Chemoproteogenomic stratification of the missense variant cysteinome

Abstract Cancer genomes are rife with genetic variants; one key outcome of this variation is widespread gain-of-cysteine mutations. These acquired cysteines can be both driver mutations and sites targeted by precision therapies. However, despite their ubiquity, nearly all acquired cysteines remain u...

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Main Authors: Heta Desai, Katrina H. Andrews, Kristina V. Bergersen, Samuel Ofori, Fengchao Yu, Flowreen Shikwana, Mark A. Arbing, Lisa M. Boatner, Miranda Villanueva, Nicholas Ung, Elaine F. Reed, Alexey I. Nesvizhskii, Keriann M. Backus
Format: Article
Language:English
Published: Nature Portfolio 2024-10-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-53520-x
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author Heta Desai
Katrina H. Andrews
Kristina V. Bergersen
Samuel Ofori
Fengchao Yu
Flowreen Shikwana
Mark A. Arbing
Lisa M. Boatner
Miranda Villanueva
Nicholas Ung
Elaine F. Reed
Alexey I. Nesvizhskii
Keriann M. Backus
author_facet Heta Desai
Katrina H. Andrews
Kristina V. Bergersen
Samuel Ofori
Fengchao Yu
Flowreen Shikwana
Mark A. Arbing
Lisa M. Boatner
Miranda Villanueva
Nicholas Ung
Elaine F. Reed
Alexey I. Nesvizhskii
Keriann M. Backus
author_sort Heta Desai
collection DOAJ
description Abstract Cancer genomes are rife with genetic variants; one key outcome of this variation is widespread gain-of-cysteine mutations. These acquired cysteines can be both driver mutations and sites targeted by precision therapies. However, despite their ubiquity, nearly all acquired cysteines remain unidentified via chemoproteomics; identification is a critical step to enable functional analysis, including assessment of potential druggability and susceptibility to oxidation. Here, we pair cysteine chemoproteomics—a technique that enables proteome-wide pinpointing of functional, redox sensitive, and potentially druggable residues—with genomics to reveal the hidden landscape of cysteine genetic variation. Our chemoproteogenomics platform integrates chemoproteomic, whole exome, and RNA-seq data, with a customized two-stage false discovery rate (FDR) error controlled proteomic search, which is further enhanced with a user-friendly FragPipe interface. Chemoproteogenomics analysis reveals that cysteine acquisition is a ubiquitous feature of both healthy and cancer genomes that is further elevated in the context of decreased DNA repair. Reference cysteines proximal to missense variants are also found to be pervasive, supporting heretofore untapped opportunities for variant-specific chemical probe development campaigns. As chemoproteogenomics is further distinguished by sample-matched combinatorial variant databases and is compatible with redox proteomics and small molecule screening, we expect widespread utility in guiding proteoform-specific biology and therapeutic discovery.
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spelling doaj-art-8497dd94edd44189a1d7fe0683afc5b42025-08-20T02:18:35ZengNature PortfolioNature Communications2041-17232024-10-0115112410.1038/s41467-024-53520-xChemoproteogenomic stratification of the missense variant cysteinomeHeta Desai0Katrina H. Andrews1Kristina V. Bergersen2Samuel Ofori3Fengchao Yu4Flowreen Shikwana5Mark A. Arbing6Lisa M. Boatner7Miranda Villanueva8Nicholas Ung9Elaine F. Reed10Alexey I. Nesvizhskii11Keriann M. Backus12Biological Chemistry Department, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLADepartment of Pathology and Laboratory Medicine, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLADepartment of Pathology, University of MichiganBiological Chemistry Department, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLABiological Chemistry Department, David Geffen School of Medicine, UCLADepartment of Pathology and Laboratory Medicine, David Geffen School of Medicine, UCLADepartment of Pathology, University of MichiganBiological Chemistry Department, David Geffen School of Medicine, UCLAAbstract Cancer genomes are rife with genetic variants; one key outcome of this variation is widespread gain-of-cysteine mutations. These acquired cysteines can be both driver mutations and sites targeted by precision therapies. However, despite their ubiquity, nearly all acquired cysteines remain unidentified via chemoproteomics; identification is a critical step to enable functional analysis, including assessment of potential druggability and susceptibility to oxidation. Here, we pair cysteine chemoproteomics—a technique that enables proteome-wide pinpointing of functional, redox sensitive, and potentially druggable residues—with genomics to reveal the hidden landscape of cysteine genetic variation. Our chemoproteogenomics platform integrates chemoproteomic, whole exome, and RNA-seq data, with a customized two-stage false discovery rate (FDR) error controlled proteomic search, which is further enhanced with a user-friendly FragPipe interface. Chemoproteogenomics analysis reveals that cysteine acquisition is a ubiquitous feature of both healthy and cancer genomes that is further elevated in the context of decreased DNA repair. Reference cysteines proximal to missense variants are also found to be pervasive, supporting heretofore untapped opportunities for variant-specific chemical probe development campaigns. As chemoproteogenomics is further distinguished by sample-matched combinatorial variant databases and is compatible with redox proteomics and small molecule screening, we expect widespread utility in guiding proteoform-specific biology and therapeutic discovery.https://doi.org/10.1038/s41467-024-53520-x
spellingShingle Heta Desai
Katrina H. Andrews
Kristina V. Bergersen
Samuel Ofori
Fengchao Yu
Flowreen Shikwana
Mark A. Arbing
Lisa M. Boatner
Miranda Villanueva
Nicholas Ung
Elaine F. Reed
Alexey I. Nesvizhskii
Keriann M. Backus
Chemoproteogenomic stratification of the missense variant cysteinome
Nature Communications
title Chemoproteogenomic stratification of the missense variant cysteinome
title_full Chemoproteogenomic stratification of the missense variant cysteinome
title_fullStr Chemoproteogenomic stratification of the missense variant cysteinome
title_full_unstemmed Chemoproteogenomic stratification of the missense variant cysteinome
title_short Chemoproteogenomic stratification of the missense variant cysteinome
title_sort chemoproteogenomic stratification of the missense variant cysteinome
url https://doi.org/10.1038/s41467-024-53520-x
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