Precisely patterned nanofibres made from extendable protein multiplexes

Bethel, Neville P.; Borst, Andrew J.; Parmeggiani, Fabio; Bick, Matthew J.; Brunette, TJ; Nguyen, Hannah; Kang, Alex; Bera, Asim K.; Carter, Lauren; Miranda, Marcos C.; Kibler, Ryan D.; Lamb, Mila; Li, Xinting; Sankaran, Banumathi; Baker, David

doi:10.1038/s41557-023-01314-x

Title: Precisely patterned nanofibres made from extendable protein multiplexes

Journal Article · 04 September 2023 · Nature Chemistry

DOI: https://doi.org/10.1038/s41557-023-01314-x · OSTI ID:2281206

^[1];

^[2]; Bick, Matthew J. ^[1]; Brunette, TJ ^[1]; Nguyen, Hannah ^[1]; Kang, Alex ^[1];

^[1]; Carter, Lauren ^[1];

^[1];

^[1]; Lamb, Mila ^[1]; Li, Xinting ^[1];

^[3];

^[1]

University of Washington, Seattle, WA (United States)
University of Bristol (United Kingdom)
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Molecular systems with coincident cyclic and superhelical symmetry axes have considerable advantages for materials design as they can be readily lengthened or shortened by changing the length of the constituent monomers. Among proteins, alpha-helical coiled coils have such symmetric, extendable architectures, but are limited by the relatively fixed geometry and flexibility of the helical protomers. Here we describe a systematic approach to generating modular and rigid repeat protein oligomers with coincident C₂ to C₈ and superhelical symmetry axes that can be readily extended by repeat propagation. From these building blocks, we demonstrate that a wide range of unbounded fibres can be systematically designed by introducing hydrophilic surface patches that force staggering of the monomers; the geometry of such fibres can be precisely tuned by varying the number of repeat units in the monomer and the placement of the hydrophilic patches.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States); Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)

Sponsoring Organization:: Bill & Melinda Gates Foundation (BMGF); BrisSynBio; Engineering and Physical Sciences Research Council (EPSRC); High-End Instrumentation (HEI); National Institutes of Health (NIH); USDOE Office of Science (SC), Basic Energy Sciences (BES). Scientific User Facilities (SUF); USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC02-05CH11231; AC02-06CH11357; SC0018940

OSTI ID:: 2281206

Journal Information:: Nature Chemistry, Journal Name: Nature Chemistry Journal Issue: 12 Vol. 15; ISSN 1755-4330

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

References (35)

