Search Menu
DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information
Search Scholarly Publications

Title: Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis

Abstract

The assembly of individual molecules into hierarchical structures is a promising strategy for developing novel three-dimensional materials with potential for collective behavior and properties beyond those of the individual building blocks. Virus-like particles (VLPs), inspired by the elegant assembly of virus capsids, are examples of hierarchically assembled nanoparticles constituted from a limited number of protein subunits. Here we demonstrate the construction of bulk materials with two levels of hierarchy; the formation of catalytically active VLPs through directed enzyme encapsulation into VLPs, and self-assembly of these VLP building blocks into ordered three-dimensional lattices. The resulting materials, obtained by rational design of the exterior surface of the VLP to modulate interparticle interactions, adopt a face-centered cubic lattice that is independent of the enzyme cargo within the interior. We describe the design, characterization, and implications of a hierarchical structure composed of two enzyme packaged VLPs that are catalytically coupled to synthesize isobutanol.

Authors:
ORCiD logo [1];  [1];  [2];  [2];  [3];  [4];  [4]; ORCiD logo [5];  [1];  [1];  [6]; ORCiD logo [7]; ORCiD logo [1]
+ Show Author Affiliations
  1. Indiana Univ., Bloomington, IN (United States)
  2. Brookhaven National Lab. (BNL), Upton, NY (United States)
  3. Indiana Univ., Bloomington, IN (United States); Meiji Univ., Kawasaki (Japan)
  4. Montana State Univ., Bozeman, MT (United States)
  5. Univ. of Texas at Tyler, Tyler, TX (United States)
  6. Univ. of Alabama at Birmingham, Birmingham, AL (United States)
  7. Argonne National Lab. (ANL), Argonne, IL (United States)
Publication Date:
Research Org.:
Brookhaven National Laboratory (BNL), Upton, NY (United States); Argonne National Laboratory (ANL), Argonne, IL (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER)
OSTI Identifier:
1435735
Alternate Identifier(s):
OSTI ID: 1460999
Report Number(s):
BNL-203582-2018-JAAM
Journal ID: ISSN 1936-0851
Grant/Contract Number:  
SC0012704; AC02-06CH11357
Resource Type:
Accepted Manuscript
Journal Name:
ACS Nano
Additional Journal Information:
Journal Volume: 12; Journal Issue: 2; Journal ID: ISSN 1936-0851
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
36 MATERIALS SCIENCE; coupled catalysis; enzyme encapsulation; hierarchical structure; nanoreactor; self-assembly; superlattice; virus-like particle

