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Perturbed Amelogenin Protein Self-assembly Alters Nanosphere Properties Resulting in Defective Enamel Formation

Published online by Cambridge University Press:  17 March 2011

Michael L. Paine ,
YaPing Lei ,
Wen Luo  and
Malcolm L. Snead
Michael L. Paine
Affiliation:
University of Southern California, School of Dentistry 2250 Alcazar Street, CSA103 Los Angeles, CA, 90033
YaPing Lei
Affiliation:
University of Southern California, School of Dentistry 2250 Alcazar Street, CSA103 Los Angeles, CA, 90033
Wen Luo
Affiliation:
University of Southern California, School of Dentistry 2250 Alcazar Street, CSA103 Los Angeles, CA, 90033
Malcolm L. Snead
Affiliation:
University of Southern California, School of Dentistry 2250 Alcazar Street, CSA103 Los Angeles, CA, 90033
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Abstract

Dental enamel is a unique composite bioceramic material that is the hardest tissue in the vertebrate body, containing long-, thin-crystallites of substituted hydroxyapatite. Enamel functions under immense loads in a bacterial-laden environment, and generally without catastrophic failure over a lifetime for the organism. Unlike all other biogenerated hard tissues of mesodermal origin, such as bone and dentin, enamel is produced by ectoderm-derived cells called ameloblasts. Recent investigations on the formation of enamel using cell and molecular approaches have been coupled to biomechanical investigations at the nanoscale and mesoscale levels. For amelogenin, the principle protein of forming enamel, two domains have been identified that are required for the proper assembly of multimeric units of amelogenin to form nanospheres. One domain is at the amino-terminus and the other domain in the carboxyl-terminal region. Amelogenin nanospheres are believed to influence the hydroxyapatite crystal habit. Both the yeast two-hybrid assay and surface plasmon resonance have been used to examine the assembly properties of engineered amelogenin proteins. Amelogenin protein was engineered using recombinant DNA techniques to contain deletions to either of the two self-assembly domains. Amelogenin protein was also engineered to contain single amino-acid mutations/substitutions in the amino-terminal self-assembly domain; and these amino-acid changes are based upon point mutations observed in humans affected with a hereditary disturbance of enamel formation. All of these alterations reveal significant defects in amelogenin self-assembly into nanospheres in vitro. Transgenic animals containing these same amelogenin deletions illustrate the importance of a physiologically correct bio-fabrication of the enamel protein extracellular matrix to allow for the organization of the enamel prismatic structure.

Type
Research Article
Information
MRS Online Proceedings Library (OPL) , Volume 823: Symposium W – Biological and Bioinspired Materials and Devices , 2004 , W6.2
Copyright
Copyright © Materials Research Society 2004

