Synthetic peptides analogue to enamel proteins promote osteogenic differentiation of MC3T3-E1 and mesenchymal stem cells

Journal of Biomaterials and Tissue Engineering

Volumn 1, Issue 2, 2011, Pages 198-209

  Rubert, Marina ^a,b   Ramis, Joana Maria ^b   Vondrasek, Jiri ^c,d   Gayà, Antoni ^e   Lyngstadaas, Staale Petter ^a   Monjo, Marta ^a,b  

^a UNIVERSITY OF OSLO   (Norway)

^b UNIVERSITAT DE LES ILLES BALEARS   (Spain)

^c INSTITUTE OF BIOTECHNOLOGY   (Czech Republic)

^d INSTITUTE OF ORGANIC CHEMISTRY AND BIOCHEMISTRY   (Czech Republic)

^e Fundació Banc De Sang i Teixits De Les Illes Balears   (Spain)

Author keywords

Bone formation; In Vitro; Mineralization; Proline rich regions; Synthetic peptides

Indexed keywords

EID: 84861835328     PISSN: 21579083     EISSN: 21579091     Source Type: Journal    
DOI: 10.1166/jbt.2011.1018     Document Type: Article

References (65)

1. S. Weiner, I. Sagi, and L. Addadi, Structural biology. Choosing the crystallization path less traveled. Science 309, 1027 (2005).
2. T. Jin, Y. Ito, X. Luan, S. Dangaria, C. Walker, M. Allen, A. Kulkarni, C. Gibson, R. Braatz, X. Liao, and T. G. Diekwisch, Elongated polyproline motifs facilitate enamel evolution through matrix subunit compaction. PLoS Biol. 7, e1000262 (2009).
3. J. Hatakeyama, S. Fukumoto, T. Nakamura, N. Haruyama, S. Suzuki, Y. Hatakeyama, L. Shum, C. W. Gibson, Y. Yamada, and A. B. Kulkarni, Synergistic roles of amelogenin and ameloblastin. Journal of Dental Research 88, 318 (2009).
4. L. J. Ball, R. Kuhne, J. Schneider-Mergener, and H. Oschkinat, Recognition of proline-rich motifs by protein-protein-interaction domains. Angew Chem. Int. Ed. Engl. 44, 2852 (2005).
5. L. Biedermannova, K. E. Riley, K. Berka, P. Hobza, and J. Vondrasek, Another role of proline: Stabilization interactions in proteins and protein complexes concerning proline and tryptophane. Phys. Chem. Chem. Phys. 10, 6350 (2008).
6. D. Deutsch, A. Haze-Filderman, A. Blumenfeld, L. Dafni, Y. Leiser, B. Shay, Y. Gruenbaum-Cohen, E. Rosenfeld, E. Fermon, B. Zimmermann, S. Haegewald, J. P. Bernimoulin, and A. L. Taylor, Amelogenin, a major structural protein in mineralizing enamel, is also expressed in soft tissues: brain and cells of the hematopoietic system. Eur. J. Oral. Sci. 114, 183 (2006).
7. A. Haze, A. L. Taylor, A. Blumenfeld, E. Rosenfeld, Y. Leiser, L. Dafni, B. Shay, Y. Gruenbaum-Cohen, E. Fermon, S. Haegewald, J. P. Bernimoulin, and D. Deutsch, Amelogenin expression in long bone and cartilage cells and in bone marrow progenitor cells. Anat Rec (Hoboken) 290, 455 (2007).
8. C. D. Fong, R. Cerny, L. Hammarstrom, and I. Slaby, Sequential expression of an amelin gene in mesenchymal and epithelial cells during odontogenesis in rats. Eur. J. Oral. Sci. 106, 324 (1998).
9. A. Spahr, S. P. Lyngstadaas, I. Slaby, and G. Pezeshki, Ameloblastin expression during craniofacial bone formation in rats. Eur. J. Oral. Sci. 114, 504 (2006).
10. M. V. Tamburstuen, J. E. Reseland, A. Spahr, S. J. Brookes, G. Kvalheim, I. Slaby, M. L. Snead, and S. P. Lyngstadaas, Ameloblastin expression and putative autoregulation in mesenchymal cells suggest a role in early bone formation and repair. Bone 48, 406 (2011).
11. C. Du, G. B. Schneider, R. Zaharias, C. Abbott, D. Seabold, C. Stanford, and J. Moradian-Oldak, Apatite/amelogenin coating on titanium promotes osteogenic gene expression. Journal of Dental Research 84, 1070 (2005).
12. S. Lacerda-Pinheiro, D. Septier, K. Tompkins, A. Veis, M. Goldberg, and H. Chardin, Amelogenin gene splice products A+4 and A-4 implanted in soft tissue determine the reorientation of CD45-positive cells to an osteo-chondrogenic lineage. Journal of Biomedical Materials Research 79, 1015 (2006).
