R, Keeney M, Yang F, Quarto N, Longaker MT, Wan DC (2013) CD90 (Thy-1)-positive selection enhances osteogenic capacity of human adipose-derived stromal cells. Tissue Eng Part A 19:989–997
32. Gregory CA, Gunn WG, Peister A, Prockop DJ (2004) An alizarin red-based assay of mineralisation by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 1:77–84
33. Holager J (1970) Thermogravimetric examination of enamel and dentin. J Dent Res 49:546–548
34. Lim JJ, Liboff AR (1972) Thermogravimetric analysis of dentin. J Dent Res 51:509–514
35. Chen X, Lam YM (1997) Technical note: CT determination of the mineral density of dry bone specimens using the dipotassium phosphate phantom. Am J Phys Anthropol 103:557–560
36. Nazarian A, Snyder BD, Zurakowski D, Muller R (2008) Quantitated micro-computed tomography: a non-invasive method to assess equivalent bone mineral density. Bone 43:302–311
37. Smith AJ, Leaver AG (1981) Distribution of the EDTA-soluble non-collagenous organic matrix components of rabbit incisor dentine. Arch Oral Biol 26:643–649
38. Smith AJ, Smith G (1984) Proteolytic activity of rabbit incisor dentine. Archs Oral Biol 29:1049–1050
39. Dominici M, Le Blanc K, Mueller I, Slaper-Cortenbach I, Marini F, Krause D (2006) Minimal criteria for defining multipotent mesenchymal stromal cells. The International Society for Cellular Therapy position statement. Cytotherapy 8:315–317
40. Bruder SP, Kurth AA, Shea M, Hayes WC, Jaiswal N, Kadiyala S (1998) Bone regeneration by implantation of purified, culture-expanded mesenchymal stem cells. J Orthop Res 16:155–162
41. Kim HP, Ji YH, Rhee SC, Dhong ES, Park SH, Yoon ES (2012) Enhancement of bone regeneration using osteogenic-induced adipose-derived stem cells combined with demineralised bone matrix in a rat critically-sized calvarial defect model. Curr Stem Cell Res Ther 7:165–172
42. Kanafi MM, Ramesh A, Gupta PK, Bhonde RR (2013) Dental pulp stem cells immobilized in alginate microspheres in bone tissue engineering. Int Endod J. doi:10.1111/iej.12205
43. Caplan AI (2005) Mesenchymal stem cells: cell-based reconstructive therapy. Tissue Eng 11:7–8
44. Boxall SA, Jones E (2012) Markers for characterisation of bone marrow multipotent stromal cells. Stem Cells Int. doi:10.1155/2012/975871
45. Herbertson A, Aubin JE (1997) Cell sorting enriches osteogenic populations in rat bone marrow stromal cell cultures. Bone 21:491–500
46. Mollet M, Godoy-Silva R, Berdugo C, Chalmers JJ (2008) Computer simulations of the energy dissipation rate in a fluorescence-activated cell sorter: implications to cells. Biotechnol Bioeng 100:260–272
47. Harting M, Jimenez F, Pati S, Baumgartner J, Cox C (2008) Immunophenotype characterisation of rat mesenchymal stromal cells. Cytotherapy 10:243–253
48. Panchon-Pena G, Yu G, Tucker A, Wu X, Vendrell J, Bunnell BA, Gimble JM (2011) Stromal stem cells from adipose tissue and bone marrow of age-matched female donors display distinct immunophenotypic profiles. J Cello Physiol 226:843–851
49. De Cuevas M, Matunis EL (2011) The stem cell niche: lessons from the Drosophila testis. Development 138:2861–2869
50. Kern S, Eichler H, Stoeve J, Kluter H, Bieback K (2006) Comparative analysis of mesenchymal stem cells bone marrow, umbilical cord blood, or adipose tissue. Stem Cells 24:1294–1301
51. Strioga M, Viswanathan S, Darinskas A, Slaby O, Michalek J (2012) Same or not the same? Comparison of adipose tissue-derived versus bone marrow-derived mesenchymal stem and stromal cells. Stem Cells Dev 20:2724–2752
