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Repairing human tooth enamel with leucine-rich amelogenin peptide–chitosan hydrogel

Published online by Cambridge University Press:  29 February 2016

Kaushik Mukherjee ,
Qichao Ruan ,
David Liberman ,
Shane N. White  and
Janet Moradian-Oldak
Kaushik Mukherjee
Affiliation:
Center for Craniofacial Molecular Biology, Division of Biomedical Sciences, Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California 90033, USA
Qichao Ruan
Affiliation:
Center for Craniofacial Molecular Biology, Division of Biomedical Sciences, Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California 90033, USA
David Liberman
Affiliation:
Center for Craniofacial Molecular Biology, Division of Biomedical Sciences, Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California 90033, USA
Shane N. White
Affiliation:
Section of Endodontics, Constitutive & Regenerative Sciences, School of Dentistry, University of California, Los Angeles, California 90095, USA
Janet Moradian-Oldak*
Affiliation:
Center for Craniofacial Molecular Biology, Division of Biomedical Sciences, Herman Ostrow School of Dentistry, University of Southern California, Los Angeles, California 90033, USA
*
a) Address all correspondence to this author. e-mail: joldak@usc.edu
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Abstract

We have recently reported the repair of carious enamel using a full-length amelogenin–chitosan hydrogel through guided stabilization and growth of mineral clusters. The objective of this study was to further evaluate the enamel repair potential of smaller amelogenin peptides like LRAP (leucine-rich amelogenin peptide) and compare their efficiency with their full-length counterpart. The demineralized tooth slices treated with a single application of LRAP–chitosan hydrogel for 3 days showed a dense mineralized layer consisting of highly organized enamel-like apatite crystals. Focus-ion beam technique showed a seamless growth at the interface between the repaired layer and native enamel. There was a marked improvement in the surface hardness after treatment of the demineralized sample with almost 87% recovery of the hardness value to that of sound enamel sections. This current approach can inspire the design of smaller peptide analogues based on naturally occurring amelogenin as a competent, low-cost, and safe strategy for enamel biomimetics to curb the high prevalence of incipient dental caries.

Keywords

biomaterialbiomimetic (chemical reaction)transmission electron microscopy (TEM)
Type
Biomineralization and Biomimetics Reviews
Information
Journal of Materials Research , Volume 31 , Issue 5 , 14 March 2016 , pp. 556 - 563
Copyright
Copyright © Materials Research Society 2016 

