Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs

Hughes, Spencer; Wall, Joseph; Wang, Fengbin; Wang, Shengyuan; Kreutzberger, Mark; Osinski, Tomasz; Orlova, Albina; Zuo, Xiaobing; Egelman, Edward; Conticello, Vincent

doi:10.1073/pnas.1903910116

Title: Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs

Journal Article · 01 July 2019 · Proceedings of the National Academy of Sciences of the United States of America

DOI: https://doi.org/10.1073/pnas.1903910116 · OSTI ID:1525381

Hughes, Spencer ^[1]; Wall, Joseph ^[2]; Wang, Fengbin ^[3]; Wang, Shengyuan ^[1]; Kreutzberger, Mark ^[3]; Osinski, Tomasz ^[3]; Orlova, Albina ^[3]; Zuo, Xiaobing ^[4]; Egelman, Edward ^[3]; Conticello, Vincent ^[1]

Emory Univ., Atlanta, GA (United States)
Brookhaven National Lab. (BNL), Upton, NY (United States)
Univ. of Virginia, Charlottesville, VA (United States)
Argonne National Lab. (ANL), Argonne, IL (United States)

Tandem repeat proteins exhibit native designability and represent potentially useful scaffolds for the construction of synthetic biomimetic assemblies. We have designed two synthetic peptides, HEAT R1 and LRV M3Δ1, based on the consensus sequences of single repeats of thermophilic HEAT (PBS HEAT) and Leucine- Rich Variant (LRV) structural motifs, respectively. Self-assembly of the peptides afforded high aspect-ratio helical helical nanotubes. Cryo-electron microscopy with direct electron detection was employed to analyze the structures of the solvated filaments. Three dimensional reconstructions from the cryo-EM maps led to atomic models for the HEAT R1 and LRV M3Δ1 filaments at resolutions of 6.0 Å and 4.4 Å, respectively. Surprisingly, despite sequence similarity at the lateral packing interface, HEAT R1 and LRV M3Δ1 filaments adopt the opposite helical hand and differ significantly in helical geometry, while retaining a local conformation similar to previously characterized repeat proteins of the same class. The differences in the two filaments could be rationalized on the basis of differences in cohesive interactions at the lateral and axial interfaces. These structural data reinforce previous observations regarding the structural plasticity of helical protein assemblies and the need for high resolution structural analysis. Despite these observations, the native designability of tandem repeat proteins offers the opportunity to engineer novel helical nanotubes. Furthermore, the resultant nanotubes have independently addressable and chemically distinguishable interior and exterior surfaces that would facilitate applications in selective recognition, transport, and release.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Brookhaven National Laboratory (BNL), Upton, NY (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)

Grant/Contract Number:: SC0012704

OSTI ID:: 1525381

Report Number(s):: BNL--211762-2019-JAAM

Journal Information:: Proceedings of the National Academy of Sciences of the United States of America, Journal Name: Proceedings of the National Academy of Sciences of the United States of America Journal Issue: 29 Vol. 116; ISSN 0027-8424

Publisher:: National Academy of Sciences, Washington, DC (United States)Copyright Statement

Country of Publication:: United States

Language:: English

References (79)

