An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein

The mis-folding and aggregation of intrinsically disordered proteins (IDPs) such as α-synuclein (αS) underlie the pathogenesis of various neurodegenerative disorders. However, targeting αS with small molecules faces challenges due to the lack of defined ligand-binding pockets in its disordered struc...

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Main Authors: Sneha Menon, Subinoy Adhikari, Jagannath Mondal
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-12-01
Series:eLife
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Online Access:https://elifesciences.org/articles/97709
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author Sneha Menon
Subinoy Adhikari
Jagannath Mondal
author_facet Sneha Menon
Subinoy Adhikari
Jagannath Mondal
author_sort Sneha Menon
collection DOAJ
description The mis-folding and aggregation of intrinsically disordered proteins (IDPs) such as α-synuclein (αS) underlie the pathogenesis of various neurodegenerative disorders. However, targeting αS with small molecules faces challenges due to the lack of defined ligand-binding pockets in its disordered structure. Here, we implement a deep artificial neural network-based machine learning approach, which is able to statistically distinguish the fuzzy ensemble of conformational substates of αS in neat water from those in aqueous fasudil (small molecule of interest) solution. In particular, the presence of fasudil in the solvent either modulates pre-existing states of αS or gives rise to new conformational states of αS, akin to an ensemble-expansion mechanism. The ensembles display strong conformation-dependence in residue-wise interaction with the small molecule. A thermodynamic analysis indicates that small-molecule modulates the structural repertoire of αS by tuning protein backbone entropy, however entropy of the water remains unperturbed. Together, this study sheds light on the intricate interplay between small molecules and IDPs, offering insights into entropic modulation and ensemble expansion as key biophysical mechanisms driving potential therapeutics.
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spelling doaj-art-3fdc90b371e34eb682e9f28a9d083d882025-08-20T01:58:05ZengeLife Sciences Publications LtdeLife2050-084X2024-12-011310.7554/eLife.97709An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synucleinSneha Menon0https://orcid.org/0000-0003-1079-8928Subinoy Adhikari1Jagannath Mondal2https://orcid.org/0000-0003-1090-5199Tata Institute of Fundamental Research, Hyderabad, IndiaTata Institute of Fundamental Research, Hyderabad, IndiaTata Institute of Fundamental Research, Hyderabad, IndiaThe mis-folding and aggregation of intrinsically disordered proteins (IDPs) such as α-synuclein (αS) underlie the pathogenesis of various neurodegenerative disorders. However, targeting αS with small molecules faces challenges due to the lack of defined ligand-binding pockets in its disordered structure. Here, we implement a deep artificial neural network-based machine learning approach, which is able to statistically distinguish the fuzzy ensemble of conformational substates of αS in neat water from those in aqueous fasudil (small molecule of interest) solution. In particular, the presence of fasudil in the solvent either modulates pre-existing states of αS or gives rise to new conformational states of αS, akin to an ensemble-expansion mechanism. The ensembles display strong conformation-dependence in residue-wise interaction with the small molecule. A thermodynamic analysis indicates that small-molecule modulates the structural repertoire of αS by tuning protein backbone entropy, however entropy of the water remains unperturbed. Together, this study sheds light on the intricate interplay between small molecules and IDPs, offering insights into entropic modulation and ensemble expansion as key biophysical mechanisms driving potential therapeutics.https://elifesciences.org/articles/97709alpha synucleinsmall moleculemachine learning
spellingShingle Sneha Menon
Subinoy Adhikari
Jagannath Mondal
An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
eLife
alpha synuclein
small molecule
machine learning
title An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
title_full An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
title_fullStr An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
title_full_unstemmed An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
title_short An integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α-synuclein
title_sort integrated machine learning approach delineates an entropic expansion mechanism for the binding of a small molecule to α synuclein
topic alpha synuclein
small molecule
machine learning
url https://elifesciences.org/articles/97709
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