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Chemical gradients in human enamel crystallites

Nature volume 583, pages 66–71 (2020)Cite this article

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A Publisher Correction to this article was published on 21 July 2020

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Abstract

Dental enamel is a principal component of teeth1, and has evolved to bear large chewing forces, resist mechanical fatigue and withstand wear over decades2. Functional impairment and loss of dental enamel, caused by developmental defects or tooth decay (caries), affect health and quality of life, with associated costs to society3. Although the past decade has seen progress in our understanding of enamel formation (amelogenesis) and the functional properties of mature enamel, attempts to repair lesions in this material or to synthesize it in vitro have had limited success4,5,6. This is partly due to the highly hierarchical structure of enamel and additional complexities arising from chemical gradients7,8,9. Here we show, using atomic-scale quantitative imaging and correlative spectroscopies, that the nanoscale crystallites of hydroxylapatite (Ca5(PO4)3(OH)), which are the fundamental building blocks of enamel, comprise two nanometric layers enriched in magnesium flanking a core rich in sodium, fluoride and carbonate ions; this sandwich core is surrounded by a shell with lower concentration of substitutional defects. A mechanical model based on density functional theory calculations and X-ray diffraction data predicts that residual stresses arise because of the chemical gradients, in agreement with preferential dissolution of the crystallite core in acidic media. Furthermore, stresses may affect the mechanical resilience of enamel. The two additional layers of hierarchy suggest a possible new model for biological control over crystal growth during amelogenesis, and hint at implications for the preservation of biomarkers during tooth development.

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Fig. 1: The hierarchical architecture of human enamel.
Fig. 2: Atomic-scale structure and composition of human enamel crystallites.
Fig. 3: Chemical gradients in human enamel crystallites and the amorphous intergranular phase.
Fig. 4: Effect of substitution on mechanical and chemical properties of human enamel crystallites.
Fig. 5: A model for human enamel crystallite growth during amelogenesis.

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Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request. Source data are provided with this paper.

Code availability

This manuscript primarily made use of commercial (IVAS, Origin, Matlab, MDI Jade, APEX2, Thermo Scientific Qtegra ISDS, COMSOL Multiphysics, TEM Imaging and Analysis, DigitalMicrograph, AZtec, Adobe Illustrator) and freely available (DEMETER, OLEX2, SHELX, Quantum ESPRESSO, Cornell Spectrum Imager, ImageJ) software packages for acquisition, processing and visualization of data. MCR was performed using custom code using the Matlab mcr.m package from the Eigenvector Research PLS_toolbox, as described elsewhere43. In addition, custom code written for the Mathematica and Matlab environments was used for file conversions, plotting and visualization. This code is available from the corresponding author upon reasonable request.

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Acknowledgements

This work was supported in part by the National Institute of Health–National Institute of Dental and Craniofacial Research (NIH-NIDCR R03 DE025303-01, R01 DE025702-01), the National Science Foundation (DMR-1508399), the NSF Platform for the Accelerated Realization, Analysis and Discovery of Interface Materials (PARADIM) under Cooperative Agreement no. DMR-1539918, and the University of Virginia. K.A.D. was in part supported by a 3M fellowship. The Canadian National Sciences and Engineering Research Council in part supported L.M.G. K.A.D. and M.J.C. were supported in part by the Northwestern University Graduate School Cluster in Biotechnology, Systems and Synthetic Biology, which is affiliated with the Biotechnology Training Program. L.S. was supported by a Deutsche Forschungsgemeinschaft research fellowship (STE2689/1-1). This work made use of the following core facilities operated by Northwestern University: NUCAPT, which received support from NSF (DMR-0420532), ONR (N00014-0400798, N00014-0610539, N00014-0910781 and N00014-1712870), and the Initiative for Sustainability and Energy at Northwestern University (ISEN); MatCI; NUANCE and EPIC, which received support from the International Institute for Nanotechnology (IIN), the Keck Foundation, and the State of Illinois, through the IIN; IMSERC; the Jerome B. Cohen X-Ray Diffraction Facility; QBIC, which received support from NASA Ames Research Center (NNA06CB93G). NUCAPT, MatCI, NUANCE and EPIC were further supported by the MRSEC programme (NSF DMR-1720139) at the Materials Research Center; NUCAPT, NUANCE, EPIC and IMSERC were also supported by the Soft and Hybrid Nanotechnology Experimental (SHyNE) Resource (NSF ECCS-1542205). This work made use of the Cornell Center for Materials Research (CCMR) Shared Facilities supported through the NSF MRSEC Program (no. DMR-1719875). The Titan Themis 300 was acquired through NSF-MRI-1429155, with additional support from Cornell University, the Weill Institute, and the Kavli Institute at Cornell. This work made use of the Rivanna cluster maintained by the Advanced Research Computing Services at the University of Virginia. Portions of this work were performed at the Canadian Light Source (CLS), which received support from The Natural Sciences and Engineering Research Council of Canada, the National Research Council of Canada, the Canadian Institutes of Health Research, the Province of Saskatchewan, Western Economic Diversification Canada, and the University of Saskatchewan. The authors thank P. Akers, M. Stohle and G. Borden for providing de-identified human premolars, and C. Malliakas, K. MacRenaris, M. Thomas and especially K. Rice for technical support.

