High-fat diet fuels prostate cancer progression by rewiring the metabolome and amplifying the MYC program

Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer m...

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Published in:	Nature communications Vol. 10; no. 1; pp. 4358 - 14
Main Authors:	Labbé, David P., Zadra, Giorgia, Yang, Meng, Reyes, Jaime M., Lin, Charles Y., Cacciatore, Stefano, Ebot, Ericka M., Creech, Amanda L., Giunchi, Francesca, Fiorentino, Michelangelo, Elfandy, Habiba, Syamala, Sudeepa, Karoly, Edward D., Alshalalfa, Mohammed, Erho, Nicholas, Ross, Ashley, Schaeffer, Edward M., Gibb, Ewan A., Takhar, Mandeep, Den, Robert B., Lehrer, Jonathan, Karnes, R. Jeffrey, Freedland, Stephen J., Davicioni, Elai, Spratt, Daniel E., Ellis, Leigh, Jaffe, Jacob D., DʼAmico, Anthony V., Kantoff, Philip W., Bradner, James E., Mucci, Lorelei A., Chavarro, Jorge E., Loda, Massimo, Brown, Myles
Format:	Journal Article
Language:	English
Published:	London Nature Publishing Group UK 25.09.2019 Nature Publishing Group Nature Portfolio
Subjects:	38/15 38/39 631/67/2324 631/67/2327 64/110 64/60 692/4028/67/589/466 692/499 692/53/2422 82/58 Aged Animals Cell Line, Tumor Cell Proliferation - drug effects Cell Proliferation - genetics Diet Diet, High-Fat - adverse effects Disease Progression Gene Expression Regulation, Neoplastic - drug effects High fat diet Humanities and Social Sciences Humans Low fat diet Male Metabolism Metabolome - drug effects Mice, Transgenic Middle Aged Mimicry multidisciplinary Myc protein Nutrient deficiency Prostate cancer Prostatic Neoplasms - etiology Prostatic Neoplasms - genetics Prostatic Neoplasms - metabolism Proto-Oncogene Proteins c-myc - genetics Proto-Oncogene Proteins c-myc - metabolism Rewiring Science Science (multidisciplinary) Transcription Tumor Burden - drug effects Tumor Burden - genetics Tumors
ISSN:	2041-1723, 2041-1723
Online Access:	Get full text
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Abstract	Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet. Prostate cancer progression may be enhanced by a high-fat diet. Here the authors show that a diet high in saturated fats enhance the MYC-driven transcriptional program, a feature that independently predicts prostate cancer progression and death.
AbstractList	Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet. Prostate cancer progression may be enhanced by a high-fat diet. Here the authors show that a diet high in saturated fats enhance the MYC-driven transcriptional program, a feature that independently predicts prostate cancer progression and death. Prostate cancer progression may be enhanced by a high-fat diet. Here the authors show that a diet high in saturated fats enhance the MYC-driven transcriptional program, a feature that independently predicts prostate cancer progression and death. Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet. Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet. Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet. Prostate cancer progression may be enhanced by a high-fat diet. Here the authors show that a diet high in saturated fats enhance the MYC-driven transcriptional program, a feature that independently predicts prostate cancer progression and death. Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet.Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression and mortality, but the molecular underpinnings of this association are poorly understood. Here, we demonstrate in a murine prostate cancer model, that high-fat diet (HFD) enhances the MYC transcriptional program through metabolic alterations that favour histone H4K20 hypomethylation at the promoter regions of MYC regulated genes, leading to increased cellular proliferation and tumour burden. Saturated fat intake (SFI) is also associated with an enhanced MYC transcriptional signature in prostate cancer patients. The SFI-induced MYC signature independently predicts prostate cancer progression and death. Finally, switching from a high-fat to a low-fat diet, attenuates the MYC transcriptional program in mice. Our findings suggest that in primary prostate cancer, dietary SFI contributes to tumour progression by mimicking MYC over expression, setting the stage for therapeutic approaches involving changes to the diet.
