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Illuminating the Reaction Pathways of Viromimetic Assembly

[Image: see text] The coassembly of well-defined biological nanostructures relies on a delicate balance between attractive and repulsive interactions between biomolecular building blocks. Viral capsids are a prototypical example, where coat proteins exhibit not only self-interactions but also intera...

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Autores principales: Cingil, Hande E., Boz, Emre B., Biondaro, Giovanni, de Vries, Renko, Cohen Stuart, Martien A., Kraft, Daniela J., van der Schoot, Paul, Sprakel, Joris
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Chemical Society 2017
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5388896/
https://www.ncbi.nlm.nih.gov/pubmed/28326772
http://dx.doi.org/10.1021/jacs.7b01401
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author Cingil, Hande E.
Boz, Emre B.
Biondaro, Giovanni
de Vries, Renko
Cohen Stuart, Martien A.
Kraft, Daniela J.
van der Schoot, Paul
Sprakel, Joris
author_facet Cingil, Hande E.
Boz, Emre B.
Biondaro, Giovanni
de Vries, Renko
Cohen Stuart, Martien A.
Kraft, Daniela J.
van der Schoot, Paul
Sprakel, Joris
author_sort Cingil, Hande E.
collection PubMed
description [Image: see text] The coassembly of well-defined biological nanostructures relies on a delicate balance between attractive and repulsive interactions between biomolecular building blocks. Viral capsids are a prototypical example, where coat proteins exhibit not only self-interactions but also interact with the cargo they encapsulate. In nature, the balance between antagonistic and synergistic interactions has evolved to avoid kinetic trapping and polymorphism. To date, it has remained a major challenge to experimentally disentangle the complex kinetic reaction pathways that underlie successful coassembly of biomolecular building blocks in a noninvasive approach with high temporal resolution. Here we show how macromolecular force sensors, acting as a genome proxy, allow us to probe the pathways through which a viromimetic protein forms capsids. We uncover the complex multistage process of capsid assembly, which involves recruitment and complexation, followed by allosteric growth of the proteinaceous coat. Under certain conditions, the single-genome particles condense into capsids containing multiple copies of the template. Finally, we derive a theoretical model that quantitatively describes the kinetics of recruitment and growth. These results shed new light on the origins of the pathway complexity in biomolecular coassembly.
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spelling pubmed-53888962017-04-13 Illuminating the Reaction Pathways of Viromimetic Assembly Cingil, Hande E. Boz, Emre B. Biondaro, Giovanni de Vries, Renko Cohen Stuart, Martien A. Kraft, Daniela J. van der Schoot, Paul Sprakel, Joris J Am Chem Soc [Image: see text] The coassembly of well-defined biological nanostructures relies on a delicate balance between attractive and repulsive interactions between biomolecular building blocks. Viral capsids are a prototypical example, where coat proteins exhibit not only self-interactions but also interact with the cargo they encapsulate. In nature, the balance between antagonistic and synergistic interactions has evolved to avoid kinetic trapping and polymorphism. To date, it has remained a major challenge to experimentally disentangle the complex kinetic reaction pathways that underlie successful coassembly of biomolecular building blocks in a noninvasive approach with high temporal resolution. Here we show how macromolecular force sensors, acting as a genome proxy, allow us to probe the pathways through which a viromimetic protein forms capsids. We uncover the complex multistage process of capsid assembly, which involves recruitment and complexation, followed by allosteric growth of the proteinaceous coat. Under certain conditions, the single-genome particles condense into capsids containing multiple copies of the template. Finally, we derive a theoretical model that quantitatively describes the kinetics of recruitment and growth. These results shed new light on the origins of the pathway complexity in biomolecular coassembly. American Chemical Society 2017-03-22 2017-04-05 /pmc/articles/PMC5388896/ /pubmed/28326772 http://dx.doi.org/10.1021/jacs.7b01401 Text en Copyright © 2017 American Chemical Society This is an open access article published under a Creative Commons Non-Commercial No Derivative Works (CC-BY-NC-ND) Attribution License (http://pubs.acs.org/page/policy/authorchoice_ccbyncnd_termsofuse.html) , which permits copying and redistribution of the article, and creation of adaptations, all for non-commercial purposes.
spellingShingle Cingil, Hande E.
Boz, Emre B.
Biondaro, Giovanni
de Vries, Renko
Cohen Stuart, Martien A.
Kraft, Daniela J.
van der Schoot, Paul
Sprakel, Joris
Illuminating the Reaction Pathways of Viromimetic Assembly
title Illuminating the Reaction Pathways of Viromimetic Assembly
title_full Illuminating the Reaction Pathways of Viromimetic Assembly
title_fullStr Illuminating the Reaction Pathways of Viromimetic Assembly
title_full_unstemmed Illuminating the Reaction Pathways of Viromimetic Assembly
title_short Illuminating the Reaction Pathways of Viromimetic Assembly
title_sort illuminating the reaction pathways of viromimetic assembly
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC5388896/
https://www.ncbi.nlm.nih.gov/pubmed/28326772
http://dx.doi.org/10.1021/jacs.7b01401
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