Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays

In response to an ever-increasing demand of new small molecules therapeutics, numerous chemical and genetic tools have been developed to interrogate compound mechanism of action. Owing to its ability to approximate compound-dependent changes in thermal stability, the proteome-wide thermal shift assa...

Full description

Saved in:
Bibliographic Details
Main Authors: Jonathan G Van Vranken, Jiaming Li, Julian Mintseris, Ting-Yu Wei, Catherine M Sniezek, Meagan Gadzuk-Shea, Steven P Gygi, Devin K Schweppe
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2024-11-01
Series:eLife
Subjects:
Online Access:https://elifesciences.org/articles/95595
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1850195344435970048
author Jonathan G Van Vranken
Jiaming Li
Julian Mintseris
Ting-Yu Wei
Catherine M Sniezek
Meagan Gadzuk-Shea
Steven P Gygi
Devin K Schweppe
author_facet Jonathan G Van Vranken
Jiaming Li
Julian Mintseris
Ting-Yu Wei
Catherine M Sniezek
Meagan Gadzuk-Shea
Steven P Gygi
Devin K Schweppe
author_sort Jonathan G Van Vranken
collection DOAJ
description In response to an ever-increasing demand of new small molecules therapeutics, numerous chemical and genetic tools have been developed to interrogate compound mechanism of action. Owing to its ability to approximate compound-dependent changes in thermal stability, the proteome-wide thermal shift assay has emerged as a powerful tool in this arsenal. The most recent iterations have drastically improved the overall efficiency of these assays, providing an opportunity to screen compounds at a previously unprecedented rate. Taking advantage of this advance, we quantified more than one million thermal stability measurements in response to multiple classes of therapeutic and tool compounds (96 compounds in living cells and 70 compounds in lysates). When interrogating the dataset as a whole, approximately 80% of compounds (with quantifiable targets) caused a significant change in the thermal stability of an annotated target. There was also a wealth of evidence portending off-target engagement despite the extensive use of the compounds in the laboratory and/or clinic. Finally, the combined application of cell- and lysate-based assays, aided in the classification of primary (direct ligand binding) and secondary (indirect) changes in thermal stability. Overall, this study highlights the value of these assays in the drug development process by affording an unbiased and reliable assessment of compound mechanism of action.
format Article
id doaj-art-8bf3b9c5353e41d7be11802c16d7f60c
institution OA Journals
issn 2050-084X
language English
publishDate 2024-11-01
publisher eLife Sciences Publications Ltd
record_format Article
series eLife
spelling doaj-art-8bf3b9c5353e41d7be11802c16d7f60c2025-08-20T02:13:47ZengeLife Sciences Publications LtdeLife2050-084X2024-11-011310.7554/eLife.95595Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assaysJonathan G Van Vranken0https://orcid.org/0000-0002-8931-852XJiaming Li1Julian Mintseris2Ting-Yu Wei3Catherine M Sniezek4Meagan Gadzuk-Shea5Steven P Gygi6https://orcid.org/0000-0001-7626-0034Devin K Schweppe7https://orcid.org/0000-0002-3241-6276Department of Cell Biology, Harvard Medical School, Boston, United StatesDepartment of Cell Biology, Harvard Medical School, Boston, United StatesDepartment of Cell Biology, Harvard Medical School, Boston, United StatesDepartment of Cell Biology, Harvard Medical School, Boston, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesDepartment of Cell Biology, Harvard Medical School, Boston, United StatesDepartment of Genome Sciences, University of Washington, Seattle, United StatesIn response to an ever-increasing demand of new small molecules therapeutics, numerous chemical and genetic tools have been developed to interrogate compound mechanism of action. Owing to its ability to approximate compound-dependent changes in thermal stability, the proteome-wide thermal shift assay has emerged as a powerful tool in this arsenal. The most recent iterations have drastically improved the overall efficiency of these assays, providing an opportunity to screen compounds at a previously unprecedented rate. Taking advantage of this advance, we quantified more than one million thermal stability measurements in response to multiple classes of therapeutic and tool compounds (96 compounds in living cells and 70 compounds in lysates). When interrogating the dataset as a whole, approximately 80% of compounds (with quantifiable targets) caused a significant change in the thermal stability of an annotated target. There was also a wealth of evidence portending off-target engagement despite the extensive use of the compounds in the laboratory and/or clinic. Finally, the combined application of cell- and lysate-based assays, aided in the classification of primary (direct ligand binding) and secondary (indirect) changes in thermal stability. Overall, this study highlights the value of these assays in the drug development process by affording an unbiased and reliable assessment of compound mechanism of action.https://elifesciences.org/articles/95595proteomicsthermal proteome profilinghuman cell lineschemoproteomicskinase inhibitors
spellingShingle Jonathan G Van Vranken
Jiaming Li
Julian Mintseris
Ting-Yu Wei
Catherine M Sniezek
Meagan Gadzuk-Shea
Steven P Gygi
Devin K Schweppe
Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
eLife
proteomics
thermal proteome profiling
human cell lines
chemoproteomics
kinase inhibitors
title Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
title_full Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
title_fullStr Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
title_full_unstemmed Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
title_short Large-scale characterization of drug mechanism of action using proteome-wide thermal shift assays
title_sort large scale characterization of drug mechanism of action using proteome wide thermal shift assays
topic proteomics
thermal proteome profiling
human cell lines
chemoproteomics
kinase inhibitors
url https://elifesciences.org/articles/95595
work_keys_str_mv AT jonathangvanvranken largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT jiamingli largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT julianmintseris largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT tingyuwei largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT catherinemsniezek largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT meagangadzukshea largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT stevenpgygi largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays
AT devinkschweppe largescalecharacterizationofdrugmechanismofactionusingproteomewidethermalshiftassays