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References

1. Mosher, D. F., Sottile, J., Wu, C., and McDonald, J. A., Curr. Opin. Cell Bio. 4, 810 (1992).CrossRefGoogle Scholar
2. Yamada, Y. and Kleinman, H. K., Curr. Opin. Cell Biol. 4, 819 (1992).CrossRefGoogle Scholar
3. Miner, J. H., Curr. Opin. Nephrol. Hypertens. 7, 13 (1998).Google Scholar
4. Simmer, J. P. and Fincham, A. G., Crit. Rev. Oral Biol. Med. 6, 84 (1995).CrossRefGoogle Scholar
5. Paine, M. L., Zhu, D. H., Luo, W., Bringas, P. J., Goldberg, M., White, S. N., Lei, Y. P., Sarikaya, M., Fong, H. K., and Snead, M. L., J. Struct. Biol. 132, 191 (2000).CrossRefGoogle Scholar
6. Greenberg, G., Bringas, P. J., and Slavkin, H. C., Differentiation 25, 32 (1983).CrossRefGoogle Scholar
7. Snead, M. L., Zeichner-David, M., Chandra, T., Robson, K. J., Woo, S. L., and Slavkin, H. C., Proc. Natl. Acad. Sci. USA 80, 7254 (1983).CrossRefGoogle Scholar
8. Gibson, C., Golub, E., Abrams, W., Shen, G., Ding, W., and Rosenbloom, J., Biochem. 31, 8384 (1992).CrossRefGoogle Scholar
9. Hu, C.-C., Fukae, M., Uchida, T., Qian, Q., Zhang, C. H., Ryu, O. H., Tanabe, T., Yamakoshi, Y., Murakami, C., Dohi, N., Shimizu, M., and Simmer, J. P., J. Dent. Res. 76, 1720 (1997).CrossRefGoogle Scholar
10. Krebsbach, P. H., Lee, S. K., Matsuki, Y., Kozac, C., Yamada, K. M., and Yamada, Y., J. Biol. Chem. 271, 4431 (1996).CrossRefGoogle Scholar
11. Fong, C. D., Slaby, I., and Hammarstrom, L., J. Bone Min. Res. 11, 892 (1996).CrossRefGoogle Scholar
12. Cerny, R., Slaby, I., Hammarstrom, L., and Wurtz, T., J. Bone Min. Res. 11, 883 (1996).CrossRefGoogle Scholar
13. Hu, C.-C., Fukae, M., Uchida, T., Qian, Q., Zhang, C. H., Ryu, O. H., Tanabe, T., Yamakoshi, Y., Murakami, C., Dohi, N., Shimizu, M., and Simmer, P. J., J. Dent. Res. 76, 648 (1997).CrossRefGoogle Scholar
14. Ryu, O., Hu, J. C., Yamakoshi, Y., Villemain, J. L., Cao, X., Zhang, C., Bartlett, J. D., and Simmer, J. P., Eur. J. Oral Sci. 110, 358 (2002).CrossRefGoogle Scholar
15. Nelson, P. S., Gan, L., Ferguson, C., Moss, P., Gelinas, R., Hood, L., and Wang, K., Proc. Natl. Acad. Sci. U S A 96, 3114 (1999).CrossRefGoogle Scholar
16. Bartlett, J. D., Ryu, O. H., Xue, J., Simmer, J. P., and Margolis, H. C., Connect. Tissue Res. 39, 405 (1998).CrossRefGoogle Scholar
17. Bartlett, J. D. and Simmer, J. P., Crit. Rev. Oral Biol. Med. 10, 425 (1999).CrossRefGoogle Scholar
18. Langerstrom, M., Dahl, N., Nakahori, Y., Nakagome, Y., Backman, B., Landegren, U., and Pettersson, U., Genomics 10, 971 (1991).CrossRefGoogle Scholar
19. Aldred, M. J., Crawford, P. J. M., Roberts, E., and Thomas, N. S., Hum. Genet. 90, 413 (1992).CrossRefGoogle Scholar
20. Lagerstrom-Fermer, M. and Landegren, U., Conn. Tissue Res. 32, 241 (1995).CrossRefGoogle Scholar
21. Gibson, C. W., Yuan, Z. A., Hall, B., Longenecker, G., Chen, E., Thyagarajan, T., Sreenath, T., Wright, J. T., Decker, S., Piddington, R., Harrison, G., and Kulkarni, A. B., J. Biol. Chem. 276, 31871 (2001).CrossRefGoogle Scholar
22. Hart, P. S., Hart, T. C., Gibson, C. W., and Wright, J. T., Arch. Oral Biol. 45, 79 (2000).CrossRefGoogle Scholar
23. Wright, J. T., Hart, P. S., Aldred, M. J., Seow, K., Crawford, P. J., Hong, S. P., Gibson, C. W., and Hart, T. C., Connect. Tissue Res. 44 (Suppl. 1), 72 (2003).CrossRefGoogle Scholar
24. Hart, P. S., Hart, T. C., Simmer, J. P., and Wright, J. T., Arch. Oral Biol. 47, 255 (2002).CrossRefGoogle Scholar
25. Hart, P. S., Aldred, M. J., Crawford, P. J., Wright, N. J., Hart, T. C., and Wright, J. T., Arch. Oral Biol. 47, 261 (2002).CrossRefGoogle Scholar
26. Snead, M. L., Connect. Tissue Res. 44 (Suppl 1), 52 (2003).CrossRefGoogle Scholar
27. Snead, M. L., Lau, E. C., Zeichner-David, M., Fincham, A. G., Woo, S. L., and Slavkin, H. C., Biochem. Biophys. Res. Commun. 129, 812 (1985).CrossRefGoogle Scholar
