Cited by 2,517Prostate Cancer Treatment and ResearchCancer Genomics and DiagnosticsChromatin Remodeling and Cancer

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The mutational landscape of lethal castration-resistant prostate cancer

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Grasso, Catherine S., Wu, Yi-Mi, Robinson, Dan R., Cao, Xuhong, Dhanasekaran, Saravana M., Khan, Amjad P., Quist, Michael J., Jing, Xiaojun, Lonigro, Robert J., Brenner, J. Chad, Asangani, Irfan A., Ateeq, Bushra, Chun, Sang Y., Siddiqui, Javed, Sam, Lee, Anstett, Matt, Mehra, Rohit, Prensner, John R., Palanisamy, Nallasivam, Ryslik, Gregory A., Vandin, Fabio, Raphael, Benjamin J., Kunju, Lakshmi P., Rhodes, Daniel R., Pienta, Kenneth J., Chinnaiyan, Arul M., Tomlins, Scott A.·2012·Nature

DOI 10.1038/nature11125PMC PMC3396711

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Abstract

Characterization of the prostate cancer transcriptome and genome has identified chromosomal rearrangements and copy number gains and losses, including ETS gene family fusions, PTEN loss and androgen receptor (AR) amplification, which drive prostate cancer development and progression to lethal, metastatic castration-resistant prostate cancer (CRPC). However, less is known about the role of mutations. Here we sequenced the exomes of 50 lethal, heavily pre-treated metastatic CRPCs obtained at rapid autopsy (including three different foci from the same patient) and 11 treatment-naive, high-grade localized prostate cancers. We identified low overall mutation rates even in heavily treated CRPCs (2.00 per megabase) and confirmed the monoclonal origin of lethal CRPC. Integrating exome copy number analysis identified disruptions of CHD1 that define a subtype of ETS gene family fusion-negative prostate cancer. Similarly, we demonstrate that ETS2, which is deleted in approximately one-third of CRPCs (commonly through TMPRSS2:ERG fusions), is also deregulated through mutation. Furthermore, we identified recurrent mutations in multiple chromatin- and histone-modifying genes, including MLL2 (mutated in 8.6% of prostate cancers), and demonstrate interaction of the MLL complex with the AR, which is required for AR-mediated signalling. We also identified novel recurrent mutations in the AR collaborating factor FOXA1, which is mutated in 5 of 147 (3.4%) prostate cancers (both untreated localized prostate cancer and CRPC), and showed that mutated FOXA1 represses androgen signalling and increases tumour growth. Proteins that physically interact with the AR, such as the ERG gene fusion product, FOXA1, MLL2, UTX (also known as KDM6A) and ASXL1 were found to be mutated in CRPC. In summary, we describe the mutational landscape of a heavily treated metastatic cancer, identify novel mechanisms of AR signalling deregulated in prostate cancer, and prioritize candidates for future study.

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Authors: Grasso, C. S., Wu, Y.-M., Robinson, D. R., Cao, X., Dhanasekaran, S. M., Khan, A. P., Quist, M. J., Jing, X., Lonigro, R. J., Brenner, J. C., Asangani, I. A., Ateeq, B., Chun, S. Y., Siddiqui, J., Sam, L., Anstett, M., Mehra, R., Prensner, J. R., Palanisamy, N., Ryslik, G. A., Vandin, F., Raphael, B. J., Kunju, L. P., Rhodes, D. R., Pienta, K. J., Chinnaiyan, A. M., & Tomlins, S. A.
Affiliations: University of Michigan (US)
Howard Hughes Medical Institute (US)
Yale University (US)
Brown University (US)
Corresponding author: Pienta, Kenneth J.
Chinnaiyan, Arul M.
ORCID: Grasso, Catherine S.
Robinson, Dan R.
Cao, Xuhong
Dhanasekaran, Saravana M.
Khan, Amjad P.
Jing, Xiaojun
Brenner, J. Chad
Asangani, Irfan A.
Ateeq, Bushra
Siddiqui, Javed
Mehra, Rohit
Prensner, John R.
Palanisamy, Nallasivam
Ryslik, Gregory A.
Vandin, Fabio
Raphael, Benjamin J.
Kunju, Lakshmi P.
Rhodes, Daniel R.
Pienta, Kenneth J.
Chinnaiyan, Arul M.
Tomlins, Scott A.
Venue: Nature
Publisher: Springer Science and Business Media LLC
Published: 2012-05-20
Volume: 487
Issue: 7406
Pages: 239-243
ISSN: 0028-0836 (ISSN-L)
1476-4687
DOI: 10.1038/nature11125
PMC: PMC3396711
OpenAlex: W2051025382
Cited by: 2,517
References: 23
Citations by year: 2026: 75 · 2025: 128 · 2024: 136 · 2023: 181 · 2022: 178 · 2021: 199 · 2020: 233 · 2019: 193 · 2018: 205 · 2017: 195 · 2016: 194 · 2015: 212 · 2014: 177 · 2013: 169 · 2012: 33
FWCI: 152.73
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.springer.com/tdm (tdm)
Locations: Nature (publishedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
RePEc: Research Papers in Economics (submittedVersion)
Padua Research Archive (University of Padova) (submittedVersion)
Funders: Howard Hughes Medical Institute
National Institutes of Health (5r01ca013287-14)
National Cancer Institute (P50-CA-69568, R01CA132874, U01CA111275, R01CA13287, P50CA069568, T32CA140044, P30CA046592, T32CA009676, U01CA113913)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Prostate Cancer Treatment and Research
Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords: castration-resistant prostate cancer, metastatic prostate cancer, somatic mutations, copy number alterations, chromatin modifiers, androgen receptor, FOXA1, KMT2D, TMPRSS2-ERG fusion, PTEN loss, androgen receptor amplification, chromosomal rearrangements
MeSH terms: Cells, Cultured, Humans, Male, Molecular Sequence Data, Mutation, Orchiectomy, Prostatic Neoplasms, Receptors, Androgen, Signal Transduction, Sequence Alignment, Cell Proliferation, Hepatocyte Nuclear Factor 3-alpha

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The mutational landscape of lethal castration-resistant prostate cancer

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