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Integrative Clinical Genomics of Advanced Prostate Cancer
Open accessAbstract
Toward development of a precision medicine framework for metastatic, castration-resistant prostate cancer (mCRPC), we established a multi-institutional clinical sequencing infrastructure to conduct prospective whole-exome and transcriptome sequencing of bone or soft tissue tumor biopsies from a cohort of 150 mCRPC affected individuals. Aberrations of AR, ETS genes, TP53, and PTEN were frequent (40%-60% of cases), with TP53 and AR alterations enriched in mCRPC compared to primary prostate cancer. We identified new genomic alterations in PIK3CA/B, R-spondin, BRAF/RAF1, APC, β-catenin, and ZBTB16/PLZF. Moreover, aberrations of BRCA2, BRCA1, and ATM were observed at substantially higher frequencies (19.3% overall) compared to those in primary prostate cancers. 89% of affected individuals harbored a clinically actionable aberration, including 62.7% with aberrations in AR, 65% in other cancer-related genes, and 8% with actionable pathogenic germline alterations. This cohort study provides clinically actionable information that could impact treatment decisions for these affected individuals.
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“The androgen receptor (AR) is a critical driver of prostate cancer (PCa).”
From Genome-scale CRISPR screens identify PTGES3 as a direct modulator of androgen receptor function in advanced prostate cancer (2025) · cites this paper as [1]
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Self-citationIncreased Survival with Enzalutamide in Prostate Cancer after Chemotherapy
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Self-citationAbiraterone and Increased Survival in Metastatic Prostate Cancer
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Self-citationRecurrent Fusion of TMPRSS2 and ETS Transcription Factor Genes in Prostate Cancer
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Self-citationIntegrative Genomic Profiling of Human Prostate Cancer
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Self-citationInhibition of Poly(ADP-Ribose) Polymerase in Tumors from BRCA Mutation Carriers
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Self-citationEnzalutamide in Metastatic Prostate Cancer before Chemotherapy
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Self-citationAbiraterone in Metastatic Prostate Cancer without Previous Chemotherapy
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Self-citationAR-V7 and Resistance to Enzalutamide and Abiraterone in Prostate Cancer
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Self-citationMutation of the Androgen-Receptor Gene in Metastatic Androgen-Independent Prostate Cancer
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Self-citationRecurrent R-spondin fusions in colon cancer
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Self-citationDistinct classes of chromosomal rearrangements create oncogenic ETS gene fusions in prostate cancer
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Self-citationCastro, E., Goh, C. L., Olmos, D., Saunders, E. J., Leongamornlert, D. A., Tymrakiewicz, M., Mahmud, N., Dadaev, T., Govindasami, K., Guy, M., et al. (2013) · Journal of Clinical Oncology · doi:10.1200/jco.2012.43.1882 · Cited by 854
Targeting Wnt-driven cancer through the inhibition of Porcupine by LGK974
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“Affected individuals s with aberrations in RNF43, ZNRF3, or RSPO2 (overall 6% of affected individuals) are predicted to respond to porcupine inhibitors (Liu et al., 2013).”
TopHat-Fusion: an algorithm for discovery of novel fusion transcripts
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“Paired-end transcriptome sequencing reads were aligned to the human reference genome (GRCh37/hg19) using a RNA-seq spliced read mapper Tophat2 (Kim and Salzberg, 2011) (Tophat 2.0.4), with ‘‘–fusion-search’’ option turned on to detect potential gene fusion transcripts.”
MethodInfluentialIntegrated genomic characterization of adrenocortical carcinoma
Assié, G., Letouzé, E., Fassnacht, M., Jouinot, A., Luscap, W., Barreau, O., Omeiri, H., Rodriguez, S., Perlemoine, K., René-Corail, F., et al. (2014) · Nature Genetics · doi:10.1038/ng.2953 · Cited by 732 · cited 1×
“Through integrative analysis, we identified alterations in RNF43 and ZNRF3, which were recently described in colorectal, endometrial, and adrenocortical cancers (Assié et al., 2014; Giannakis et al., 2014) and were mutually exclusive with APC alterations (Figure 6A).”