Citation Formats

Uchida, Masaki, McCoy, Kimberly, Fukuto, Masafumi, Yang, Lin, Yoshimura, Hideyuki, Miettinen, Heini M., LaFrance, Ben, Patterson, Dustin P., Schwarz, Benjamin, Karty, Jonathan A., Prevelige, Jr., Peter E., Lee, Byeongdu, and Douglas, Trevor. Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis. United States: N. p., 2017. Web. doi:10.1021/acsnano.7b06049.
Copy to clipboard
Uchida, Masaki, McCoy, Kimberly, Fukuto, Masafumi, Yang, Lin, Yoshimura, Hideyuki, Miettinen, Heini M., LaFrance, Ben, Patterson, Dustin P., Schwarz, Benjamin, Karty, Jonathan A., Prevelige, Jr., Peter E., Lee, Byeongdu, & Douglas, Trevor. Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis. United States. https://doi.org/10.1021/acsnano.7b06049
Copy to clipboard
Uchida, Masaki, McCoy, Kimberly, Fukuto, Masafumi, Yang, Lin, Yoshimura, Hideyuki, Miettinen, Heini M., LaFrance, Ben, Patterson, Dustin P., Schwarz, Benjamin, Karty, Jonathan A., Prevelige, Jr., Peter E., Lee, Byeongdu, and Douglas, Trevor. Mon . "Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis". United States. https://doi.org/10.1021/acsnano.7b06049. https://www.osti.gov/servlets/purl/1435735.
Copy to clipboard
@article{osti_1435735,
title = {Modular Self-Assembly of Protein Cage Lattices for Multistep Catalysis},
author = {Uchida, Masaki and McCoy, Kimberly and Fukuto, Masafumi and Yang, Lin and Yoshimura, Hideyuki and Miettinen, Heini M. and LaFrance, Ben and Patterson, Dustin P. and Schwarz, Benjamin and Karty, Jonathan A. and Prevelige, Jr., Peter E. and Lee, Byeongdu and Douglas, Trevor},
abstractNote = {The assembly of individual molecules into hierarchical structures is a promising strategy for developing novel three-dimensional materials with potential for collective behavior and properties beyond those of the individual building blocks. Virus-like particles (VLPs), inspired by the elegant assembly of virus capsids, are examples of hierarchically assembled nanoparticles constituted from a limited number of protein subunits. Here we demonstrate the construction of bulk materials with two levels of hierarchy; the formation of catalytically active VLPs through directed enzyme encapsulation into VLPs, and self-assembly of these VLP building blocks into ordered three-dimensional lattices. The resulting materials, obtained by rational design of the exterior surface of the VLP to modulate interparticle interactions, adopt a face-centered cubic lattice that is independent of the enzyme cargo within the interior. We describe the design, characterization, and implications of a hierarchical structure composed of two enzyme packaged VLPs that are catalytically coupled to synthesize isobutanol.},
doi = {10.1021/acsnano.7b06049},
journal = {ACS Nano},
number = 2,
volume = 12,
place = {United States},
year = {Mon Nov 13 00:00:00 EST 2017},
month = {Mon Nov 13 00:00:00 EST 2017}
}
Copy to clipboard
Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record
https://doi.org/10.1021/acsnano.7b06049
Copyright Statement
Other availability
Search WorldCat Search WorldCat to find libraries that may hold this journal
Citation Metrics:
Cited by: 68 works
Citation information provided by
Web of Science
Save / Share:
Export Metadata
Save to My Library
You must Sign In or Create an Account in order to save documents to your library.

Works referenced in this record:

DNA-programmable nanoparticle crystallization
journal, January 2008

  • Park, Sung Yong; Lytton-Jean, Abigail K. R.; Lee, Byeongdu
  • Nature, Vol. 451, Issue 7178, p. 553-556
  • DOI: 10.1038/nature06508

Nanoparticle Superlattice Engineering with DNA
journal, October 2011

DNA-mediated engineering of multicomponent enzyme crystals
journal, March 2015

  • Brodin, Jeffrey D.; Auyeung, Evelyn; Mirkin, Chad A.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 15
  • DOI: 10.1073/pnas.1503533112

DNA-guided crystallization of colloidal nanoparticles
journal, January 2008

  • Nykypanchuk, Dmytro; Maye, Mathew M.; van der Lelie, Daniel
  • Nature, Vol. 451, Issue 7178, p. 549-552
  • DOI: 10.1038/nature06560

A general strategy for the DNA-mediated self-assembly of functional nanoparticles into heterogeneous systems
journal, October 2013

  • Zhang, Yugang; Lu, Fang; Yager, Kevin G.
  • Nature Nanotechnology, Vol. 8, Issue 11
  • DOI: 10.1038/nnano.2013.209

Structural diversity in binary nanoparticle superlattices
journal, January 2006

  • Shevchenko, Elena V.; Talapin, Dmitri V.; Kotov, Nicholas A.
  • Nature, Vol. 439, Issue 7072, p. 55-59
  • DOI: 10.1038/nature04414

Electrostatic Self-Assembly of Binary Nanoparticle Crystals with a Diamond-Like Lattice
journal, February 2006

  • Kalsin, A. M.; Fialkowski, M.; Paszewski, M.
  • Science, Vol. 312, Issue 5772, p. 420-424
  • DOI: 10.1126/science.1125124

Re-entrant solidification in polymer–colloid mixtures as a consequence of competing entropic and enthalpic attractions
journal, October 2014

