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Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins

Dynamic noncovalent interactions are pivotal to the structure and function of biological proteins and have been used in bioinspired materials for similar roles. Metal-coordination bonds, in particular, are especially tunable and enable control over static and dynamic properties when incorporated int...

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Autores principales: Khare, Eesha, Grewal, Darshdeep S., Buehler, Markus J.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: The Royal Society of Chemistry 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194279/
https://www.ncbi.nlm.nih.gov/pubmed/37092811
http://dx.doi.org/10.1039/d3nr01287e
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author Khare, Eesha
Grewal, Darshdeep S.
Buehler, Markus J.
author_facet Khare, Eesha
Grewal, Darshdeep S.
Buehler, Markus J.
author_sort Khare, Eesha
collection PubMed
description Dynamic noncovalent interactions are pivotal to the structure and function of biological proteins and have been used in bioinspired materials for similar roles. Metal-coordination bonds, in particular, are especially tunable and enable control over static and dynamic properties when incorporated into synthetic materials. Despite growing efforts to engineer metal-coordination bonds to produce strong, tough, and self-healing materials, the systematic characterization of the exact contribution of these bonds towards mechanical strength and the effect of geometric arrangements is missing, limiting the full design potential of these bonds. In this work, we engineer the cooperative rupture of metal-coordination bonds to increase the rupture strength of metal-coordinated peptide dimers. Utilizing all-atom steered molecular dynamics simulations on idealized bidentate histidine-Ni(2+) coordinated peptides, we show that histidine-Ni(2+) bonds can rupture cooperatively in groups of two to three bonds. We find that there is a strength limit, where adding additional coordination bonds does not contribute to the additional increase in the protein rupture strength, likely due to the highly heterogeneous rupture behavior exhibited by the coordination bonds. Further, we show that this coordination bond limit is also found natural metal-coordinated biological proteins. Using these insights, we quantitatively suggest how other proteins can be rationally designed with dynamic noncovalent interactions to exhibit cooperative bond breaking behavior. Altogether, this work provides a quantitative analysis of the cooperativity and intrinsic strength limit for metal-coordination bonds with the aim of advancing clear guiding molecular principles for the mechanical design of metal-coordinated materials.
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spelling pubmed-101942792023-05-19 Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins Khare, Eesha Grewal, Darshdeep S. Buehler, Markus J. Nanoscale Chemistry Dynamic noncovalent interactions are pivotal to the structure and function of biological proteins and have been used in bioinspired materials for similar roles. Metal-coordination bonds, in particular, are especially tunable and enable control over static and dynamic properties when incorporated into synthetic materials. Despite growing efforts to engineer metal-coordination bonds to produce strong, tough, and self-healing materials, the systematic characterization of the exact contribution of these bonds towards mechanical strength and the effect of geometric arrangements is missing, limiting the full design potential of these bonds. In this work, we engineer the cooperative rupture of metal-coordination bonds to increase the rupture strength of metal-coordinated peptide dimers. Utilizing all-atom steered molecular dynamics simulations on idealized bidentate histidine-Ni(2+) coordinated peptides, we show that histidine-Ni(2+) bonds can rupture cooperatively in groups of two to three bonds. We find that there is a strength limit, where adding additional coordination bonds does not contribute to the additional increase in the protein rupture strength, likely due to the highly heterogeneous rupture behavior exhibited by the coordination bonds. Further, we show that this coordination bond limit is also found natural metal-coordinated biological proteins. Using these insights, we quantitatively suggest how other proteins can be rationally designed with dynamic noncovalent interactions to exhibit cooperative bond breaking behavior. Altogether, this work provides a quantitative analysis of the cooperativity and intrinsic strength limit for metal-coordination bonds with the aim of advancing clear guiding molecular principles for the mechanical design of metal-coordinated materials. The Royal Society of Chemistry 2023-04-14 /pmc/articles/PMC10194279/ /pubmed/37092811 http://dx.doi.org/10.1039/d3nr01287e Text en This journal is © The Royal Society of Chemistry https://creativecommons.org/licenses/by-nc/3.0/
spellingShingle Chemistry
Khare, Eesha
Grewal, Darshdeep S.
Buehler, Markus J.
Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title_full Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title_fullStr Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title_full_unstemmed Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title_short Bond clusters control rupture force limit in shear loaded histidine-Ni(2+) metal-coordinated proteins
title_sort bond clusters control rupture force limit in shear loaded histidine-ni(2+) metal-coordinated proteins
topic Chemistry
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10194279/
https://www.ncbi.nlm.nih.gov/pubmed/37092811
http://dx.doi.org/10.1039/d3nr01287e
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AT buehlermarkusj bondclusterscontrolruptureforcelimitinshearloadedhistidineni2metalcoordinatedproteins