Personalized Oncology Through Integrative High-Throughput Sequencing: A Pilot Study
Roychowdhury, S., Iyer, M. K., Robinson, D. R., Lonigro, R. J., Wu, Y.-M., Cao, X., Sundaram, S. K., Sam, L. T., Balbin, O. A., Quist, M. J., et al. (2011) · Science Translational Medicine · doi:10.1126/scitranslmed.3003161 · Cited by 638 · cited 1×
“Interestingly, even when AR was not considered, 65% of cases harbored a putatively clinically actionable alteration (defined as predicting response or resistance to a therapy, having diagnostic or prognostic utility across tumor types) (Table S8) (Roychowdhury et al., 2011; Van Allen et al., 2014c).”
Self-citationSomatic ERCC2 Mutations Correlate with Cisplatin Sensitivity in Muscle-Invasive Urothelial Carcinoma
Allen, E. M. V., Mouw, K. W., Kim, P., Iyer, G., Wagle, N., Al‐Ahmadie, H. A., Zhu, C., Ostrovnaya, I., Kryukov, G. V., O’Connor, K. W., et al. (2014) · Cancer Discovery · doi:10.1158/2159-8290.cd-14-0623 · Cited by 630
Self-citationProposed Morphologic Classification of Prostate Cancer With Neuroendocrine Differentiation
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“7%) exhibited small-cell neuroendocrine features (Epstein et al., 2014) (Figure 1D).”
Self-citationPTEN-deficient cancers depend on PIK3CB
Wee, S., Wiederschain, D., Maira, S., Loo, A. T., Miller, C., deBeaumont, R. S., Stegmeier, F., Yao, Y.-M. M., & Lengauer, C. (2008) · Proceedings of the National Academy of Sciences of the United States of America · doi:10.1073/pnas.0802655105 · Cited by 565 · cited 12×
“This included biallelic loss of PTEN, as well as hotspot mutations, amplifications and activating fusions in PIK3CA, and p.E17K activating mutations in AKT1 (Figure S2).”
InfluentialAllen, E. M. V., Wagle, N., Stojanov, P., Perrin, D., Cibulskis, K., Marlow, S., Jané‐Valbuena, J., Friedrich, D. C., Kryukov, G. V., Carter, S. L., et al. (2014) · Nature Medicine · doi:10.1038/nm.3559 · Cited by 533
Self-citationRNF43 is frequently mutated in colorectal and endometrial cancers
Giannakis, M., Hodis, E., Mu, X. J., Yamauchi, M., Rosenbluh, J., Cibulskis, K., Saksena, G., Lawrence, M. S., Qian, Z. R., Nishihara, R., et al. (2014) · Nature Genetics · doi:10.1038/ng.3127 · Cited by 490
Self-citationRearrangements of the RAF kinase pathway in prostate cancer, gastric cancer and melanoma
Palanisamy, N., Ateeq, B., Sundaram, S. K., Pflueger, D., Ramnarayanan, K., Shankar, S., Han, B., Cao, Q., Cao, X., Suleman, K., et al. (2010) · Nature Medicine · doi:10.1038/nm.2166 · Cited by 460 · cited 1×
“RAF kinase fusions in 3% of mCPRC affected individuals would suggest the use of pan-RAF inhibitors or MEK inhibitors (Palanisamy et al., 2010).”
