De Novo Design of Self-Assembling Helical Protein Filaments

Shen, Hao; Fallas, Jorge A.; Lynch, Eric; Sheffler, William H.; Parry, Bradley; Jannetty, Nicholas; Decarreau, Justin; Wagenbach, Michael; Vicente, Juan Jesus; Chen, Jiajun; Wang, Lei; Dowling, Quinton; Oberdorfer, Gustav; Stewart, Lance; Wordeman, Linda; De Yoreo, James J.; Jacobs-Wagner, Christine; Kollman, Justin M.; Baker, David

doi:10.1126/science.aau3775

De Novo Design of Self-Assembling Helical Protein Filaments

Journal Article · 09 November 2018 · Science

DOI:https://doi.org/10.1126/science.aau3775· OSTI ID:1525979

Shen, Hao ^[1]; Fallas, Jorge A. ^[1]; Lynch, Eric ^[1]; Sheffler, William H. ^[2]; Parry, Bradley ^[3]; Jannetty, Nicholas ^[3]; Decarreau, Justin ^[1]; Wagenbach, Michael ^[1]; Vicente, Juan Jesus ^[1]; Chen, Jiajun ^[4]; Wang, Lei ^[4]; Dowling, Quinton ^[1]; Oberdorfer, Gustav ^[1]; Stewart, Lance ^[1]; Wordeman, Linda ^[1]; De Yoreo, James J. ^[5]; Jacobs-Wagner, Christine ^[3]; Kollman, Justin M. ^[1]; Baker, David ^[1]

University of Washington
UNIVERSITY OF WASHINGTON
Yale University
UNIVERSITY PROGRAMS
BATTELLE (PACIFIC NW LAB)

We describe a general computational approach to designing self-assembling helical filaments from monomeric proteins and use this approach to design proteins that assemble into micrometer-scale filaments with a wide range of geometries in vivo and in vitro. Cryo–electron microscopy structures of six designs are close to the computational design models. The filament building blocks are idealized repeat proteins, and thus the diameter of the filaments can be systematically tuned by varying the number of repeat units. The assembly and disassembly of the filaments can be controlled by engineered anchor and capping units built from monomers lacking one of the interaction surfaces. The ability to generate dynamic, highly ordered structures that span micrometers from protein monomers opens up possibilities for the fabrication of new multiscale metamaterials.

Research Organization:: Pacific Northwest National Laboratory (PNNL), Richland, WA (United States)

Sponsoring Organization:: USDOE

DOE Contract Number:: AC05-76RL01830

OSTI ID:: 1525979

Report Number(s):: PNNL-SA-141425

Journal Information:: Science, Vol. 362, Issue 6415

Country of Publication:: United States

Language:: English

References (33)

