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Reprogramming of the FOXA1 cistrome in treatment-emergent neuroendocrine prostate cancer

Sylvan Baca, David Takeda, Ji-Heui Seo, Justin Hwang, Sheng Yu Ku, Rand Arafeh, Taylor Arnoff, Supreet Agarwal, Connor Bell, Edward O'Connor, Xintao Qiu, Sarah Abu Alaiwi, Rosario Corona, Marcos Fonseca, Claudia Giambartolomei, Paloma Cejas, Klothilda Lim, Monica He, Anjali Sheahan, Amin Nassar, Jacob Berchuck, Lisha Brown, Holly Nguyen, Ilsa Coleman, Arja Kaipainen, Navonil De Sarkar, Peter Nelson, Colm Morrissey, Keegan Korthauer, Mark Pomerantz, Leigh Ellis, Bogdan Pasaniuc, Kate Lawrenson, Kathleen Kelly, Amina Zoubeidi, William Hahn, Himisha Beltran, Henry Long, Myles Brown, Eva Corey, Matthew Freedman,

Lineage plasticity, the ability of a cell to alter its identity, is an increasingly common mechanism of adaptive resistance to targeted therapy in cancer. An archetypal example is the development of neuroendocrine prostate cancer (NEPC) after treatment of prostate adenocarcinoma (PRAD) with inhibitors of androgen signaling. NEPC is an aggressive ... Read more >>

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FOXA2 promotes prostate cancer growth in the bone.

Zachary M Connelly, Renjie Jin, Jianghong Zhang, Shu Yang, Siyuan Cheng, Mingxia Shi, Justin Mm Cates, Runhua Shi, David J DeGraff, Peter S Nelson, Yunlong Liu, Colm Morrissey, Eva Corey, Xiuping Yu,

Bone metastasis frequently occurs in advanced-stage prostate cancer (PCa) patients. Understanding the mechanisms that promote PCa-mediated bone destruction is important for the identification of therapeutic targets against this lethal disease. We found that forkhead box A2 (FOXA2) is expressed in a subset of PCa bone metastasis specimens. To determine the ... Read more >>

Am J Transl Res (American journal of translational research)
[2020, 12(9):5619-5629]

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Subtype Heterogeneity and Epigenetic Convergence in Neuroendocrine Prostate Cancer

Paloma Cejas, Yingtian Xie, Alba Font-Tello, Klothilda Lim, Sudeepa Syamala, Xintao Qiu, Alok Tewari, Neel Shah, Holly Nguyen, Radhika Patel, Lisha Brown, Ilsa Coleman, Wenzel Hackeng, Lodewijk Brosens, Koen M.A. Dreijerink, Leigh Ellis, Sarah Abou Alaiwi, Ji-Heui Seo, Mark Pomerantz, Alessandra Dall’Agnese, Jett Crowdis, Eliezer Van Allen, Joaquim Bellmunt, Colm Morrisey, Peter Nelson, James DeCaprio, Anna Farago, Nicholas Dyson, Benjamin Drapkin, Shirley Liu, Matthew Freedman, Michael Haffner, Eva Corey, Myles Brown, Henry Long,

Abstract Neuroendocrine carcinomas (NEC) are tumors expressing markers of neuronal differentiation that can arise at different anatomic sites but have strong histological and clinical similarities. Here we report the chromatin landscapes of a range of human NECs and show convergence to the activation of a common epigenetic program. With a ... Read more >>

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Chromatin binding of FOXA1 is promoted by LSD1-mediated demethylation in prostate cancer.

Shuai Gao, Sujun Chen, Dong Han, Zifeng Wang, Muqing Li, Wanting Han, Anna Besschetnova, Mingyu Liu, Feng Zhou, David Barrett, My Phu Luong, Jude Owiredu, Yi Liang, Musaddeque Ahmed, Jessica Petricca, Susan Patalano, Jill A Macoska, Eva Corey, Sen Chen, Steven P Balk, Housheng Hansen He, Changmeng Cai,

FOXA1 functions as a pioneer transcription factor by facilitating the access to chromatin for steroid hormone receptors, such as androgen receptor and estrogen receptor1-4, but mechanisms regulating its binding to chromatin remain elusive. LSD1 (KDM1A) acts as a transcriptional repressor by demethylating mono/dimethylated histone H3 lysine 4 (H3K4me1/2)5,6, but also ... Read more >>

Nat Genet (Nature genetics)
[2020, 52(10):1011-1017]

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Prostate cancer reactivates developmental epigenomic programs during metastatic progression.

