Amelogenin enhances the osteogenic differentiation of mesenchymal stem cells derived from bone marrow

Cells Tissues Organs

Volumn 196, Issue 5, 2012, Pages 411-419

  Tanimoto, K ^a   Huang, Y C ^a   Tanne, Y ^a   Kunimatsu, R ^a   Michida, M ^a   Yoshioka, M ^a   Ozaki, N ^a   Sasamoto, T ^a   Yoshimi, Y ^a   Kato, Y ^a   Tanne, K ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

Amelogenin; Bone regeneration; Cell biology; Differentiation; Mesenchymal stem cell

Indexed keywords

ALIZARIN RED S; ALKALINE PHOSPHATASE; AMELOGENIN; BONE SIALOPROTEIN; CALCIUM; CELL MARKER; COLLAGEN TYPE 1; MESSENGER RNA; OSTEOPONTIN; RECOMBINANT HUMAN FULL LENGTH AMELOGENIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

ALKALINE PHOSPHATASE BLOOD LEVEL; ARTICLE; BONE MARROW CELL; BONE MARROW CULTURE; BONE MINERALIZATION; CALCIUM BONE LEVEL; CELL DIFFERENTIATION; CELL ISOLATION; CONTROLLED STUDY; CULTURE MEDIUM; HUMAN; HUMAN CELL; INTENSITY MODULATED RADIATION THERAPY; MESENCHYMAL STEM CELL; OSTEOBLAST; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION;

AMELOGENIN; BONE MARROW CELLS; CELL DIFFERENTIATION; CELLS, CULTURED; HUMANS; MESENCHYMAL STROMAL CELLS; OSTEOGENESIS; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84867743864     PISSN: 14226405     EISSN: 14226421     Source Type: Journal    
DOI: 10.1159/000335912     Document Type: Article

References (50)

