Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles

Abstract Hydrogen bond cooperativity (HBC) is the phenomenon where the collective strengthening of hydrogen bonds, by mutual polarization and non-additive electrostatic effects, in a network exceeds the sum of individual interactions. HBC has been well-studied in α-helices and β-sheets, where it cri...

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Main Authors: Rubén López-Sánchez, Miguel Mompeán, Douglas V. Laurents
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Communications Chemistry
Online Access:https://doi.org/10.1038/s42004-025-01576-1
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author Rubén López-Sánchez
Miguel Mompeán
Douglas V. Laurents
author_facet Rubén López-Sánchez
Miguel Mompeán
Douglas V. Laurents
author_sort Rubén López-Sánchez
collection DOAJ
description Abstract Hydrogen bond cooperativity (HBC) is the phenomenon where the collective strengthening of hydrogen bonds, by mutual polarization and non-additive electrostatic effects, in a network exceeds the sum of individual interactions. HBC has been well-studied in α-helices and β-sheets, where it critically stabilizes amyloid structures. During the last 20 years, several natural proteins were characterized which contain multiple aligned and hydrogen-bonded polyproline II (PPII) helices. HBC was recently reported for these PPII helices when arranged along one parallel layer, but its existence in the more abundant antiparallel or mixed parallel/antiparallel PPII assemblies is still unknown. Utilizing computational approaches validated through experimental observables, we report that both canonical CO···HN and non-canonical CO···HαCα hydrogen bonds exhibit mutual reinforcement, revealing a complex hydrogen bonding scheme that manifests HBC in antiparallel PPII helices and in mixed parallel/antiparallel orientations. These findings have fundamental relevance for understanding protein conformational stability and implications for PPII helices as a structural building block for protein design.
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spelling doaj-art-d203f0c9645e457296556831a0fa7cbf2025-08-20T03:03:27ZengNature PortfolioCommunications Chemistry2399-36692025-07-018111610.1038/s42004-025-01576-1Orientation affects hydrogen bonding cooperativity in polyproline II helical bundlesRubén López-Sánchez0Miguel Mompeán1Douglas V. Laurents2Instituto de Química Física “Blas Cabrera” - CSICInstituto de Química Física “Blas Cabrera” - CSICInstituto de Química Física “Blas Cabrera” - CSICAbstract Hydrogen bond cooperativity (HBC) is the phenomenon where the collective strengthening of hydrogen bonds, by mutual polarization and non-additive electrostatic effects, in a network exceeds the sum of individual interactions. HBC has been well-studied in α-helices and β-sheets, where it critically stabilizes amyloid structures. During the last 20 years, several natural proteins were characterized which contain multiple aligned and hydrogen-bonded polyproline II (PPII) helices. HBC was recently reported for these PPII helices when arranged along one parallel layer, but its existence in the more abundant antiparallel or mixed parallel/antiparallel PPII assemblies is still unknown. Utilizing computational approaches validated through experimental observables, we report that both canonical CO···HN and non-canonical CO···HαCα hydrogen bonds exhibit mutual reinforcement, revealing a complex hydrogen bonding scheme that manifests HBC in antiparallel PPII helices and in mixed parallel/antiparallel orientations. These findings have fundamental relevance for understanding protein conformational stability and implications for PPII helices as a structural building block for protein design.https://doi.org/10.1038/s42004-025-01576-1
spellingShingle Rubén López-Sánchez
Miguel Mompeán
Douglas V. Laurents
Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
Communications Chemistry
title Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
title_full Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
title_fullStr Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
title_full_unstemmed Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
title_short Orientation affects hydrogen bonding cooperativity in polyproline II helical bundles
title_sort orientation affects hydrogen bonding cooperativity in polyproline ii helical bundles
url https://doi.org/10.1038/s42004-025-01576-1
work_keys_str_mv AT rubenlopezsanchez orientationaffectshydrogenbondingcooperativityinpolyprolineiihelicalbundles
AT miguelmompean orientationaffectshydrogenbondingcooperativityinpolyprolineiihelicalbundles
AT douglasvlaurents orientationaffectshydrogenbondingcooperativityinpolyprolineiihelicalbundles