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Persistent organic pollutants promote aggressiveness in prostate cancer

Oncogene volume 42, pages 2854–2867 (2023)Cite this article

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Abstract

Increasing evidence points towards a causal link between exposure to persistent organic pollutants (POPs) with increased incidence and aggressivity of various cancers. Among these POPs, dioxin and PCB-153 are widely found in our environment and represent a significant source of contamination. Dioxin exposure has already been linked to cancer such as non-Hodgkin’s lymphoma, but remains to be more extensively investigated in other cancers. Potential implications of dioxin and PCB-153 in prostate cancer progression spurred us to challenge both ex vivo and in vivo models with low doses of these POPs. We found that dioxin or PCB-153 exposure increased hallmarks of growth and metastasis of prostate cancer cells ex vivo and in grafted NOD-SCID mice. Exposure induced histopathological carcinoma-like patterns in the Ptenpc−/− mice. We identified up-regulation of Acetyl-CoA Acetyltransferase-1 (ACAT1) involved in ketone bodies pathway as a potential target. Mechanistically, genetic inhibition confirmed that ACAT1 mediated dioxin effect on cell migration. Using public prostate cancer datasets, we confirmed the deregulation of ACAT1 and associated gene encoded ketone bodies pathway enzymes such as OXCT1, BDH1 and HMGCL in advanced prostate cancer. To further explore this link between dioxin and ACAT1 deregulation, we analyzed a unique prostate-tumour tissue collection from the USA veterans exposed to agent orange, known to be highly contaminated by dioxin because of industrial production. We found that ACAT1 histoscore is significantly increased in exposed patients. Our studies reveal the implication of dioxin and PCB-153 to induce a prometastatic programme in prostate tumours and identify ACAT1 deregulation as a key event in this process.

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Fig. 1: Dioxin and PCB-153 promotes growth of mouse prostate organoids and of PCa cells.
Fig. 2: Dioxin and PCB-153 induce migration and invasion of PCa cells in vivo.
Fig. 3: Ptenpc−/− mice chronically exposed to dioxin and PCB-153 exhibit hallmarks of carcinoma development.
Fig. 4: Dioxin and PCB-153 target ACAT1 deregulation to increase migration of PCa cells.
Fig. 5: Dioxin and PCB-153 enhance invasive phenotype in vivo and is correlated with ACAT1 overexpression.
Fig. 6: AHR binds Acat1 promoter in response to dioxin and PCB-153.
Fig. 7: ACAT1 is a marker of dioxin exposure in PCa.

Data availability

All data are available in the main text or the supplementary materials.

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Acknowledgements

The authors thank Sandrine Plantade, Philippe Mazuel and Khirredine Ouchen for mouse care, Anip@th technical staff (iGReD, Clermont-Ferrand) for histological analyses, SC3 and CLIC platforms (iGReD, Clermont-Ferrand) for cell manipulations and imaging, Bioinformatic platform (iGReD, Clermont-Ferrand) for computational analysis, Jean-Paul Saru for western blot analyses. We thank Dr. Arun Sreekumar and Dr. Jie Gohlke (Baylor College of Medecine, Houston) for help and fruitful discussions in the preparation/interpretation of TMA analysis. We warmly thank Kathleen Gates for careful editing of the manuscript. Part of this study was supported by Région Auvergne Rhône Alpes, Fond Européen de Développement Régional (FEDER), Plan National de Recherche sur les Perturbateurs Endocriniens (13-MRES-PNRPE-1-CVS043), Plan-Cancer 2014-2019 for Jean Marc Lobaccaro and Silvère Baron, and Ligue contre le Cancer Rhône Alpes Auvergne et Saône et Loire for Cyrille de Joussineau. JB is a postdoc funded by Plan-Cancer 2014-2019. Prostate Cancer Foundation - VALOR Challenge grant provided support for MI and JJ in the acquisition/prep of PCa tissues. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

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Authors and Affiliations

  1. Université Clermont Auvergne, iGReD, CNRS UMR 6293, INSERM U1103, 28, place Henri Dunant, BP38, 63001, Clermont-Ferrand, France

