Elucidating the role of water in collagen self-assembly by isotopically modulating collagen hydration.
collagen tissue
hydration
mechanics
molecular structure
Journal
Proceedings of the National Academy of Sciences of the United States of America
ISSN: 1091-6490
Titre abrégé: Proc Natl Acad Sci U S A
Pays: United States
ID NLM: 7505876
Informations de publication
Date de publication:
12 Mar 2024
12 Mar 2024
Historique:
medline:
11
3
2024
pubmed:
7
3
2024
entrez:
7
3
2024
Statut:
ppublish
Résumé
Water is known to play an important role in collagen self-assembly, but it is still largely unclear how water-collagen interactions influence the assembly process and determine the fibril network properties. Here, we use the H[Formula: see text]O/D[Formula: see text]O isotope effect on the hydrogen-bond strength in water to investigate the role of hydration in collagen self-assembly. We dissolve collagen in H[Formula: see text]O and D[Formula: see text]O and compare the growth kinetics and the structure of the collagen assemblies formed in these water isotopomers. Surprisingly, collagen assembly occurs ten times faster in D[Formula: see text]O than in H[Formula: see text]O, and collagen in D[Formula: see text]O self-assembles into much thinner fibrils, that form a more inhomogeneous and softer network, with a fourfold reduction in elastic modulus when compared to H[Formula: see text]O. Combining spectroscopic measurements with atomistic simulations, we show that collagen in D[Formula: see text]O is less hydrated than in H[Formula: see text]O. This partial dehydration lowers the enthalpic penalty for water removal and reorganization at the collagen-water interface, increasing the self-assembly rate and the number of nucleation centers, leading to thinner fibrils and a softer network. Coarse-grained simulations show that the acceleration in the initial nucleation rate can be reproduced by the enhancement of electrostatic interactions. These results show that water acts as a mediator between collagen monomers, by modulating their interactions so as to optimize the assembly process and, thus, the final network properties. We believe that isotopically modulating the hydration of proteins can be a valuable method to investigate the role of water in protein structural dynamics and protein self-assembly.
Identifiants
pubmed: 38451946
doi: 10.1073/pnas.2313162121
doi:
Substances chimiques
Water
059QF0KO0R
Collagen
9007-34-5
Hydrogen
7YNJ3PO35Z
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e2313162121Subventions
Organisme : Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)
ID : V1.Veni.212.240
Organisme : Ministerie van Onderwijs, Cultuur en Wetenschap (OCW)
ID : 024.003.019
Organisme : Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO)
ID : OCENW.GROOT.2019.022
Déclaration de conflit d'intérêts
Competing interests statement:The authors declare no competing interest.
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