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Single-Cell Atlas of the Human Breast Highlights Changes in BRCA Mutation Carriers

NEW YORK – A team led by researchers at the University of Cambridge has assembled a Human Breast Cell Atlas (HBCA), based on single-cell RNA sequencing data, that is providing insights into everything from typical breast cell dynamics to changes leading to breast cancer.

As they reported in Nature Genetics on Thursday, the researchers performed RNA sequencing on more than 800,000 individual cells from frozen breast samples of 55 women between the ages of 19 and 65 years.

"The scale of this dataset has enabled us to delve into the entire breast composition, encompassing not only the epithelium but also the surrounding microenvironment," co-senior and co-corresponding author Walid Khaled, a researcher affiliated with the University of Cambridge and the Wellcome-MRC Cambridge Stem Cell Institute, and his colleagues wrote, calling the atlas "a rich resource that can be used to inform novel approaches for early detection and prevention of breast cancer."

Tissue donors included 22 women who had breast reduction surgery, the team noted, along with 27 who underwent prophylactic mastectomy based on their family history or because they were carriers of high-risk BRCA1/BRCA2 variants. The remaining six participants had high-risk BRCA1 variants and underwent contralateral mastectomy on the unaffected breast after a previous breast cancer diagnosis. The samples all came from the Breast Cancer Now Tissue Bank, established by a UK charity.

Based on expression data from the individual breast cells, the investigators highlighted 41 distinct cell subclusters falling into epithelial, stromal, and immune cell type categories. By incorporating additional information on the donors, they were able to tease out cell type and cell subcluster shifts influenced by the women's age, birth history, and germline mutation status.

In participants with high-risk BRCA1 or BRCA2 variants, for example, the data revealed immune cell expression changes consistent with immune exhaustion in noncancerous breast tissue — results backed up by subsequent immunohistochemistry experiments.

The results hinted that immune cells may start to lose the ability to effectively remove breast cells containing DNA mutations or damage stemming from impaired DNA double-strand break repair in the presence of BRCA1/2 variants that have been linked to increased breast and ovarian cancer risk.

"Our results suggest that in carriers of BRCA mutations, the immune system is failing to kill off damaged breast cells which in turn seem to be working to keep these immune cells at bay," Khaled said in a statement, adding that the work points to the "potential for a preventative treatment other than surgery for carriers of BRCA breast cancer gene mutations."

Members of the team are reportedly exploring immunotherapy-based options for staving off breast cancer development in individuals carrying risky versions of BRCA1 or BRCA2, an approach they are initially exploring in mouse models.

"Drugs already exist that can overcome [the detected] block in immune cell function," Khaled explained, "but so far, they've only been approved for late-stage disease."

To confirm and extend their findings, the researchers also brought together data from half a dozen prior breast single-cell RNA-seq studies to put together a collection that spanned more than 2.1 million cells from 286 individuals, which they called the integrated HBCA (iHBCA).

In particular, the authors suggested that the iHBCA "provides a framework for seamless integration of future sequencing datasets as we move toward larger cohorts that better represent the wider population."