Alzheimer’s amyloid fibrils: structure and assembly Serpell, Louise C. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease, Vol. 1502, Issue 1 https://doi.org/10.1016/S0925-4439(00)00029-6	journal	July 2000
Intermediate Filaments: Molecular Structure, Assembly Mechanism, and Integration Into Functionally Distinct Intracellular Scaffolds Herrmann, Harald; Aebi, Ueli Annual Review of Biochemistry, Vol. 73, Issue 1 https://doi.org/10.1146/annurev.biochem.73.011303.073823	journal	June 2004
Turnover rates of different collagen types measured by isotope ratio mass spectrometry Rucklidge, Garry J.; Milne, George; McGaw, Brian A. Biochimica et Biophysica Acta (BBA) - General Subjects, Vol. 1156, Issue 1 https://doi.org/10.1016/0304-4165(92)90095-C	journal	December 1992
Atomic model of the actin filament Holmes, Kenneth C.; Popp, David; Gebhard, Werner Nature, Vol. 347, Issue 6288 https://doi.org/10.1038/347044a0	journal	September 1990
High-Resolution Model of the Microtubule Nogales, Eva; Whittaker, Michael; Milligan, Ronald A. Cell, Vol. 96, Issue 1 https://doi.org/10.1016/S0092-8674(00)80961-7	journal	January 1999
Refined Atomic Model of the Four-Layer Aggregate of the Tobacco Mosaic Virus Coat Protein at 2.4-Å Resolution Bhyravbhatla, Balaji; Watowich, Stanley J.; Caspar, Donald L. D. Biophysical Journal, Vol. 74, Issue 1 https://doi.org/10.1016/S0006-3495(98)77819-1	journal	January 1998
Polar Assembly in a Designed Protein Fiber Smith, Andrew M.; Acquah, Steve F. A.; Bone, Neil Angewandte Chemie International Edition, Vol. 44, Issue 2 https://doi.org/10.1002/anie.200461599	journal	January 2005
Multi-hierarchical self-assembly of a collagen mimetic peptide from triple helix to nanofibre and hydrogel O'Leary, Lesley E. R.; Fallas, Jorge A.; Bakota, Erica L. Nature Chemistry, Vol. 3, Issue 10 https://doi.org/10.1038/nchem.1123	journal	August 2011
Review self-assembly of amphipathic β-sheet peptides: Insights and applications Bowerman, Charles J.; Nilsson, Bradley L. Biopolymers, Vol. 98, Issue 3 https://doi.org/10.1002/bip.22058	journal	January 2012
Self-Assembling Peptide Nanotubes Hartgerink, Jeffrey D.; Granja, Juan R.; Milligan, Ronald A. Journal of the American Chemical Society, Vol. 118, Issue 1 https://doi.org/10.1021/ja953070s	journal	January 1996
Structural Plasticity of Helical Nanotubes Based on Coiled-Coil Assemblies Egelman, E. H.; Xu, C.; DiMaio, F. Structure, Vol. 23, Issue 2 https://doi.org/10.1016/j.str.2014.12.008	journal	February 2015
Modular Design of Self-Assembling Peptide-Based Nanotubes Burgess, Natasha C.; Sharp, Thomas H.; Thomas, Franziska Journal of the American Chemical Society, Vol. 137, Issue 33 https://doi.org/10.1021/jacs.5b03973	journal	August 2015
Rational Design of Helical Nanotubes from Self-Assembly of Coiled-Coil Lock Washers Xu, Chunfu; Liu, Rui; Mehta, Anil K. Journal of the American Chemical Society, Vol. 135, Issue 41 https://doi.org/10.1021/ja4074529	journal	October 2013
Erratum: Corrigendum: Design of a hyperstable 60-subunit protein icosahedron Hsia, Yang; Bale, Jacob B.; Gonen, Shane Nature, Vol. 540, Issue 7631 https://doi.org/10.1038/nature20108	journal	October 2016
Accurate design of co-assembling multi-component protein nanomaterials King, Neil P.; Bale, Jacob B.; Sheffler, William Nature, Vol. 510, Issue 7503 https://doi.org/10.1038/nature13404	journal	May 2014
Design of ordered two-dimensional arrays mediated by noncovalent protein-protein interfaces Gonen, S.; DiMaio, F.; Gonen, T. Science, Vol. 348, Issue 6241 https://doi.org/10.1126/science.aaa9897	journal	June 2015
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
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
The iterative helical real space reconstruction method: Surmounting the problems posed by real polymers Egelman, Edward H. Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.015	journal	January 2007
A robust algorithm for the reconstruction of helical filaments using single-particle methods Egelman, Edward H. Ultramicroscopy, Vol. 85, Issue 4 https://doi.org/10.1016/S0304-3991(00)00062-0	journal	December 2000
RELION: Implementation of a Bayesian approach to cryo-EM structure determination Scheres, Sjors H. W. Journal of Structural Biology, Vol. 180, Issue 3, p. 519-530 https://doi.org/10.1016/j.jsb.2012.09.006	journal	December 2012
FREALIGN: High-resolution refinement of single particle structures Grigorieff, Nikolaus Journal of Structural Biology, Vol. 157, Issue 1 https://doi.org/10.1016/j.jsb.2006.05.004	journal	January 2007
Accurate de novo design of hyperstable constrained peptides Bhardwaj, Gaurav; Mulligan, Vikram Khipple; Bahl, Christopher D. Nature, Vol. 538, Issue 7625 https://doi.org/10.1038/nature19791	journal	September 2016
Protein production by auto-induction in high-density shaking cultures Studier, F. William Protein Expression and Purification, Vol. 41, Issue 1, p. 207-234 https://doi.org/10.1016/j.pep.2005.01.016	journal	May 2005
Overview of Electron Crystallography of Membrane Proteins: Crystallization and Screening Strategies Using Negative Stain Electron Microscopy Nannenga, Brent L.; Iadanza, Matthew G.; Vollmar, Breanna S. Current Protocols in Protein Science, Vol. 72, Issue 1 https://doi.org/10.1002/0471140864.ps1715s72	journal	April 2013
Fiji: an open-source platform for biological-image analysis Schindelin, Johannes; Arganda-Carreras, Ignacio; Frise, Erwin Nature Methods, Vol. 9, Issue 7 https://doi.org/10.1038/nmeth.2019	journal	June 2012
Automated molecular microscopy: The new Leginon system Suloway, Christian; Pulokas, James; Fellmann, Denis Journal of Structural Biology, Vol. 151, Issue 1 https://doi.org/10.1016/j.jsb.2005.03.010	journal	July 2005
MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy Zheng, Shawn Q.; Palovcak, Eugene; Armache, Jean-Paul Nature Methods, Vol. 14, Issue 4 https://doi.org/10.1038/nmeth.4193	journal	February 2017
Gctf: Real-time CTF determination and correction Zhang, Kai Journal of Structural Biology, Vol. 193, Issue 1 https://doi.org/10.1016/j.jsb.2015.11.003	journal	January 2016
Appion: An integrated, database-driven pipeline to facilitate EM image processing Lander, Gabriel C.; Stagg, Scott M.; Voss, Neil R. Journal of Structural Biology, Vol. 166, Issue 1 https://doi.org/10.1016/j.jsb.2009.01.002	journal	April 2009
High-resolution Electron Microscopy of Helical Specimens: A Fresh Look at Tobacco Mosaic Virus Sachse, Carsten; Chen, James Z.; Coureux, Pierre-Damien Journal of Molecular Biology, Vol. 371, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.088	journal	August 2007
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
CellProfiler: image analysis software for identifying and quantifying cell phenotypes Carpenter, Anne E.; Jones, Thouis R.; Lamprecht, Michael R. Genome Biology, Vol. 7, Issue 10 https://doi.org/10.1186/gb-2006-7-10-r100	journal	October 2006

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