Charting γ-secretase substrates by explainable AI

Abstract Proteases recognize substrates by decoding sequence information—an essential cellular process elusive when recognition motifs are absent. Here, we unravel this problem for γ-secretase, an intramembrane-cleaving protease associated with Alzheimer’s disease and cancer, by developing Comparati...

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Main Authors: Stephan Breimann, Frits Kamp, Gabriele Basset, Claudia Abou-Ajram, Gökhan Güner, Kanta Yanagida, Masayasu Okochi, Stephan A. Müller, Stefan F. Lichtenthaler, Dieter Langosch, Dmitrij Frishman, Harald Steiner
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60638-z
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Summary:Abstract Proteases recognize substrates by decoding sequence information—an essential cellular process elusive when recognition motifs are absent. Here, we unravel this problem for γ-secretase, an intramembrane-cleaving protease associated with Alzheimer’s disease and cancer, by developing Comparative Physicochemical Profiling (CPP), a sequence-based algorithm for identifying interpretable physicochemical features. We show that CPP deciphers a γ-secretase substrate signature with single-residue resolution, which can explain the conformational transitions observed in substrates upon γ-secretase binding. Using machine learning, we predict the entire human γ-secretase substrate scope, revealing numerous previously unknown substrates. Our approach outperforms state-of-the-art protein language models, improving prediction accuracy from 60% to 90%, and achieves an 88% success rate in experimental validation. Building on these advancements, we identify pathways and diseases not linked before to γ-secretase. Generally, CPP decodes physicochemical signatures—a concept that extends beyond sequence motifs. We anticipate that our approach will be broadly applicable to diverse molecular recognition processes.
ISSN:2041-1723