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References

REFERENCES

Chai, H., Lee, J.J.W., Constantino, P.J., Lucas, P.W., and Lawn, B.R.: Remarkable resilience of teeth. Proc. Natl. Acad. Sci. U. S. A. 106, 7289–7293 (2009).Google Scholar
Moradian-Oldak, J.: Protein-mediated enamel mineralization. Front. Biosci. 17, 1996–2023 (2012).CrossRefGoogle ScholarPubMed
Cate, A.R.T.: Tooth enamel—Its composition properties and fundamental structure. J. Anat. 100, 416 (1966).Google Scholar
Fincham, A.G., Moradian-Oldak, J., and Simmer, J.P.: The structural biology of the developing dental enamel matrix. J. Struct. Biol. 126, 270–299 (1999).Google Scholar
Moradian-Oldak, J.: Amelogenins: Assembly, processing and control of crystal morphology. Matrix Biol. 20, 293–305 (2001).CrossRefGoogle ScholarPubMed
Deyhle, H., White, S.N., Bunk, O., and Beckmann, F., Muller, B.: Nanostructure of carious tooth enamel lesion. Acta Biomater. 10, 355–364 (2014).CrossRefGoogle ScholarPubMed
Ruan, Q. and Moradian-Oldak, J.: Amelogenin and enamel biomimetics. J. Mater. Chem. B 3, 3112–3129 (2015).Google Scholar
Kirkham, J., Firth, A., Vernals, D., Boden, N., Robinson, C., Shore, R.C., Brookes, S.J., and Aggeli, A.: Self-assembling peptide scaffolds promote enamel remineralization. J. Dent. Res. 86, 426–430 (2007).Google Scholar
Mann, S., Fletcher, J., Walsh, D., and Fowler, C.E.: Electrospun mats of PVP/ACP nanofibres for remineralization of enamel tooth surfaces. CrystEngComm 13, 3692–3697 (2011).Google Scholar
Fan, Y., Xu, X., Zhang, J.F., Twomley, J.T., Wen, Z.T., Liao, S., Lallier, T., Hagan, J.L., and Sun, Z.: Novel amelogenin-releasing hydrogel for remineralization of enamel artificial caries. J. Bioact. Compat. Polym. 27(6), 585–603 (2012).Google Scholar
Reynolds, E.C., Cochrane, N.J., Saranathan, S., Cai, F., and Cross, K.J.: Enamel subsurface lesion remineralisation with casein phosphopeptide stabilised solutions of calcium, phosphate and fluoride. Caries Res. 42, 88–97 (2008).Google Scholar
Yamagishi, K., Onuma, K., Suzuki, T., Okada, F., Tagami, J., Otsuki, M., and Senawangse, P.: Materials chemistry: A synthetic enamel for rapid tooth repair. Nature 433(7028), 819 (2005).CrossRefGoogle ScholarPubMed
Ruan, Q.C., Zhang, Y.Z., Yang, X.D., Nutt, S., and Moradian-Oldak, J.: An amelogenin-chitosan matrix promotes assembly of an enamel-like layer with a dense interface. Acta Biomater. 9, 7289–7297 (2013).Google Scholar
Ruan, Q.C. and Moradian-Oldak, J.: Development of amelogenin-chitosan hydrogel for in vitro enamel regrowth with a dense interface. J. Visualized Exp. (89), e51606 (2014).Google Scholar
Habelitz, S., DenBesten, P.K., Marshall, S.J., Marshall, G.W., and Li, W.: Self-assembly and effect on crystal growth of the leucine-rich amelogenin peptide. Eur. J. Oral Sci. 114, 315–319 (2006).Google Scholar
Tarasevich, B.J., Perez-Salas, U., Masica, D.L., Philo, J., Kienzle, P., Krueger, S., Majkrzak, C.F., Gray, J.L., and Shaw, W.J.: Neutron reflectometry studies of the adsorbed structure of the amelogenin, LRAP. J. Phys. Chem. B 117, 3098–3109 (2013).CrossRefGoogle ScholarPubMed
Shaw, W.J., Ferris, K., Tarasevich, B., and Larson, J.L.: The structure and orientation of the C-terminus of LRAP. Biophys. J. 94, 3247–3257 (2008).Google Scholar
Addadi, L., Moradianoldak, J., Furedimilhofer, H., Weiner, S., and Veis, A.: Stereochemical aspects of crystal regulation in calcium phosphate-associated mineralized tissues. Int. Congr. Ser. 1002, 153–162 (1992).Google Scholar
Addadi, L. and Weiner, S.: Interactions between acidic proteins and crystals—Stereochemical requirements in biomineralization. Proc. Natl. Acad. Sci. U. S. A. 82, 4110–4114 (1985).Google Scholar
DeOliveira, D.B. and Laursen, R.A.: Control of calcite crystal morphology by a peptide designed to bind to a specific surface. J. Am. Chem. Soc. 119, 10627–10631 (1997).Google Scholar
Tarasevich, B.J., Philo, J.S., Maluf, N.K., Krueger, S., Buchko, G.W., Lin, G.Y., and Shaw, W.J.: The leucine-rich amelogenin protein (LRAP) is primarily monomeric and unstructured in physiological solution. J. Struct. Biol. 190, 81–91 (2015).Google Scholar
Tarasevich, B.J., Lea, S., and Shaw, W.J.: The leucine rich amelogenin protein (LRAP) adsorbs as monomers or dimers onto surfaces. J. Struct. Biol. 169, 266–276 (2010).Google Scholar
Le Norcy, E., Kwak, S.Y., Wiedemann-Bidlack, F.B., Beniash, E., Yamakoshi, Y., Simmer, J.P., and Margolis, H.C.: Leucine-rich amelogenin peptides regulate mineralization in vitro. J. Dent. Res. 90, 1091–1097 (2011).Google Scholar