The First Water-Soluble 310-Helical Peptides Formaggio, Fernando; Crisma, Marco; Rossi, Paola Chemistry, Vol. 6, Issue 24 https://doi.org/10.1002/1521-3765(20001215)6:24<4498::AID-CHEM4498>3.0.CO;2-4	journal	December 2000
Quantifying End-to-End Conformational Communication of Chirality through an Achiral Peptide Chain Clayden, Jonathan; Castellanos, Alejandro; Solà, Jordi Angewandte Chemie, Vol. 121, Issue 32 https://doi.org/10.1002/ange.200901892	journal	June 2009
Quantifying End-to-End Conformational Communication of Chirality through an Achiral Peptide Chain Clayden, Jonathan; Castellanos, Alejandro; Solà, Jordi Angewandte Chemie International Edition, Vol. 48, Issue 32 https://doi.org/10.1002/anie.200901892	journal	July 2009
Calorimetric study of a series of designed repeat proteins: Modular structure and modular folding Cortajarena, Aitziber L.; Regan, Lynne Protein Science, Vol. 20, Issue 2 https://doi.org/10.1002/pro.564	journal	January 2011
A human sterile alpha motif domain polymerizome Knight, Mary Jane; Leettola, Catherine; Gingery, Mari Protein Science, Vol. 20, Issue 10 https://doi.org/10.1002/pro.703	journal	August 2011
PIER: Protein interface recognition for structural proteomics Kufareva, Irina; Budagyan, Levon; Raush, Eugene Proteins: Structure, Function, and Bioinformatics, Vol. 67, Issue 2 https://doi.org/10.1002/prot.21233	journal	February 2007
Hot spots-A review of the protein-protein interface determinant amino-acid residues Moreira, Irina S.; Fernandes, Pedro A.; Ramos, Maria J. Proteins: Structure, Function, and Bioinformatics, Vol. 68, Issue 4 https://doi.org/10.1002/prot.21396	journal	June 2007
Structure of ribgrass mosaic virus at 2.9 å resolution evolution and taxonomy of tobamoviruses 1 1Edited by I. A. Wilson Wang, Hong; Culver, James N.; Stubbs, Gerald Journal of Molecular Biology, Vol. 269, Issue 5 https://doi.org/10.1006/jmbi.1997.1048	journal	July 1997
Three-Dimensional Structure of the Armadillo Repeat Region of β-Catenin Huber, Andrew H.; Nelson, W. James; Weis, William I. Cell, Vol. 90, Issue 5 https://doi.org/10.1016/S0092-8674(00)80352-9	journal	September 1997
The Structure of the Protein Phosphatase 2A PR65/A Subunit Reveals the Conformation of Its 15 Tandemly Repeated HEAT Motifs Groves, Matthew R.; Hanlon, Neil; Turowski, Patric Cell, Vol. 96, Issue 1 https://doi.org/10.1016/S0092-8674(00)80963-0	journal	January 1999
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
When protein folding is simplified to protein coiling: the continuum of solenoid protein structures Kobe, Bostjan; Kajava, Andrey V. Trends in Biochemical Sciences, Vol. 25, Issue 10 https://doi.org/10.1016/S0968-0004(00)01667-4	journal	October 2000
Three-dimensional reconstruction of helical polymers Egelman, Edward H. Archives of Biochemistry and Biophysics, Vol. 581 https://doi.org/10.1016/j.abb.2015.04.004	journal	September 2015
Direct Observation of Parallel Folding Pathways Revealed Using a Symmetric Repeat Protein System Aksel, Tural; Barrick, Doug Biophysical Journal, Vol. 107, Issue 1 https://doi.org/10.1016/j.bpj.2014.04.058	journal	July 2014
Unified Polymerization Mechanism for the Assembly of ASC-Dependent Inflammasomes Lu, Alvin; Magupalli, Venkat Giri; Ruan, Jianbin Cell, Vol. 156, Issue 6 https://doi.org/10.1016/j.cell.2014.02.008	journal	March 2014
Structure of a Chaperone-Usher Pilus Reveals the Molecular Basis of Rod Uncoiling Hospenthal, Manuela K.; Redzej, Adam; Dodson, Karen Cell, Vol. 164, Issue 1-2 https://doi.org/10.1016/j.cell.2015.11.049	journal	January 2016
