Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors

Target-based screening of covalent fragment libraries with mass spectrometry has emerged as a powerful strategy to identify chemical starting points for small molecule inhibitors or find new binding pockets on proteins of interest. These libraries span diverse chemical space with a modest number of...

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Main Authors: Scott B. Ficarro, Zachary H. Marto, Nicholas M. Girardi, Dingyu Deng, Isabella Jaen Maisonet, Guillaume Adelmant, Laura E. Fleming, Mona Sharafi, Isidoro Tavares, Andrew Zhao, HyoJeon Kim, Hyuk-Soo Seo, Sirano Dhe-Paganon, Sara J. Buhrlage, Jarrod A. Marto
Format: Article
Language:English
Published: Elsevier 2024-12-01
Series:SLAS Discovery
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Online Access:http://www.sciencedirect.com/science/article/pii/S2472555224000601
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author Scott B. Ficarro
Zachary H. Marto
Nicholas M. Girardi
Dingyu Deng
Isabella Jaen Maisonet
Guillaume Adelmant
Laura E. Fleming
Mona Sharafi
Isidoro Tavares
Andrew Zhao
HyoJeon Kim
Hyuk-Soo Seo
Sirano Dhe-Paganon
Sara J. Buhrlage
Jarrod A. Marto
author_facet Scott B. Ficarro
Zachary H. Marto
Nicholas M. Girardi
Dingyu Deng
Isabella Jaen Maisonet
Guillaume Adelmant
Laura E. Fleming
Mona Sharafi
Isidoro Tavares
Andrew Zhao
HyoJeon Kim
Hyuk-Soo Seo
Sirano Dhe-Paganon
Sara J. Buhrlage
Jarrod A. Marto
author_sort Scott B. Ficarro
collection DOAJ
description Target-based screening of covalent fragment libraries with mass spectrometry has emerged as a powerful strategy to identify chemical starting points for small molecule inhibitors or find new binding pockets on proteins of interest. These libraries span diverse chemical space with a modest number of compounds. Screening covalent fragments against purified protein targets reduces the demands on the mass spectrometer with respect to absolute throughput, detection limit, and dynamic range. Given these relaxed analytical requirements, we sought to develop an open-source, medium-throughput mass spectrometry system for target-based covalent fragment screening. Our platform comprises automated, dual LC desalting columns integrated with electrospray ionization for rapid sample introduction and mass spectrometry detection. The system is operated through a simple Python graphical user interface running on commodity microcontroller boards which allow integration with diverse liquid chromatography and mass spectrometry instruments. We provide scripts for fragment pooling, construction of sample batches, along with routines for data processing and visualization. The system enables primary screening of ∼10,000 covalent fragments per day in pooled format. In a proof-of-concept study we executed primary and secondary screens to identify 27 hit fragments against UCHL1, a deubiquitinating enzyme that is emerging as a drug target of interest across multiple clinical indications. We validated and triaged these covalent compounds through a series of orthogonal biochemical and chemoproteomic assays. The most promising chloroacetamide covalent fragment inhibited UCHL1 activity in vitro (IC50 < 5 µM) and exhibited dose-dependent binding along with good selectivity against 57 cellular DUBs as quantified by activity-based protein profiling.
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spelling doaj-art-4332138746db43fda20fad84946e548d2025-08-20T01:58:27ZengElsevierSLAS Discovery2472-55522024-12-0129810019810.1016/j.slasd.2024.100198Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitorsScott B. Ficarro0Zachary H. Marto1Nicholas M. Girardi2Dingyu Deng3Isabella Jaen Maisonet4Guillaume Adelmant5Laura E. Fleming6Mona Sharafi7Isidoro Tavares8Andrew Zhao9HyoJeon Kim10Hyuk-Soo Seo11Sirano Dhe-Paganon12Sara J. Buhrlage13Jarrod A. Marto14Department of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USA; Center for Emergent Drug Targets, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USA; Center for Emergent Drug Targets, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Biological Chemistry and Molecular Pharmacology, Harvard Medical School, Boston, MA, USA; Center for Emergent Drug Targets, Dana-Farber Cancer Institute, Boston, MA, USADepartment of Cancer Biology and the Linde Program in Cancer Chemical Biology, Dana-Farber Cancer Institute, Boston, MA, USA; Blais Proteomics Center, Dana-Farber Cancer Institute, Boston, MA, USA; Center for Emergent Drug Targets, Dana-Farber Cancer Institute, Boston, MA, USA; Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA; Corresponding author at: Department of Cancer Biology, Dana-Farber Cancer Institute, 360 Longwood Avenue, LC 2205, Boston, MA 02215-5450, USA.Target-based screening of covalent fragment libraries with mass spectrometry has emerged as a powerful strategy to identify chemical starting points for small molecule inhibitors or find new binding pockets on proteins of interest. These libraries span diverse chemical space with a modest number of compounds. Screening covalent fragments against purified protein targets reduces the demands on the mass spectrometer with respect to absolute throughput, detection limit, and dynamic range. Given these relaxed analytical requirements, we sought to develop an open-source, medium-throughput mass spectrometry system for target-based covalent fragment screening. Our platform comprises automated, dual LC desalting columns integrated with electrospray ionization for rapid sample introduction and mass spectrometry detection. The system is operated through a simple Python graphical user interface running on commodity microcontroller boards which allow integration with diverse liquid chromatography and mass spectrometry instruments. We provide scripts for fragment pooling, construction of sample batches, along with routines for data processing and visualization. The system enables primary screening of ∼10,000 covalent fragments per day in pooled format. In a proof-of-concept study we executed primary and secondary screens to identify 27 hit fragments against UCHL1, a deubiquitinating enzyme that is emerging as a drug target of interest across multiple clinical indications. We validated and triaged these covalent compounds through a series of orthogonal biochemical and chemoproteomic assays. The most promising chloroacetamide covalent fragment inhibited UCHL1 activity in vitro (IC50 < 5 µM) and exhibited dose-dependent binding along with good selectivity against 57 cellular DUBs as quantified by activity-based protein profiling.http://www.sciencedirect.com/science/article/pii/S2472555224000601Deubiquitinating enzymesUCHL1Open-source hardware and softwareCovalent fragment screeningElectrophilic fragmentsIntact protein LC–MS screening
spellingShingle Scott B. Ficarro
Zachary H. Marto
Nicholas M. Girardi
Dingyu Deng
Isabella Jaen Maisonet
Guillaume Adelmant
Laura E. Fleming
Mona Sharafi
Isidoro Tavares
Andrew Zhao
HyoJeon Kim
Hyuk-Soo Seo
Sirano Dhe-Paganon
Sara J. Buhrlage
Jarrod A. Marto
Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
SLAS Discovery
Deubiquitinating enzymes
UCHL1
Open-source hardware and software
Covalent fragment screening
Electrophilic fragments
Intact protein LC–MS screening
title Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
title_full Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
title_fullStr Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
title_full_unstemmed Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
title_short Open-source electrophilic fragment screening platform to identify chemical starting points for UCHL1 covalent inhibitors
title_sort open source electrophilic fragment screening platform to identify chemical starting points for uchl1 covalent inhibitors
topic Deubiquitinating enzymes
UCHL1
Open-source hardware and software
Covalent fragment screening
Electrophilic fragments
Intact protein LC–MS screening
url http://www.sciencedirect.com/science/article/pii/S2472555224000601
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