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

Abstract

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 proteinsmore » 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.« less

Authors:
 [1];  [2];  [3];  [1];  [3];  [3];  [3];  [4];  [3];  [1]
  1. Emory Univ., Atlanta, GA (United States)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Univ. of Virginia, Charlottesville, VA (United States)
  4. Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Brookhaven National Lab. (BNL), Upton, NY (United States); Argonne National Lab. (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Institutes of Health (NIH); National Science Foundation (NSF)
OSTI Identifier:
1525381
Alternate Identifier(s):
OSTI ID: 1563920
Report Number(s):
BNL-211762-2019-JAAM
Journal ID: ISSN 0027-8424
Grant/Contract Number:  
SC0012704; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
Proceedings of the National Academy of Sciences of the United States of America
Additional Journal Information:
Journal Volume: 116; Journal Issue: 29; Journal ID: ISSN 0027-8424
Publisher:
National Academy of Sciences, Washington, DC (United States)
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Tandem Repeat Proteins; Cryo-EM; Helical Nanotube; Self-Assembly; cryo-EM; helical nanotube; self-assembly; tandem repeat proteins

Citation Formats

Hughes, Spencer, Wall, Joseph, Wang, Fengbin, Wang, Shengyuan, Kreutzberger, Mark, Osinski, Tomasz, Orlova, Albina, Zuo, Xiaobing, Egelman, Edward, and Conticello, Vincent. Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs. United States: N. p., 2019. Web. doi:10.1073/pnas.1903910116.
Hughes, Spencer, Wall, Joseph, Wang, Fengbin, Wang, Shengyuan, Kreutzberger, Mark, Osinski, Tomasz, Orlova, Albina, Zuo, Xiaobing, Egelman, Edward, & Conticello, Vincent. Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs. United States. doi:10.1073/pnas.1903910116.
Hughes, Spencer, Wall, Joseph, Wang, Fengbin, Wang, Shengyuan, Kreutzberger, Mark, Osinski, Tomasz, Orlova, Albina, Zuo, Xiaobing, Egelman, Edward, and Conticello, Vincent. Mon . "Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs". United States. doi:10.1073/pnas.1903910116.
@article{osti_1525381,
title = {Ambidextrous Helical Nanotubes from Self-Assembly of Designed Helical Hairpin Motifs},
author = {Hughes, Spencer and Wall, Joseph and Wang, Fengbin and Wang, Shengyuan and Kreutzberger, Mark and Osinski, Tomasz and Orlova, Albina and Zuo, Xiaobing and Egelman, Edward and Conticello, Vincent},
abstractNote = {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.},
doi = {10.1073/pnas.1903910116},
journal = {Proceedings of the National Academy of Sciences of the United States of America},
number = 29,
volume = 116,
place = {United States},
year = {2019},
month = {7}
}

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Works referenced in this record:

Induction of one-handed helical oligo(p-benzamide)s by domino effect based on planar-axial-helical chirality relay
journal, January 2009

  • Kamikawa, Ken; Fukumoto, Keisuke; Yoshihara, Kohei
  • Chemical Communications, Issue 10
  • DOI: 10.1039/b818123c

A human sterile alpha motif domain polymerizome
journal, August 2011

  • Knight, Mary Jane; Leettola, Catherine; Gingery, Mari
  • Protein Science, Vol. 20, Issue 10
  • DOI: 10.1002/pro.703

The Fourier transform of actin and other helical systems with cumulative random angular disorder
journal, November 1982


The NMR–Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope
journal, January 2015

  • Morag, Omry; Sgourakis, Nikolaos G.; Baker, David
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 4
  • DOI: 10.1073/pnas.1415393112

Exploring the repeat protein universe through computational protein design
journal, December 2015

  • Brunette, Tj; Parmeggiani, Fabio; Huang, Po-Ssu
  • Nature, Vol. 528, Issue 7583
  • DOI: 10.1038/nature16162

Hot spots-A review of the protein-protein interface determinant amino-acid residues
journal, June 2007

  • Moreira, Irina S.; Fernandes, Pedro A.; Ramos, Maria J.
  • Proteins: Structure, Function, and Bioinformatics, Vol. 68, Issue 4
  • DOI: 10.1002/prot.21396

PIER: Protein interface recognition for structural proteomics
journal, February 2007

