High clonal diversity and spatial genetic admixture in early prostate cancer and surrounding normal tissue

Ning Zhang, Luuk Harbers, Michele Simonetti, Constantin Diekmann, Quentin Verron, Enrico Berrino, Sara E. Bellomo, Gabriel M. C. Longo, Michael Ratz, Niklas Schultz, Firas Tarish, Peng Su, Bo Han, Wanzhong Wang, Sofia Onorato, Dora Grassini, Roberto Ballarino, Silvia Giordano, Qifeng Yang, Anna Sapino, Jonas Frisén, Kanar Alkass, Henrik Druid, Vassilis Roukos, Thomas Helleday, Caterina Marchiò, Magda Bienko and Nicola Crosetto ()
Additional contact information
Ning Zhang: Karolinska Institutet
Luuk Harbers: Karolinska Institutet
Michele Simonetti: Karolinska Institutet
Constantin Diekmann: Karolinska Institutet
Quentin Verron: Karolinska Institutet
Enrico Berrino: FPO – IRCCS, Candiolo
Sara E. Bellomo: FPO – IRCCS, Candiolo
Gabriel M. C. Longo: Institute of Molecular Biology (IMB)
Michael Ratz: Karolinska Institute
Niklas Schultz: Science for Life Laboratory
Firas Tarish: Södersjukhuset
Peng Su: Qilu Hospital of Shandong University
Bo Han: Qilu Hospital of Shandong University
Wanzhong Wang: Karolinska Institutet
Sofia Onorato: Karolinska Institutet
Dora Grassini: University of Turin
Roberto Ballarino: Karolinska Institutet
Silvia Giordano: FPO – IRCCS, Candiolo
Qifeng Yang: Qilu Hospital of Shandong University
Anna Sapino: FPO – IRCCS, Candiolo
Jonas Frisén: Karolinska Institute
Kanar Alkass: Karolinska Institute
Henrik Druid: Karolinska Institutet
Vassilis Roukos: Institute of Molecular Biology (IMB)
Thomas Helleday: Science for Life Laboratory
Caterina Marchiò: FPO – IRCCS, Candiolo
Magda Bienko: Karolinska Institutet
Nicola Crosetto: Karolinska Institutet

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: Abstract Somatic copy number alterations (SCNAs) are pervasive in advanced human cancers, but their prevalence and spatial distribution in early-stage, localized tumors and their surrounding normal tissues are poorly characterized. Here, we perform multi-region, single-cell DNA sequencing to characterize the SCNA landscape across tumor-rich and normal tissue in two male patients with localized prostate cancer. We identify two distinct karyotypes: ‘pseudo-diploid’ cells harboring few SCNAs and highly aneuploid cells. Pseudo-diploid cells form numerous small-sized subclones ranging from highly spatially localized to broadly spread subclones. In contrast, aneuploid cells do not form subclones and are detected throughout the prostate, including normal tissue regions. Highly localized pseudo-diploid subclones are confined within tumor-rich regions and carry deletions in multiple tumor-suppressor genes. Our study reveals that SCNAs are widespread in normal and tumor regions across the prostate in localized prostate cancer patients and suggests that a subset of pseudo-diploid cells drive tumorigenesis in the aging prostate.

Date: 2024
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DOI: 10.1038/s41467-024-47664-z

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