13. S. P. Lyngstadaas, E. Lundberg, H. Ekdahl, C. Andersson, and S. Gestrelius, Autocrine growth factors in human periodontal ligament cells cultured on enamel matrix derivative. J. Clin. Periodontol. 28, 181 (2001).
14. T. Nagano, S. Oida, S. Suzuki, T. Iwata, Y. Yamakoshi, Y. Ogata, K. Gomi, T. Arai, and M. Fukae, Porcine enamel protein fractions contain transforming growth factor-beta1. Journal of Periodontology 77, 1688 (2006).
15. J. Svensson, C. Andersson, J. E. Reseland, P. Lyngstadaas, and L. Bulow, Histidine tag fusion increases expression levels of active recombinant amelogenin in Escherichia coli. Protein Expression and Purification 48, 134 (2006).
16. A. Veis, K. Tompkins, K. Alvares, K. Wei, L. Wang, X. S. Wang, A. G. Brownell, S. M. Jengh, and K. E. Healy, Specific amelogenin gene splice products have signaling effects on cells in culture and in implants in vivo. J. Biol. Chem. 275, 41263 (2000).
17. R. Warotayanont, D. Zhu, M. L. Snead, and Y. Zhou, Leucine-rich amelogenin peptide induces osteogenesis in mouse embryonic stem cells. Biochemical and Biophysical Research Communications 367, 1 (2008).
18. D. D. Bosshardt, Biological mediators and periodontal regeneration: A review of enamel matrix proteins at the cellular and molecular levels. J. Clin. Periodontol. 35, 87 (2008).
19. S. P. Lyngstadaas, J. C. Wohlfahrt, S. J. Brookes, M. L. Paine, M. L. Snead, and J. E. Reseland, Enamel matrix proteins; old molecules for new applications. Orthodontics & Craniofacial Research 12, 243 (2009).
20. A. Sculean, F. Schwarz, J. Becker, and M. Brecx, The application of an enamel matrix protein derivative (Emdogain) in regenerative periodontal therapy: A review. Med. Princ. Pract. 16, 167 (2007).
21. J. He, J. Jiang, K. E. Safavi, L. S. Spangberg, and Q. Zhu, Emdogain promotes osteoblast proliferation and differentiation and stimulates osteoprotegerin expression. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 97, 239 (2004).
22. J. Jiang, A. F. Fouad, K. E. Safavi, L. S. Spangberg, and Q. Zhu, Effects of enamel matrix derivative on gene expression of primary osteoblasts. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 91, 95 (2001).
23. J. E. Reseland, S. Reppe, A. M. Larsen, H. S. Berner, F. P. Reinholt, K. M. Gautvik, I. Slaby, and S. P. Lyngstadaas, The effect of enamel matrix derivative on gene expression in osteoblasts. Eur. J. Oral. Sci. 114, 205 (2006).
24. T. Iwata, Y. Morotome, T. Tanabe, M. Fukae, I. Ishikawa, and S. Oida, Noggin blocks osteoinductive activity of porcine enamel extracts. Journal of Dental Research 81, 387 (2002).
25. M. Ohyama, N. Suzuki, Y. Yamaguchi, M. Maeno, K. Otsuka, and K. Ito, Effect of enamel matrix derivative on the differentiation of C2C12 cells. Journal of Periodontology 73, 543 (2002).
26. Z. Schwartz, D. L. Carnes, Jr., R. Pulliam, C. H. Lohmann, V. L. Sylvia, Y. Liu, D. D. Dean, D. L. Cochran, and B. D. Boyan, Porcine fetal enamel matrix derivative stimulates proliferation but not differentiation of pre-osteoblastic 2T9 cells, inhibits proliferation and stimulates differentiation of osteoblast-like MG63 cells, and increases proliferation and differentiation of normal human osteoblast NHOst cells. Journal of Periodontology 71, 1287 (2000).
27. J. C. Rincon, Y. Xiao, W. G. Young, and P. M. Bartold, Enhanced proliferation, attachment and osteopontin expression by porcine periodontal cells exposed to Emdogain. Archives of Oral Biology 50, 1047 (2005).
28. E. Shimizu, R. Saito, Y. Nakayama, Y. Nakajima, N. Kato, H. Takai, D. S. Kim, M. Arai, J. Simmer, and Y. Ogata, 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. Journal of Periodontology 76, 1482 (2005).
29. Y. Tokiyasu, T. Takata, E. Saygin, and M. Somerman, Enamel factors regulate expression of genes associated with cementoblasts. Journal of Periodontology 71, 1829 (2000).