Self-citationBeltran, H., Yelensky, R., Frampton, G. M., Park, K., Downing, S. R., MacDonald, T. Y., Jarosz, M. V., Lipson, D., Tagawa, S. T., Nanus, D. M., et al. (2012) · European Urology · doi:10.1016/j.eururo.2012.08.053 · Cited by 450
Self-citationthe ICGC Prostate Group, Cooper, C. S., Eeles, R. A., Wedge, D. C., Loo, P. V., Gundem, G., Alexandrov, L. B., Kremeyer, B., Butler, A. P., Lynch, A. G., et al. (2015) · Nature Genetics · doi:10.1038/ng.3221 · Cited by 431 · cited 14×
“This will require iterative sampling of pre-treatment and resistant tumors from matching affected individuals and may warrant multire- 1224 Cell 161, 1215–1228, May 21, 2015 ª2015 Elsevier Inc. gional biopsies from affected individuals (if feasible) given heterogeneity in mCRPC (Carreira et al., 2014; Gundem et al., 2…”
InfluentialSelf-citationTracking the origins and drivers of subclonal metastatic expansion in prostate cancer
Hong, M. K. H., Macintyre, G., Wedge, D. C., Loo, P. V., Patel, K., Lunke, S., Alexandrov, L. B., Sloggett, C., Cmero, M., Marass, F., et al. (2015) · Nature Communications · doi:10.1038/ncomms7605 · Cited by 367 · cited 1×
“, 1995) and in the androgen signaling pathway (Beltran et al., 2013; Grasso et al., 2012; Gundem et al., 2015; Hong et al., 2015), although these studies were performed predominantly using autopsy samples or preclinical models with limited cohort sizes.”
Copy number alteration burden predicts prostate cancer relapse
Hieronymus, H., Schultz, N. D., Gopalan, A., Carver, B. S., Chang, M. T., Xiao, Y., Heguy, A., Huberman, K. H., Bernstein, M. L., Assel, M. J., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1411446111 · Cited by 366 · cited 1×
“…additional alterations in AR (Taplin et al., 1995) and in the androgen signaling pathway (Beltran et al., 2013; Grasso et al., 2012; Gundem et al., 2015; Hong et al., 2015), although these studies were performed predominantly using autopsy samples or preclinical models with limited cohort sizes.”
Self-citationBeta-catenin mutations in human prostate cancer.
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Tumor clone dynamics in lethal prostate cancer
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“functional AR mutations (T878A and Q903H), which may further suggest intra-tumor heterogeneity emerging in the CRPC setting (Carreira et al., 2014).”
Self-citationLalonde, E., Ishkanian, A. S., Sykes, J., Fraser, M., Ross-Adams, H., Erho, N., Dunning, M. J., Halim, S., Lamb, A. D., Moon, N. C., et al. (2014) · The Lancet Oncology · doi:10.1016/s1470-2045(14)71021-6 · Cited by 342 · cited 1×
“Although certain primary prostate cancer alterations or signatures have prognostic clinical significance (Hieronymus et al., 2014; Lalonde et al., 2014), the therapeutic impact of primary prostate cancer genomic events has not yet been realized.”
Weston, V., Oldreive, C., Skowrońska, A., Oscier, D. G., Pratt, G., Dyer, M. J. S., Smith, G. C. M., Powell, J. E., Rudzki, Z., Kearns, P. R., et al. (2010) · Blood · doi:10.1182/blood-2010-01-265769 · Cited by 304 · cited 2×
“This cohort study provides clinically actionable information that could impact treatment decisions for these affected individuals.”
