A single‐cell RNA expression atlas of normal, preneoplastic and tumorigenic states in the human breast

To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the...

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Veröffentlicht in:	The EMBO journal Jg. 40; H. 11; S. e107333 - n/a
Hauptverfasser:	Pal, Bhupinder, Chen, Yunshun, Vaillant, François, Capaldo, Bianca D, Joyce, Rachel, Song, Xiaoyu, Bryant, Vanessa L, Penington, Jocelyn S, Di Stefano, Leon, Tubau Ribera, Nina, Wilcox, Stephen, Mann, Gregory B, Papenfuss, Anthony T, Lindeman, Geoffrey J, Smyth, Gordon K, Visvader, Jane E
Format:	Journal Article
Sprache:	Englisch
Veröffentlicht:	London Nature Publishing Group UK 01.06.2021 Springer Nature B.V John Wiley and Sons Inc
Schlagworte:	BRCA1 carriers BRCA1 protein Breast cancer Breast Neoplasms - classification Breast Neoplasms - genetics Breast Neoplasms - metabolism Breast Neoplasms - pathology Carcinogenesis - genetics Carcinogenesis - metabolism Carcinogenesis - pathology CD8 antigen CD8-Positive T-Lymphocytes - metabolism Clonal selection Copy number Cycles EMBO03 EMBO19 EMBO22 ErbB-2 protein Estrogen receptors Estrogens Female Fibroblasts Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genetic Heterogeneity Heterogeneity Humans Immunoregulation Immunotherapy Leukocyte migration LN metastasis Lymph nodes Lymphatic system Lymphocytes Lymphocytes T Macrophages Mammary gland Mammary glands Mammary Glands, Human - cytology Mammary Glands, Human - metabolism Mammary Glands, Human - pathology Menopause Metastases microenvironment Microenvironments Mutation Preneoplasia Receptors Resource RNA-Seq Single-Cell Analysis single‐cell RNA‐seq Stroma Transcriptomes Tumor cells Tumor Microenvironment Tumors microenvironment single‐cell RNA‐seq breast cancer carriers LN metastasis single-cell RNA-seq BRCA1 carriers
ISSN:	0261-4189, 1460-2075, 1460-2075
Online-Zugang:	Volltext
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Abstract	To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post‐menopausal women. Single‐cell profiling of 34 treatment‐naive primary tumors, including estrogen receptor (ER) + , HER2 + , and triple‐negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1 +/– tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8 + T cells characterized triple‐negative and HER2 + cancers but not ER + tumors, while all subtypes comprised cycling tumor‐associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER + tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large‐scale integration of patient samples provides a high‐resolution map of cell diversity in normal and cancerous human breast. Synopsis To examine global changes in breast heterogeneity across different states, this gene expression resource integrates large‐scale patient samples from diverse tissue states and breast cancer subtypes, offering a refined high‐resolution map of cell diversity in the normal and cancerous human mammary gland. Single‐cell transcriptome analyses profile > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and metastatic lymph nodes. Pre‐ to post‐menopause transition is associated with marked stromal changes, with decreased PDGFRb and matrix‐associated genes in fibroblasts. Progression from preneoplasia to tumors correlates with increased immune infiltration in BRCA1 mutation carriers. Tumor epithelial compartments show comparable diversity in different breast cancer subtypes. Cycling CD8 + T‐cells are reduced in estrogen receptor (ER) + tumors, suggesting different immunoregulatory patterns. Both clonal selection and mass migration contribute to lymph node metastases in patients with ER + cancer. Graphical Abstract A large‐scale gene expression resource integrates diverse tissue samples and reveals unexpected heterogeneity of breast cancer subtypes.