30. S. Keila, C. E. Nemcovsky, O. Moses, Z. Artzi, and M. Weinreb, In vitro effects of enamel matrix proteins on rat bone marrow cells and gingival fibroblasts. Journal of Dental Research 83, 134 (2004).
31. S. Yoneda, D. Itoh, S. Kuroda, H. Kondo, A. Umezawa, K. Ohya, T. Ohyama, and S. Kasugai, The effects of enamel matrix derivative (EMD) on osteoblastic cells in culture and bone regeneration in a rat skull defect. Journal of Periodontal Research 38, 333 (2003).
32. F. Rathe, R. Junker, B. M. Chesnutt, and J. A. Jansen, The effect of enamel matrix derivative (Emdogain) on bone formation: A systematic review. Tissue Engineering 15, 215 (2009).
33. M. Kantlehner, P. Schaffner, D. Finsinger, J. Meyer, A. Jonczyk, B. Diefenbach, B. Nies, G. Holzemann, S. L. Goodman, and H. Kessler, Surface coating with cyclic RGD peptides stimulates osteoblast adhesion and proliferation as well as bone formation. Chembiochem 1, 107 (2000).
34. R. S. Bhatnagar, J. J. Qian, A. Wedrychowska, M. Sadeghi, Y. M. Wu, and N. Smith, Design of biomimetic habitats for tissue engineering with P-15, a synthetic peptide analogue of collagen. Tissue Eng. 5, 53 (1999).
35. M. Thorwarth, S. Schultze-Mosgau, F. Wehrhan, S. Srour, J. Wiltfang, F. W. Neukam, and K. A. Schlegel, Enhanced bone regeneration with a synthetic cell-binding peptide-in vivo results. Biochemical and Biophysical Research Communications 329, 789 (2005).
36. D. Itoh, S. Yoneda, S. Kuroda, H. Kondo, A. Umezawa, K. Ohya, T. Ohyama, and S. Kasugai, Enhancement of osteogenesis on hydroxyapatite surface coated with synthetic peptide (EEEEEEEPRGDT) in vitro. Journal of Biomedical Materials Research 62, 292 (2002).
37. C. D. Reyes, T. A. Petrie, K. L. Burns, Z. Schwartz, and A. J. Garcia, Biomolecular surface coating to enhance orthopaedic tissue healing and integration. Biomaterials 28, 3228 (2007).
38. J. Maupetit, P. Derreumaux, and P. Tuffery, A fast method for largescale de novo peptide and miniprotein structure prediction. J. Comput. Chem. 31, 726 (2010).
39. J. Maupetit, P. Derreumaux, and P. Tuffery, PEP-FOLD: an online resource for de novo peptide structure prediction. Nucleic Acids Res. 37, W498 (2009).
40. W. D. Cornell, P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Merz, D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman, A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. Journal of the American Chemical Society 117, 5179 (1995).
41. V. Hornak, R. Abel, A. Okur, B. Strockbine, A. Roitberg, and C. Simmerling, Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins 65, 712 (2006).
42. W. L. Jorgensen, J. Chandrasekhar, J. D. Madura, R. W. Impey, and M. L. Klein, Comparison of simple potential functions for simulating liquid water. The Journal of Chemical Physics 79, 926 (1983).
43. M. Dominici, K. Le Blanc, I. Mueller, I. Slaper-Cortenbach, F. Marini, D. Krause, R. Deans, A. Keating, D. Prockop, and E. Horwitz, Minimal criteria for defining multipotent mesenchymal stromal cells. The international society for cellular therapy position statement. Cytotherapy 8, 315 (2006).
44. E. Hinoi, S. Fujimori, and Y. Yoneda, Modulation of cellular differentiation by N-methyl-D-aspartate receptors in osteoblasts. FASEB J. 17, 1532 (2003).
45. W. J. Peterson, K. H. Tachiki, and D. T. Yamaguchi, Serial passage of MC3T3-E1 cells down-regulates proliferation during osteogenesis in vitro. Cell Prolif. 37, 325 (2004).
46. S. Bobis, D. Jarocha, and M. Majka, Mesenchymal stem cells: Characteristics and clinical applications. Folia Histochem Cytobiol. 44, 215 (2006).
47. D. R. Davenport, J. M. Mailhot, J. C. Wataha, M. A. Billman, M. M. Sharawy, and M. K. Shrout, Effects of enamel matrix protein application on the viability, proliferation, and attachment of human periodontal ligament fibroblasts to diseased root surfaces in vitro. J. Clin. Periodontol. 30, 125 (2003).