Structure of the Bacterial Sex F Pilus Reveals an Assembly of a Stoichiometric Protein-Phospholipid Complex Costa, Tiago R. D.; Ilangovan, Aravindan; Ukleja, Marta Cell, Vol. 166, Issue 6 https://doi.org/10.1016/j.cell.2016.08.025	journal	September 2016
Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers Wang, Fengbin; Gu, Yangqi; O’Brien, J. Patrick Cell, Vol. 177, Issue 2 https://doi.org/10.1016/j.cell.2019.03.029	journal	April 2019
The Structure of a Filamentous Bacteriophage Wang, Ying A.; Yu, Xiong; Overman, Stacy Journal of Molecular Biology, Vol. 361, Issue 2 https://doi.org/10.1016/j.jmb.2006.06.027	journal	August 2006
Inference of Macromolecular Assemblies from Crystalline State Krissinel, Evgeny; Henrick, Kim Journal of Molecular Biology, Vol. 372, Issue 3 https://doi.org/10.1016/j.jmb.2007.05.022	journal	September 2007
Design, Production and Molecular Structure of a New Family of Artificial Alpha-helicoidal Repeat Proteins (αRep) Based on Thermostable HEAT-like Repeats Urvoas, Agathe; Guellouz, Asma; Valerio-Lepiniec, Marie Journal of Molecular Biology, Vol. 404, Issue 2 https://doi.org/10.1016/j.jmb.2010.09.048	journal	November 2010
A General Computational Approach for Repeat Protein Design Parmeggiani, Fabio; Huang, Po-Ssu; Vorobiev, Sergey Journal of Molecular Biology, Vol. 427, Issue 2 https://doi.org/10.1016/j.jmb.2014.11.005	journal	January 2015
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
Self-assembly of repeat proteins: Concepts and design of new interfaces Sanchez-deAlcazar, Daniel; Mejias, Sara H.; Erazo, Kevin Journal of Structural Biology, Vol. 201, Issue 2 https://doi.org/10.1016/j.jsb.2017.09.002	journal	February 2018
Structural Polymorphism in Bacterial EspA Filaments Revealed by Cryo-EM and an Improved Approach to Helical Reconstruction Wang, Ying A.; Yu, Xiong; Yip, Calvin Structure, Vol. 14, Issue 7 https://doi.org/10.1016/j.str.2006.05.018	journal	July 2006
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
The Cryoelectron Microscopy Structure of the Type 1 Chaperone-Usher Pilus Rod Hospenthal, Manuela K.; Zyla, Dawid; Costa, Tiago R. D. Structure, Vol. 25, Issue 12 https://doi.org/10.1016/j.str.2017.10.004	journal	December 2017
Molecular, Local, and Network-Level Basis for the Enhanced Stiffness of Hydrogel Networks Formed from Coassembled Racemic Peptides: Predictions from Pauling and Corey Nagy-Smith, Katelyn; Beltramo, Peter J.; Moore, Eric ACS Central Science, Vol. 3, Issue 6 https://doi.org/10.1021/acscentsci.7b00115	journal	May 2017
Helical Polymers: Synthesis, Structures, and Functions Yashima, Eiji; Maeda, Katsuhiro; Iida, Hiroki Chemical Reviews, Vol. 109, Issue 11 https://doi.org/10.1021/cr900162q	journal	November 2009
Design and Characterization of Programmable DNA Nanotubes Rothemund, Paul W. K.; Ekani-Nkodo, Axel; Papadakis, Nick Journal of the American Chemical Society, Vol. 126, Issue 50 https://doi.org/10.1021/ja044319l	journal	December 2004
A New Folding Paradigm for Repeat Proteins Kajander, Tommi; Cortajarena, Aitziber L.; Main, Ewan R. G. Journal of the American Chemical Society, Vol. 127, Issue 29 https://doi.org/10.1021/ja0524494	journal	July 2005
Chiral Induction in Quinoline-Derived Oligoamide Foldamers: Assignment of Helical Handedness and Role of Steric Effects Dolain, Christel; Jiang, Hua; Léger, Jean-Michel Journal of the American Chemical Society, Vol. 127, Issue 37 https://doi.org/10.1021/ja0527828	journal	September 2005
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
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
