Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics

Abstract With the growth of clinical cancer single-cell RNA sequencing studies, robust differential expression methods for case/control analyses (e.g., treatment responders vs. non-responders) using gene signatures are pivotal to nominate hypotheses for further investigation. However, many commonly...

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Main Authors: Shreya Johri, Kevin Bi, Breanna M. Titchen, Jingxin Fu, Jake Conway, Jett P. Crowdis, Natalie I. Vokes, Zenghua Fan, Lawrence Fong, Jihye Park, David Liu, Meng Xiao He, Eliezer M. Van Allen
Format: Article
Language:English
Published: Nature Portfolio 2025-03-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-57377-6
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author Shreya Johri
Kevin Bi
Breanna M. Titchen
Jingxin Fu
Jake Conway
Jett P. Crowdis
Natalie I. Vokes
Zenghua Fan
Lawrence Fong
Jihye Park
David Liu
Meng Xiao He
Eliezer M. Van Allen
author_facet Shreya Johri
Kevin Bi
Breanna M. Titchen
Jingxin Fu
Jake Conway
Jett P. Crowdis
Natalie I. Vokes
Zenghua Fan
Lawrence Fong
Jihye Park
David Liu
Meng Xiao He
Eliezer M. Van Allen
author_sort Shreya Johri
collection DOAJ
description Abstract With the growth of clinical cancer single-cell RNA sequencing studies, robust differential expression methods for case/control analyses (e.g., treatment responders vs. non-responders) using gene signatures are pivotal to nominate hypotheses for further investigation. However, many commonly used methods produce a large number of false positives, do not adequately represent the patient-specific hierarchical structure of clinical single-cell RNA sequencing data, or account for sample-driven confounders. Here, we present a nonparametric statistical method, BEANIE, for differential expression of gene signatures between clinically relevant groups that addresses these issues. We demonstrate its use in simulated and real-world clinical datasets in breast cancer, lung cancer and melanoma. BEANIE outperforms existing methods in specificity while maintaining sensitivity, as demonstrated in simulations. Overall, BEANIE provides a methodological strategy to inform biological insights into unique and shared differentially expressed gene signatures across different tumor states, with utility in single-study, meta-analysis, and cross-validation across cell types.
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spelling doaj-art-a4fc5340e7204c0ca4fa0a239af0f83b2025-08-20T02:59:32ZengNature PortfolioNature Communications2041-17232025-03-0116111410.1038/s41467-025-57377-6Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomicsShreya Johri0Kevin Bi1Breanna M. Titchen2Jingxin Fu3Jake Conway4Jett P. Crowdis5Natalie I. Vokes6Zenghua Fan7Lawrence Fong8Jihye Park9David Liu10Meng Xiao He11Eliezer M. Van Allen12Department of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Thoracic and Head and Neck Oncology, MD Anderson Cancer CenterDivision of Hematology/Oncology, University of CaliforniaDivision of Hematology/Oncology, University of CaliforniaDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteDepartment of Medical Oncology, Dana-Farber Cancer InstituteAbstract With the growth of clinical cancer single-cell RNA sequencing studies, robust differential expression methods for case/control analyses (e.g., treatment responders vs. non-responders) using gene signatures are pivotal to nominate hypotheses for further investigation. However, many commonly used methods produce a large number of false positives, do not adequately represent the patient-specific hierarchical structure of clinical single-cell RNA sequencing data, or account for sample-driven confounders. Here, we present a nonparametric statistical method, BEANIE, for differential expression of gene signatures between clinically relevant groups that addresses these issues. We demonstrate its use in simulated and real-world clinical datasets in breast cancer, lung cancer and melanoma. BEANIE outperforms existing methods in specificity while maintaining sensitivity, as demonstrated in simulations. Overall, BEANIE provides a methodological strategy to inform biological insights into unique and shared differentially expressed gene signatures across different tumor states, with utility in single-study, meta-analysis, and cross-validation across cell types.https://doi.org/10.1038/s41467-025-57377-6
spellingShingle Shreya Johri
Kevin Bi
Breanna M. Titchen
Jingxin Fu
Jake Conway
Jett P. Crowdis
Natalie I. Vokes
Zenghua Fan
Lawrence Fong
Jihye Park
David Liu
Meng Xiao He
Eliezer M. Van Allen
Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
Nature Communications
title Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
title_full Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
title_fullStr Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
title_full_unstemmed Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
title_short Dissecting tumor cell programs through group biology estimation in clinical single-cell transcriptomics
title_sort dissecting tumor cell programs through group biology estimation in clinical single cell transcriptomics
url https://doi.org/10.1038/s41467-025-57377-6
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