Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity

Abstract Multi-domain signaling enzymes are often regulated through extensive inter-domain interactions, and disruption of inter-domain interfaces by mutations can lead to aberrant signaling and diseases. For example, the tyrosine phosphatase SHP2 contains two phosphotyrosine recognition domains tha...

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Main Authors: Ziyuan Jiang, Anne E. van Vlimmeren, Deepti Karandur, Alyssa Semmelman, Neel H. Shah
Format: Article
Language:English
Published: Nature Portfolio 2025-07-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-60641-4
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author Ziyuan Jiang
Anne E. van Vlimmeren
Deepti Karandur
Alyssa Semmelman
Neel H. Shah
author_facet Ziyuan Jiang
Anne E. van Vlimmeren
Deepti Karandur
Alyssa Semmelman
Neel H. Shah
author_sort Ziyuan Jiang
collection DOAJ
description Abstract Multi-domain signaling enzymes are often regulated through extensive inter-domain interactions, and disruption of inter-domain interfaces by mutations can lead to aberrant signaling and diseases. For example, the tyrosine phosphatase SHP2 contains two phosphotyrosine recognition domains that auto-inhibit its catalytic domain. SHP2 is canonically activated by binding of these non-catalytic domains to phosphoproteins, which destabilizes its auto-inhibited state, and several mutations at the main auto-inhibitory interface have been shown to hyperactivate SHP2 in cancers and developmental disorders. Hundreds of clinically observed mutations in SHP2 have not been characterized, but their locations suggest alternative modes of dysregulation. Here, we perform deep mutational scanning on full-length SHP2 and the isolated phosphatase domain to dissect mechanisms of dysregulation. Our analysis reveals mechanistically diverse mutational effects and identifies key intra- and inter-domain interactions that contribute to SHP2 activity, dynamics, and regulation. Our datasets also provide insights into the potential pathogenicity of previously uncharacterized clinical variants.
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spelling doaj-art-875bf83656474df59f4e8bbf55df8ac22025-08-20T04:01:35ZengNature PortfolioNature Communications2041-17232025-07-0116111710.1038/s41467-025-60641-4Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicityZiyuan Jiang0Anne E. van Vlimmeren1Deepti Karandur2Alyssa Semmelman3Neel H. Shah4Department of Chemistry, Columbia UniversityDepartment of Chemistry, Columbia UniversityDepartment of Biochemistry, Vanderbilt UniversityDepartment of Chemistry, Columbia UniversityDepartment of Chemistry, Columbia UniversityAbstract Multi-domain signaling enzymes are often regulated through extensive inter-domain interactions, and disruption of inter-domain interfaces by mutations can lead to aberrant signaling and diseases. For example, the tyrosine phosphatase SHP2 contains two phosphotyrosine recognition domains that auto-inhibit its catalytic domain. SHP2 is canonically activated by binding of these non-catalytic domains to phosphoproteins, which destabilizes its auto-inhibited state, and several mutations at the main auto-inhibitory interface have been shown to hyperactivate SHP2 in cancers and developmental disorders. Hundreds of clinically observed mutations in SHP2 have not been characterized, but their locations suggest alternative modes of dysregulation. Here, we perform deep mutational scanning on full-length SHP2 and the isolated phosphatase domain to dissect mechanisms of dysregulation. Our analysis reveals mechanistically diverse mutational effects and identifies key intra- and inter-domain interactions that contribute to SHP2 activity, dynamics, and regulation. Our datasets also provide insights into the potential pathogenicity of previously uncharacterized clinical variants.https://doi.org/10.1038/s41467-025-60641-4
spellingShingle Ziyuan Jiang
Anne E. van Vlimmeren
Deepti Karandur
Alyssa Semmelman
Neel H. Shah
Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
Nature Communications
title Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
title_full Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
title_fullStr Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
title_full_unstemmed Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
title_short Deep mutational scanning of the multi-domain phosphatase SHP2 reveals mechanisms of regulation and pathogenicity
title_sort deep mutational scanning of the multi domain phosphatase shp2 reveals mechanisms of regulation and pathogenicity
url https://doi.org/10.1038/s41467-025-60641-4
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