Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements

Abstract The RAS/ERK pathway plays a central role in diagnosis and therapy for many cancers. ERK activity is highly dynamic within individual cells and drives cell proliferation, metabolism, and other processes through effector proteins including c-Myc, c-Fos, Fra-1, and Egr-1. These proteins are se...

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Main Authors: Abhineet Ram, Michael Pargett, Yongin Choi, Devan Murphy, Carolyn Teragawa, Markhus Cabel, Nont Kosaisawe, Gerald Quon, John G. Albeck
Format: Article
Language:English
Published: Nature Portfolio 2025-05-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-58348-7
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author Abhineet Ram
Michael Pargett
Yongin Choi
Devan Murphy
Carolyn Teragawa
Markhus Cabel
Nont Kosaisawe
Gerald Quon
John G. Albeck
author_facet Abhineet Ram
Michael Pargett
Yongin Choi
Devan Murphy
Carolyn Teragawa
Markhus Cabel
Nont Kosaisawe
Gerald Quon
John G. Albeck
author_sort Abhineet Ram
collection DOAJ
description Abstract The RAS/ERK pathway plays a central role in diagnosis and therapy for many cancers. ERK activity is highly dynamic within individual cells and drives cell proliferation, metabolism, and other processes through effector proteins including c-Myc, c-Fos, Fra-1, and Egr-1. These proteins are sensitive to the dynamics of ERK activity, but it is not clear to what extent the pattern of ERK activity in an individual cell determines effector protein expression, or how much information about ERK dynamics is embedded in the pattern of effector expression. Here, we evaluate these relationships using live-cell biosensor measurements of ERK activity, multiplexed with immunofluorescence staining for downstream target proteins of the pathway. Combining these datasets with linear regression, machine learning, and differential equation models, we develop an interpretive framework for immunofluorescence data, wherein Fra-1 and pRb levels imply long-term activation of ERK signaling, while Egr-1 and c-Myc indicate more recent activation. Analysis of multiple cancer cell lines reveals a distorted relationship between ERK activity and cell state in malignant cells. We show that this framework can infer various classes of ERK dynamics from effector protein stains within a heterogeneous population, providing a basis for annotating ERK dynamics within fixed cells.
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spelling doaj-art-b0b8f739d72f4e5694ff89b5639c51702025-08-20T01:53:14ZengNature PortfolioNature Communications2041-17232025-05-0116111810.1038/s41467-025-58348-7Deciphering the history of ERK activity from fixed-cell immunofluorescence measurementsAbhineet Ram0Michael Pargett1Yongin Choi2Devan Murphy3Carolyn Teragawa4Markhus Cabel5Nont Kosaisawe6Gerald Quon7John G. Albeck8Department of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaDepartment of Molecular and Cellular Biology, University of CaliforniaAbstract The RAS/ERK pathway plays a central role in diagnosis and therapy for many cancers. ERK activity is highly dynamic within individual cells and drives cell proliferation, metabolism, and other processes through effector proteins including c-Myc, c-Fos, Fra-1, and Egr-1. These proteins are sensitive to the dynamics of ERK activity, but it is not clear to what extent the pattern of ERK activity in an individual cell determines effector protein expression, or how much information about ERK dynamics is embedded in the pattern of effector expression. Here, we evaluate these relationships using live-cell biosensor measurements of ERK activity, multiplexed with immunofluorescence staining for downstream target proteins of the pathway. Combining these datasets with linear regression, machine learning, and differential equation models, we develop an interpretive framework for immunofluorescence data, wherein Fra-1 and pRb levels imply long-term activation of ERK signaling, while Egr-1 and c-Myc indicate more recent activation. Analysis of multiple cancer cell lines reveals a distorted relationship between ERK activity and cell state in malignant cells. We show that this framework can infer various classes of ERK dynamics from effector protein stains within a heterogeneous population, providing a basis for annotating ERK dynamics within fixed cells.https://doi.org/10.1038/s41467-025-58348-7
spellingShingle Abhineet Ram
Michael Pargett
Yongin Choi
Devan Murphy
Carolyn Teragawa
Markhus Cabel
Nont Kosaisawe
Gerald Quon
John G. Albeck
Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
Nature Communications
title Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
title_full Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
title_fullStr Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
title_full_unstemmed Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
title_short Deciphering the history of ERK activity from fixed-cell immunofluorescence measurements
title_sort deciphering the history of erk activity from fixed cell immunofluorescence measurements
url https://doi.org/10.1038/s41467-025-58348-7
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