  • Kufareva, Irina; Budagyan, Levon; Raush, Eugene
  • Proteins: Structure, Function, and Bioinformatics, Vol. 67, Issue 2
  • DOI: 10.1002/prot.21233

A robust algorithm for the reconstruction of helical filaments using single-particle methods
journal, December 2000


F-actin is a helix with a random variable twist
journal, July 1982

  • Egelman, E. H.; Francis, N.; DeRosier, D. J.
  • Nature, Vol. 298, Issue 5870
  • DOI: 10.1038/298131a0

Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats
journal, December 1993

  • Kobe, Bostjan; Deisenhofer, Johann
  • Nature, Vol. 366, Issue 6457
  • DOI: 10.1038/366751a0

Physical basis of amyloid fibril polymorphism
journal, February 2018


Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement
journal, February 2015

  • DiMaio, Frank; Song, Yifan; Li, Xueming
  • Nature Methods, Vol. 12, Issue 4
  • DOI: 10.1038/nmeth.3286

De novo design of self-assembling helical protein filaments
journal, November 2018


Zinc-binding structure of a catalytic amyloid from solid-state NMR
journal, May 2017

  • Lee, Myungwoon; Wang, Tuo; Makhlynets, Olga V.
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
  • DOI: 10.1073/pnas.1706179114

Functional role of the type 1 pilus rod structure in mediating host-pathogen interactions
journal, January 2018

  • Spaulding, Caitlin N.; Schreiber, Henry Louis; Zheng, Weili
  • eLife, Vol. 7
  • DOI: 10.7554/eLife.31662

Three-Dimensional Structure of the Armadillo Repeat Region of β-Catenin
journal, September 1997


Tandem repeats in proteins: From sequence to structure
journal, September 2012


Helical Polymers: Synthesis, Structures, and Functions
journal, November 2009

  • Yashima, Eiji; Maeda, Katsuhiro; Iida, Hiroki
  • Chemical Reviews, Vol. 109, Issue 11
  • DOI: 10.1021/cr900162q

Proteins evolve on the edge of supramolecular self-assembly
journal, August 2017

  • Garcia-Seisdedos, Hector; Empereur-Mot, Charly; Elad, Nadav
  • Nature, Vol. 548, Issue 7666
  • DOI: 10.1038/nature23320

Molecular structure of monomorphic peptide fibrils within a kinetically trapped hydrogel network
journal, July 2015

  • Nagy-Smith, Katelyn; Moore, Eric; Schneider, Joel
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 32
  • DOI: 10.1073/pnas.1509313112

A New Folding Paradigm for Repeat Proteins
journal, July 2005

  • Kajander, Tommi; Cortajarena, Aitziber L.; Main, Ewan R. G.
  • Journal of the American Chemical Society, Vol. 127, Issue 29
  • DOI: 10.1021/ja0524494

Quantifying End-to-End Conformational Communication of Chirality through an Achiral Peptide Chain
journal, July 2009

  • Clayden, Jonathan; Castellanos, Alejandro; Solà, Jordi
  • Angewandte Chemie International Edition, Vol. 48, Issue 32
  • DOI: 10.1002/anie.200901892

The Structure of the Protein Phosphatase 2A PR65/A Subunit Reveals the Conformation of Its 15 Tandemly Repeated HEAT Motifs
journal, January 1999


High-resolution structure of the presynaptic RAD51 filament on single-stranded DNA by electron cryo-microscopy
journal, September 2016

  • Short, Judith M.; Liu, Yang; Chen, Shaoxia
  • Nucleic Acids Research
  • DOI: 10.1093/nar/gkw783

Interconnecting Gold Islands with DNA Origami Nanotubes
journal, December 2010

  • Ding, Baoquan; Wu, Hao; Xu, Wei
  • Nano Letters, Vol. 10, Issue 12
  • DOI: 10.1021/nl1033073

Three-dimensional reconstruction of helical polymers
journal, September 2015


Atomic model of the type III secretion system needle
journal, May 2012

  • Loquet, Antoine; Sgourakis, Nikolaos G.; Gupta, Rashmi
  • Nature, Vol. 486, Issue 7402
  • DOI: 10.1038/nature11079

