Protein nanoribbons template enamel mineralization

Proc Natl Acad Sci U S A. 2020 Aug 11;117(32):19201-19208. doi: 10.1073/pnas.2007838117. Epub 2020 Jul 31.

Abstract

As the hardest tissue formed by vertebrates, enamel represents nature's engineering masterpiece with complex organizations of fibrous apatite crystals at the nanometer scale. Supramolecular assemblies of enamel matrix proteins (EMPs) play a key role as the structural scaffolds for regulating mineral morphology during enamel development. However, to achieve maximum tissue hardness, most organic content in enamel is digested and removed at the maturation stage, and thus knowledge of a structural protein template that could guide enamel mineralization is limited at this date. Herein, by examining a gene-modified mouse that lacked enzymatic degradation of EMPs, we demonstrate the presence of protein nanoribbons as the structural scaffolds in developing enamel matrix. Using in vitro mineralization assays we showed that both recombinant and enamel-tissue-based amelogenin nanoribbons are capable of guiding fibrous apatite nanocrystal formation. In accordance with our understanding of the natural process of enamel formation, templated crystal growth was achieved by interaction of amelogenin scaffolds with acidic macromolecules that facilitate the formation of an amorphous calcium phosphate precursor which gradually transforms into oriented apatite fibers along the protein nanoribbons. Furthermore, this study elucidated that matrix metalloproteinase-20 is a critical regulator of the enamel mineralization as only a recombinant analog of a MMP20-cleavage product of amelogenin was capable of guiding apatite mineralization. This study highlights that supramolecular assembly of the scaffold protein, its enzymatic processing, and its ability to interact with acidic carrier proteins are critical steps for proper enamel development.

Keywords: biomineralization; enamel; hydroxyapatite; nanoribbon structure; protein assembly.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amelogenesis
  • Amelogenin / chemistry*
  • Amelogenin / metabolism
  • Animals
  • Apatites / chemistry
  • Apatites / metabolism
  • Dental Enamel / chemistry
  • Dental Enamel / metabolism*
  • Dental Enamel Proteins / chemistry
  • Dental Enamel Proteins / metabolism
  • Mice
  • Nanofibers / chemistry

Substances

  • Amelogenin
  • Apatites
  • Dental Enamel Proteins
  • enamel matrix proteins