Complex MSH2 and MSH6 mutations in hypermutated microsatellite unstable advanced prostate cancer
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“Interestingly, three out of four mCRPC tumors exhibited hypermutation and harbored alterations in the mismatch repair pathway genes MLH1 or MSH2 (Figures 2 and 7C), corroborating a recent report identifying structural alterations in MSH2 and MSH6 mismatch repair genes in hypermutated prostate cancers (Pritchard et al.…”
Self-citationSchwartz, S., Wongvipat, J., Trigwell, C. B., Hancox, U. J., Carver, B. S., Rodrik-Outmezguine, V. S., Will, M., Yellen, P., de Stanchina, E., Baselga, J. M., et al. (2014) · Cancer Cell · doi:10.1016/j.ccell.2014.11.008 · Cited by 250
Self-citationGeng, C., He, B., Xu, L., Barbieri, C. E., Eedunuri, V. K., Chew, S. A., Zimmermann, M., Bond, R., Shou, J., Li, C., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1304502110 · Cited by 243
Self-citationDiscovery of non-ETS gene fusions in human prostate cancer using next-generation RNA sequencingPreprint
Pflueger, D., Terry, S., Sboner, A., Habegger, L., Esgueva, R., Lin, P.-C., Svensson, M. A., Kitabayashi, N., Moss, B. J., MacDonald, T. Y., et al. (2010) · Genome Research · doi:10.1101/gr.110684.110 · Cited by 197 · cited 1×
“Multiple studies have identified recurrent somatic mutations, copy number alterations, and oncogenic structural DNA rearrangements (chromoplexy) in primary prostate cancer (Baca et al., 2013; Barbieri et al., 2012; Berger et al., 2011; Cooper et al., 2015; Pflueger et al., 2011; Taylor et al., 2010; Tomlins et al., 20…”
Self-citationTargeting cell cycle and hormone receptor pathways in cancer
Comstock, C. E. S., Augello, M. A., Goodwin, J. F., de Leeuw, R., Schiewer, M. J., Ostrander, W. F., Burkhart, R. A., McClendon, A. K., McCue, P. A., Trabulsi, E. J., et al. (2013) · Oncogene · doi:10.1038/onc.2013.83 · Cited by 116
Characterization of KRAS Rearrangements in Metastatic Prostate Cancer
Wang, X.-S., Shankar, S., Dhanasekaran, S. M., Ateeq, B., Sasaki, A. T., Jing, X., Robinson, D., Cao, Q., Prensner, J. R., Yocum, A. K., et al. (2011) · Cancer Discovery · doi:10.1158/2159-8274.cd-10-0022 · Cited by 106
Self-citationDetection of Somatic Copy Number Alterations in Cancer Using Targeted Exome Capture Sequencing
Lonigro, R. J., Grasso, C. S., Robinson, D. R., Jing, X., Wu, Y.-M., Cao, X., Quist, M. J., Tomlins, S. A., Pienta, K. J., & Chinnaiyan, A. M. (2011) · Neoplasia · doi:10.1593/neo.111252 · Cited by 87 · cited 1×
“Copy number aberrations were quantified and reported for each gene as the segmented normalized log2-transformed exon coverage ratios between each tumor sample and matched normal sample (Lonigro et al., 2011).”
Self-citationCharacterization of Bone Metastases from Rapid Autopsies of Prostate Cancer Patients
Mehra, R., Kumar‐Sinha, C., Shankar, S., Lonigro, R. J., Jing, X., Philips, N. E., Siddiqui, J., Han, B., Cao, X., Smith, D. C., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-3120 · Cited by 83 · cited 1×
“Prospective genomic characterization of fresh biopsy samples from living mCRPC affected individuals has been limited due to challenges in obtaining adequate tumor tissue, especially from bone biopsies (Mehra et al., 2011; Van Allen et al., 2014a), which is the most common site of metastatic disease.”
Self-citationHsieh, C.-L., Botta, G., Gao, S., Li, T., Allen, E. M. V., Treacy, D. J., Cai, C., He, H. H., Sweeney, C. J., Brown, M. A., et al. (2015) · Cancer Research · doi:10.1158/0008-5472.can-14-3602 · Cited by 65 · cited 1×
“, 2006), with loss of ZBTB16 upregulating the MAPK signaling pathway (Hsieh et al., 2015).”
Self-citationKikugawa, T., Kinugasa, Y., Shiraishi, K., Nanba, D., Nakashiro, K., Tanji, N., Yokoyama, M., & Higashiyama, S. (2006) · The Prostate · doi:10.1002/pros.20443 · Cited by 54 · cited 1×
“ZBTB16 has been previously implicated in prostate cancer tumorigenesis and androgen resistance in preclinical models (Cao et al., 2013; Kikugawa et al., 2006), with loss of ZBTB16 upregulating the MAPK signaling pathway (Hsieh et al.”