AbstractList	To examine global changes in breast heterogeneity across different states, we determined the single-cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1+/- tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post-menopausal women. Single-cell profiling of 34 treatment-naive primary tumors, including estrogen receptor (ER)+ , HER2+ , and triple-negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1+/- tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8+ T cells characterized triple-negative and HER2+ cancers but not ER+ tumors, while all subtypes comprised cycling tumor-associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER+ tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large-scale integration of patient samples provides a high-resolution map of cell diversity in normal and cancerous human breast.To examine global changes in breast heterogeneity across different states, we determined the single-cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1+/- tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post-menopausal women. Single-cell profiling of 34 treatment-naive primary tumors, including estrogen receptor (ER)+ , HER2+ , and triple-negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1+/- tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8+ T cells characterized triple-negative and HER2+ cancers but not ER+ tumors, while all subtypes comprised cycling tumor-associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER+ tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large-scale integration of patient samples provides a high-resolution map of cell diversity in normal and cancerous human breast. To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1+/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post‐menopausal women. Single‐cell profiling of 34 treatment‐naive primary tumors, including estrogen receptor (ER)+, HER2+, and triple‐negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1+/– tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8+ T cells characterized triple‐negative and HER2+ cancers but not ER+ tumors, while all subtypes comprised cycling tumor‐associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER+ tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large‐scale integration of patient samples provides a high‐resolution map of cell diversity in normal and cancerous human breast. To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post‐menopausal women. Single‐cell profiling of 34 treatment‐naive primary tumors, including estrogen receptor (ER) + , HER2 + , and triple‐negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1 +/– tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8 + T cells characterized triple‐negative and HER2 + cancers but not ER + tumors, while all subtypes comprised cycling tumor‐associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER + tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large‐scale integration of patient samples provides a high‐resolution map of cell diversity in normal and cancerous human breast. Synopsis To examine global changes in breast heterogeneity across different states, this gene expression resource integrates large‐scale patient samples from diverse tissue states and breast cancer subtypes, offering a refined high‐resolution map of cell diversity in the normal and cancerous human mammary gland. Single‐cell transcriptome analyses profile > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and metastatic lymph nodes. Pre‐ to post‐menopause transition is associated with marked stromal changes, with decreased PDGFRb and matrix‐associated genes in fibroblasts. Progression from preneoplasia to tumors correlates with increased immune infiltration in BRCA1 mutation carriers. Tumor epithelial compartments show comparable diversity in different breast cancer subtypes. Cycling CD8 + T‐cells are reduced in estrogen receptor (ER) + tumors, suggesting different immunoregulatory patterns. Both clonal selection and mass migration contribute to lymph node metastases in patients with ER + cancer. Graphical Abstract A large‐scale gene expression resource integrates diverse tissue samples and reveals unexpected heterogeneity of breast cancer subtypes. To examine global changes in breast heterogeneity across different states, we determined the single-cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1 tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post-menopausal women. Single-cell profiling of 34 treatment-naive primary tumors, including estrogen receptor (ER) , HER2 , and triple-negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1 tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8 T cells characterized triple-negative and HER2 cancers but not ER tumors, while all subtypes comprised cycling tumor-associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large-scale integration of patient samples provides a high-resolution map of cell diversity in normal and cancerous human