  • Feng, Lang; Laderman, Bezia; Sacanna, Stefano
  • Nature Materials, Vol. 14, Issue 1
  • DOI: 10.1038/nmat4109

Functional Porous Coordination Polymers
journal, April 2004

  • Kitagawa, Susumu; Kitaura, Ryo; Noro, Shin-ichiro
  • Angewandte Chemie International Edition, Vol. 43, Issue 18, p. 2334-2375
  • DOI: 10.1002/anie.200300610

Self-Assembly at All Scales
journal, March 2002

  • Whitesides, George M.; Grzybowski, Bartosz
  • Science, Vol. 295, Issue 5564, p. 2418-2421
  • DOI: 10.1126/science.1070821

Diverse Bacterial Microcompartment Organelles
journal, September 2014

  • Chowdhury, C.; Sinha, S.; Chun, S.
  • Microbiology and Molecular Biology Reviews, Vol. 78, Issue 3
  • DOI: 10.1128/MMBR.00009-14

Atomic-Level Models of the Bacterial Carboxysome Shell
journal, February 2008

Viruses: Making Friends with Old Foes
journal, May 2006

Self-assembly and optically triggered disassembly of hierarchical dendron–virus complexes
journal, March 2010

  • Kostiainen, Mauri A.; Kasyutich, Oksana; Cornelissen, Jeroen J. L. M.
  • Nature Chemistry, Vol. 2, Issue 5
  • DOI: 10.1038/nchem.592

Electrostatic assembly of binary nanoparticle superlattices using protein cages
journal, December 2012

  • Kostiainen, Mauri A.; Hiekkataipale, Panu; Laiho, Ari
  • Nature Nanotechnology, Vol. 8, Issue 1
  • DOI: 10.1038/nnano.2012.220

Self-assembly and modular functionalization of three-dimensional crystals from oppositely charged proteins
journal, July 2014

  • Liljeström, Ville; Mikkilä, Joona; Kostiainen, Mauri A.
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5445

Electrostatic Self-Assembly of Soft Matter Nanoparticle Cocrystals with Tunable Lattice Parameters
journal, October 2015

  • Liljeström, Ville; Seitsonen, Jani; Kostiainen, Mauri A.
  • ACS Nano, Vol. 9, Issue 11
  • DOI: 10.1021/acsnano.5b04912

DNA-controlled assembly of a NaTl lattice structure from gold nanoparticles and protein nanoparticles
journal, October 2010

  • Cigler, Petr; Lytton-Jean, Abigail K. R.; Anderson, Daniel G.
  • Nature Materials, Vol. 9, Issue 11, p. 918-922
  • DOI: 10.1038/nmat2877

A Metal Organic Framework with Spherical Protein Nodes: Rational Chemical Design of 3D Protein Crystals
journal, September 2015

  • Sontz, Pamela A.; Bailey, Jake B.; Ahn, Sunhyung
  • Journal of the American Chemical Society, Vol. 137, Issue 36
  • DOI: 10.1021/jacs.5b07463

Higher Order Assembly of Virus-like Particles (VLPs) Mediated by Multi-valent Protein Linkers
journal, January 2015

Biomimetic self-templating supramolecular structures
journal, October 2011

  • Chung, Woo-Jae; Oh, Jin-Woo; Kwak, Kyungwon
  • Nature, Vol. 478, Issue 7369
  • DOI: 10.1038/nature10513

Natural supramolecular building blocks: from virus coat proteins to viral nanoparticles
journal, January 2012

  • Liu, Zhi; Qiao, Jing; Niu, Zhongwei
  • Chemical Society Reviews, Vol. 41, Issue 18
  • DOI: 10.1039/c2cs35108k

Using Synthetically Modified Proteins to Make New Materials
journal, September 2011

  • Witus, Leah S.; Francis, Matthew B.
  • Accounts of Chemical Research, Vol. 44, Issue 9
  • DOI: 10.1021/ar2001292

Directed Evolution of a Protein Container
journal, February 2011

A virus-based single-enzyme nanoreactor
journal, September 2007

  • Comellas-Aragonès, Marta; Engelkamp, Hans; Claessen, Victor I.
  • Nature Nanotechnology, Vol. 2, Issue 10
  • DOI: 10.1038/nnano.2007.299