28. Fincham, A. G., Moradian-Oldak, J., Diekwisch, T. G. H., Lyaruu, D. M., Wright, J. T., Bringas, P. Jr., and Slavkin, H. C., J. Struct. Biol. 115, 50 (1995).CrossRefGoogle Scholar
29. Lench, N. J. and Winter, G. B., Hum. Mutat. 5, 252 (1995).CrossRefGoogle Scholar
30. Collier, P. M., Sauk, J. J., Rosenbloom, J., Yuan, Z. A., and Gibson, C. W., Archs Oral Biol. 42, 235 (1997).CrossRefGoogle Scholar
31. Moradian-Oldak, J., Paine, M. L., Lei, Y. P., Fincham, A. G., and Snead, M. L., J. Struct. Biol. 131, 27 (2000).CrossRefGoogle Scholar
32. Paine, M. L., Lei, Y. P., Dickerson, K., and Snead, M. L., J. Biol. Chem. 277, 17112 (2002).CrossRefGoogle Scholar
33. Doi, Y., Eanes, E. D., Shimokawa, H., and Termine, J. D., J. Dent. Res. 63, 98 (1984).CrossRefGoogle Scholar
34. Aoba, T., Moreno, E. C., Kresak, M., and Tanabe, T., J. Dent. Res. 68, 1331 (1989).CrossRefGoogle Scholar
35. Fincham, A. G., Moradian-Oldak, J., Simmer, J. P., Sarte, P. E., Lau, E. C., Diekwisch, T. G. H., and Slavkin, H. C., J. Struct. Biol. 112, 103 (1994).CrossRefGoogle Scholar
36. Moradian-Oldak, J., Simmer, P. J., Lau, E. C., Sarte, P. E., Slavkin, H. C., and Fincham, A. G., Biopolymers 34, 1339 (1994).CrossRefGoogle Scholar
37. Robinson, C., Fuchs, P., and Weatherell, J. A., J. Crystal Growth 53, 160 (1981).CrossRefGoogle Scholar
38. Fincham, A. G. and Moradian-Oldak, J., Connect. Tiss. Res. 32, 119 (1995).CrossRefGoogle Scholar
39. Paine, M. L. and Snead, M. L., J. Bone Min. Res. 12, 221 (1997).CrossRefGoogle Scholar
40. Fields, S. and Song, O., Nature 340, 245 (1989).CrossRefGoogle Scholar
41. Nielsen, V. H., Bendixen, C., Arnbjerg, J., Sorensen, C. M., Jensen, H. E., Shukri, N. M., and Thomsen, B., Mamm. Genome 11, 1087 (2000).CrossRefGoogle Scholar
42. Kirkham, J., Zhang, J., Brookes, S. J., Shore, R. C., Wood, S. R., Smith, D. A., Wallwork, M. L., Ryu, O. H., and Robinson, C., J. Dent. Res. 79, 1943 (2000).CrossRefGoogle Scholar
43. Wen, H. B., Fincham, A. G., and Moradian-Oldak, J., Matrix Biol. 20, 387 (2001).CrossRefGoogle Scholar
44. White, S. N., Paine, M. L., Sarikaya, M., Fong, H., Yu, Z., Li, Z. C., and Snead, M. L., J. Am. Ceram. Soc. 83, 238 (2000).CrossRefGoogle Scholar
45. Ravassipour, D. B., Hart, P. S., Ritter, A. V., Yamauchi, M., Gibson, C., and Wright, J. T., J. Dent. Res. 79, 1476 (2000).CrossRefGoogle Scholar
46. Snead, M. L., Paine, M. L., Chen, L. S., Yoshida, B., Luo, W., Zhu, D.-H., Lei, Y.-P., Liu, Y.-H., and Maxson, R. E. J., Connect. Tissue Res. 35, 41 (1996).CrossRefGoogle Scholar
47. Snead, M. L., Paine, M. L., Luo, W., Zhu, D.-H., Yoshida, B., Lei, Y.-P., Chen, L. S., Paine, C. T., Burstein, J. M., Jitpukdeebudintra, S., White, S. N., and Bringas, P. J., Connect. Tissue Res. 38, 279 (1998).CrossRefGoogle Scholar
48. Zhou, Y. L. and Snead, M. L., J. Biol. Chem. 275, 12273 (2000).CrossRefGoogle Scholar
49. Dunglas, C., Septier, D., Paine, M. L., Zhu, D. H., Snead, M. L., and Goldberg, M., Calcif. Tissue Int. 71, 155 (2002).CrossRefGoogle Scholar
50. Fong, H., Heidel, D., Sarikaya, M., White, S. N., Paine, M. L., Luo, W., and Snead, M. L., J. Bone Miner. Res. 18, 2052 (2003).CrossRefGoogle Scholar
51. Paine, M. L., Luo, W., Zhu, D. H., Bringas, P. J., and Snead, M. L., J. Bone Miner. Res. 18, 466 (2003).CrossRefGoogle Scholar
52. Paine, M. L., Wang, H. J., Luo, W., Krebsbach, P. H., and Snead, M. L., J. Biol. Chem. 278, 19447 (2003).CrossRefGoogle Scholar
53. Paine, M. L., Zhu, D. H., Luo, W., and Snead, M. L., Cells, Tissues Organs 176, 7 (2004).CrossRefGoogle Scholar
54. Moradian-Oldak, J., Bouropoulos, N., Wang, L., and Gharakhanian, N., Matrix Biol. 21, 197 (2002).CrossRefGoogle Scholar
55. Sarikaya, M., Proc. Natl. Acad. Sci. USA 96, 13611 (1999).CrossRefGoogle Scholar
56. Sarikaya, M., Tamerler, C., Jen, A. K., Schulten, K., and Baneyx, F., Nat. Mater. 2 (9), 577 (2003).CrossRefGoogle Scholar