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

Akkineni, SusrutUniversity of Washington, Seattle,Pacific Northwest National Laboratory (author)

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.

Zhu, ChengUniversity of Colorado at Boulder (author)
Chen, JiajunUniversity of Washington, Seattle,Pacific Northwest National Laboratory (author)
Song, MiaoPacific Northwest National Laboratory,University of Washington, Seattle (author)
Hoff, Samuel E.University of Colorado at Boulder (author)
Bonde, JohanLund University,Lunds universitet,Tillämpad biokemi,Centrum för tillämpade biovetenskaper,Kemiska institutionen,Institutioner vid LTH,Lunds Tekniska Högskola,Pure and Applied Biochemistry,Center for Applied Life Sciences,Department of Chemistry,Departments at LTH,Faculty of Engineering, LTH(Swepub:lu)tbio-jsv (author)
Tao, JinhuiJordan University of Science and Technology,Pacific Northwest National Laboratory (author)
Heinz, HendrikUniversity of Colorado at Boulder (author)
Habelitz, StefanUniversity of California, San Francisco (author)
De Yoreo, James J.University of Washington, Seattle,Pacific Northwest National Laboratory (author)
University of Washington, SeattlePacific Northwest National Laboratory (creator_code:org_t)

In:Proceedings of the National Academy of Sciences of the United States of America: Proceedings of the National Academy of Sciences119:191091-6490
In:Proceedings of the National Academy of Sciences: Proceedings of the National Academy of Sciences119:190027-8424

By the author/editor: Akkineni, Susrut; Zhu, Cheng; Chen, Jiajun; Song, Miao; Hoff, Samuel E.; Bonde, Johan; show more...; Tao, Jinhui; Heinz, Hendrik; Habelitz, Stefan; De Yoreo, James ...; show less...

About the subject

NATURAL SCIENCES: NATURAL SCIENCES; and Biological Scien ...; and Biochemistry and ...

MEDICAL AND HEALTH SCIENCES: MEDICAL AND HEAL ...; and Clinical Medicin ...; and Dentistry

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