Design, Production and Molecular Structure of a New Family of Artificial Alpha-helicoidal Repeat Proteins (αRep) Based on Thermostable HEAT-like Repeats
journal, November 2010

  • Urvoas, Agathe; Guellouz, Asma; Valerio-Lepiniec, Marie
  • Journal of Molecular Biology, Vol. 404, Issue 2
  • DOI: 10.1016/j.jmb.2010.09.048

Control of repeat-protein curvature by computational protein design
journal, January 2015

  • Park, Keunwan; Shen, Betty W.; Parmeggiani, Fabio
  • Nature Structural & Molecular Biology, Vol. 22, Issue 2
  • DOI: 10.1038/nsmb.2938

Inference of Macromolecular Assemblies from Crystalline State
journal, September 2007


Crystal structure of a 12 ANK repeat stack from human ankyrinR
journal, December 2002


X-ray Crystallographic Structure of a Giant Double-Walled Peptide Nanotube Formed by a Macrocyclic β-Sheet Containing Aβ 16–22
journal, June 2017

  • Chen, Kevin H.; Corro, Kelsey A.; Le, Stephanie P.
  • Journal of the American Chemical Society, Vol. 139, Issue 24
  • DOI: 10.1021/jacs.7b03890

Unusual Arginine Formations in Protein Function and Assembly: Rings, Strings, and Stacks
journal, April 2012

  • Neves, Marco A. C.; Yeager, Mark; Abagyan, Ruben
  • The Journal of Physical Chemistry B, Vol. 116, Issue 23
  • DOI: 10.1021/jp3009699

The structure of the E. coli recA protein monomer and polymer
journal, January 1992

  • Story, Randall M.; Weber, Irene T.; Steitz, Thomas A.
  • Nature, Vol. 355, Issue 6358
  • DOI: 10.1038/355318a0

Direct Observation of Parallel Folding Pathways Revealed Using a Symmetric Repeat Protein System
journal, July 2014


Design and Characterization of Programmable DNA Nanotubes
journal, December 2004

  • Rothemund, Paul W. K.; Ekani-Nkodo, Axel; Papadakis, Nick
  • Journal of the American Chemical Society, Vol. 126, Issue 50
  • DOI: 10.1021/ja044319l

Self-assembly of repeat proteins: Concepts and design of new interfaces
journal, February 2018

  • Sanchez-deAlcazar, Daniel; Mejias, Sara H.; Erazo, Kevin
  • Journal of Structural Biology, Vol. 201, Issue 2
  • DOI: 10.1016/j.jsb.2017.09.002

Calorimetric study of a series of designed repeat proteins: Modular structure and modular folding
journal, January 2011

  • Cortajarena, Aitziber L.; Regan, Lynne
  • Protein Science, Vol. 20, Issue 2
  • DOI: 10.1002/pro.564

Heparin-induced tau filaments are polymorphic and differ from those in Alzheimer’s and Pick’s diseases
journal, February 2019


Structural Plasticity of Helical Nanotubes Based on Coiled-Coil Assemblies
journal, February 2015


A leucine-rich repeat variant with a novel repetitive protein structural motif
journal, December 1996

  • Peters, John W.; Stowell, Michael H. B.; Rees, Douglas C.
  • Nature Structural Biology, Vol. 3, Issue 12
  • DOI: 10.1038/nsb1296-991

Chiral Induction in Quinoline-Derived Oligoamide Foldamers:  Assignment of Helical Handedness and Role of Steric Effects
journal, September 2005

  • Dolain, Christel; Jiang, Hua; Léger, Jean-Michel
  • Journal of the American Chemical Society, Vol. 127, Issue 37
  • DOI: 10.1021/ja0527828

Designed Ankyrin Repeat Proteins (DARPins): Binding Proteins for Research, Diagnostics, and Therapy
journal, January 2015


Atomic-level evidence for packing and positional amyloid polymorphism by segment from TDP-43 RRM2
journal, March 2018

  • Guenther, Elizabeth L.; Ge, Peng; Trinh, Hamilton
  • Nature Structural & Molecular Biology, Vol. 25, Issue 4
  • DOI: 10.1038/s41594-018-0045-5

When protein folding is simplified to protein coiling: the continuum of solenoid protein structures
journal, October 2000


Computational design of a leucine-rich repeat protein with a predefined geometry
journal, November 2014

