Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer

Abstract Identifying molecular drivers in triple-negative breast cancer (TNBC) is crucial. While HER2-low expression predicts response to novel antibody-drug conjugates, its biological influence on TNBC biology is unknown. We performed a comprehensive multi-omics analysis, integrating genomic, epige...

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Main Authors: Andrés F. Bedoya-López, Sookyung Ahn, Miquel Ensenyat-Mendez, Javier I. J. Orozco, Sandra Iñiguez-Muñoz, Pere Llinàs-Arias, Samantha M. Thomas, Jennifer L. Baker, Peggy S. Sullivan, Jitin Makker, Julie B. Steele, Sunil M. Kurian, Diego M. Marzese, Maggie L. DiNome
Format: Article
Language:English
Published: Nature Portfolio 2025-08-01
Series:npj Precision Oncology
Online Access:https://doi.org/10.1038/s41698-025-01023-3
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author Andrés F. Bedoya-López
Sookyung Ahn
Miquel Ensenyat-Mendez
Javier I. J. Orozco
Sandra Iñiguez-Muñoz
Pere Llinàs-Arias
Samantha M. Thomas
Jennifer L. Baker
Peggy S. Sullivan
Jitin Makker
Julie B. Steele
Sunil M. Kurian
Diego M. Marzese
Maggie L. DiNome
author_facet Andrés F. Bedoya-López
Sookyung Ahn
Miquel Ensenyat-Mendez
Javier I. J. Orozco
Sandra Iñiguez-Muñoz
Pere Llinàs-Arias
Samantha M. Thomas
Jennifer L. Baker
Peggy S. Sullivan
Jitin Makker
Julie B. Steele
Sunil M. Kurian
Diego M. Marzese
Maggie L. DiNome
author_sort Andrés F. Bedoya-López
collection DOAJ
description Abstract Identifying molecular drivers in triple-negative breast cancer (TNBC) is crucial. While HER2-low expression predicts response to novel antibody-drug conjugates, its biological influence on TNBC biology is unknown. We performed a comprehensive multi-omics analysis, integrating genomic, epigenomic, transcriptomic, and proteomic profiling to characterize HER2-low TNBC. We generated genome-wide DNA methylation profiles from a multi-institutional cohort and integrated our data with three independent cohorts (TCGA, SCAN-B, I-SPY2). TNBC cases were categorized as HER2-zero (IHC 0) or HER2-low TNBC (IHC 1+/2+, ISH non-amplified). Among 506 patients (HER2-low, n = 288; HER2-zero, n = 218), HER2-low TNBC exhibited significantly lower tumor mutational burden (P = 0.02). Epigenetic analysis identified 5287 differentially methylated sites, with consistent hypermethylation of HLA genes in HER2-low tumors. Transcriptomic analyses revealed significant downregulation of genes enriched in immune response pathways (e.g., leukocyte activation, T-cell signaling) in HER2-low TNBC (adjusted P < 0.001). Immune cell deconvolution showed reduced immune cell infiltration in the HER2-low tumor microenvironment (P = 0.002). Higher expression of five immune-related genes, downregulated in HER2-low, correlated with improved relapse-free (HR = 0.52; P < 0.001) and overall survival (HR = 0.36; P < 0.001). HER2-low TNBC tumors display distinct molecular features compared to HER2-zero, imparting an immune-evasive phenotype. These findings provide critical insights into the unique biology of HER2-low TNBC, warranting further clinical investigation.
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spelling doaj-art-40d6e8a2add1475b8000e46b73a35d242025-08-20T03:07:20ZengNature Portfolionpj Precision Oncology2397-768X2025-08-019111210.1038/s41698-025-01023-3Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancerAndrés F. Bedoya-López0Sookyung Ahn1Miquel Ensenyat-Mendez2Javier I. J. Orozco3Sandra Iñiguez-Muñoz4Pere Llinàs-Arias5Samantha M. Thomas6Jennifer L. Baker7Peggy S. Sullivan8Jitin Makker9Julie B. Steele10Sunil M. Kurian11Diego M. Marzese12Maggie L. DiNome13Cancer Epigenetics Laboratory, Health Research Institute of the Balearic Islands (IdISBa)Department of Surgery, Duke University School of MedicineDepartment of Surgery, Duke University School of MedicineSaint John’s Cancer Institute, Providence Saint John’s Health CenterCancer Epigenetics Laboratory, Health Research Institute of the Balearic Islands (IdISBa)Cancer Epigenetics Laboratory, Health Research Institute of the Balearic Islands (IdISBa)Department of Biostatistics & Bioinformatics, Duke University School of MedicineDepartment of Surgery, University of California Los AngelesDepartment of Pathology and Laboratory Medicine, University of California Los AngelesDepartment of Pathology and Laboratory Medicine, University of California Los AngelesDepartment of Pathology and Laboratory Medicine, Scripps Clinic Medical GroupScripps Clinic Biorepository and BioinformaticsCancer Epigenetics Laboratory, Health Research Institute of the Balearic Islands (IdISBa)Department of Surgery, Duke University School of MedicineAbstract Identifying molecular drivers in triple-negative breast cancer (TNBC) is crucial. While HER2-low expression predicts response to novel antibody-drug conjugates, its biological influence on TNBC biology is unknown. We performed a comprehensive multi-omics analysis, integrating genomic, epigenomic, transcriptomic, and proteomic profiling to characterize HER2-low TNBC. We generated genome-wide DNA methylation profiles from a multi-institutional cohort and integrated our data with three independent cohorts (TCGA, SCAN-B, I-SPY2). TNBC cases were categorized as HER2-zero (IHC 0) or HER2-low TNBC (IHC 1+/2+, ISH non-amplified). Among 506 patients (HER2-low, n = 288; HER2-zero, n = 218), HER2-low TNBC exhibited significantly lower tumor mutational burden (P = 0.02). Epigenetic analysis identified 5287 differentially methylated sites, with consistent hypermethylation of HLA genes in HER2-low tumors. Transcriptomic analyses revealed significant downregulation of genes enriched in immune response pathways (e.g., leukocyte activation, T-cell signaling) in HER2-low TNBC (adjusted P < 0.001). Immune cell deconvolution showed reduced immune cell infiltration in the HER2-low tumor microenvironment (P = 0.002). Higher expression of five immune-related genes, downregulated in HER2-low, correlated with improved relapse-free (HR = 0.52; P < 0.001) and overall survival (HR = 0.36; P < 0.001). HER2-low TNBC tumors display distinct molecular features compared to HER2-zero, imparting an immune-evasive phenotype. These findings provide critical insights into the unique biology of HER2-low TNBC, warranting further clinical investigation.https://doi.org/10.1038/s41698-025-01023-3
spellingShingle Andrés F. Bedoya-López
Sookyung Ahn
Miquel Ensenyat-Mendez
Javier I. J. Orozco
Sandra Iñiguez-Muñoz
Pere Llinàs-Arias
Samantha M. Thomas
Jennifer L. Baker
Peggy S. Sullivan
Jitin Makker
Julie B. Steele
Sunil M. Kurian
Diego M. Marzese
Maggie L. DiNome
Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
npj Precision Oncology
title Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
title_full Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
title_fullStr Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
title_full_unstemmed Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
title_short Epigenetic determinants of an immune-evasive phenotype in HER2-low triple-negative breast cancer
title_sort epigenetic determinants of an immune evasive phenotype in her2 low triple negative breast cancer
url https://doi.org/10.1038/s41698-025-01023-3
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