Hyperpolarised 13C-MRI identifies the emergence of a glycolytic cell population within intermediate-risk human prostate cancer

Nikita Sushentsev, Mary A. McLean, Anne Y. Warren, Arnold J. V. Benjamin, Cara Brodie, Amy Frary, Andrew B. Gill, Julia Jones, Joshua D. Kaggie, Benjamin W. Lamb, Matthew J. Locke, Jodi L. Miller, Ian G. Mills, Andrew N. Priest, Fraser J. L. Robb, Nimish Shah, Rolf F. Schulte, Martin J. Graves, Vincent J. Gnanapragasam, Kevin M. Brindle, Tristan Barrett () and Ferdia A. Gallagher
Additional contact information
Nikita Sushentsev: Addenbrooke’s Hospital and University of Cambridge
Mary A. McLean: Addenbrooke’s Hospital and University of Cambridge
Anne Y. Warren: Cambridge University Hospitals NHS Foundation Trust
Arnold J. V. Benjamin: Addenbrooke’s Hospital and University of Cambridge
Cara Brodie: University of Cambridge
Amy Frary: Addenbrooke’s Hospital and University of Cambridge
Andrew B. Gill: Addenbrooke’s Hospital and University of Cambridge
Julia Jones: University of Cambridge
Joshua D. Kaggie: Addenbrooke’s Hospital and University of Cambridge
Benjamin W. Lamb: Cambridge University Hospitals NHS Foundation Trust
Matthew J. Locke: Addenbrooke’s Hospital and University of Cambridge
Jodi L. Miller: University of Cambridge
Ian G. Mills: Queen’s University Belfast
Andrew N. Priest: Addenbrooke’s Hospital and University of Cambridge
Fraser J. L. Robb: GE Healthcare
Nimish Shah: Cambridge University Hospitals NHS Foundation Trust
Rolf F. Schulte: GE Healthcare
Martin J. Graves: Addenbrooke’s Hospital and University of Cambridge
Vincent J. Gnanapragasam: Cambridge University Hospitals NHS Foundation Trust
Kevin M. Brindle: University of Cambridge
Tristan Barrett: Addenbrooke’s Hospital and University of Cambridge
Ferdia A. Gallagher: Addenbrooke’s Hospital and University of Cambridge

Nature Communications, 2022, vol. 13, issue 1, 1-12

Abstract: Abstract Hyperpolarised magnetic resonance imaging (HP 13C-MRI) is an emerging clinical technique to detect [1-13C]lactate production in prostate cancer (PCa) following intravenous injection of hyperpolarised [1-13C]pyruvate. Here we differentiate clinically significant PCa from indolent disease in a low/intermediate-risk population by correlating [1-13C]lactate labelling on MRI with the percentage of Gleason pattern 4 (%GP4) disease. Using immunohistochemistry and spatial transcriptomics, we show that HP 13C-MRI predominantly measures metabolism in the epithelial compartment of the tumour, rather than the stroma. MRI-derived tumour [1-13C]lactate labelling correlated with epithelial mRNA expression of the enzyme lactate dehydrogenase (LDHA and LDHB combined), and the ratio of lactate transporter expression between the epithelial and stromal compartments (epithelium-to-stroma MCT4). We observe similar changes in MCT4, LDHA, and LDHB between tumours with primary Gleason patterns 3 and 4 in an independent TCGA cohort. Therefore, HP 13C-MRI can metabolically phenotype clinically significant disease based on underlying metabolic differences in the epithelial and stromal tumour compartments.

Date: 2022
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DOI: 10.1038/s41467-022-28069-2

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