AlphaFold-SFA: Accelerated sampling of cryptic pocket opening, protein-ligand binding and allostery by AlphaFold, slow feature analysis and metadynamics

Author:

Vats Shray,Bobrovs Raitis,Söderhjelm Pär,Bhakat SoumendranathORCID

Abstract

Sampling rare events in proteins is crucial for comprehending complex phenomena like cryptic pocket opening, where transient structural changes expose new binding sites. Understanding these rare events also sheds light on protein-ligand binding and allosteric communications, where distant site interactions influence protein function. Traditional unbiased molecular dynamics simulations often fail to sample such rare events, as the free energy barrier between metastable states is large relative to the thermal energy. This renders these events inaccessible on the timescales typically simulated by unbiased molecular dynamics, limiting our understanding of these critical processes. In this paper, we proposed a novel unsupervised learning approach termed as slow feature analysis (SFA) which aims to extract slowly varying features from high-dimensional temporal data. SFA trained on small unbiased molecular dynamics simulations launched from AlphaFold generated conformational ensembles manages to capture rare events governing cryptic pocket opening, protein-ligand binding, and allosteric communications in a kinase. Metadynamics simulations using SFA as collective variables manage to sample ‘deep’ cryptic pocket opening within a few hundreds of nanoseconds which was beyond the reach of microsecond long unbiased molecular dynamics simulations. SFA augmented metadynamics also managed to capture conformational plasticity of protein upon ligand binding/unbinding and provided novel insights into allosteric communication in receptor-interacting protein kinase 2 (RIPK2) which dictates protein-protein interaction. Taken together, our results show how SFA acts as a dimensionality reduction tool which bridges the gap between AlphaFold, molecular dynamics simulation and metadynamics in context of capturing rare events in biomolecules, extending the scope of structure-based drug discovery in the era of AlphaFold.

Publisher

Public Library of Science (PLoS)

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