  • Rämisch, Sebastian; Weininger, Ulrich; Martinsson, Jonas
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
  • DOI: 10.1073/pnas.1413638111

The First Water-Soluble 310-Helical Peptides
journal, December 2000


Molecular Structure of RADA16-I Designer Self-Assembling Peptide Nanofibers
journal, August 2013

  • Cormier, Ashley R.; Pang, Xiaodong; Zimmerman, Maxwell I.
  • ACS Nano, Vol. 7, Issue 9
  • DOI: 10.1021/nn401562f


journal, January 2015


Rational design of α-helical tandem repeat proteins with closed architectures
journal, December 2015

  • Doyle, Lindsey; Hallinan, Jazmine; Bolduc, Jill
  • Nature, Vol. 528, Issue 7583
  • DOI: 10.1038/nature16191

Structure of ribgrass mosaic virus at 2.9 å resolution evolution and taxonomy of tobamoviruses 1 1Edited by I. A. Wilson
journal, July 1997

  • Wang, Hong; Culver, James N.; Stubbs, Gerald
  • Journal of Molecular Biology, Vol. 269, Issue 5
  • DOI: 10.1006/jmbi.1997.1048

A General Computational Approach for Repeat Protein Design
journal, January 2015

  • Parmeggiani, Fabio; Huang, Po-Ssu; Vorobiev, Sergey
  • Journal of Molecular Biology, Vol. 427, Issue 2
  • DOI: 10.1016/j.jmb.2014.11.005

Rational Design of Helical Nanotubes from Self-Assembly of Coiled-Coil Lock Washers
journal, October 2013

  • Xu, Chunfu; Liu, Rui; Mehta, Anil K.
  • Journal of the American Chemical Society, Vol. 135, Issue 41
  • DOI: 10.1021/ja4074529

Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers
journal, April 2019


Structure of the Bacterial Sex F Pilus Reveals an Assembly of a Stoichiometric Protein-Phospholipid Complex
journal, September 2016


The Cryoelectron Microscopy Structure of the Type 1 Chaperone-Usher Pilus Rod
journal, December 2017


A structural model of flagellar filament switching across multiple bacterial species
journal, October 2017


Designed peptides that assemble into cross-α amyloid-like structures
journal, July 2018


New tools for the analysis and validation of cryo-EM maps and atomic models
journal, September 2018

  • Afonine, Pavel V.; Klaholz, Bruno P.; Moriarty, Nigel W.
  • Acta Crystallographica Section D Structural Biology, Vol. 74, Issue 9
  • DOI: 10.1107/S2059798318009324

The Structure of a Filamentous Bacteriophage
journal, August 2006


Cryo-transmission electron microscopy structure of a gigadalton peptide fiber of de novo design
journal, July 2012

  • Sharp, T. H.; Bruning, M.; Mantell, J.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 33
  • DOI: 10.1073/pnas.1118622109

DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires
journal, January 2004

  • Liu, D.; Park, S. H.; Reif, J. H.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 3
  • DOI: 10.1073/pnas.0305860101

Structure and stability of designed TPR protein superhelices: unusual crystal packing and implications for natural TPR proteins
journal, June 2007

  • Kajander, Tommi; Cortajarena, Aitziber L.; Mochrie, Simon
  • Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 7
  • DOI: 10.1107/S0907444907024353

Structure of a Chaperone-Usher Pilus Reveals the Molecular Basis of Rod Uncoiling
journal, January 2016


Unified Polymerization Mechanism for the Assembly of ASC-Dependent Inflammasomes
journal, March 2014


Modular Design of Self-Assembling Peptide-Based Nanotubes
journal, August 2015

  • Burgess, Natasha C.; Sharp, Thomas H.; Thomas, Franziska
  • Journal of the American Chemical Society, Vol. 137, Issue 33
  • DOI: 10.1021/jacs.5b03973

    Works referencing / citing this record:

    Quantifying End-to-End Conformational Communication of Chirality through an Achiral Peptide Chain
    journal, July 2009

    • Clayden, Jonathan; Castellanos, Alejandro; Solà, Jordi
    • Angewandte Chemie International Edition, Vol. 48, Issue 32
    • DOI: 10.1002/anie.200901892