1. Aubin, J.E., F. Liu (1996) The osteoblast lineage; in Bilezikian, L.G., L.G. Raisz, G.A. Rodan (eds): Principles of Bone iology. San Diego, Academic Press, pp 51-67.
2. Bianco, P., M. Riminucci, G. Silvestrini, E. Bonucci, J.D. Termine, L.W. Fisher, P.G. Robey (1993) Localization of bone sialoprotein (BSP) to Golgi and post-Golgi secretory structures in osteoblasts and to discrete sites in early bone matrix. J Histochem Cytochem 41: 193-203.
3. Briquet, A., S. Dubois, S. Bekaert, M. Dolhet, Y. Beguin, A. Gothot (2009) Prolonged ex vivo culture of human bone marrow mesenchymal stem cells influences their supportive activity toward NOD/SCID-repopulating cells and committed progenitor cells of B lymphoid and myeloid lineages. Haematologica 95: 47-56.
4. Butler, W.T. (1989) The nature and significance of osteopontin. Connect Tissue Res 23: 123-136.
5. Castillo, A.B., C.R. Jacobs (2010) Mesenchymal stem cell mechanobiology. Curr Osteoporos Rep 8: 98-104.
6. Cook, N.R., P.E. Row, H.W. Davidson (2004) Lysosome associated membrane protein 1 (LAMP1) traffics directly from the TGN to early endosomes. Traffic 5: 685-699.
7. DenBesten, P.K., Y. Yan, J.D. Featherstone, J.F. Hilton, C.E. Smith, W. Li (2002) Effects of fluoride on rat dental enamel matrix proteinases. Arch Oral Biol 47: 763-770.
8. Du, C., G. Falini, S. Fermani, C. Abbott, J. Moradian-Oldak (2005) Supramolecular assembly of amelogenin nanospheres into birefringent microribbons. Science 307: 1450- 1454.
9. Ducy, P., C. Desbois, B. Boyce, G. Pinero, B. Story, C. Dunstan, E. Smith, J. Bonadio, S. Goldstein, C. Gundberg, A. Bradley, G. Karsenty (1996) Increased bone formation in osteocalcin-deficient mice. Nature 382: 448- 452.
10. Fincham, A.G., J. Moradian-Oldak, J.P. Simmer (1999) The structural biology of the developing dental enamel matrix. J Struct Biol 126: 270-299.
11. Fong, C.D., L. Hammarstrom (2000) Expression of amelin and amelogenin in epithelial root sheath remnants of fully formed rat molars. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 90: 218-223.
12. Gregory, C.A., W.G. Gunn, A. Peister, D.J. Prockop (2004) An alizarin red-based assay of mineralization by adherent cells in culture: Comparison with cetylpyridinium chloride extraction. Anal Biochem 329: 77- 84.
13. Grigoriadis, A.E., J.N. Heersche, J.E. Aubin (1988) Differentiation of muscle, fat, cartilage, and bone from progenitor cells present in a bone-derived clonal cell population: Effect of dexamethasone. J Cell Biol 106: 2139- 2151.
14. Hammarstrom, L. (1997) Enamel matrix, cementum development and regeneration. J Clin Periodontol 24: 658-668.
15. Hammarstrom, L., L. Heijl, S. Gestrelius (1997) Periodontal regeneration in a buccal dehiscence model in monkeys after application of enamel matrix proteins. J Clin Periodontol 24: 669-677.
16. Hatakeyama, J., T. Sreenath, Y. Hatakeyama, T. Thyagarajan, L. Shum, C.W. Gibson, J.T. Wright, A.B. Kulkarni (2003) The receptor activator of nuclear factor-kappa B ligandmediated osteoclastogenic pathway is elevated in amelogenin-null mice. J Biol Chem 278: 35743-35748.
17. Haylock, D.N., S.K. Nilsson (2006) Osteopontin: A bridge between bone and blood. Br J Haematol 134: 467-474.
18. Haze, A., A.L. Taylor, A. Blumenfeld, E. Rosenfeld, Y. Leiser, L. Dafni, B. Shay, Y. Gruenbaum-Cohen, E. Fermon, S. Haegewald, J.P. Bernimoulin, D. Deutsch (2007) Amelogenin expression in long bone and cartilage cells and in bone marrow progenitor cells. Anat Rec (Hoboken) 290: 455-460.
19. Haze, A., A.L. Taylor, S. Haegewald, Y. Leiser, B. Shay, E. Rosenfeld, Y. Gruenbaum- Cohen, L. Dafni, B. Zimmermann, K. Heikinheimo, C.W. Gibson, L.W. Fisher, M.F. Young, A. Blumenfeld, J.P. Bernimoulin, D. Deutsch (2009) Regeneration of bone and periodontal ligament induced by recombinant amelogenin after periodontitis. J Cell Mol Med 13: 1110-1124.
20. He, J., J. Jiang, K.E. Safavi, L.S. Spangberg, Q. Zhu (2004) Emdogain promotes osteoblast proliferation and differentiation and stimulates osteoprotegerin expression. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97: 239-245.
21. Heijl, L. (1997) Periodontal regeneration with enamel matrix derivative in one human experimental defect. A case report. J Clin Periodontol 24: 693-696.
22. Inage, T., H. Shimokawa, K. Wakao, S. Sasaki (1996) Gene expression and localization of amelogenin in the rat incisor. Adv Dent Res 10: 201-207.
23. Iwata, T., Y. Morotome, T. Tanabe, M. Fukae, I. Ishikawa, S. Oida (2002) Noggin blocks osteoinductive activity of porcine enamel extracts. J Dent Res 81: 387-391.
24. Janones, D.S., L.F. Massa, V.E. Arana- Chavez (2005) Immunocytochemical examination of the presence of amelogenin during the root development of rat molars. Arch Oral Biol 50: 527-532.
25. Jue, S.S., W.Y. Lee, Y.D. Kwon, Y.R. Kim, A. Pae, B. Lee (2010) The effects of enamel matrix derivative on the proliferation and differentiation of human mesenchymal stem cells. Clin Oral Implants Res 21: 741-746.
26. Kawase, T., K. Okuda, M. Momose, Y. Kato, H. Yoshie, D.M. Burns (2001) Enamel matrix derivative (Emdogain) rapidly stimulates phosphorylation of the MAP kinase family and nuclear accumulation of Smad2 in both oral epithelial and fibroblastic human cells. J Periodontal Res 36: 367-376.