PLZF Mediates the PTEN/AKT/FOXO3a Signaling in Suppression of Prostate Tumorigenesis
Cao, J., Zhu, S., Zhou, W., Li, J., Liu, C., Xuan, H., Yan, J., Zheng, L., Zhou, L., Yu, J., et al. (2013) · PLoS ONE · doi:10.1371/journal.pone.0077922 · Cited by 38 · cited 1×
“ZBTB16 has been previously implicated in prostate cancer tumorigenesis and androgen resistance in preclinical models (Cao et al., 2013; Kikugawa et al., 2006), with loss of ZBTB16 upregulating the MAPK signaling pathway (Hsieh et al.”
Successful whole-exome sequencing from a prostate cancer bone metastasis biopsy
Allen, E. M. V., Foye, A., Wagle, N., Kim, W., Carter, S. L., McKenna, A., Simko, J. P., Garraway, L. A., & Febbo, P. G. (2013) · Prostate Cancer and Prostatic Diseases · doi:10.1038/pcan.2013.37 · Cited by 31 · cited 6×
“Prospective genomic characterization of fresh biopsy samples from living mCRPC affected individuals has been limited due to challenges in obtaining adequate tumor tissue, especially from bone biopsies (Mehra et al., 2011; Van Allen et al., 2014a), which is the most common site of metastatic disease.”
MethodInfluentialSelf-citationMateo, J., Hall, E., Sandhu, S. K., Omlin, A. G., Miranda, S., Carreira, S., GOODALL, J. C., Gillman, A., Mossop, H., Ralph, C., et al. (2014) · Annals of Oncology · doi:10.1093/annonc/mdu438.20 · Cited by 15 · cited 2×
“Importantly, multiple affected individuals in this trial who experienced clinical benefit harbored biallelic BRCA2 loss, providing further evidence of clinical actionability (Mateo et al., 2014).”
Self-citationProstate cancer-associated markers.
Chu, T. M. (1990) · PubMed · Cited by 8
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Self-citation
Metadata
- Authors
- Robinson, D., Van Allen, E. M., Wu, Y.-M., Schultz, N., Lonigro, R. J., Mosquera, J.-M., Montgomery, B., Taplin, M.-E., Pritchard, C. C., Attard, G., Beltran, H., Abida, W., Bradley, R. K., Vinson, J., Cao, X., Vats, P., Kunju, L. P., Hussain, M., Feng, F. Y., Tomlins, S. A., Cooney, K. A., Smith, D. C., Brennan, C., Siddiqui, J., Mehra, R., Chen, Y., Rathkopf, D. E., Morris, M. J., Solomon, S. B., Durack, J. C., Reuter, V. E., Gopalan, A., Gao, J., Loda, M., Lis, R. T., Bowden, M., Balk, S. P., Gaviola, G., Sougnez, C., Gupta, M., Yu, E. Y., Mostaghel, E. A., Cheng, H. H., Mulcahy, H., True, L. D., Plymate, S. R., Dvinge, H., Ferraldeschi, R., Flohr, P., Miranda, S., Zafeiriou, Z., Tunariu, N., Mateo, J., Perez-Lopez, R., Demichelis, F., Robinson, B. D., Schiffman, M., Nanus, D. M., Tagawa, S. T., Sigaras, A., Eng, K. W., Elemento, O., Sboner, A., Heath, E. I., Scher, H. I., Pienta, K. J., Kantoff, P., de Bono, J. S., Rubin, M. A., Nelson, P. S., Garraway, L. A., Sawyers, C. L., & Chinnaiyan, A. M.
- Affiliations
- University of Michigan (US)
- Memorial Sloan Kettering Cancer Center (US)
- NewYork–Presbyterian Hospital (US)
- University of Washington (US)
- Dana-Farber Cancer Institute (US)
- Royal Marsden NHS Foundation Trust (GB)
- Howard Hughes Medical Institute (US)
- Broad Institute (US)
- Brigham and Women's Hospital (US)
- Beth Israel Deaconess Medical Center (US)
- University of Washington Medical Center (US)
- University of Trento (IT)
- Cornell University (US)
- Wayne State University (US)
- Johns Hopkins University (US)
- Corresponding author
- Sawyers, Charles L.