ArticleNumber	4358
Author	Giunchi, Francesca Karnes, R. Jeffrey Kantoff, Philip W. Alshalalfa, Mohammed Takhar, Mandeep Syamala, Sudeepa Ross, Ashley Yang, Meng Ebot, Ericka M. Ellis, Leigh Labbé, David P. Reyes, Jaime M. Den, Robert B. Cacciatore, Stefano Erho, Nicholas Fiorentino, Michelangelo Freedland, Stephen J. DʼAmico, Anthony V. Chavarro, Jorge E. Lin, Charles Y. Lehrer, Jonathan Bradner, James E. Creech, Amanda L. Jaffe, Jacob D. Loda, Massimo Schaeffer, Edward M. Davicioni, Elai Karoly, Edward D. Spratt, Daniel E. Brown, Myles Zadra, Giorgia Mucci, Lorelei A. Gibb, Ewan A. Elfandy, Habiba
Author_xml	– sequence: 1 givenname: David P. orcidid: 0000-0001-8864-8765 surname: Labbé fullname: Labbé, David P. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute, Division of Urology, Department of Surgery, McGill University and Research Institute of the McGill University Health Centre – sequence: 2 givenname: Giorgia orcidid: 0000-0002-8123-1358 surname: Zadra fullname: Zadra, Giorgia organization: Department of Oncologic Pathology, Dana-Farber Cancer Institute, Department of Pathology, Brigham and Women’s Hospital – sequence: 3 givenname: Meng surname: Yang fullname: Yang, Meng organization: Department of Nutrition, Harvard T.H. Chan School of Public Health – sequence: 4 givenname: Jaime M. orcidid: 0000-0001-7895-2472 surname: Reyes fullname: Reyes, Jaime M. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 5 givenname: Charles Y. surname: Lin fullname: Lin, Charles Y. organization: Department of Molecular and Human Genetics, Baylor College of Medicine – sequence: 6 givenname: Stefano orcidid: 0000-0001-7052-7156 surname: Cacciatore fullname: Cacciatore, Stefano organization: Cancer Genomics Group, International Centre for Genetic Engineering and Biotechnology – sequence: 7 givenname: Ericka M. surname: Ebot fullname: Ebot, Ericka M. organization: Department of Epidemiology, Harvard T.H. Chan School of Public Health – sequence: 8 givenname: Amanda L. surname: Creech fullname: Creech, Amanda L. organization: The Broad Institute of MIT and Harvard University – sequence: 9 givenname: Francesca surname: Giunchi fullname: Giunchi, Francesca organization: Pathology Service, Addarii Institute of Oncology, S-Orsola-Malpighi Hospital – sequence: 10 givenname: Michelangelo surname: Fiorentino fullname: Fiorentino, Michelangelo organization: Pathology Service, Addarii Institute of Oncology, S-Orsola-Malpighi Hospital – sequence: 11 givenname: Habiba surname: Elfandy fullname: Elfandy, Habiba organization: Department of Oncologic Pathology, Dana-Farber Cancer Institute – sequence: 12 givenname: Sudeepa surname: Syamala fullname: Syamala, Sudeepa organization: Department of Oncologic Pathology, Dana-Farber Cancer Institute – sequence: 13 givenname: Edward D. surname: Karoly fullname: Karoly, Edward D. organization: Metabolon – sequence: 14 givenname: Mohammed surname: Alshalalfa fullname: Alshalalfa, Mohammed organization: Decipher Biosciences – sequence: 15 givenname: Nicholas surname: Erho fullname: Erho, Nicholas organization: Decipher Biosciences – sequence: 16 givenname: Ashley surname: Ross fullname: Ross, Ashley organization: James Buchanan Brady Urological Institute, Johns Hopkins Medical Institutions – sequence: 17 givenname: Edward M. surname: Schaeffer fullname: Schaeffer, Edward M. organization: Northwestern University Feinberg School of Medicine – sequence: 18 givenname: Ewan A. surname: Gibb fullname: Gibb, Ewan A. organization: Decipher Biosciences – sequence: 19 givenname: Mandeep surname: Takhar fullname: Takhar, Mandeep organization: Decipher Biosciences – sequence: 20 givenname: Robert B. surname: Den fullname: Den, Robert B. organization: Department of Radiation Oncology, Sidney Kimmel Medical College at Thomas Jefferson University – sequence: 21 givenname: Jonathan surname: Lehrer fullname: Lehrer, Jonathan organization: Decipher Biosciences – sequence: 22 givenname: R. 