27. Kemoun, P., S. Gronthos, M.L. Snead, J. Rue, B. Courtois, F. Vaysse, J.P. Salles, G. Brunel (2011) The role of cell surface markers and enamel matrix derivatives on human periodontal ligament mesenchymal progenitor responses in vitro. Biomaterials 32: 7375-7388.
28. Kemoun, P., S. Laurencin-Dalicieux, J. Rue, J.C. Farges, I. Gennero, F. Conte-Auriol, F. Briand-Mesange, M. Gadelorge, H. Arzate, A.S. Narayanan, G. Brunel, J.P. Salles (2007) Human dental follicle cells acquire cementoblast features under stimulation by BMP-2/-7 and enamel matrix derivatives (EMD) in vitro. Cell Tissue Res 329: 283-294.
29. Li, W., C. Gao, Y. Yan, P. DenBesten (2003) X-linked amelogenesis imperfecta may result from decreased formation of tyrosine rich amelogenin peptide (TRAP). Arch Oral Biol 48: 177-183.
30. Lyngstadaas, S.P., E. Lundberg, H. Ekdahl, C. Andersson, S. Gestrelius (2001) Autocrine growth factors in human periodontal ligament cells cultured on enamel matrix derivative. J Clin Periodontol 28: 181-188.
31. McCulloch, C.A., A.H. Melcher (1983) Cell density and cell generation in the periodontal ligament of mice. Am J Anat 167: 43-58.
32. Mygind, T., M. Stiehler, A. Baatrup, H. Li, X. Zou, A. Flyvbjerg, M. Kassem, C. Bunger (2007) Mesenchymal stem cell ingrowth and differentiation on coralline hydroxyapatite scaffolds. Biomaterials 28: 1036-1047.
33. Nebgen, D.R., H. Inoue, B. Sabsay, K. Wei, C.S. Ho, A. Veis (1999) Identification of the chondrogenic-inducing activity from bovine dentin (bCIA) as a low-molecular-mass amelogenin polypeptide. J Dent Res 78: 1484- 1494.
34. Neuhuber, B., S.A. Swanger, L. Howard, A. Mackay, I. Fischer (2008) Effects of plating density and culture time on bone marrow stromal cell characteristics. Exp Hematol 36: 1176-1185.
35. Papagerakis, P., M. MacDougall, D. Hotton, I. Bailleul-Forestier, M. Oboeuf, A. Berdal (2003) Expression of amelogenin in odontoblasts. Bone 32: 228-240.
36. Pittenger, M.F., A.M. Mackay, S.C. Beck, R.K. Jaiswal, R. Douglas, J.D. Mosca, M.A. Moorman, D.W. Simonetti, S. Craig, D.R. Marshak (1999) Multilineage potential of adult human mesenchymal stem cells. Science 284: 143-147.
37. Reseland, J.E., S. Reppe, A.M. Larsen, H.S. Berner, F.P. Reinholt, K.M. Gautvik, I. Slaby, S.P. Lyngstadaas (2006) The effect of enamel matrix derivative on gene expression in osteoblasts. Eur J Oral Sci 114(suppl 1): 205- 211.
38. Saito, K., I. Konishi, M. Nishiguchi, T. Hoshino, T. Fujiwara (2008) Amelogenin binds to both heparan sulfate and bone morphogenetic protein 2 and pharmacologically suppresses the effect of noggin. Bone 43: 371-376.
39. Sasano, Y., J.X. Zhu, S. Kamakura, S. Kusunoki, I. Mizoguchi, M. Kagayama (2000) Expression of major bone extracellular matrix proteins during embryonic osteogenesis in rat mandibles. Anat Embryol (Berl) 202: 31- 37.
40. Shimizu, E., R. Saito, Y. Nakayama, Y. Nakajima, N. Kato, H. Takai, D.S. Kim, M. Arai, J. Simmer, Y. Ogata (2005) Amelogenin stimulates bone sialoprotein (BSP) expression through fibroblast growth factor 2 response element and transforming growth factor-beta1 activation element in the promoter of the BSP gene. J Periodontol 76: 1482-1489.
41. Tanabe, T., M. Fukae, T. Uchida, M. Shimizu (1992) The localization and characterization of proteinases for the initial cleavage of porcine amelogenin. Calcif Tissue Int 51: 213- 217.
42. Tompkins, K., A. George, A. Veis (2006) Characterization of a mouse amelogenin [A- 4]/M59 cell surface receptor. Bone 38: 172- 180.
43. Tsutsumi, S., A. Shimazu, K. Miyazaki, H. Pan, C. Koike, E. Yoshida, K. Takagishi, Y. Kato (2001) Retention of multilineage differentiation potential of mesenchymal cells during proliferation in response to FGF. Biochem Biophys Res Commun 288: 413-419.
44. Veis, A. (2003) Amelogenin gene splice products: Potential signaling molecules. Cell Mol Life Sci 60: 38-55.
45. Wakida, K., N. Amizuka, C. Murakami, T. Satoda, M. Fukae, J.P. Simmer, H. Ozawa, T. Uchida (1999) Maturation ameloblasts of the porcine tooth germ do not express amelogenin. Histochem Cell Biol 111: 297-303.
46. Weissman, I.L. (2000) Stem cells: Units of development, units of regeneration, and units in evolution. Cell 100: 157-168.
47. Wen, X., W.P. Cawthorn, O.A. MacDougald, S.I. Stupp, M.L. Snead, Y. Zhou (2011) The influence of leucine-rich amelogenin peptide on MSC fate by inducing Wnt10b expression. Biomaterials 32: 6478-6486.
48. Xu, L., H. Harada, A. Taniguchi (2008) The effects of LAMP1 and LAMP3 on M180 amelogenin uptake, localization and amelogenin mRNA induction by amelogenin protein. J Biochem 144: 531-537.
49. Zhang, H., K. Tompkins, J. Garrigues, M.L. Snead, C.W. Gibson, M.J. Somerman (2010) Full length amelogenin binds to cell surface LAMP-1 on tooth root/periodontium associated cells. Arch Oral Biol 55: 417-425.
50. Zhu, J.X., Y. Sasano, I. Takahashi, I. Mizoguchi, M. Kagayama (2001) Temporal and spatial gene expression of major bone extracellular matrix molecules during embryonic mandibular osteogenesis in rats. Histochem J 33: 25-35.