    Julio Buñay, Christelle Damon-Soubeyrant, Angélique De Haze, Jean-Paul Saru, Amalia Trousson, Cyrille de Joussineau, Erwan Bouchareb, Ayhan Kocer, Marine Vialat, Sarah Dallel, Françoise Degoul, Yoan Renaud, Laurent Morel, Jean-Marc Lobaccaro & Silvère Baron

  2. Groupe Cancer Clermont Auvergne, 28, place Henri Dunant, BP38, 63001, Clermont-Ferrand, France

    Julio Buñay, Myriam Kossai, Christelle Damon-Soubeyrant, Angélique De Haze, Jean-Paul Saru, Amalia Trousson, Cyrille de Joussineau, Erwan Bouchareb, Ayhan Kocer, Marine Vialat, Sarah Dallel, Françoise Degoul, Frédérique Penault-Llorca, Yoan Renaud, Laurent Morel, Jean-Marc Lobaccaro & Silvère Baron

  3. Centre de Recherche en Nutrition Humaine d’Auvergne, 58 Boulevard Montalembert, F-63009, Clermont-Ferrand, France

    Julio Buñay, Christelle Damon-Soubeyrant, Angélique De Haze, Jean-Paul Saru, Amalia Trousson, Cyrille de Joussineau, Erwan Bouchareb, Ayhan Kocer, Marine Vialat, Sarah Dallel, Françoise Degoul, Yoan Renaud, Laurent Morel, Jean-Marc Lobaccaro & Silvère Baron

  4. Centre Jean Perrin, Université Clermont Auvergne, INSERM, U1240 Imagerie Moléculaire et Stratégies Théranostiques, F-63000, Clermont Ferrand, France

    Myriam Kossai & Frédérique Penault-Llorca

  5. Service d’Endocrinologie, Diabétologie et Maladies Métaboliques, CHU Clermont Ferrand, Hôpital Gabriel Montpied, F-63003, Clermont-Ferrand, France

    Sarah Dallel

  6. Université Côte d’Azur, INSERM U1065, C3M, Equipe Labellisée Ligue Nationale contre le Cancer, 2022, F-06204, Nice, France

    Frédéric Bost

  7. Université Côte d’Azur, Institut de Pharmacologie Moléculaire et Cellulaire (IPMC), CNRS UMR7275, Sophia-Antipolis, Valbonne, France

    Stephan Clavel

  8. Service d’Urologie, CHU Clermont-Ferrand, UMR1240 INSERM, Université Clermont-Auvergne, Clermont Ferrand, France

    Marie-Pierre Valli & Laurent Guy

  9. Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway

    Jason Matthews

  10. Department of Molecular and Cellular Biology, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Michael Ittmann

  11. Center for Metabolism and Experimental Therapeutics, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Michael Ittmann

  12. Dan L Duncan Comprehensive Cancer Center, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Michael Ittmann & Jeffrey Jones

  13. Department of Pathology and Immunology, Baylor College of Medicine, One Baylor Plaza, and Michael E. DeBakey VAMC Houston, Houston, TX, 77030, USA

    Michael Ittmann

  14. Department of Urology, Baylor College of Medicine, One Baylor Plaza, Houston, TX, 77030, USA

    Jeffrey Jones

  15. Operative Care Line, Urology Section, Michael E. DeBakey Veterans Affairs Medical Center, Houston, TX, 77030, USA

    Jeffrey Jones

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  1. Julio Buñay
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  10. Marine Vialat
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  15. Frédérique Penault-Llorca
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  21. Jeffrey Jones
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  22. Laurent Morel
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  23. Jean-Marc Lobaccaro
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Acquisition of the data: Jb, SB, JML, SD, EB, JPS, ADH. TMA conception and analysis: MI, JJ, MPV, LG, CDS, FPL, MK. Microscopic and confocal imaging: JB, CDS, MV, CdJ. AHR ChIPseq analysis: JB, YR, JM. Conception and design of the manuscript: JB, JML, SB. Analysis and interpretation of the data: JB, JML, SB. Drafting of the manuscript: JB, JML, SB. Critically revising the manuscript: JB, JML, SB, AT, FD, AK, SC, FB.

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Correspondence to Silvère Baron.

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Buñay, J., Kossai, M., Damon-Soubeyrant, C. et al. Persistent organic pollutants promote aggressiveness in prostate cancer. Oncogene 42, 2854–2867 (2023). https://doi.org/10.1038/s41388-023-02788-2

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