Templated assembly of organic–inorganic materials using the core shell structure of the P22 bacteriophage
journal, January 2011

  • Reichhardt, Courtney; Uchida, Masaki; O'Neil, Alison
  • Chemical Communications, Vol. 47, Issue 22
  • DOI: 10.1039/c1cc11215e

Selective Biotemplated Synthesis of TiO 2 Inside a Protein Cage
journal, December 2014

  • Bedwell, Gregory J.; Zhou, Ziyou; Uchida, Masaki
  • Biomacromolecules, Vol. 16, Issue 1
  • DOI: 10.1021/bm501443e

Use of the interior cavity of the P22 capsid for site-specific initiation of atom-transfer radical polymerization with high-density cargo loading
journal, August 2012

  • Lucon, Janice; Qazi, Shefah; Uchida, Masaki
  • Nature Chemistry, Vol. 4, Issue 10
  • DOI: 10.1038/nchem.1442

Site-Directed Coordination Chemistry with P22 Virus-like Particles
journal, December 2011

  • Uchida, Masaki; Morris, David S.; Kang, Sebyung
  • Langmuir, Vol. 28, Issue 4
  • DOI: 10.1021/la203866c

Genetically Programmed In Vivo Packaging of Protein Cargo and Its Controlled Release from Bacteriophage P22
journal, June 2011

  • O'Neil, Alison; Reichhardt, Courtney; Johnson, Benjamin
  • Angewandte Chemie International Edition, Vol. 50, Issue 32
  • DOI: 10.1002/anie.201102036

Scaffolding protein regulates the polymerization of P22 coat subunits into icosahedral shells in vitro
journal, August 1988

Mechanism of Scaffolding-Directed Virus Assembly Suggested by Comparison of Scaffolding-Containing and Scaffolding-Lacking P22 Procapsids
journal, June 1999

Functional domains of bacteriophage P22 scaffolding protein
journal, August 1998

  • Parker, Matthew H.; Casjens, Sherwood; Prevelige, Peter E.
  • Journal of Molecular Biology, Vol. 281, Issue 1
  • DOI: 10.1006/jmbi.1998.1917

The Structure of an Infectious P22 Virion Shows the Signal for Headful DNA Packaging
journal, June 2006

Nanoreactors by Programmed Enzyme Encapsulation Inside the Capsid of the Bacteriophage P22
journal, May 2012

  • Patterson, Dustin P.; Prevelige, Peter E.; Douglas, Trevor
  • ACS Nano, Vol. 6, Issue 6
  • DOI: 10.1021/nn300545z

Encapsulation of an Enzyme Cascade within the Bacteriophage P22 Virus-Like Particle
journal, November 2013

  • Patterson, Dustin P.; Schwarz, Benjamin; Waters, Ryan S.
  • ACS Chemical Biology, Vol. 9, Issue 2
  • DOI: 10.1021/cb4006529

Self-assembling biomolecular catalysts for hydrogen production
journal, December 2015

  • Jordan, Paul C.; Patterson, Dustin P.; Saboda, Kendall N.
  • Nature Chemistry, Vol. 8, Issue 2
  • DOI: 10.1038/nchem.2416

Stabilizing viral nano-reactors for nerve-agent degradation
journal, January 2013

  • O'Neil, Alison; Prevelige, Peter E.; Douglas, Trevor
  • Biomaterials Science, Vol. 1, Issue 8
  • DOI: 10.1039/c3bm60063g

Constructing catalytic antimicrobial nanoparticles by encapsulation of hydrogen peroxide producing enzyme inside the P22 VLP
journal, January 2014

  • Patterson, Dustin P.; McCoy, Kimberly; Fijen, Carel
  • Journal of Materials Chemistry B, Vol. 2, Issue 36
  • DOI: 10.1039/C4TB00983E

Location of the Bacteriophage P22 Coat Protein C-Terminus Provides Opportunities for the Design of Capsid-Based Materials
journal, August 2013

