Amyloid-like amelogenin nanoribbons template mineralization via a low-energy interface of ion binding sites

Akkineni, Susrut; Zhu, Cheng; Chen, Jiajun; Song, Miao; Hoff, Samuel; Bonde, Johan; Tao, Jinhui; Heinz, Hendrik; Habelitz, Stefan; De Yoreo, James J.

doi:10.1073/pnas.2106965119

Title: Amyloid-like amelogenin nanoribbons template mineralization via a low-energy interface of ion binding sites

Journal Article · Tue May 10 00:00:00 EDT 2022 · Proceedings of the National Academy of Sciences of the United States of America

DOI:https://doi.org/10.1073/pnas.2106965119· OSTI ID:1875075

^[1];

^[2]; Chen, Jiajun ^[1]; Song, Miao ^[1]; Hoff, Samuel ^[2];

^[3];

^[4]; Heinz, Hendrik ^[2];

^[5]; De Yoreo, James J. ^[1]

Univ. of Washington, Seattle, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Univ. of Colorado, Boulder, CO (United States)
Lund Univ. (Sweden)
Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
University California San Francisco; Univ. of California, San Francisco, CA (United States)

Protein scaffolds direct the organization of amorphous precursors that transform into mineralized tissues, but the templating mechanism remains elusive. Motivated by models for the biomineralization of tooth enamel, wherein amyloid-like amelogenin nanoribbons guide the mineralization of apatite filaments, we investigated the impact of nanoribbon structure, sequence, and chemistry on amorphous calcium phosphate (ACP) nucleation. Using full-length human amelogenin and peptide analogs with an amyloid-like domain, films of β-sheet nanoribbons were self-assembled on graphite and characterized by in situ atomic force microscopy and molecular dynamics simulations. All sequences substantially reduce nucleation barriers for ACP by creating low-energy interfaces, while phosphoserines along the length of the nanoribbons dramatically enhance kinetic factors associated with ion binding. Furthermore, the distribution of negatively charged residues along the nanoribbons presents a potential match to the Ca–Ca distances of the multi-ion complexes that constitute ACP. These findings show that amyloid-like amelogenin nanoribbons provide potent scaffolds for ACP mineralization by presenting energetically and stereochemically favorable templates of calcium phosphate ion binding and suggest enhanced surface wetting toward calcium phosphates in general.

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Research Organization:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Environmental Molecular Sciences Lab. (EMSL); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Advanced Light Source (ALS); Argonne National Lab. (ANL), Argonne, IL (United States). Argonne Leadership Computing Facility (ALCF)

Sponsoring Organization:: USDOE Office of Science (SC); National Institutes of Heath (NIH); National Institute of Dental and Craniofacial Research (NIDCR); University of Colorado-Boulder; Colorado State University; National Science Foundation (NSF)

Grant/Contract Number:: AC05-76RL01830; R01-DE025709, NSFOAC-1931587; NSFCMMI-1940335; AC02-06CH11357; NSF ACI-1532235; NSF ACI-1532236

OSTI ID:: 1875075

Report Number(s):: PNNL-SA-173995

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Vol. 119, Issue 19; ISSN 0027-8424

Publisher:: National Academy of SciencesCopyright Statement

Country of Publication:: United States

Language:: English

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59 BASIC BIOLOGICAL SCIENCES
enamel
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calcium phosphate
nucleation
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Title: Amyloid-like amelogenin nanoribbons template mineralization via a low-energy interface of ion binding sites

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