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Single-cell analysis of human primary prostate cancer reveals the heterogeneity of tumor-associated epithelial cell states

View ORCID ProfileHanbing Song, Hannah N.W. Weinstein, Paul Allegakoen, Marc H. Wadsworth II, Jamie Xie, View ORCID ProfileHeiko Yang, Felix Y. Feng, Peter R. Carroll, Bruce Wang, View ORCID ProfileMatthew R. Cooperberg, View ORCID ProfileAlex K. Shalek, View ORCID ProfileFranklin W. Huang
doi: https://doi.org/10.1101/2020.11.06.359802
Hanbing Song
1Division of Hematology/Oncology, Department of Medicine; Helen Diller Family Comprehensive Cancer Center; Bakar Computational Health Sciences Institute; Institute for Human Genetics; University of California, San Francisco, San Francisco, CA 94143, USA
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  • ORCID record for Hanbing Song
Hannah N.W. Weinstein
1Division of Hematology/Oncology, Department of Medicine; Helen Diller Family Comprehensive Cancer Center; Bakar Computational Health Sciences Institute; Institute for Human Genetics; University of California, San Francisco, San Francisco, CA 94143, USA
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Paul Allegakoen
1Division of Hematology/Oncology, Department of Medicine; Helen Diller Family Comprehensive Cancer Center; Bakar Computational Health Sciences Institute; Institute for Human Genetics; University of California, San Francisco, San Francisco, CA 94143, USA
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Marc H. Wadsworth II
2The Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, 400 Technology Square, Cambridge, MA 02139, USA; Institute for Medical Engineering and Science (IMES), Department of Chemistry, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main St., Cambridge, MA 02142, USA
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Jamie Xie
1Division of Hematology/Oncology, Department of Medicine; Helen Diller Family Comprehensive Cancer Center; Bakar Computational Health Sciences Institute; Institute for Human Genetics; University of California, San Francisco, San Francisco, CA 94143, USA
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Heiko Yang
3Department of Urology; Helen Diller Family Comprehensive Cancer Center; University of California, San Francisco, 550 16th Street, 6th Floor, San Francisco, CA 94143, USA
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Felix Y. Feng
4Departments of Radiation Oncology, Urology, and Medicine, Helen Diller Family Comprehensive Cancer Center; University of California, San Francisco, Helen Diller Family Cancer Research Building, 1450 Third Street, Room 383, San Francisco, CA 94143, USA
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Peter R. Carroll
5Department of Urology; Helen Diller Family Comprehensive Cancer Center; University of California, San Francisco, 550 16th Street, 6th Floor, San Francisco, CA 94143, USA
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Bruce Wang
6Division of Gastroenterology, Department of Medicine, University of California, San Francisco, CA 94143, USA
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Matthew R. Cooperberg
7Department of Urology; Epidemiology & Biostatistics; Helen Diller Family Comprehensive Cancer Center; University of California, San Francisco, 550 16th Street, 6th Floor, San Francisco, CA 94143, USA
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Alex K. Shalek
2The Ragon Institute of Massachusetts General Hospital, Massachusetts Institute of Technology and Harvard University, 400 Technology Square, Cambridge, MA 02139, USA; Institute for Medical Engineering and Science (IMES), Department of Chemistry, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology, 77 Massachusetts Avenue, Cambridge, MA 02139, USA; Broad Institute of Massachusetts Institute of Technology and Harvard, 415 Main St., Cambridge, MA 02142, USA
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Franklin W. Huang
1Division of Hematology/Oncology, Department of Medicine; Helen Diller Family Comprehensive Cancer Center; Bakar Computational Health Sciences Institute; Institute for Human Genetics; University of California, San Francisco, San Francisco, CA 94143, USA
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  • For correspondence: Franklin.Huang@ucsf.edu
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Abstract

Prostate cancer is the second most common malignancy in men worldwide and consists of a mixture of tumor and non-tumor cell types. To characterize the prostate cancer tumor microenvironment, we performed single-cell RNA-sequencing on prostate biopsies, prostatectomy specimens, and patient-derived organoids from localized prostate cancer patients. We identify a population of tumor-associated club cells that may act as progenitor cells and uncover heterogeneous cellular states in prostate epithelial cells marked by high androgen signaling states that are enriched in prostate cancer. ERG- tumor cells, compared to ERG+ cells, demonstrate shared heterogeneity with surrounding luminal epithelial cells and appear to give rise to common tumor microenvironment responses. Finally, we show that prostate epithelial organoids recapitulate tumor-associated epithelial cell states and are enriched with distinct cell types and states from their parent tissues. Our results provide diagnostically relevant insights and advance our understanding of the cellular states associated with prostate carcinogenesis.

Competing Interest Statement

A.K.S. reports compensation for consulting and/or SAB membership from Merck, Honeycomb Biotechnologies, Cellarity, Repertoire Immune Medicines, Orche Bio, and Dahlia Biosciences. F.Y.F. reports compensation for consulting and/or SAB membership from Astellas, Bayer, Blue Earth Diagnostics, Celgene, Genentech, Janssen Oncology, Myovant, Roivant, Sanofi, PFS Genomics, and SerImmune.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Single-cell analysis of human primary prostate cancer reveals the heterogeneity of tumor-associated epithelial cell states
Hanbing Song, Hannah N.W. Weinstein, Paul Allegakoen, Marc H. Wadsworth II, Jamie Xie, Heiko Yang, Felix Y. Feng, Peter R. Carroll, Bruce Wang, Matthew R. Cooperberg, Alex K. Shalek, Franklin W. Huang
bioRxiv 2020.11.06.359802; doi: https://doi.org/10.1101/2020.11.06.359802
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Single-cell analysis of human primary prostate cancer reveals the heterogeneity of tumor-associated epithelial cell states
Hanbing Song, Hannah N.W. Weinstein, Paul Allegakoen, Marc H. Wadsworth II, Jamie Xie, Heiko Yang, Felix Y. Feng, Peter R. Carroll, Bruce Wang, Matthew R. Cooperberg, Alex K. Shalek, Franklin W. Huang
bioRxiv 2020.11.06.359802; doi: https://doi.org/10.1101/2020.11.06.359802

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