X-ray Crystallographic Structure of a Giant Double-Walled Peptide Nanotube Formed by a Macrocyclic β-Sheet Containing Aβ _16–22 Chen, Kevin H.; Corro, Kelsey A.; Le, Stephanie P. Journal of the American Chemical Society, Vol. 139, Issue 24 https://doi.org/10.1021/jacs.7b03890	journal	June 2017
Unusual Arginine Formations in Protein Function and Assembly: Rings, Strings, and Stacks Neves, Marco A. C.; Yeager, Mark; Abagyan, Ruben The Journal of Physical Chemistry B, Vol. 116, Issue 23 https://doi.org/10.1021/jp3009699	journal	April 2012
Interconnecting Gold Islands with DNA Origami Nanotubes Ding, Baoquan; Wu, Hao; Xu, Wei Nano Letters, Vol. 10, Issue 12 https://doi.org/10.1021/nl1033073	journal	December 2010
Molecular Structure of RADA16-I Designer Self-Assembling Peptide Nanofibers Cormier, Ashley R.; Pang, Xiaodong; Zimmerman, Maxwell I. ACS Nano, Vol. 7, Issue 9 https://doi.org/10.1021/nn401562f	journal	August 2013
F-actin is a helix with a random variable twist Egelman, E. H.; Francis, N.; DeRosier, D. J. Nature, Vol. 298, Issue 5870 https://doi.org/10.1038/298131a0	journal	July 1982
The structure of the E. coli recA protein monomer and polymer Story, Randall M.; Weber, Irene T.; Steitz, Thomas A. Nature, Vol. 355, Issue 6358 https://doi.org/10.1038/355318a0	journal	January 1992
Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats Kobe, Bostjan; Deisenhofer, Johann Nature, Vol. 366, Issue 6457 https://doi.org/10.1038/366751a0	journal	December 1993
Atomic model of the type III secretion system needle Loquet, Antoine; Sgourakis, Nikolaos G.; Gupta, Rashmi Nature, Vol. 486, Issue 7402 https://doi.org/10.1038/nature11079	journal	May 2012
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
Rational design of α-helical tandem repeat proteins with closed architectures Doyle, Lindsey; Hallinan, Jazmine; Bolduc, Jill Nature, Vol. 528, Issue 7583 https://doi.org/10.1038/nature16191	journal	December 2015
Proteins evolve on the edge of supramolecular self-assembly Garcia-Seisdedos, Hector; Empereur-Mot, Charly; Elad, Nadav Nature, Vol. 548, Issue 7666 https://doi.org/10.1038/nature23320	journal	August 2017
Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement DiMaio, Frank; Song, Yifan; Li, Xueming Nature Methods, Vol. 12, Issue 4 https://doi.org/10.1038/nmeth.3286	journal	February 2015
CryoEM structure of the Methanospirillum hungatei archaellum reveals structural features distinct from the bacterial flagellum and type IV pilus Poweleit, Nicole; Ge, Peng; Nguyen, Hong H. Nature Microbiology, Vol. 2, Issue 3 https://doi.org/10.1038/nmicrobiol.2016.222	journal	December 2016
A leucine-rich repeat variant with a novel repetitive protein structural motif Peters, John W.; Stowell, Michael H. B.; Rees, Douglas C. Nature Structural Biology, Vol. 3, Issue 12 https://doi.org/10.1038/nsb1296-991	journal	December 1996
Control of repeat-protein curvature by computational protein design Park, Keunwan; Shen, Betty W.; Parmeggiani, Fabio Nature Structural & Molecular Biology, Vol. 22, Issue 2 https://doi.org/10.1038/nsmb.2938	journal	January 2015
A structural model of flagellar filament switching across multiple bacterial species Wang, Fengbin; Burrage, Andrew M.; Postel, Sandra Nature Communications, Vol. 8, Issue 1 https://doi.org/10.1038/s41467-017-01075-5	journal	October 2017
Physical basis of amyloid fibril polymorphism Close, William; Neumann, Matthias; Schmidt, Andreas Nature Communications, Vol. 9, Issue 1 https://doi.org/10.1038/s41467-018-03164-5	journal	February 2018
Errors in the deposited SFTSV L protein structure Cusack, Stephen; Rosenthal, Maria Nature Microbiology, Vol. 6, Issue 5 https://doi.org/10.1038/s41564-021-00901-3	journal	April 2021
