ACS Publications. Most Trusted. Most Cited. Most Read
My Activity
CONTENT TYPES

Experimental Evaluation of Coevolution in a Self-Assembling Particle

  • Emily C. Hartman
    Emily C. Hartman
    Department of Chemistry, University of California, Berkeley, California 94720-1460, United States
  • Marco J. Lobba
    Marco J. Lobba
    Department of Chemistry, University of California, Berkeley, California 94720-1460, United States
  • Andrew H. Favor
    Andrew H. Favor
    Department of Chemistry, University of California, Berkeley, California 94720-1460, United States
  • Stephanie A. Robinson
    Stephanie A. Robinson
    Department of Chemistry, University of California, Berkeley, California 94720-1460, United States
  • Matthew B. Francis*
    Matthew B. Francis
    Department of Chemistry, University of California, Berkeley, California 94720-1460, United States
    Materials Sciences Division, Lawrence Berkeley National Laboratories, Berkeley, California 94720-1460, United States
    *E-mail: [email protected]
  • , and 
  • Danielle Tullman-Ercek*
    Danielle Tullman-Ercek
    Department of Chemical and Biological Engineering, Northwestern University, 2145 Sheridan Road, Technological Institute E136, Evanston, Illinois 60208-3120, United States
    *E-mail: [email protected]
Cite this: Biochemistry 2019, 58, 11, 1527–1538
Publication Date (Web):November 12, 2018
https://doi.org/10.1021/acs.biochem.8b00948
Copyright © 2018 American Chemical Society

    Article Views

    1506

    Altmetric

    -

    Citations

    LEARN ABOUT THESE METRICS
    Other access options
    Supporting Info (4)»

    Abstract

    Abstract Image

    Protein evolution occurs via restricted evolutionary paths that are influenced by both previous and subsequent mutations. This effect, termed epistasis, is critical in population genetics, drug resistance, and immune escape; however, the effect of epistasis on the level of protein fitness is less well characterized. We generated and characterized a 6615-member library of all two-amino acid combinations in a highly mutable loop of a virus-like particle. This particle is a model of protein self-assembly and a promising vehicle for drug delivery and imaging. In addition to characterizing the effect of all double mutants on assembly, thermostability, and acid stability, we observed many instances of epistasis, in which combinations of mutations are either more deleterious or more beneficial than expected. These results were used to generate rules governing the effects of multiple mutations on the self-assembly of the virus-like particle.

    Read this article

    To access this article, please review the available access options below.

    Get instant access

    Purchase Access

    Read this article for 48 hours. Check out below using your ACS ID or as a guest.

    Recommended

    Access through Your Institution

    You may have access to this article through your institution.

    Your institution does not have access to this content. You can change your affiliated institution below.

    Supporting Information

    ARTICLE SECTIONS
    Jump To

    The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.biochem.8b00948.

    • Data Set 1: Primers for library generation, high-throughput sequencing, and individual variant cloning (XLSX)

    • Data Set 2: Complete dataset for assembly- and heat-selected 2D AFLs (XLSX)

    • Data Set 3: List of candidate two amino acid variants exhibiting epistasis (XLSX)

    • Additional figures, primers, complete 2D AFL scores, and epistatic scores (PDF)

    Terms & Conditions

    Electronic Supporting Information files are available without a subscription to ACS Web Editions. The American Chemical Society holds a copyright ownership interest in any copyrightable Supporting Information. Files available from the ACS website may be downloaded for personal use only. Users are not otherwise permitted to reproduce, republish, redistribute, or sell any Supporting Information from the ACS website, either in whole or in part, in either machine-readable form or any other form without permission from the American Chemical Society. For permission to reproduce, republish and redistribute this material, requesters must process their own requests via the RightsLink permission system. Information about how to use the RightsLink permission system can be found at http://pubs.acs.org/page/copyright/permissions.html.

    Cited By

    This article is cited by 12 publications.

