Aging-Associated Alterations in Mammary Epithelia and Stroma Revealed by Single-Cell RNA Sequencing
Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged mur...
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| Published in | Cell reports (Cambridge) Vol. 33; no. 13; p. 108566 |
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| Main Authors | , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
29.12.2020
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| Abstract | Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk.
[Display omitted]
•scRNA-seq captures aging-associated alterations in mammary epithelia and stroma•Identification of luminal and macrophage subpopulations reveals lineage complexity•Aging correlates with alveolar maturation and potential cellular functional decline•Aging is coupled to a potentially pro-tumorigenic and inflammatory microenvironment
Using single-cell RNA-sequencing, Li et al. compare mammary epithelia and stroma in young and aged mice. Age-dependent changes at cell and gene levels provide evidence suggesting alveolar maturation, functional deterioration, and potential pro-tumorigenic and inflammatory alterations. Additionally, identification of heterogeneous luminal and macrophage subpopulations underscores the complexity of mammary lineages. |
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| AbstractList | Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk. Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk. Using single-cell RNA-sequencing, Li et al. compare mammary epithelia and stroma in young and aged mice. Age-dependent changes at cell and gene levels provide evidence suggesting alveolar maturation, functional deterioration, and potential pro-tumorigenic and inflammatory alterations. Additionally, identification of heterogeneous luminal and macrophage subpopulations underscores the complexity of mammary lineages. Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk.Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk. Aging is closely associated with increased susceptibility to breast cancer, yet there have been limited systematic studies of aging-induced alterations in the mammary gland. Here, we leverage high-throughput single-cell RNA sequencing to generate a detailed transcriptomic atlas of young and aged murine mammary tissues. By analyzing epithelial, stromal, and immune cells, we identify age-dependent alterations in cell proportions and gene expression, providing evidence that suggests alveolar maturation and physiological decline. The analysis also uncovers potential pro-tumorigenic mechanisms coupled to the age-associated loss of tumor suppressor function and change in microenvironment. In addition, we identify a rare, age-dependent luminal population co-expressing hormone-sensing and secretory-alveolar lineage markers, as well as two macrophage populations expressing distinct gene signatures, underscoring the complex heterogeneity of the mammary epithelia and stroma. Collectively, this rich single-cell atlas reveals the effects of aging on mammary physiology and can serve as a useful resource for understanding aging-associated cancer risk. [Display omitted] •scRNA-seq captures aging-associated alterations in mammary epithelia and stroma•Identification of luminal and macrophage subpopulations reveals lineage complexity•Aging correlates with alveolar maturation and potential cellular functional decline•Aging is coupled to a potentially pro-tumorigenic and inflammatory microenvironment Using single-cell RNA-sequencing, Li et al. compare mammary epithelia and stroma in young and aged mice. Age-dependent changes at cell and gene levels provide evidence suggesting alveolar maturation, functional deterioration, and potential pro-tumorigenic and inflammatory alterations. Additionally, identification of heterogeneous luminal and macrophage subpopulations underscores the complexity of mammary lineages. |
| ArticleNumber | 108566 |
| Author | Tsiobikas, Christina Rosenbluth, Jennifer Moore, Kaitlin Oren, Yaara Pinello, Luca Brugge, Joan S. Gray, G. Kenneth Guerriero, Jennifer L. Gupta, Kushali P. Regev, Aviv Li, Carman Man-Chung Steinbaugh, Michael J. Shapiro, Hana Chen, Huidong Selfors, Laura M. |
| AuthorAffiliation | 5 Breast Tumor Immunology Laboratory, Dana-Farber Cancer Institute, Boston, MA 02115, USA 7 Present address: Genentech, 1 DNA Way, South San Francisco, CA 94080, USA 8 Lead Contact 4 Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA 1 Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA 3 Molecular Pathology Unit & Cancer Center, Massachusetts General Hospital Research Institute and Harvard Medical School, Charlestown, MA 02129, USA 2 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA 6 Division of Breast Surgery, Department of Surgery, Brigham and Women’s Hospital, Boston, MA 02115, USA |