    Calorimetric study of a series of designed repeat proteins: Modular structure and modular folding
    journal, January 2011

    • Cortajarena, Aitziber L.; Regan, Lynne
    • Protein Science, Vol. 20, Issue 2
    • DOI: 10.1002/pro.564

    A human sterile alpha motif domain polymerizome
    journal, August 2011

    • Knight, Mary Jane; Leettola, Catherine; Gingery, Mari
    • Protein Science, Vol. 20, Issue 10
    • DOI: 10.1002/pro.703

    PIER: Protein interface recognition for structural proteomics
    journal, February 2007

    • Kufareva, Irina; Budagyan, Levon; Raush, Eugene
    • Proteins: Structure, Function, and Bioinformatics, Vol. 67, Issue 2
    • DOI: 10.1002/prot.21233

    Hot spots-A review of the protein-protein interface determinant amino-acid residues
    journal, June 2007

    • Moreira, Irina S.; Fernandes, Pedro A.; Ramos, Maria J.
    • Proteins: Structure, Function, and Bioinformatics, Vol. 68, Issue 4
    • DOI: 10.1002/prot.21396

    Structure of ribgrass mosaic virus at 2.9 å resolution evolution and taxonomy of tobamoviruses 1 1Edited by I. A. Wilson
    journal, July 1997

    • Wang, Hong; Culver, James N.; Stubbs, Gerald
    • Journal of Molecular Biology, Vol. 269, Issue 5
    • DOI: 10.1006/jmbi.1997.1048

    Three-dimensional reconstruction of helical polymers
    journal, September 2015


    Direct Observation of Parallel Folding Pathways Revealed Using a Symmetric Repeat Protein System
    journal, July 2014


    Unified Polymerization Mechanism for the Assembly of ASC-Dependent Inflammasomes
    journal, March 2014


    Structure of a Chaperone-Usher Pilus Reveals the Molecular Basis of Rod Uncoiling
    journal, January 2016


    Structure of the Bacterial Sex F Pilus Reveals an Assembly of a Stoichiometric Protein-Phospholipid Complex
    journal, September 2016


    Structure of Microbial Nanowires Reveals Stacked Hemes that Transport Electrons over Micrometers
    journal, April 2019


    The Structure of a Filamentous Bacteriophage
    journal, August 2006


    Inference of Macromolecular Assemblies from Crystalline State
    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
    journal, November 2010

    • Urvoas, Agathe; Guellouz, Asma; Valerio-Lepiniec, Marie
    • Journal of Molecular Biology, Vol. 404, Issue 2
    • DOI: 10.1016/j.jmb.2010.09.048

    A General Computational Approach for Repeat Protein Design
    journal, January 2015

    • Parmeggiani, Fabio; Huang, Po-Ssu; Vorobiev, Sergey
    • Journal of Molecular Biology, Vol. 427, Issue 2
    • DOI: 10.1016/j.jmb.2014.11.005

    Tandem repeats in proteins: From sequence to structure
    journal, September 2012


    Self-assembly of repeat proteins: Concepts and design of new interfaces
    journal, February 2018

    • Sanchez-deAlcazar, Daniel; Mejias, Sara H.; Erazo, Kevin
    • Journal of Structural Biology, Vol. 201, Issue 2
    • DOI: 10.1016/j.jsb.2017.09.002

    Structural Plasticity of Helical Nanotubes Based on Coiled-Coil Assemblies
    journal, February 2015


    The Cryoelectron Microscopy Structure of the Type 1 Chaperone-Usher Pilus Rod
    journal, December 2017


    Helical Polymers: Synthesis, Structures, and Functions
    journal, November 2009

    • Yashima, Eiji; Maeda, Katsuhiro; Iida, Hiroki
    • Chemical Reviews, Vol. 109, Issue 11
    • DOI: 10.1021/cr900162q

    Design and Characterization of Programmable DNA Nanotubes
    journal, December 2004

    • Rothemund, Paul W. K.; Ekani-Nkodo, Axel; Papadakis, Nick
    • Journal of the American Chemical Society, Vol. 126, Issue 50
    • DOI: 10.1021/ja044319l

    A New Folding Paradigm for Repeat Proteins
    journal, July 2005

    • Kajander, Tommi; Cortajarena, Aitziber L.; Main, Ewan R. G.
    • Journal of the American Chemical Society, Vol. 127, Issue 29
    • DOI: 10.1021/ja0524494