  • Servid, Amy; Jordan, Paul; O’Neil, Alison
  • Biomacromolecules, Vol. 14, Issue 9
  • DOI: 10.1021/bm400796c

Three-Dimensional Binary Superlattices of Oppositely Charged Colloids
journal, September 2005

Structure of crystals of hard colloidal spheres
journal, December 1989

Real-Space Imaging of Nucleation and Growth in Colloidal Crystallization
journal, April 2001

Stabilizing colloidal crystals by leveraging void distributions
journal, July 2014

  • Mahynski, Nathan A.; Panagiotopoulos, Athanassios Z.; Meng, Dong
  • Nature Communications, Vol. 5, Issue 1
  • DOI: 10.1038/ncomms5472

Non-fermentative pathways for synthesis of branched-chain higher alcohols as biofuels
journal, January 2008

  • Atsumi, Shota; Hanai, Taizo; Liao, James C.
  • Nature, Vol. 451, Issue 7174, p. 86-89
  • DOI: 10.1038/nature06450

Microbial engineering for the production of advanced biofuels
journal, August 2012

  • Peralta-Yahya, Pamela P.; Zhang, Fuzhong; del Cardayre, Stephen B.
  • Nature, Vol. 488, Issue 7411
  • DOI: 10.1038/nature11478

Enzyme Immobilization: The Quest for Optimum Performance
journal, June 2007

Modifying enzyme activity and selectivity by immobilization
journal, January 2013

  • Rodrigues, Rafael C.; Ortiz, Claudia; Berenguer-Murcia, Ángel
  • Chem. Soc. Rev., Vol. 42, Issue 15
  • DOI: 10.1039/C2CS35231A

Materials-based strategies for multi-enzyme immobilization and co-localization: A review: Multi-Enzyme Co-localization
journal, November 2013

  • Jia, Feng; Narasimhan, Balaji; Mallapragada, Surya
  • Biotechnology and Bioengineering, Vol. 111, Issue 2
  • DOI: 10.1002/bit.25136

Purification of the coat and scaffolding proteins from procapsids of bacteriophage P22
journal, July 1981

Self-Assembled Virus-like Particles with Magnetic Cores
journal, August 2007

  • Huang, Xinlei; Bronstein, Lyudmila M.; Retrum, John
  • Nano Letters, Vol. 7, Issue 8
  • DOI: 10.1021/nl071083l

Biochemical and molecular characterization of ?-ketoisovalerate decarboxylase, an enzyme involved in the formation of aldehydes from amino acids by
journal, September 2004

Structure-guided engineering of Lactococcus lactis alcohol dehydrogenase LlAdhA for improved conversion of isobutyraldehyde to isobutanol
journal, March 2013

Molecular Genetics of Bacteriophage P22 Scaffolding Protein's Functional Domains
journal, May 2005

  • Weigele, Peter R.; Sampson, Laura; Winn-Stapley, Danella
  • Journal of Molecular Biology, Vol. 348, Issue 4
  • DOI: 10.1016/j.jmb.2005.03.004

Implementation of P22 Viral Capsids as Nanoplatforms
journal, October 2010

  • Kang, Sebyung; Uchida, Masaki; O’Neil, Alison
  • Biomacromolecules, Vol. 11, Issue 10
  • DOI: 10.1021/bm100877q
    Sort by:
    [ × clear filter / sort ]

    Works referencing / citing this record:

    Direct visualization of single virus restoration after damage in real time
    journal, April 2018

    • de Pablo, Pedro J.; Hernando-Pérez, Mercedes; Carrasco, Carolina
    • Journal of Biological Physics, Vol. 44, Issue 2
    • DOI: 10.1007/s10867-018-9492-9

    Metal‐dependent assembly of a protein nano‐cage
    journal, August 2019

    • Cristie‐David, Ajitha S.; Marsh, E. Neil G.
    • Protein Science
    • DOI: 10.1002/pro.3676

    Crystallizing protein assemblies via free and grafted linkers
    journal, January 2019