- Chinnaiyan, Arul M.
- ORCID
- Robinson, Dan
- Schultz, Nikolaus
- Mosquera, Juan-Miguel
- Montgomery, Bruce
- Taplin, Mary-Ellen
- Pritchard, Colin C.
- Attard, Gerhardt
- Beltran, Himisha
- Abida, Wassim
- Bradley, Robert K.
- Vinson, Jake
- Cao, Xuhong
- Vats, Pankaj
- Kunju, Lakshmi P.
- Hussain, Maha
- Feng, Felix Y.
- Tomlins, Scott A.
- Cooney, Kathleen A.
- Smith, David C.
- Brennan, Christine
- Siddiqui, Javed
- Mehra, Rohit
- Chen, Yu
- Rathkopf, Dana E.
- Morris, Michael J.
- Solomon, Stephen B.
- Durack, Jeremy C.
- Gopalan, Anuradha
- Gao, Jianjiong
- Loda, Massimo
- Lis, Rosina T.
- Bowden, Michaela
- Gupta, Manaswi
- Yu, Evan Y.
- Mostaghel, Elahe A.
- Cheng, Heather H.
- Mulcahy, Hyojeong
- True, Lawrence D.
- Plymate, Stephen R.
- Dvinge, Heidi
- Flohr, Penny
- Miranda, Susana
- Zafeiriou, Zafeiris
- Tunariu, Nina
- Demichelis, Francesca
- Robinson, Brian D.
- Schiffman, Marc
- Nanus, David M.
- Tagawa, Scott T.
- Sigaras, Alexandros
- Eng, Kenneth W.
- Elemento, Olivier
- Sboner, Andrea
- Heath, Elisabeth I.
- Scher, Howard I.
- Pienta, Kenneth J.
- Kantoff, Philip
- Rubin, Mark A.
- Nelson, Peter S.
- Garraway, Levi A.
- Sawyers, Charles L.
- Chinnaiyan, Arul M.
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2015-05
- Volume
- 161
- Issue
- 5
- Pages
- 1215-1228
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4484602
- OpenAlex
- W1578291413
- Cited by
- 3,645
- References
- 64
- Citations by year
- 2026: 178 · 2025: 258 · 2024: 320 · 2023: 363 · 2022: 360 · 2021: 392 · 2020: 378 · 2019: 346 · 2018: 358 · 2017: 355 · 2016: 263 · 2015: 63
- FWCI
- 273.95
- Type
- journal article
- Language
- en
- Update notices
- erratum (2015-07-16)
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Iris (University of Trento) (submittedVersion)
- Funders
- Howard Hughes Medical Institute
- Cancer Research UK (13239)
- National Institute for Health and Care Research (CL-2008-22-001)
- Prostate Cancer UK (CEO13_2-002, PG12-49)
- National Institutes of Health (DP2OD002750)
- Medical Research Council (MR/M003272/1)
- National Human Genome Research Institute (UM1HG006508)
- National Cancer Institute (P50 CA 90381, R01CA136578, L30 CA111031, K08CA188615, R21CA128352, U01CA111275, P50CA090381, R01CA131945, UO1CA111275, L30 CA103810, R01CA116337, R01CA129435, P50CA069568, K08CA115927, R01CA092629, R01CA155169, R01CA193910, R01CA085912, P30CA008748, P01CA163227, P50CA097186, P50CA186786, P50CA092629, P30CA006516, R01CA193837)
- National Institute of General Medical Sciences (T32GM007266, R01GM107427)
- 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
- metastatic castration-resistant prostate cancer, exome sequencing, transcriptome sequencing, actionable genomic alterations, androgen receptor alterations, ETS gene fusions, TP53, PTEN, R-spondin, APC, β-catenin, BRCA2, BRCA1, ATM, germline pathogenic variants, precision medicine
- MeSH terms
- Humans, Male, Mutation, Neoplasm Metastasis, Cohort Studies, Gene Expression Profiling, Prostatic Neoplasms, Castration-Resistant
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