Designed peptides that assemble into cross-α amyloid-like structures Zhang, Shao-Qing; Huang, Hai; Yang, Junjiao Nature Chemical Biology, Vol. 14, Issue 9 https://doi.org/10.1038/s41589-018-0105-5	journal	July 2018
Atomic-level evidence for packing and positional amyloid polymorphism by segment from TDP-43 RRM2 Guenther, Elizabeth L.; Ge, Peng; Trinh, Hamilton Nature Structural & Molecular Biology, Vol. 25, Issue 4 https://doi.org/10.1038/s41594-018-0045-5	journal	March 2018
Reciprocal regulation of cellular mechanics and metabolism Evers, Tom M. J.; Holt, Liam J.; Alberti, Simon Nature Metabolism, Vol. 3, Issue 4 https://doi.org/10.1038/s42255-021-00384-w	journal	April 2021
Induction of one-handed helical oligo(p-benzamide)s by domino effect based on planar-axial-helical chirality relay Kamikawa, Ken; Fukumoto, Keisuke; Yoshihara, Kohei Chemical Communications, Issue 10 https://doi.org/10.1039/b818123c	journal	January 2009
DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires Liu, D.; Park, S. H.; Reif, J. H. Proceedings of the National Academy of Sciences, Vol. 101, Issue 3 https://doi.org/10.1073/pnas.0305860101	journal	January 2004
Cryo-transmission electron microscopy structure of a gigadalton peptide fiber of de novo design Sharp, T. H.; Bruning, M.; Mantell, J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 33 https://doi.org/10.1073/pnas.1118622109	journal	July 2012
Computational design of a leucine-rich repeat protein with a predefined geometry Rämisch, Sebastian; Weininger, Ulrich; Martinsson, Jonas Proceedings of the National Academy of Sciences, Vol. 111, Issue 50 https://doi.org/10.1073/pnas.1413638111	journal	November 2014
The NMR–Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope Morag, Omry; Sgourakis, Nikolaos G.; Baker, David Proceedings of the National Academy of Sciences, Vol. 112, Issue 4 https://doi.org/10.1073/pnas.1415393112	journal	January 2015
Molecular structure of monomorphic peptide fibrils within a kinetically trapped hydrogel network Nagy-Smith, Katelyn; Moore, Eric; Schneider, Joel Proceedings of the National Academy of Sciences, Vol. 112, Issue 32 https://doi.org/10.1073/pnas.1509313112	journal	July 2015
Zinc-binding structure of a catalytic amyloid from solid-state NMR Lee, Myungwoon; Wang, Tuo; Makhlynets, Olga V. Proceedings of the National Academy of Sciences, Vol. 114, Issue 24 https://doi.org/10.1073/pnas.1706179114	journal	May 2017
The structure of the tetratricopeptide repeats of protein phosphatase 5: implications for TPR-mediated protein-protein interactions Das, A. K. The EMBO Journal, Vol. 17, Issue 5 https://doi.org/10.1093/emboj/17.5.1192	journal	March 1998
Crystal structure of a 12 ANK repeat stack from human ankyrinR Michaely, P. The EMBO Journal, Vol. 21, Issue 23 https://doi.org/10.1093/emboj/cdf651	journal	December 2002
High-resolution structure of the presynaptic RAD51 filament on single-stranded DNA by electron cryo-microscopy Short, Judith M.; Liu, Yang; Chen, Shaoxia Nucleic Acids Research https://doi.org/10.1093/nar/gkw783	journal	September 2016
The Fourier transform of actin and other helical systems with cumulative random angular disorder Egelman, E. H.; DeRosier, D. J. Acta Crystallographica Section A, Vol. 38, Issue 6 https://doi.org/10.1107/S0567739482001624	journal	November 1982
Structure and stability of designed TPR protein superhelices: unusual crystal packing and implications for natural TPR proteins Kajander, Tommi; Cortajarena, Aitziber L.; Mochrie, Simon Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 7 https://doi.org/10.1107/S0907444907024353	journal	June 2007