breast. To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1+/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post‐menopausal women. Single‐cell profiling of 34 treatment‐naive primary tumors, including estrogen receptor (ER)+, HER2+, and triple‐negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1+/– tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8+ T cells characterized triple‐negative and HER2+ cancers but not ER+ tumors, while all subtypes comprised cycling tumor‐associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER+ tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large‐scale integration of patient samples provides a high‐resolution map of cell diversity in normal and cancerous human breast. Synopsis To examine global changes in breast heterogeneity across different states, this gene expression resource integrates large‐scale patient samples from diverse tissue states and breast cancer subtypes, offering a refined high‐resolution map of cell diversity in the normal and cancerous human mammary gland. Single‐cell transcriptome analyses profile > 340,000 cells encompassing normal breast, preneoplastic BRCA1+/– tissue, the major breast cancer subtypes, and metastatic lymph nodes. Pre‐ to post‐menopause transition is associated with marked stromal changes, with decreased PDGFRb and matrix‐associated genes in fibroblasts. Progression from preneoplasia to tumors correlates with increased immune infiltration in BRCA1 mutation carriers. Tumor epithelial compartments show comparable diversity in different breast cancer subtypes. Cycling CD8+ T‐cells are reduced in estrogen receptor (ER)+ tumors, suggesting different immunoregulatory patterns. Both clonal selection and mass migration contribute to lymph node metastases in patients with ER+ cancer. A large‐scale gene expression resource integrates diverse tissue samples and reveals unexpected heterogeneity of breast cancer subtypes. To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal breast, preneoplastic BRCA1 +/– tissue, the major breast cancer subtypes, and pairs of tumors and involved lymph nodes. Elucidation of the normal breast microenvironment revealed striking changes in the stroma of post‐menopausal women. Single‐cell profiling of 34 treatment‐naive primary tumors, including estrogen receptor (ER)+, HER2+, and triple‐negative breast cancers, revealed comparable diversity among cancer cells and a discrete subset of cycling cells. The transcriptomes of preneoplastic BRCA1 +/– tissue versus tumors highlighted global changes in the immune microenvironment. Within the tumor immune landscape, proliferative CD8+ T cells characterized triple‐negative and HER2+ cancers but not ER+ tumors, while all subtypes comprised cycling tumor‐associated macrophages, thus invoking potentially different immunotherapy targets. Copy number analysis of paired ER+ tumors and lymph nodes indicated seeding by genetically distinct clones or mass migration of primary tumor cells into axillary lymph nodes. This large‐scale integration of patient samples provides a high‐resolution map of cell diversity in normal and cancerous human breast. A large‐scale gene expression resource integrates diverse tissue samples and reveals unexpected heterogeneity of breast cancer subtypes.
Author	Chen, Yunshun Wilcox, Stephen Visvader, Jane E Pal, Bhupinder Capaldo, Bianca D Song, Xiaoyu Papenfuss, Anthony T Mann, Gregory B Smyth, Gordon K Joyce, Rachel Penington, Jocelyn S Di Stefano, Leon Vaillant, François Lindeman, Geoffrey J Bryant, Vanessa L Tubau Ribera, Nina
AuthorAffiliation	The Peter MacCallum Cancer Centre, Melbourne, Vic, Australia
AuthorAffiliation_xml	– name: The Peter MacCallum Cancer Centre, Melbourne, Vic, Australia – name: 2 Department of Medical Biology The University of Melbourne Parkville Vic Australia – name: 14 School of Mathematics and Statistics The University of Melbourne Parkville Vic Australia – name: 3 School of Cancer Medicine La Trobe University Bundoora Vic Australia – name: 7 Centre for Dynamic Imaging Parkville Vic Australia – name: 9 The Royal Melbourne Hospital Parkville Vic Australia – name: 6 Immunology Division The Walter and Eliza Hall Institute of Medical Research Parkville Vic Australia – name: 11 The Royal Women’s Hospital Parkville Vic Australia – name: 1 ACRF Cancer Biology and Stem Cells Division The Walter and Eliza Hall Institute of Medical Research Parkville Vic Australia – name: 5 Bioinformatics Division The Walter and Eliza Hall Institute of Medical Research Parkville Vic Australia – name: 10 The Peter MacCallum Cancer Centre Melbourne Vic Australia – name: 8 Advanced Technology and Biology Division The Walter and Eliza Hall Institute of Medical Research Parkville Vic Australia – name: 13 Department of Medicine The University of Melbourne Parkville Vic Australia – name: 4 Olivia Newton‐John Cancer Research Institute Heidelberg Vic Australia – name: 12 The Department of Surgery The University of Melbourne Parkville Vic Australia