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Author notes

  1. Michael J. Zachman

    Present address: Center for Nanophase Materials Sciences, Oak Ridge National Laboratory, Oak Ridge, TN, USA

  2. These authors contributed equally: Karen A. DeRocher, Paul J. M. Smeets

Authors and Affiliations

  1. Department of Materials Science and Engineering, Northwestern University, Evanston, IL, USA

    Karen A. DeRocher, Paul J. M. Smeets, Linus Stegbauer, Michael J. Cohen, Lyle M. Gordon, James M. Rondinelli & Derk Joester

  2. School of Applied and Engineering Physics, Cornell University, Ithaca, NY, USA

    Berit H. Goodge, Michael J. Zachman & Lena F. Kourkoutis

  3. Kavli Institute at Cornell for Nanoscale Science, Cornell University, Ithaca, NY, USA

    Berit H. Goodge & Lena F. Kourkoutis

  4. Department of Materials Science and Engineering, University of Virginia, Charlottesville, VA, USA

    Prasanna V. Balachandran

  5. Department of Mechanical and Aerospace Engineering, University of Virginia, Charlottesville, VA, USA

    Prasanna V. Balachandran

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Contributions

The experiments and simulations were designed by K.A.D., P.J.M.S., L.S., P.V.B., J.M.R., D.J. STEM experiments were performed by P.J.M.S., B.H.G. and M.J.Z., with additional help in analysis and simulations provided by M.J.Z. and L.F.K. APT data were collected and analysed by K.A.D., with D.J. assisting the analysis. The finite-element model was developed by K.A.D. and D.J. using DFT calculations performed by P.V.B., and synthetic Mg-rich OHAp crystals made and analysed by L.S. XAS data were collected and analysed by L.M.G. and M.J.C. K.A.D., P.J.M.S., B.H.G., P.V.B., M.J.Z., L.F.K., J.M.R. and D.J. were all involved in preparing the manuscript.

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Correspondence to Derk Joester.

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Supplementary information

Supplementary Information

This file contains Supplementary Methods, Tables, Discussion, and References, organized by experimental technique (1: STEM; 2: XAS; 3: APT; 4: FEM; 5: SEM) with an additional chapter that details the proposed model for amelogenesis in greater detail. This section contains 21 Supplementary Figures, 9 Supplementary Tables, and 40 references.

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Supplementary Data

This zipped file contains source data for Supplementary Figures 4–7 and 14–17.

Video 1

Ion positions in a human enamel crystallite. All 24Mg2+ (magenta), 40Ca19F+ (blue), 23Na+ (turquoise), and COxHy+ ions (red) are rendered for a 30 nm thick slice through a human enamel crystallite (crystallite D in Supplementary Fig. S10a). Note that dataset was rotated such that view direction (x axis) is approximately parallel to the Mg layers. The animation shows rotation about the z axis, which is normal to the Mg layers. This visualization was scripted using the Matlab R2019b platform (The MathWorks).

Video 2

Core-shell and sandwich structure of human enamel crystallite. The reconstruction was rotated as in Video 1, voxelized (1 nm isotropic voxels) and smoothed. Iso-concentration surfaces and iso-caps for 24Mg2+ (magenta, ciso = 0.1 nm−3), 23Na+ (turquoise, 0.3 nm−3), and COxHy+ ions (red, 0.12 nm−3) were rendered together with that for 40Ca19F+ (blue, 0.07 nm−3) for the same slice as in Video 1, but ions outside the central crystallite are not shown. The animation shows one revolution about the z axis, followed by an oscillatory tilt series about the y axis. This visualization was scripted using the Matlab R2019b platform (The MathWorks).

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DeRocher, K.A., Smeets, P.J.M., Goodge, B.H. et al. Chemical gradients in human enamel crystallites. Nature 583, 66–71 (2020). https://doi.org/10.1038/s41586-020-2433-3

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