52. Gough JE, Jones JR, Hench LL (2004) Nodule formation and mineralisation of human primary osteoblasts cultured on a porous bioactive glass scaffold. Biomaterials 25:2039–2046
53. Balic A, Mina M (2010) Characterization of progenitor cells in pulps of murine incisors. J Dent Res 89:1287–1292
54. Ito K, Yamada Y, Nakamura S, Ueda M (2011) Osteogenic potential of effective bone engineering using dental pulp stem cells, bone marrow stem cells and periosteal cells for osseointegration of dental implants. Int J Oral Maxillofac Implants 26:94754
55. Begue-Kirn C, Smith AJ, Ruch JV, Wozney JM, Purchio A, Hartmann D, Lesot H (1992) Effects of dentin proteins, transforming growth factor beta 1 (TGF beta 1) and bone morphogenetic protein 2 (BMP2) on the differentiation of odontoblasts in vitro. Int J Dev Biol 36:491–503
56. Butler WT, Brunn JC, Qin C (2003) Dentin extracellular matrix (ECM) proteins: comparison to bone ECM and contribution to dynamics of dentinogenesis. Connect Tissue Res 44:171–178
57. Goldberg M, Smith AJ (2004) Cells and extracellular matrices of dentin and pulp: a biological basis for repair and tissue engineering. Crit Rev Oral Biol Med 15:13–27
58. Henning T, Lorenz H, Thiel A, Goetzke K, Dickhut A, Gieger F, Richter W (2007) Reduced chondrogenic potential of adipose tissue derived stromal cells correlates with an altered TGFbeta receptor and BMP profile and is overcome by BMP-6. J Cell Physiol 211:682–691
59. Kumar A, Ruan M, Clifton K, Syed F, Khosla S, Oursler MJ (2012) TGF-β mediates suppression of adipogenesis by estradiol through connective tissue growth factor induction. Endocrinology 153:254–263
60. Ruan H, Hacohen N, Golub TR, Van Parijs L, Lodish HF (2002) Tumor necrosis factor-alpha suppresses adipocyte-specific genes and activates expression of preadipocyte genes in 3T3-L1 adipocytes: nuclear factor-kappaB activation by TNF-alpha is obligatory. Diabetes 51:1319–1336
61. Suzawa M, Takada I, Yanagisawa J, Ohtake F, Ogawa S, Yamauchi T, Kadowaki T, Takeuchi Y, Shibuya H, Gotoh Y, Matsumoto K, Kato S (2003) Cytokines suppress adipogenesis and PPAR-gamma function through the TAK1/TAKB1/NIK cascade. Nat Cell Biol 5:224–230
62. Graham L, Cooper PR, Cassidy N, Nor JE, Sloan AJ, Smith AJ (2006) The effect of calcium hydroxide on solubilisation of bio-active dentine matrix components. Biomaterials 27:2865–2873
63. Cooper PR, Takahashi Y, Graham LW, Simon S, Imazato S, Smith AJ (2010) Inflammation-regeneration interplay in the dentine-pulp complex. J Dent 38:687–697
64. Finkelman RD, Mohan S, Jennings JC, Taylor AK, Jepsen S, Baylink DJ (1990) Quantitation of growth factors IGF-I, SGF/IGF-II, and TGF-beta in human dentin. J Bone Miner Res 5:717–723
65. Roberts-Clark DJ, Smith AJ (2000) Angiogenic growth factors in human dentine matrix. Arch Oral Biol 45:1013–1016
66. Levi B, James AW, Wan DC, Glotzback JP, Commons GW, Longaker MT (2010) Regulation of human adipose-derived stromal cell osteogenic differentiation by insulin-like growth factor-1 and platelet-derived growth factor-alpha. Plast Reconstr Surg 126:41–52
67. Garcia JM, Martins MD, Jaeger RG, Marques MM (2003) Immunolocalisation of bone extracellular matrix proteins (type I collagen, osteonectin and bone sialoprotein) in human dental pulp and cultured pulp cells. Int Endod J 36:404–410
68. Qin C, D’Souza R, Feng JQ (2007) Dentin matrix protein 1 (DMP1): new and important roles for biomineralisation and phosphate homeostasis. J Dent Res 86:1134–1141
69. Tang SY, Allison T (2013) Regulation of postnatal bone homeostasis by TGFβ. Bonekey Rep 9:255