Coiled-coils: The long and short of it Truebestein, Linda; Leonard, Thomas A. BioEssays, Vol. 38, Issue 9 https://doi.org/10.1002/bies.201600062	journal	August 2016
UCSF Chimera?A visualization system for exploratory research and analysis Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Journal of Computational Chemistry, Vol. 25, Issue 13 https://doi.org/10.1002/jcc.20084	journal	January 2004
MolProbity: More and better reference data for improved all-atom structure validation: PROTEIN SCIENCE.ORG Williams, Christopher J.; Headd, Jeffrey J.; Moriarty, Nigel W. Protein Science, Vol. 27, Issue 1 https://doi.org/10.1002/pro.3330	journal	November 2017
UCSF ChimeraX : Structure visualization for researchers, educators, and developers Pettersen, Eric F.; Goddard, Thomas D.; Huang, Conrad C. Protein Science, Vol. 30, Issue 1 https://doi.org/10.1002/pro.3943	journal	October 2020
The Structure of α-Helical Coiled Coils Lupas, Andrei N.; Gruber, Markus Fibrous Proteins: Coiled-Coils, Collagen and Elastomers, p. 37-38 https://doi.org/10.1016/S0065-3233(05)70003-6	book	January 2005
Accurate SAXS Profile Computation and its Assessment by Contrast Variation Experiments Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Biophysical Journal, Vol. 105, Issue 4 https://doi.org/10.1016/j.bpj.2013.07.020	journal	August 2013
Probing Designability via a Generalized Model of Helical Bundle Geometry Grigoryan, Gevorg; DeGrado, William F. Journal of Molecular Biology, Vol. 405, Issue 4 https://doi.org/10.1016/j.jmb.2010.08.058	journal	January 2011
Automated electron microscope tomography using robust prediction of specimen movements Mastronarde, David N. Journal of Structural Biology, Vol. 152, Issue 1 https://doi.org/10.1016/j.jsb.2005.07.007	journal	October 2005
Tandem repeats in proteins: From sequence to structure Kajava, Andrey V. Journal of Structural Biology, Vol. 179, Issue 3 https://doi.org/10.1016/j.jsb.2011.08.009	journal	September 2012
SPRING – An image processing package for single-particle based helical reconstruction from electron cryomicrographs Desfosses, Ambroise; Ciuffa, Rodolfo; Gutsche, Irina Journal of Structural Biology, Vol. 185, Issue 1 https://doi.org/10.1016/j.jsb.2013.11.003	journal	January 2014
Self-Assembling 2D Arrays with de Novo Protein Building Blocks Chen, Zibo; Johnson, Matthew C.; Chen, Jiajun Journal of the American Chemical Society, Vol. 141, Issue 22 https://doi.org/10.1021/jacs.9b01978	journal	May 2019
Exploring the repeat protein universe through computational protein design Brunette, Tj; Parmeggiani, Fabio; Huang, Po-Ssu Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16162	journal	December 2015
Design of coiled-coil protein-origami cages that self-assemble in vitro and in vivo Ljubetič, Ajasja; Lapenta, Fabio; Gradišar, Helena Nature Biotechnology, Vol. 35, Issue 11 https://doi.org/10.1038/nbt.3994	journal	October 2017
Computational design of self-assembling cyclic protein homo-oligomers Fallas, Jorge A.; Ueda, George; Sheffler, William Nature Chemistry, Vol. 9, Issue 4 https://doi.org/10.1038/nchem.2673	journal	December 2016
Comprehensive macromolecular conformations mapped by quantitative SAXS analyses Hura, Greg L.; Budworth, Helen; Dyer, Kevin N. Nature Methods, Vol. 10, Issue 6 https://doi.org/10.1038/nmeth.2453	journal	April 2013
EMRinger: side chain–directed model and map validation for 3D cryo-electron microscopy Barad, Benjamin A.; Echols, Nathaniel; Wang, Ray Yu-Ruei Nature Methods, Vol. 12, Issue 10 https://doi.org/10.1038/nmeth.3541	journal	August 2015
cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination Punjani, Ali; Rubinstein, John L.; Fleet, David J. Nature Methods, Vol. 14, Issue 3 https://doi.org/10.1038/nmeth.4169	journal	February 2017
Programmable design of orthogonal protein heterodimers Chen, Zibo; Boyken, Scott E.; Jia, Mengxuan Nature, Vol. 565, Issue 7737 https://doi.org/10.1038/s41586-018-0802-y	journal	December 2018
Highly accurate protein structure prediction with AlphaFold Jumper, John; Evans, Richard; Pritzel, Alexander Nature https://doi.org/10.1038/s41586-021-03819-2	journal	July 2021
Algorithm discovery by protein folding game players Khatib, F.; Cooper, S.; Tyka, M. D. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1115898108	journal	November 2011
Design, synthesis, and characterization of protein origami based on self-assembly of a brick and staple artificial protein pair Moreaud, Laureen; Viollet, Sébastien; Urvoas, Agathe Proceedings of the National Academy of Sciences, Vol. 120, Issue 11 https://doi.org/10.1073/pnas.2218428120	journal	March 2023
FoXS, FoXSDock and MultiFoXS: Single-state and multi-state structural modeling of proteins and their complexes based on SAXS profiles Schneidman-Duhovny, Dina; Hammel, Michal; Tainer, John A. Nucleic Acids Research, Vol. 44, Issue W1 https://doi.org/10.1093/nar/gkw389	journal	May 2016
Protein complex prediction with AlphaFold-Multimer Evans, Richard; O???Neill, Michael; Pritzel, Alexander https://doi.org/10.1101/2021.10.04.463034	preprint	March 2022
Phaser crystallographic software McCoy, Airlie J.; Grosse-Kunstleve, Ralf W.; Adams, Paul D. Journal of Applied Crystallography, Vol. 40, Issue 4 https://doi.org/10.1107/S0021889807021206	journal	July 2007
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
XDS Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2 https://doi.org/10.1107/S0907444909047337	journal	January 2010
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Features and development of Coot Emsley, P.; Lohkamp, B.; Scott, W. G. Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 4 https://doi.org/10.1107/S0907444910007493	journal	March 2010
Overview of the CCP 4 suite and current developments Winn, Martyn D.; Ballard, Charles C.; Cowtan, Kevin D. Acta Crystallographica Section D Biological Crystallography, Vol. 67, Issue 4 https://doi.org/10.1107/S0907444910045749	journal	March 2011
ISOLDE : a physically realistic environment for model building into low-resolution electron-density maps Croll, Tristan Ian Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 6 https://doi.org/10.1107/S2059798318002425	journal	April 2018
De novo design of self-assembling helical protein filaments Shen, Hao; Fallas, Jorge A.; Lynch, Eric Science, Vol. 362, Issue 6415 https://doi.org/10.1126/science.aau3775	journal	November 2018
Computational design of mechanically coupled axle-rotor protein assemblies Courbet, A.; Hansen, J.; Hsia, Y. Science, Vol. 376, Issue 6591 https://doi.org/10.1126/science.abm1183	journal	April 2022
Robust deep learning–based protein sequence design using ProteinMPNN Dauparas, J.; Anishchenko, I.; Bennett, N. Science, Vol. 378, Issue 6615 https://doi.org/10.1126/science.add2187	journal	October 2022
Modeling Symmetric Macromolecular Structures in Rosetta3 DiMaio, Frank; Leaver-Fay, Andrew; Bradley, Phil PLoS ONE, Vol. 6, Issue 6 https://doi.org/10.1371/journal.pone.0020450	journal	June 2011
Automated structure refinement of macromolecular assemblies from cryo-EM maps using Rosetta Wang, Ray Yu-Ruei; Song, Yifan; Barad, Benjamin A. eLife, Vol. 5 https://doi.org/10.7554/eLife.17219	journal	September 2016

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