Author_xml	– sequence: 1 givenname: Bhupinder orcidid: 0000-0002-3684-4331 surname: Pal fullname: Pal, Bhupinder organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne, School of Cancer Medicine, La Trobe University, Olivia Newton‐John Cancer Research Institute – sequence: 2 givenname: Yunshun orcidid: 0000-0003-4911-5653 surname: Chen fullname: Chen, Yunshun organization: Department of Medical Biology, The University of Melbourne, Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 3 givenname: François orcidid: 0000-0003-3229-3760 surname: Vaillant fullname: Vaillant, François organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 4 givenname: Bianca D surname: Capaldo fullname: Capaldo, Bianca D organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 5 givenname: Rachel surname: Joyce fullname: Joyce, Rachel organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 6 givenname: Xiaoyu surname: Song fullname: Song, Xiaoyu organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne – sequence: 7 givenname: Vanessa L surname: Bryant fullname: Bryant, Vanessa L organization: Department of Medical Biology, The University of Melbourne, Immunology Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 8 givenname: Jocelyn S surname: Penington fullname: Penington, Jocelyn S organization: Department of Medical Biology, The University of Melbourne, Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 9 givenname: Leon surname: Di Stefano fullname: Di Stefano, Leon organization: Department of Medical Biology, The University of Melbourne, Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 10 givenname: Nina surname: Tubau Ribera fullname: Tubau Ribera, Nina organization: Centre for Dynamic Imaging, Advanced Technology and Biology Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 11 givenname: Stephen surname: Wilcox fullname: Wilcox, Stephen organization: Advanced Technology and Biology Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 12 givenname: Gregory B surname: Mann fullname: Mann, Gregory B organization: The Royal Melbourne Hospital, The Peter MacCallum Cancer Centre, The Royal Women’s Hospital, The Department of Surgery, The University of Melbourne – sequence: 14 givenname: Anthony T surname: Papenfuss fullname: Papenfuss, Anthony T organization: Department of Medical Biology, The University of Melbourne, Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research – sequence: 15 givenname: Geoffrey J orcidid: 0000-0001-9386-2416 surname: Lindeman fullname: Lindeman, Geoffrey J organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, The Royal Melbourne Hospital, The Peter MacCallum Cancer Centre, Department of Medicine, The University of Melbourne – sequence: 16 givenname: Gordon K orcidid: 0000-0001-9221-2892 surname: Smyth fullname: Smyth, Gordon K email: smyth@wehi.edu.au organization: Bioinformatics Division, The Walter and Eliza Hall Institute of Medical Research, School of Mathematics and Statistics, The University of Melbourne – sequence: 17 givenname: Jane E orcidid: 0000-0001-9173-6977 surname: Visvader fullname: Visvader, Jane E email: visvader@wehi.edu.au organization: ACRF Cancer Biology and Stem Cells Division, The Walter and Eliza Hall Institute of Medical Research, Department of Medical Biology, The University of Melbourne
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/33950524$$D View this record in MEDLINE/PubMed
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Snippet	To examine global changes in breast heterogeneity across different states, we determined the single‐cell transcriptomes of > 340,000 cells encompassing normal... To examine global changes in breast heterogeneity across different states, we determined the single-cell transcriptomes of > 340,000 cells encompassing normal...
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SubjectTerms	BRCA1 carriers BRCA1 protein Breast cancer Breast Neoplasms - classification Breast Neoplasms - genetics Breast Neoplasms - metabolism Breast Neoplasms - pathology Carcinogenesis - genetics Carcinogenesis - metabolism Carcinogenesis - pathology CD8 antigen CD8-Positive T-Lymphocytes - metabolism Clonal selection Copy number Cycles EMBO03 EMBO19 EMBO22 ErbB-2 protein Estrogen receptors Estrogens Female Fibroblasts Gene expression Gene Expression Profiling Gene Expression Regulation, Neoplastic Genetic Heterogeneity Heterogeneity Humans Immunoregulation Immunotherapy Leukocyte migration LN metastasis Lymph nodes Lymphatic system Lymphocytes Lymphocytes T Macrophages Mammary gland Mammary glands Mammary Glands, Human - cytology Mammary Glands, Human - metabolism Mammary Glands, Human - pathology Menopause Metastases microenvironment Microenvironments Mutation Preneoplasia Receptors Resource RNA-Seq Single-Cell Analysis single‐cell RNA‐seq Stroma Transcriptomes Tumor cells Tumor Microenvironment Tumors
Title	A single‐cell RNA expression atlas of normal, preneoplastic and tumorigenic states in the human breast
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