Shafiei, F., Hossein, B.G., Farajollahi, M.M., Fathollah, M., Marjan, B., and Tahereh, J.K.: Leucine-rich amelogenin peptide (LRAP) as a surface primer for biomimetic remineralization of superficial enamel defects: An in vitro study. Scanning 37, 179–185 (2015).CrossRefGoogle ScholarPubMed
Boabaid, F., Gibson, C.W., Kuehl, M.A., Berry, J.E., Snead, M.L., Nociti, F.H., Katchburian, E., and Somerman, M.J.: Leucine-rich amelogenin peptide: A candidate signaling molecule during cementogenesis. J. Periodontol. 75, 1126–1136 (2004).Google Scholar
Warotayanont, R., Zhu, D.H., Snead, M.L., and Zhou, Y.: Leucine-rich amelogenin peptide induces osteogenesis in mouse embryonic stem cells. Biochem. Biophys. Res. Commun. 367, 1–6 (2008).Google Scholar
Robinson, C., Shore, R.C., Brookes, S.J., Strafford, S., Wood, S.R., and Kirkham, J.: The chemistry of enamel caries. Crit. Rev. Oral Biol. Med. 11, 481–495 (2000).CrossRefGoogle ScholarPubMed
Busch, S., Schwarz, U., and Kniep, R.: Chemical and structural investigations of biomimetically grown fluorapatite–gelatin composite aggregates. Adv. Funct. Mater. 13, 189–198 (2003).Google Scholar
Prymak, O., Sokolova, V., Peitsch, T., and Epple, M.: The crystallization of fluoroapatite dumbbells from supersaturated aqueous solution. Cryst. Growth Des. 6, 498–506 (2006).Google Scholar
Al Sagheer, F.A., Al-Sughayer, M.A., Muslim, S., and Elsabee, M.Z.: Extraction and characterization of chitin and chitosan from marine sources in Arabian Gulf. Carbohydr. Polym. 77, 410–419 (2009).Google Scholar
Lagarto, A., Merino, N., Valdes, O., Dominguez, J., Spencer, E., de la Paz, N., and Aparicio, G.: Safety evaluation of chitosan and chitosan acid salts from Panurilus argus lobster. Int. J. Biol. Macromol. 72, 1343–1350 (2015).CrossRefGoogle ScholarPubMed
Tarasevich, B.J., Lea, S., Bernt, W., Engelhard, M., and Shaw, W.J.: Adsorption of amelogenin onto self-assembled and fluoroapatite surfaces. J. Phys. Chem. B 113, 1833–1842 (2009).Google Scholar
Tarasevich, B.J., Lea, S., Bernt, W., Engelhard, M.H., and Shaw, W.J.: Rapid communication changes in the quaternary structure of amelogenin when adsorbed onto surfaces. Biopolymers 91, 103–107 (2009).Google Scholar
Chen, C.L., Bromley, K.M., Moradian-Oldak, J., and DeYoreo, J.J.: In situ AFM study of amelogenin assembly and disassembly dynamics on charged surfaces provides insights on matrix protein self-assembly. J. Am. Chem. Soc. 133, 17406–17413 (2011).Google Scholar
Elhadj, S., De Yoreo, J.J., Hoyer, J.R., and Dove, P.M.: Role of molecular charge and hydrophilicity in regulating the kinetics of crystal growth. Proc. Natl. Acad. Sci. U. S. A. 103, 19237–19242 (2006).Google Scholar
Piana, S., Jones, F., Taylor, Z., Raiteri, P., and Gale, J.D.: Exploring the role of ions and amino acids in directing the growth of minerals from solution. Mineral. Mag. 72, 273–276 (2008).Google Scholar
Yang, X.D., Xie, B.Q., Wang, L.J., Qin, Y.L., Henneman, Z.J., and Nancollas, G.H.: Influence of magnesium ions and amino acids on the nucleation and growth of hydroxyapatite. CrystEngComm 13, 1153–1158 (2011).Google Scholar
Bowman, K. and Leong, K.W.: Chitosan nanoparticles for oral drug and gene delivery. Int. J. Nanomed. 1(2), 117–128 (2006).Google Scholar
Stephan, R.M.: pH and dental caries. J. Dent. Res. 26, 340 (1947).Google Scholar
Masica, D.L., Gray, J.J., and Shaw, W.J.: Partial high-resolution structure of phosphorylated and non-phosphorylated leucine-rich amelogenin protein adsorbed to hydroxyapatite. J. Phys. Chem. C 115, 13775−13785 (2011).Google Scholar
Kwak, S-Y., Wiedemann-Bidlack, R.B., Beniash, E., Yamakoshi, Y., Simmer, J.P., Litman, A., and Margolis, H.C.: Role of 20-kDa amelogenin (P148) phosphorylation in calcium phosphate formation in vitro. J. Biol. Chem. 284, 18972−18979 (2009).Google Scholar
Lu, J-X., Xu, S.Y., and Shaw, W.J.: Phosphorylation and ionic strength alter the LRAP–HAP interface in the N-terminus. Biochemistry 52, 2196−2205 (2013).Google Scholar
Gkioni, K., Leeuwenburgh, S.C.G., Douglas, T.E.L., Mikos, A.G., and Jansen, J.A.: Mineralization of hydrogels for bone regeneration. Tissue Eng. 16, 577–585 (2010).Google Scholar
Ruan, Q., Liberman, D., Bapat', R., Balakrishna, K.C., Phark, J-H., and Moradian-Oldak, J.: Efficacy of amelogenin-chitosan hydrogel in biomimetic repair of human enamel in pH-cycling systems. J. Biomed. Eng. Health Inform 2(1), 123–124 (2016).Google Scholar
Prajapati, S., Tao, J., Ruan, Q., De Yoreo, J.J., and Moradian-oldak, J.: Matrix Metalloproteinase-20 mediates dental enamel biomineralization by preventing protein occlusion inside apatite crystals. Biomaterials 75, 260–270 (2016).Google Scholar
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