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

Author

Listed:
  • Hanbing Song

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Hannah N. W. Weinstein

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Paul Allegakoen

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Marc H. Wadsworth

    (Massachusetts Institute of Technology and Harvard University
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Jamie Xie

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Heiko Yang

    (University of California, San Francisco
    University of California, San Francisco)

  • Ethan A. Castro

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Kevin L. Lu

    (University of California, San Francisco)

  • Bradley A. Stohr

    (University of California, San Francisco)

  • Felix Y. Feng

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

  • Peter R. Carroll

    (University of California, San Francisco
    University of California, San Francisco)

  • Bruce Wang

    (University of California)

  • Matthew R. Cooperberg

    (University of California, San Francisco
    University of California, San Francisco
    Division of Hematology and Oncology, Department of Medicine, San Francisco Veterans Affairs Medical Center)

  • Alex K. Shalek

    (Massachusetts Institute of Technology and Harvard University
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology
    Massachusetts Institute of Technology)

  • Franklin W. Huang

    (University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco
    University of California, San Francisco)

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 perform single-cell RNA-sequencing on prostate biopsies, prostatectomy specimens, and patient-derived organoids from localized prostate cancer patients. We uncover heterogeneous cellular states in prostate epithelial cells marked by high androgen signaling states that are enriched in prostate cancer and identify a population of tumor-associated club cells that may be associated with prostate carcinogenesis. ERG-negative tumor cells, compared to ERG-positive 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 harbor 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.

Suggested Citation

  • Hanbing Song & Hannah N. W. Weinstein & Paul Allegakoen & Marc H. Wadsworth & Jamie Xie & Heiko Yang & Ethan A. Castro & Kevin L. Lu & Bradley A. Stohr & Felix Y. Feng & Peter R. Carroll & Bruce Wang , 2022. "Single-cell analysis of human primary prostate cancer reveals the heterogeneity of tumor-associated epithelial cell states," Nature Communications, Nature, vol. 13(1), pages 1-20, December.
    • Handle: RePEc:nat:natcom:v:13:y:2022:i:1:d:10.1038_s41467-021-27322-4
    DOI: 10.1038/s41467-021-27322-4
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    Cited by:

    1. Chih-Wei Chou & Chia-Nung Hung & Cheryl Hsiang-Ling Chiu & Xi Tan & Meizhen Chen & Chien-Chin Chen & Moawiz Saeed & Che-Wei Hsu & Michael A. Liss & Chiou-Miin Wang & Zhao Lai & Nathaniel Alvarez & Paw, 2023. "Phagocytosis-initiated tumor hybrid cells acquire a c-Myc-mediated quasi-polarization state for immunoevasion and distant dissemination," Nature Communications, Nature, vol. 14(1), pages 1-20, December.
    2. Hong Yuen Wong & Quanhu Sheng & Amanda B. Hesterberg & Sarah Croessmann & Brenda L. Rios & Khem Giri & Jorgen Jackson & Adam X. Miranda & Evan Watkins & Kerry R. Schaffer & Meredith Donahue & Elizabet, 2022. "Single cell analysis of cribriform prostate cancer reveals cell intrinsic and tumor microenvironmental pathways of aggressive disease," Nature Communications, Nature, vol. 13(1), pages 1-21, December.
    3. Nikita Sushentsev & Gregory Hamm & Lucy Flint & Daniel Birtles & Aleksandr Zakirov & Jack Richings & Stephanie Ling & Jennifer Y. Tan & Mary A. McLean & Vinay Ayyappan & Ines Horvat Menih & Cara Brodi, 2024. "Metabolic imaging across scales reveals distinct prostate cancer phenotypes," Nature Communications, Nature, vol. 15(1), pages 1-22, December.
    4. Mindy K. Graham & Rulin Wang & Roshan Chikarmane & Bulouere Abel & Ajay Vaghasia & Anuj Gupta & Qizhi Zheng & Jessica Hicks & Polina Sysa-Shah & Xin Pan & Nicole Castagna & Jianyong Liu & Jennifer Mey, 2024. "Convergent alterations in the tumor microenvironment of MYC-driven human and murine prostate cancer," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    5. Taghreed Hirz & Shenglin Mei & Hirak Sarkar & Youmna Kfoury & Shulin Wu & Bronte M. Verhoeven & Alexander O. Subtelny & Dimitar V. Zlatev & Matthew W. Wszolek & Keyan Salari & Evan Murray & Fei Chen &, 2023. "Dissecting the immune suppressive human prostate tumor microenvironment via integrated single-cell and spatial transcriptomic analyses," Nature Communications, Nature, vol. 14(1), pages 1-20, December.

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