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Jeffrey organization: Department of Urology, Mayo Clinic Rochester – sequence: 23 givenname: Stephen J. surname: Freedland fullname: Freedland, Stephen J. organization: Department of Surgery, Division of Urology, Center for Integrated Research on Cancer and Lifestyle, Samuel Oschin Comprehensive Cancer Center, Cedars-Sinai Medical Center, Surgery Section, Durham Veteran Affairs Medical Center – sequence: 24 givenname: Elai surname: Davicioni fullname: Davicioni, Elai organization: Decipher Biosciences – sequence: 25 givenname: Daniel E. surname: Spratt fullname: Spratt, Daniel E. organization: Department of Radiation Oncology, University of Michigan – sequence: 26 givenname: Leigh orcidid: 0000-0003-4739-5049 surname: Ellis fullname: Ellis, Leigh organization: Department of Oncologic Pathology, Dana-Farber Cancer Institute, Department of Pathology, Brigham and Women’s Hospital, The Broad Institute of MIT and Harvard University – sequence: 27 givenname: Jacob D. orcidid: 0000-0001-9845-1210 surname: Jaffe fullname: Jaffe, Jacob D. organization: The Broad Institute of MIT and Harvard University – sequence: 28 givenname: Anthony V. surname: DʼAmico fullname: DʼAmico, Anthony V. organization: Department of Radiation Oncology, Dana-Farber Cancer Institute and Brigham and Women’s Hospital, Harvard Medical School – sequence: 29 givenname: Philip W. surname: Kantoff fullname: Kantoff, Philip W. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Department of Medicine, Memorial Sloan Kettering Cancer Center – sequence: 30 givenname: James E. orcidid: 0000-0002-2718-4415 surname: Bradner fullname: Bradner, James E. organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School – sequence: 31 givenname: Lorelei A. surname: Mucci fullname: Mucci, Lorelei A. organization: Department of Epidemiology, Harvard T.H. Chan School of Public Health, Channing Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 32 givenname: Jorge E. surname: Chavarro fullname: Chavarro, Jorge E. organization: Department of Nutrition, Harvard T.H. Chan School of Public Health, Department of Epidemiology, Harvard T.H. Chan School of Public Health, Channing Division of Network Medicine, Brigham and Women’s Hospital, Harvard Medical School – sequence: 33 givenname: Massimo surname: Loda fullname: Loda, Massimo email: mloda@med.cornell.edu organization: Department of Oncologic Pathology, Dana-Farber Cancer Institute, Department of Pathology, Brigham and Women’s Hospital, The Broad Institute of MIT and Harvard University, Department of Pathology and Laboratory Medicine, Weil Cornell Medicine, New York Presbyterian-Weill Cornell Campus – sequence: 34 givenname: Myles surname: Brown fullname: Brown, Myles email: myles_brown@dfci.harvard.edu organization: Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Center for Functional Cancer Epigenetics, Dana-Farber Cancer Institute
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/31554818$$D View this record in MEDLINE/PubMed
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Snippet	Systemic metabolic alterations associated with increased consumption of saturated fat and obesity are linked with increased risk of prostate cancer progression... Prostate cancer progression may be enhanced by a high-fat diet. Here the authors show that a diet high in saturated fats enhance the MYC-driven transcriptional...
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Title	High-fat diet fuels prostate cancer progression by rewiring the metabolome and amplifying the MYC program
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