    • Dahal, Yuba Raj; Olvera de la Cruz, Monica
    • Soft Matter, Vol. 15, Issue 21
    • DOI: 10.1039/c9sm00693a

    A review on virus protein self-assembly
    journal, November 2019

    Application of Plant Viruses as a Biotemplate for Nanomaterial Fabrication
    journal, September 2018

    Structural nanotechnology: three-dimensional cryo-EM and its use in the development of nanoplatforms for in vitro catalysis
    journal, January 2019

    • de Ruiter, Mark V.; Klem, Robin; Luque, Daniel
    • Nanoscale, Vol. 11, Issue 10
    • DOI: 10.1039/c8nr09204d

    Highly ordered protein cage assemblies: A toolkit for new materials
    journal, August 2019

    • Korpi, Antti; Anaya‐Plaza, Eduardo; Välimäki, Salla
    • WIREs Nanomedicine and Nanobiotechnology, Vol. 12, Issue 1
    • DOI: 10.1002/wnan.1578

    Multi‐Component Self‐Assembly of Proteins and Inorganic Particles: From Discrete Structures to Biomimetic Materials
    journal, April 2019

    • Künzle, Matthias; Lach, Marcel; Beck, Tobias
    • Israel Journal of Chemistry, Vol. 59, Issue 10
    • DOI: 10.1002/ijch.201900013

    Asymmetric bifunctional protein nanoparticles through redesign of self-assembly
    journal, January 2019

    • Sosa, Santiago; Rossi, Andrés H.; Szalai, Alan M.
    • Nanoscale Advances, Vol. 1, Issue 5
    • DOI: 10.1039/c8na00375k

    Nanoreactor Design Based on Self-Assembling Protein Nanocages
    journal, January 2019

    • Ren, Huimei; Zhu, Shaozhou; Zheng, Guojun
    • International Journal of Molecular Sciences, Vol. 20, Issue 3
    • DOI: 10.3390/ijms20030592

    Fabrication of Nanoreaction Clusters with Dual-Functionalized Protein Cage Nanobuilding Blocks
    journal, July 2018

    Computational studies of shape control of charged deformable nanocontainers
    journal, January 2019

    • Brunk, Nicholas E.; Jadhao, Vikram
    • Journal of Materials Chemistry B, Vol. 7, Issue 41
    • DOI: 10.1039/c9tb01003c

    Phthalocyanine–Virus Nanofibers as Heterogeneous Catalysts for Continuous‐Flow Photo‐Oxidation Processes
    journal, August 2019

    • Anaya‐Plaza, Eduardo; Aljarilla, Ana; Beaune, Grégory
    • Advanced Materials, Vol. 31, Issue 39
    • DOI: 10.1002/adma.201902582

    Protein cage assembly across multiple length scales
    journal, January 2018

    • Aumiller, William M.; Uchida, Masaki; Douglas, Trevor
    • Chemical Society Reviews, Vol. 47, Issue 10
    • DOI: 10.1039/c7cs00818j

    Peptide-directed encapsulation of inorganic nanoparticles into protein containers
    journal, January 2018

    • Künzle, Matthias; Mangler, Johanna; Lach, Marcel
    • Nanoscale, Vol. 10, Issue 48
    • DOI: 10.1039/c8nr06236f

    Virus-derived materials: bury the hatchet with old foes
    journal, January 2020

    • Wu, Jiahe; Wu, Honghui; Nakagawa, Shinsaku
    • Biomaterials Science, Vol. 8, Issue 4
    • DOI: 10.1039/c9bm01383k

    Construction of supramolecular nanotubes from protein crystals
    journal, January 2019

    • Nguyen, Tien Khanh; Negishi, Hashiru; Abe, Satoshi
    • Chemical Science, Vol. 10, Issue 4
    • DOI: 10.1039/c8sc04167a

    Application of Plant Viruses as a Biotemplate for Nanomaterial Fabrication
    journal, September 2018

      Sort by:
      [ × clear filter / sort ]

      Similar Records in DOE PAGES and OSTI.GOV collections: