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Evolution of a virus-like architecture and packaging mechanism in a repurposed bacterial protein.

Tetter S, Terasaka N, Steinauer A, Bingham RJ, Clark S, Scott AJP, Patel N, Leibundgut M, Wroblewski E, Ban N, Stockley PG, Twarock R, Hilvert D
Science 372 1220-1224 (2021)
Related entries: 7a4f, 7a4h, 7a4i, 7a4j

Cited: 19 times
EuropePMC logo PMID: 34112695

Abstract

Viruses are ubiquitous pathogens of global impact. Prompted by the hypothesis that their earliest progenitors recruited host proteins for virion formation, we have used stringent laboratory evolution to convert a bacterial enzyme that lacks affinity for nucleic acids into an artificial nucleocapsid that efficiently packages and protects multiple copies of its own encoding messenger RNA. Revealing remarkable convergence on the molecular hallmarks of natural viruses, the accompanying changes reorganized the protein building blocks into an interlaced 240-subunit icosahedral capsid that is impermeable to nucleases, and emergence of a robust RNA stem-loop packaging cassette ensured high encapsidation yields and specificity. In addition to evincing a plausible evolutionary pathway for primordial viruses, these findings highlight practical strategies for developing nonviral carriers for diverse vaccine and delivery applications.

Reviews citing this publication (9)

  1. The endoplasmic reticulum unfolded protein response - homeostasis, cell death and evolution in virus infections. Prasad V, Greber UF. FEMS Microbiol Rev 45 fuab016 (2021)
  2. Engineering Self-Assembling Protein Nanoparticles for Therapeutic Delivery. Olshefsky A, Richardson C, Pun SH, King NP. Bioconjug Chem 33 2018-2034 (2022)
  3. Biomotors, viral assembly, and RNA nanobiotechnology: Current achievements and future directions. Rolband L, Beasock D, Wang Y, Shu YG, Dinman JD, Schlick T, Zhou Y, Kieft JS, Chen SJ, Bussi G, Oukhaled A, Gao X, Šulc P, Binzel D, Bhullar AS, Liang C, Guo P, Afonin KA. Comput Struct Biotechnol J 20 6120-6137 (2022)
  4. Virus-like particles against infectious disease and cancer: guidance for the nano-architect. Hills RA, Howarth M. Curr Opin Biotechnol 73 346-354 (2022)
  5. Bacterial Nanocompartments: Structures, Functions, and Applications. McDowell HB, Hoiczyk E. J Bacteriol 204 e0034621 (2022)
  6. RNA Structures and Their Role in Selective Genome Packaging. Ye L, Ambi UB, Olguin-Nava M, Gribling-Burrer AS, Ahmad S, Bohn P, Weber MM, Smyth RP. Viruses 13 1788 (2021)
  7. Polyelectrolyte Encapsulation and Confinement within Protein Cage-Inspired Nanocompartments. Liu Q, Shaukat A, Kyllönen D, Kostiainen MA. Pharmaceutics 13 1551 (2021)
  8. Analyzing the Geometry and Dynamics of Viral Structures: A Review of Computational Approaches Based on Alpha Shape Theory, Normal Mode Analysis, and Poisson-Boltzmann Theories. Hsieh YC, Delarue M, Orland H, Koehl P. Viruses 15 1366 (2023)
  9. Methods for the directed evolution of biomolecular interactions. Xie VC, Styles MJ, Dickinson BC. Trends Biochem Sci 47 403-416 (2022)

Articles citing this publication (10)

  1. Improving the secretion of designed protein assemblies through negative design of cryptic transmembrane domains. Wang JYJ, Khmelinskaia A, Sheffler W, Miranda MC, Antanasijevic A, Borst AJ, Torres SV, Shu C, Hsia Y, Nattermann U, Ellis D, Walkey C, Ahlrichs M, Chan S, Kang A, Nguyen H, Sydeman C, Sankaran B, Wu M, Bera AK, Carter L, Fiala B, Murphy M, Baker D, Ward AB, King NP. Proc Natl Acad Sci U S A 120 e2214556120 (2023)
  2. Engineered Protein Nanocages for Concurrent RNA and Protein Packaging In Vivo. Kwon S, Giessen TW. ACS Synth Biol 11 3504-3515 (2022)
  3. Multiplex Chemical Labeling of Amino Acids for Protein Footprinting Structure Assessment. Jain R, Dhillon NS, Farquhar ER, Wang B, Li X, Kiselar J, Chance MR. Anal Chem 94 9819-9825 (2022)
  4. Dysregulation of Hepatitis B Virus Nucleocapsid Assembly in vitro by RNA-binding Small Ligands. Patel N, Abulwerdi F, Fatehi F, Manfield IW, Le Grice S, Schneekloth JS, Twarock R, Stockley PG. J Mol Biol 434 167557 (2022)
  5. In vitro functional analysis of gRNA sites regulating assembly of hepatitis B virus. Patel N, Clark S, Weiß EU, Mata CP, Bohon J, Farquhar ER, Maskell DP, Ranson NA, Twarock R, Stockley PG. Commun Biol 4 1407 (2021)
  6. Structures of honeybee-infecting Lake Sinai virus reveal domain functions and capsid assembly with dynamic motions. Chen NC, Wang CH, Yoshimura M, Yeh YQ, Guan HH, Chuankhayan P, Lin CC, Lin PJ, Huang YC, Wakatsuki S, Ho MC, Chen CJ. Nat Commun 14 545 (2023)
  7. Hallmarks of icosahedral virus capsids emerged during laboratory evolution of a bacterial enzyme. Olshefsky A, King NP. Trends Biochem Sci 46 863-865 (2021)
  8. An interaction network approach predicts protein cage architectures in bionanotechnology. Fatehi F, Twarock R. Proc Natl Acad Sci U S A 120 e2303580120 (2023)
  9. In vivo selection of synthetic nucleocapsids for tissue targeting. Olshefsky A, Benasutti H, Sylvestre M, Butterfield GL, Rocklin GJ, Richardson C, Hicks DR, Lajoie MJ, Song K, Leaf E, Treichel C, Decarreau J, Ke S, Kher G, Carter L, Chamberlain JS, Baker D, King NP, Pun SH. Proc Natl Acad Sci U S A 120 e2306129120 (2023)
  10. Intact mass spectrometry screening to optimize hydroxyl radical dose for protein footprinting. Farquhar ER, Vijayalakshmi K, Jain R, Wang B, Kiselar J, Chance MR. Biochem Biophys Res Commun 671 343-349 (2023)


Related citations provided by authors (1)

  1. Evolution of a virus-like architecture and packaging mechanism in a repurposed bacterial protein. Tetter S, Terasaka N, Steinauer A, Bingham RJ, Clark S, Scott AJP, Patel N, Leibundgut M, Wroblewski E, Ban N, Stockley PG, Twarock R, Hilvert D Biorxiv - (2021)

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