    1. Paige E. Pistono, Paul Huang, Daniel D. Brauer, Matthew B. Francis. Fitness Landscape-Guided Engineering of Locally Supercharged Virus-like Particles with Enhanced Cell Uptake Properties. ACS Chemical Biology 2022, 17 (12) , 3367-3378. https://doi.org/10.1021/acschembio.2c00318
    2. Thomas G. W. Edwardson, Mikail D. Levasseur, Stephan Tetter, Angela Steinauer, Mao Hori, Donald Hilvert. Protein Cages: From Fundamentals to Advanced Applications. Chemical Reviews 2022, 122 (9) , 9145-9197. https://doi.org/10.1021/acs.chemrev.1c00877
    3. Stephanie A. Robinson, Emily C. Hartman, Bon C. Ikwuagwu, Matthew B. Francis, Danielle Tullman-Ercek. Engineering a Virus-like Particle to Display Peptide Insertions Using an Apparent Fitness Landscape. Biomacromolecules 2020, 21 (10) , 4194-4204. https://doi.org/10.1021/acs.biomac.0c00987
    4. Thomas G. W. Edwardson, Donald Hilvert. Virus-Inspired Function in Engineered Protein Cages. Journal of the American Chemical Society 2019, 141 (24) , 9432-9443. https://doi.org/10.1021/jacs.9b03705
    5. Daniel D. Brauer, Emily C. Hartman, Daniel L. V. Bader, Zoe N. Merz, Danielle Tullman-Ercek, Matthew B. Francis. Systematic Engineering of a Protein Nanocage for High-Yield, Site-Specific Modification. Journal of the American Chemical Society 2019, 141 (9) , 3875-3884. https://doi.org/10.1021/jacs.8b10734
    6. Malvika Srivastava, Hana Rozhoňová, Joshua L Payne. Alphabet cardinality and adaptive evolution. Journal of Physics A: Mathematical and Theoretical 2023, 56 (45) , 455601. https://doi.org/10.1088/1751-8121/ad0200
    7. Oscar González-Davis, Maria V. Villagrana-Escareño, Mario A. Trujillo, Pedro Gama, Kanchan Chauhan, Rafael Vazquez-Duhalt. Virus-like nanoparticles as enzyme carriers for Enzyme Replacement Therapy (ERT). Virology 2023, 580 , 73-87. https://doi.org/10.1016/j.virol.2023.01.017
    8. Bon Ikwuagwu, Emily Hartman, Carolyn E. Mills, Danielle Tullman-Ercek. Systematic engineering of virus-like particles to identify self-assembly rules for shifting particle size. Virology 2023, 579 , 137-147. https://doi.org/10.1016/j.virol.2023.01.002
    9. Bon Ikwuagwu, Danielle Tullman-Ercek. Virus-like particles for drug delivery: a review of methods and applications. Current Opinion in Biotechnology 2022, 78 , 102785. https://doi.org/10.1016/j.copbio.2022.102785
    10. Malvika Srivastava, Joshua L. Payne, . On the incongruence of genotype-phenotype and fitness landscapes. PLOS Computational Biology 2022, 18 (9) , e1010524. https://doi.org/10.1371/journal.pcbi.1010524
    11. David P. Wilson, Danielle A. Roof. Viral Phrenology. Viruses 2021, 13 (11) , 2191. https://doi.org/10.3390/v13112191
    12. David P. Wilson. Unveiling the Hidden Rules of Spherical Viruses Using Point Arrays. Viruses 2020, 12 (4) , 467. https://doi.org/10.3390/v12040467

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    Pair your accounts.

    Export articles to Mendeley

    Get article recommendations from ACS based on references in your Mendeley library.

    You’ve supercharged your research process with ACS and Mendeley!

    STEP 1:
    Click to create an ACS ID

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    Please note: If you switch to a different device, you may be asked to login again with only your ACS ID.

    MENDELEY PAIRING EXPIRED
    Your Mendeley pairing has expired. Please reconnect