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Title: Controlling protein assembly on inorganic crystals through designed protein interfaces

Abstract

The ability of proteins and other macromolecules to interact with inorganic surfaces is essential to biological function. The proteins involved in these interactions are highly charged and often rich in carboxylic acid side chains, but the structures of most protein–inorganic interfaces are unknown. We explored the possibility of systematically designing structured protein–mineral interfaces, guided by the example of ice-binding proteins, which present arrays of threonine residues (matched to the ice lattice) that order clathrate waters into an ice-like structure. Here we design proteins displaying arrays of up to 54 carboxylate residues geometrically matched to the potassium ion (K +) sublattice on muscovite mica (001). At low K + concentration, individual molecules bind independently to mica in the designed orientations, whereas at high K + concentration, the designs form two-dimensional liquid-crystal phases, which accentuate the inherent structural bias in the muscovite lattice to produce protein arrays ordered over tens of millimetres. Incorporation of designed protein–protein interactions preserving the match between the proteins and the K + lattice led to extended self-assembled structures on mica: designed end-to-end interactions produced micrometre-long single-protein-diameter wires and a designed trimeric interface yielded extensive honeycomb arrays. The nearest-neighbour distances in these hexagonal arrays could be set digitallymore » between 7.5 and 15.9 nanometres with 2.1-nanometre selectivity by changing the number of repeat units in the monomer. In conclusion, these results demonstrate that protein–inorganic lattice interactions can be systematically programmed and set the stage for designing protein–inorganic hybrid materials.« less

Authors:
 [1];  [2];  [2]; ORCiD logo [3]
  1. Univ. of Washington, Seattle, WA (United States). Inst. for Protein Design
  2. Pacific Northwest National Lab. (PNNL), Richland, WA (United States); Univ. of Washington, Seattle, WA (United States)
  3. Univ. of Washington, Seattle, WA (United States). Inst. for Protein Design, and Howard Hughes Medical Inst.
Publication Date:
Research Org.:
Univ. of Washington, Seattle, WA (United States); Pacific Northwest National Lab. (PNNL), Richland, WA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Basic Energy Sciences (BES) (SC-22); National Institutes of Health (NIH); USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1595483
Grant/Contract Number:  
SC0019288; SC0018940; AC02-05CH11231; AC05-76RL01830
Resource Type:
Accepted Manuscript
Journal Name:
Nature (London)
Additional Journal Information:
Journal Name: Nature (London); Journal Volume: 571; Journal Issue: 7764; Journal ID: ISSN 0028-0836
Publisher:
Nature Publishing Group
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 59 BASIC BIOLOGICAL SCIENCES

Citation Formats

Pyles, Harley, Zhang, Shuai, De Yoreo, James J., and Baker, David. Controlling protein assembly on inorganic crystals through designed protein interfaces. United States: N. p., 2019. Web. doi:10.1038/s41586-019-1361-6.
Pyles, Harley, Zhang, Shuai, De Yoreo, James J., & Baker, David. Controlling protein assembly on inorganic crystals through designed protein interfaces. United States. doi:10.1038/s41586-019-1361-6.
Pyles, Harley, Zhang, Shuai, De Yoreo, James J., and Baker, David. Wed . "Controlling protein assembly on inorganic crystals through designed protein interfaces". United States. doi:10.1038/s41586-019-1361-6.
@article{osti_1595483,
title = {Controlling protein assembly on inorganic crystals through designed protein interfaces},
author = {Pyles, Harley and Zhang, Shuai and De Yoreo, James J. and Baker, David},
abstractNote = {The ability of proteins and other macromolecules to interact with inorganic surfaces is essential to biological function. The proteins involved in these interactions are highly charged and often rich in carboxylic acid side chains, but the structures of most protein–inorganic interfaces are unknown. We explored the possibility of systematically designing structured protein–mineral interfaces, guided by the example of ice-binding proteins, which present arrays of threonine residues (matched to the ice lattice) that order clathrate waters into an ice-like structure. Here we design proteins displaying arrays of up to 54 carboxylate residues geometrically matched to the potassium ion (K+) sublattice on muscovite mica (001). At low K+ concentration, individual molecules bind independently to mica in the designed orientations, whereas at high K+ concentration, the designs form two-dimensional liquid-crystal phases, which accentuate the inherent structural bias in the muscovite lattice to produce protein arrays ordered over tens of millimetres. Incorporation of designed protein–protein interactions preserving the match between the proteins and the K+ lattice led to extended self-assembled structures on mica: designed end-to-end interactions produced micrometre-long single-protein-diameter wires and a designed trimeric interface yielded extensive honeycomb arrays. The nearest-neighbour distances in these hexagonal arrays could be set digitally between 7.5 and 15.9 nanometres with 2.1-nanometre selectivity by changing the number of repeat units in the monomer. In conclusion, these results demonstrate that protein–inorganic lattice interactions can be systematically programmed and set the stage for designing protein–inorganic hybrid materials.},
doi = {10.1038/s41586-019-1361-6},
journal = {Nature (London)},
number = 7764,
volume = 571,
place = {United States},
year = {2019},
month = {7}
}

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