Resolving protein-mineral interfacial interactions during in vitro mineralization by atom probe tomography

Organic macromolecules exert remarkable control over the nucleation and growth of inorganic crystallites during (bio)mineralization, as exemplified during enamel formation where the protein amelogenin regulates the formation of hydroxyapatite (HAP). However, it is poorly understood how fundamental p...

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Published inMaterials today advances Vol. 18; p. 100378
Main Authors Taylor, Sandra D., Tao, Jinhui, Shin, Yongsoon, Buchko, Garry W., Dohnalkova, Alice, Grimm, Jack, Tarasevich, Barbara J., Ginovska, Bojana, Shaw, Wendy J., Devaraj, Arun
Format Journal Article
LanguageEnglish
Published England Elsevier Ltd 01.06.2023
Elsevier
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Summary:Organic macromolecules exert remarkable control over the nucleation and growth of inorganic crystallites during (bio)mineralization, as exemplified during enamel formation where the protein amelogenin regulates the formation of hydroxyapatite (HAP). However, it is poorly understood how fundamental processes at the organic-inorganic interface, such as protein adsorption and/or incorporation into minerals, regulates nucleation and crystal growth due to technical challenges in observing and characterizing mineral-bound organics at high-resolution. Here, atom probe tomography techniques were developed and applied to characterize amelogenin-mineralized HAP particles in vitro, revealing distinct organic-inorganic interfacial structures and processes at the nanoscale. Specifically, visualization of amelogenin across the mineralized particulate demonstrates protein can become entrapped during HAP crystal aggregation and fusion. Identification of protein signatures and structural interpretations were further supported by standards analyses, i.e., defined HAP surfaces with and without amelogenin adsorbed. These findings represent a significant advance in the characterization of interfacial structures and, more so, interpretation of fundamental organic-inorganic processes and mechanisms influencing crystal growth. Ultimately, this approach can be broadly applied to inform how potentially unique and diverse organic-inorganic interactions at different stages regulates the growth and evolution of various biominerals. [Display omitted] •In biomineralization, crystal growth is regulated by macromolecular interactions.•Mechanistic insight is limited due to challenges observing mineral-bound organics.•Utilized atom probe tomography to resolve complex interfacial structures, in vitro.•Revealed amelogenin interactions with hydroxyapatite, related to enamel formation.•Fundamental organic-inorganic processes captured, important across mineralization.
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USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF)
AC05-76RL01830; DE-015347
PNNL-SA-174054
National Institutes of Health (NIH)
USDOE Office of Science (SC), Biological and Environmental Research (BER)
ISSN:2590-0498
2590-0498
DOI:10.1016/j.mtadv.2023.100378