    Chiral Induction in Quinoline-Derived Oligoamide Foldamers:  Assignment of Helical Handedness and Role of Steric Effects
    journal, September 2005

    • Dolain, Christel; Jiang, Hua; Léger, Jean-Michel
    • Journal of the American Chemical Society, Vol. 127, Issue 37
    • DOI: 10.1021/ja0527828

    Rational Design of Helical Nanotubes from Self-Assembly of Coiled-Coil Lock Washers
    journal, October 2013

    • Xu, Chunfu; Liu, Rui; Mehta, Anil K.
    • Journal of the American Chemical Society, Vol. 135, Issue 41
    • DOI: 10.1021/ja4074529

    Modular Design of Self-Assembling Peptide-Based Nanotubes
    journal, August 2015

    • Burgess, Natasha C.; Sharp, Thomas H.; Thomas, Franziska
    • Journal of the American Chemical Society, Vol. 137, Issue 33
    • DOI: 10.1021/jacs.5b03973

    X-ray Crystallographic Structure of a Giant Double-Walled Peptide Nanotube Formed by a Macrocyclic β-Sheet Containing Aβ 16–22
    journal, June 2017

    • Chen, Kevin H.; Corro, Kelsey A.; Le, Stephanie P.
    • Journal of the American Chemical Society, Vol. 139, Issue 24
    • DOI: 10.1021/jacs.7b03890

    Unusual Arginine Formations in Protein Function and Assembly: Rings, Strings, and Stacks
    journal, April 2012

    • Neves, Marco A. C.; Yeager, Mark; Abagyan, Ruben
    • The Journal of Physical Chemistry B, Vol. 116, Issue 23
    • DOI: 10.1021/jp3009699

    Interconnecting Gold Islands with DNA Origami Nanotubes
    journal, December 2010

    • Ding, Baoquan; Wu, Hao; Xu, Wei
    • Nano Letters, Vol. 10, Issue 12
    • DOI: 10.1021/nl1033073

    Molecular Structure of RADA16-I Designer Self-Assembling Peptide Nanofibers
    journal, August 2013

    • Cormier, Ashley R.; Pang, Xiaodong; Zimmerman, Maxwell I.
    • ACS Nano, Vol. 7, Issue 9
    • DOI: 10.1021/nn401562f

    F-actin is a helix with a random variable twist
    journal, July 1982

    • Egelman, E. H.; Francis, N.; DeRosier, D. J.
    • Nature, Vol. 298, Issue 5870
    • DOI: 10.1038/298131a0

    The structure of the E. coli recA protein monomer and polymer
    journal, January 1992

    • Story, Randall M.; Weber, Irene T.; Steitz, Thomas A.
    • Nature, Vol. 355, Issue 6358
    • DOI: 10.1038/355318a0

    Crystal structure of porcine ribonuclease inhibitor, a protein with leucine-rich repeats
    journal, December 1993

    • Kobe, Bostjan; Deisenhofer, Johann
    • Nature, Vol. 366, Issue 6457
    • DOI: 10.1038/366751a0

    Atomic model of the type III secretion system needle
    journal, May 2012

    • Loquet, Antoine; Sgourakis, Nikolaos G.; Gupta, Rashmi
    • Nature, Vol. 486, Issue 7402
    • DOI: 10.1038/nature11079

    Exploring the repeat protein universe through computational protein design
    journal, December 2015

    • Brunette, Tj; Parmeggiani, Fabio; Huang, Po-Ssu
    • Nature, Vol. 528, Issue 7583
    • DOI: 10.1038/nature16162

    Rational design of α-helical tandem repeat proteins with closed architectures
    journal, December 2015

    • Doyle, Lindsey; Hallinan, Jazmine; Bolduc, Jill
    • Nature, Vol. 528, Issue 7583
    • DOI: 10.1038/nature16191

    Proteins evolve on the edge of supramolecular self-assembly
    journal, August 2017

    • Garcia-Seisdedos, Hector; Empereur-Mot, Charly; Elad, Nadav
    • Nature, Vol. 548, Issue 7666
    • DOI: 10.1038/nature23320