48. E. Zeldich, R. Koren, C. Nemcovsky, and M. Weinreb, Enamel matrix derivative stimulates human gingival fibroblast proliferation via ERK. Journal of Dental Research 86, 41 (2007).
49. S. Gestrelius, C. Andersson, D. Lidstrom, L. Hammarstrom, and M. Somerman, In vitro studies on periodontal ligament cells and enamel matrix derivative. J. Clin. Periodontol. 24, 685 (1997).
50. A. Gurpinar, M. A. Onur, Z. C. Cehreli, and F. Tasman, Effect of enamel matrix derivative on mouse fibroblasts and marrow stromal osteoblasts. Journal of Biomaterials Applications 18, 25 (2003).
51. N. Pischon, B. Zimmermann, J. P. Bernimoulin, and S. Hagewald, Effects of an enamel matrix derivative on human osteoblasts and PDL cells grown in organoid cultures. Oral Surgery, Oral Medicine, Oral Pathology, Oral Radiology, and Endodontics 102, 551 (2006).
52. L. Guida, M. Annunziata, F. Carinci, A. Di Feo, I. Passaro, and A. Oliva, In vitro biologic response of human bone marrow stromal cells to enamel matrix derivative. Journal of Periodontology 78, 2190 (2007).
53. G. S. Stein, J. B. Lian, J. L. Stein, A. J. Van Wijnen, and M. Montecino, Transcriptional control of osteoblast growth and differentiation. Physiological Reviews 76, 593 (1996).
54. J. E. Aubin, Advances in the osteoblast lineage. Biochem Cell Biol. 76, 899 (1998).
55. T. Tamura, N. Udagawa, N. Takahashi, C. Miyaura, S. Tanaka, Y. Yamada, Y. Koishihara, Y. Ohsugi, K. Kumaki, T. Taga, et al., Soluble interleukin-6 receptor triggers osteoclast formation by interleukin 6. Proc. Natl. Acad. Sci. USA 90, 11924 (1993).
56. Y. Taguchi, M. Yamamoto, T. Yamate, S. C. Lin, H. Mocharla, P. DeTogni, N. Nakayama, B. F. Boyce, E. Abe, and S. C. Manolagas, Interleukin-6-type cytokines stimulate mesenchymal progenitor differentiation toward the osteoblastic lineage. Proc. Assoc. Am. Physicians 110, 559 (1998).
57. A. Ulsamer, M. J. Ortuno, S. Ruiz, A. R. Susperregui, N. Osses, J. L. Rosa, and F. Ventura, BMP-2 induces Osterix expression through up-regulation of Dlx5 and its phosphorylation by p38. J. Biol. Chem. 283, 3816 (2008).
58. C. D. Hoemann, H. El-Gabalawy, and M. D. McKee, In vitro osteogenesis assays: Influence of the primary cell source on alkaline phosphatase activity and mineralization. Pathol. Biol. (Paris) 57, 318 (2009).
59. S. Gestrelius, S. P. Lyngstadaas, and L. Hammarstrom, Emdogain-periodontal regeneration based on biomimicry. Clinical Oral Investigations 4, 120 (2000).
60. R. Lakshminarayanan, D. Fan, C. Du, and J. Moradian-Oldak, The role of secondary structure in the entropically driven amelogenin self-assembly. Biophys. J. 93, 3664 (2007).
61. A. G. Fincham, J. Moradian-Oldak, J. P. Simmer, P. Sarte, E. C. Lau, T. Diekwisch, and H. C. Slavkin, Self-assembly of a recombinant amelogenin protein generates supramolecular structures. Journal of Structural Biology 112, 103 (1994).
62. W. J. Shaw, A. A. Campbell, M. L. Paine, and M. L. Snead, The COOH terminus of the amelogenin, LRAP, is oriented next to the hydroxyapatite surface. J. Biol. Chem. 279, 40263 (2004).
63. J. Moradian-Oldak, N. Bouropoulos, L. Wang, and N. Gharakhanian, Analysis of self-assembly and apatite binding properties of amelogenin proteins lacking the hydrophilic C-terminal. Matrix Biol. 21, 197 (2002).
64. B. T. Le and I. Woo, Alveolar cleft repair in adults using guided bone regeneration with mineralized allograft for dental implant site development: A report of 2 cases. J. Oral Maxillofac Surg. 67, 1716 (2009).
65. Z. Wang and S. Melmed, Pituitary tumor transforming gene (PTTG) transforming and transactivation activity. J. Biol. Chem. 275, 7459 (2000).