Differential chromatin accessibility and transcriptional dynamics define breast cancer subtypes and their lineages

Michael D. Iglesia, Reyka G. Jayasinghe, Siqi Chen, Nadezhda V. Terekhanova, John M. Herndon, Erik Storrs, Alla Karpova, Daniel Cui Zhou, Nataly Naser Al Deen, Andrew T. Shinkle, Rita Jui Hsien Lu, Wagma Caravan, Andrew Houston, Yanyan Zhao, Kazuhito Sato, Preet Lal, Cherease Street, Fernanda Martins Rodrigues, Austin N. Southard-Smith, André Luiz N. Targino da CostaHouxiang Zhu, Chia Kuei Mo, Lisa Crowson, Robert S. Fulton, Matthew A. Wyczalkowski, Catrina C. Fronick, Lucinda A. Fulton, Hua Sun, Sherri R. Davies, Elizabeth L. Appelbaum, Sara E. Chasnoff, Madelyn Carmody, Candace Brooks, Ruiyang Liu, Michael C. Wendl, Clara Oh, Diane Bender, Carlos Cruchaga, Oscar Harari, Andrea Bredemeyer, Kory Lavine, Ron Bose, Julie Margenthaler, Jason M. Held, Samuel Achilefu, Foluso Ademuyiwa, Rebecca Aft, Cynthia Ma, Graham A. Colditz, Tao Ju, Stephen T. Oh, James Fitzpatrick, E. Shelley Hwang, Kooresh I. Shoghi, Milan G. Chheda, Deborah J. Veis, Feng Chen, Ryan C. Fields, William E. Gillanders, Li Ding

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Breast cancer (BC) is defined by distinct molecular subtypes with different cells of origin. The transcriptional networks that characterize the subtype-specific tumor-normal lineages are not established. In this work, we applied bulk, single-cell and single-nucleus multi-omic techniques as well as spatial transcriptomics and multiplex imaging on 61 samples from 37 patients with BC to show characteristic links in gene expression and chromatin accessibility between BC subtypes and their putative cells of origin. Regulatory network analysis of transcription factors underscored the importance of BHLHE40 in luminal BC and luminal mature cells and KLF5 in basal-like tumors and luminal progenitor cells. Furthermore, we identify key genes defining the basal-like (SOX6 and KCNQ3) and luminal A/B (FAM155A and LRP1B) lineages. Exhausted CTLA4-expressing CD8+ T cells were enriched in basal-like BC, suggesting an altered means of immune dysfunction. These findings demonstrate analysis of paired transcription and chromatin accessibility at the single-cell level is a powerful tool for investigating cancer lineage and highlight transcriptional networks that define basal and luminal BC lineages.

Original languageEnglish
Pages (from-to)1713-1736
Number of pages24
JournalNature Cancer
Volume5
Issue number11
DOIs
StatePublished - Nov 2024

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