| AuthorAffiliation_xml | – name: 2 Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – name: 7 Present address: Genentech, 1 DNA Way, South San Francisco, CA 94080, USA – name: 3 Molecular Pathology Unit & Cancer Center, Massachusetts General Hospital Research Institute and Harvard Medical School, Charlestown, MA 02129, USA – name: 6 Division of Breast Surgery, Department of Surgery, Brigham and Women’s Hospital, Boston, MA 02115, USA – name: 4 Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA – name: 1 Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – name: 5 Breast Tumor Immunology Laboratory, Dana-Farber Cancer Institute, Boston, MA 02115, USA – name: 8 Lead Contact |
| Author_xml | – sequence: 1 givenname: Carman Man-Chung orcidid: 0000-0002-0577-7797 surname: Li fullname: Li, Carman Man-Chung organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 2 givenname: Hana orcidid: 0000-0002-7917-5190 surname: Shapiro fullname: Shapiro, Hana organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 3 givenname: Christina orcidid: 0000-0002-5815-4278 surname: Tsiobikas fullname: Tsiobikas, Christina organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 4 givenname: Laura M. orcidid: 0000-0002-1317-7353 surname: Selfors fullname: Selfors, Laura M. organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 5 givenname: Huidong orcidid: 0000-0003-1391-8198 surname: Chen fullname: Chen, Huidong organization: Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – sequence: 6 givenname: Jennifer orcidid: 0000-0003-1314-6976 surname: Rosenbluth fullname: Rosenbluth, Jennifer organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 7 givenname: Kaitlin orcidid: 0000-0001-6248-1522 surname: Moore fullname: Moore, Kaitlin organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 8 givenname: Kushali P. orcidid: 0000-0002-2136-5303 surname: Gupta fullname: Gupta, Kushali P. organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 9 givenname: G. Kenneth orcidid: 0000-0003-4969-670X surname: Gray fullname: Gray, G. Kenneth organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 10 givenname: Yaara surname: Oren fullname: Oren, Yaara organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA – sequence: 11 givenname: Michael J. orcidid: 0000-0002-2403-2221 surname: Steinbaugh fullname: Steinbaugh, Michael J. organization: Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA 02115, USA – sequence: 12 givenname: Jennifer L. orcidid: 0000-0002-2104-5457 surname: Guerriero fullname: Guerriero, Jennifer L. organization: Breast Tumor Immunology Laboratory, Dana-Farber Cancer Institute, Boston, MA 02115, USA – sequence: 13 givenname: Luca orcidid: 0000-0003-1109-3823 surname: Pinello fullname: Pinello, Luca organization: Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – sequence: 14 givenname: Aviv orcidid: 0000-0003-3293-3158 surname: Regev fullname: Regev, Aviv organization: Broad Institute of MIT and Harvard, Cambridge, MA 02142, USA – sequence: 15 givenname: Joan S. surname: Brugge fullname: Brugge, Joan S. email: joan_brugge@hms.harvard.edu organization: Department of Cell Biology, Harvard Medical School, Boston, MA 02115, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33378681$$D View this record in MEDLINE/PubMed |
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| Keywords | fibroblasts endothelial cells macrophages single-cell RNA-seq aging mammary epithelia and stroma luminal and myoepithelial cells |
| Language | English |
| License | This is an open access article under the CC BY license. Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 AUTHOR CONTRIBUTIONS C.M.L. and J.S.B. conceived the study and designed the experiments. C.M.L. performed the experiments and analyses with assistance from G.K.G. for tissue dissociation; A.R. for scRNA-seq; L.M.S., H.C., L.P., Y.O., and M.J.S. for bioinformatics analyses; H.S., C.T., and K.P.G. for tissue staining and microscopy; and H.S., J.R., and K.M. for FACS analysis of tissues and organoids. All authors contributed to the interpretation of experimental results. C.M.L. and J.S.B. wrote the manuscript, with contribution from all authors. J.S.B. provided funding and project supervision. |
| ORCID | 0000-0003-3293-3158 0000-0002-1317-7353 0000-0003-4969-670X 0000-0001-6248-1522 0000-0002-7917-5190 0000-0002-2104-5457 0000-0002-0577-7797 0000-0002-2136-5303 0000-0003-1109-3823 0000-0003-1314-6976 0000-0003-1391-8198 0000-0002-5815-4278 0000-0002-2403-2221 |
| OpenAccessLink | http://journals.scholarsportal.info/openUrl.xqy?doi=10.1016/j.celrep.2020.108566 |
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| PublicationDate | 2020-12-29 |
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| PublicationTitle | Cell reports (Cambridge) |
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| Publisher | Elsevier Inc |
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| Title | Aging-Associated Alterations in Mammary Epithelia and Stroma Revealed by Single-Cell RNA Sequencing |
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