New tools for the analysis and validation of cryo-EM maps and atomic models Afonine, Pavel V.; Klaholz, Bruno P.; Moriarty, Nigel W. Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 9 https://doi.org/10.1107/S2059798318009324	journal	September 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
Designed Ankyrin Repeat Proteins (DARPins): Binding Proteins for Research, Diagnostics, and Therapy Plückthun, Andreas Annual Review of Pharmacology and Toxicology, Vol. 55, Issue 1 https://doi.org/10.1146/annurev-pharmtox-010611-134654	journal	January 2015
High-resolution structure of the presynaptic RAD51 filament on single-stranded DNA by electron cryo-microscopy. Short, Judith M.; Liu, Yang; Chen, Shaoxia Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.6046	text	January 2016
High-resolution structure of the presynaptic RAD51 filament on single-stranded DNA by electron cryo-microscopy Short, Judith M.; Liu, Yang; Chen, Shaoxia Apollo - University of Cambridge Repository https://doi.org/10.17863/cam.9745	text	January 2016
Molecular, Local, and Network-Level Basis for the Enhanced Stiffness of Hydrogel Networks Formed from Coassembled Racemic Peptides: Predictions from Pauling and Corey Nagy-Smith, Katelyn; Beltramo, Peter J.; Moore, Eric ETH Zurich https://doi.org/10.3929/ethz-b-000189335	text	January 2017
The Cryoelectron Microscopy Structure of the Type 1 Chaperone-Usher Pilus Rod Hospenthal, Manuela; Zyla, Dawid; Costa, Tiago R. D. ETH Zurich https://doi.org/10.3929/ethz-b-000221817	text	January 2017
Structure of a Chaperone-Usher Pilus Reveals the Molecular Basis of Rod Uncoiling Manuela, Hospenthal,; Adam, Redzej,; Karen, Dodson, ETH Zurich https://doi.org/10.3929/ethz-b-000301920	text	January 2016
Single-particle based helical reconstruction—how to make the most of real and Fourier space Sachse, Carsten AIMS Biophysics, Vol. 2, Issue 2 https://doi.org/10.3934/biophy.2015.2.219	journal	January 2015
Designed ankyrin repeat proteins (DARPins): binding proteins for research, diagnostics, and therapy Plückthun, Andreas Annual Reviews https://doi.org/10.5167/uzh-113050	text	January 2015
Functional role of the type 1 pilus rod structure in mediating host-pathogen interactions Spaulding, Caitlin N.; Schreiber, Henry Louis; Zheng, Weili eLife, Vol. 7 https://doi.org/10.7554/eLife.31662	journal	January 2018
Heparin-induced tau filaments are polymorphic and differ from those in Alzheimer’s and Pick’s diseases Zhang, Wenjuan; Falcon, Benjamin; Murzin, Alexey G. eLife, Vol. 8 https://doi.org/10.7554/eLife.43584	journal	February 2019

Similar Records

De Novo Design of Self-Assembling Helical Protein Filaments

Journal Article · 2018 · Science · OSTI ID:1525979

Shen, Hao; Fallas, Jorge A.; Lynch, Eric; +16 more

Self-Assembly of an α-Helical Peptide into a Crystalline Two-Dimensional Nanoporous Framework

Journal Article · 2016 · Journal of the American Chemical Society · OSTI ID:1351722

Magnotti, Elizabeth L.; Hughes, Spencer A.; Dillard, Rebecca S.; +8 more

The first crystal structure of an archaeal helical repeat protein

Journal Article · 2005 · Acta Crystallographica. Section F · OSTI ID:22356142

Yoneda, Kazunari; Sakuraba, Haruhiko; Tsuge, Hideaki; +4 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
Cryo-EM
Helical Nanotube
Self-Assembly
Tandem Repeat Proteins

Title: Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs

Citation Formats

References (79)

Similar Records

Related Subjects