    Atomic-accuracy models from 4.5-Å cryo-electron microscopy data with density-guided iterative local refinement
    journal, February 2015

    • DiMaio, Frank; Song, Yifan; Li, Xueming
    • Nature Methods, Vol. 12, Issue 4
    • DOI: 10.1038/nmeth.3286

    A leucine-rich repeat variant with a novel repetitive protein structural motif
    journal, December 1996

    • Peters, John W.; Stowell, Michael H. B.; Rees, Douglas C.
    • Nature Structural Biology, Vol. 3, Issue 12
    • DOI: 10.1038/nsb1296-991

    Control of repeat-protein curvature by computational protein design
    journal, January 2015

    • Park, Keunwan; Shen, Betty W.; Parmeggiani, Fabio
    • Nature Structural & Molecular Biology, Vol. 22, Issue 2
    • DOI: 10.1038/nsmb.2938

    A structural model of flagellar filament switching across multiple bacterial species
    journal, October 2017


    Physical basis of amyloid fibril polymorphism
    journal, February 2018


    Designed peptides that assemble into cross-α amyloid-like structures
    journal, July 2018


    Atomic-level evidence for packing and positional amyloid polymorphism by segment from TDP-43 RRM2
    journal, March 2018

    • Guenther, Elizabeth L.; Ge, Peng; Trinh, Hamilton
    • Nature Structural & Molecular Biology, Vol. 25, Issue 4
    • DOI: 10.1038/s41594-018-0045-5

    Induction of one-handed helical oligo(p-benzamide)s by domino effect based on planar-axial-helical chirality relay
    journal, January 2009

    • Kamikawa, Ken; Fukumoto, Keisuke; Yoshihara, Kohei
    • Chemical Communications, Issue 10
    • DOI: 10.1039/b818123c

    DNA nanotubes self-assembled from triple-crossover tiles as templates for conductive nanowires
    journal, January 2004

    • Liu, D.; Park, S. H.; Reif, J. H.
    • Proceedings of the National Academy of Sciences, Vol. 101, Issue 3
    • DOI: 10.1073/pnas.0305860101

    Cryo-transmission electron microscopy structure of a gigadalton peptide fiber of de novo design
    journal, July 2012

    • Sharp, T. H.; Bruning, M.; Mantell, J.
    • Proceedings of the National Academy of Sciences, Vol. 109, Issue 33
    • DOI: 10.1073/pnas.1118622109

    Computational design of a leucine-rich repeat protein with a predefined geometry
    journal, November 2014

    • Rämisch, Sebastian; Weininger, Ulrich; Martinsson, Jonas
    • Proceedings of the National Academy of Sciences, Vol. 111, Issue 50
    • DOI: 10.1073/pnas.1413638111

    The NMR–Rosetta capsid model of M13 bacteriophage reveals a quadrupled hydrophobic packing epitope
    journal, January 2015

    • Morag, Omry; Sgourakis, Nikolaos G.; Baker, David
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 4
    • DOI: 10.1073/pnas.1415393112

    Molecular structure of monomorphic peptide fibrils within a kinetically trapped hydrogel network
    journal, July 2015

    • Nagy-Smith, Katelyn; Moore, Eric; Schneider, Joel
    • Proceedings of the National Academy of Sciences, Vol. 112, Issue 32
    • DOI: 10.1073/pnas.1509313112

    Zinc-binding structure of a catalytic amyloid from solid-state NMR
    journal, May 2017

    • Lee, Myungwoon; Wang, Tuo; Makhlynets, Olga V.
    • Proceedings of the National Academy of Sciences, Vol. 114, Issue 24
    • DOI: 10.1073/pnas.1706179114

    Crystal structure of a 12 ANK repeat stack from human ankyrinR
    journal, December 2002


    High-resolution structure of the presynaptic RAD51 filament on single-stranded DNA by electron cryo-microscopy
    journal, September 2016

    • Short, Judith M.; Liu, Yang; Chen, Shaoxia
    • Nucleic Acids Research
    • DOI: 10.1093/nar/gkw783

    De novo design of self-assembling helical protein filaments
    journal, November 2018


    Designed Ankyrin Repeat Proteins (DARPins): Binding Proteins for Research, Diagnostics, and Therapy
    journal, January 2015



    journal, January 2015