Mark M Pomerantz, Xintao Qiu, Yanyun Zhu, David Y Takeda, Wenting Pan, Sylvan C Baca, Alexander Gusev, Keegan D Korthauer, Tesa M Severson, Gavin Ha, Srinivas R Viswanathan, Ji-Heui Seo, Holly M Nguyen, Baohui Zhang, Bogdan Pasaniuc, Claudia Giambartolomei, Sarah A Alaiwi, Connor A Bell, Edward P O'Connor, Matthew S Chabot, David R Stillman, Rosina Lis, Alba Font-Tello, Lewyn Li, Paloma Cejas, Andries M Bergman, Joyce Sanders, Henk G van der Poel, Simon A Gayther, Kate Lawrenson, Marcos A S Fonseca, Jessica Reddy, Rosario I Corona, Gleb Martovetsky, Brian Egan, Toni Choueiri, Leigh Ellis, Isla P Garraway, Gwo-Shu Mary Lee, Eva Corey, Henry W Long, Wilbert Zwart, Matthew L Freedman,

Epigenetic processes govern prostate cancer (PCa) biology, as evidenced by the dependency of PCa cells on the androgen receptor (AR), a prostate master transcription factor. We generated 268 epigenomic datasets spanning two state transitions-from normal prostate epithelium to localized PCa to metastases-in specimens derived from human tissue. We discovered that ... Read more >>

Nat Genet (Nature genetics)
[2020, 52(8):790-799]

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Taxane resistance in prostate cancer is mediated by decreased drug-target engagement.

Ada Gjyrezi, Fang Xie, Olga Voznesensky, Prateek Khanna, Carla Calagua, Yang Bai, Justin Kung, Jim Wu, Eva Corey, Bruce Montgomery, Sandrine Mace, Diego A Gianolio, Glenn J Bubley, Steven P Balk, Paraskevi Giannakakou, Rupal S Bhatt,

Despite widespread use of taxanes, mechanisms of action and resistance in vivo remain to be established, and there is no way of predicting who will respond to therapy. This study examined prostate cancer (PCa) xenografts and patient samples to identify in vivo mechanisms of taxane action and resistance. Docetaxel drug-target ... Read more >>

J. Clin. Invest. (The Journal of clinical investigation)
[2020, 130(6):3287-3298]

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Androgen receptor-induced integrin α6β1 and Bnip3 promote survival and resistance to PI3K inhibitors in castration-resistant prostate cancer.

Eric A Nollet, Marina Cardo-Vila, Sourik S Ganguly, Jack D Tran, Veronique V Schulz, Anne Cress, Eva Corey, Cindy K Miranti,

The androgen receptor (AR) is the major driver of prostate cancer growth and survival. However, almost all patients relapse with castration-resistant disease (CRPC) when treated with anti-androgen therapy. In CRPC, AR is often aberrantly activated independent of androgen. Targeting survival pathways downstream of AR could be a viable strategy to ... Read more >>

Oncogene (Oncogene)
[2020, 39(31):5390-5404]

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Telomere lengths differ significantly between small-cell neuroendocrine prostate carcinoma and adenocarcinoma of the prostate.

Christopher M Heaphy, Michael C Haffner, Mindy K Graham, David Lim, Christine Davis, Eva Corey, Jonathan I Epstein, Mario A Eisenberger, Hao Wang, Angelo M De Marzo, Alan K Meeker, Tamara L Lotan,

Small-cell neuroendocrine carcinoma (SCNC) of the prostate is an aggressive subtype with frequent TP53 mutation and RB1 inactivation; however, the molecular phenotype remains an area of investigation. Here, we compared telomere lengths in prostatic SCNC and usual-type prostatic adenocarcinoma (AdCa). We studied 32 cases of prostatic SCNC (including 11 cases ... Read more >>

Hum. Pathol. (Human pathology)
[2020, 101:70-79]

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The expression of YAP1 is increased in high-grade prostatic adenocarcinoma but is reduced in neuroendocrine prostate cancer.

Siyuan Cheng, Nestor Prieto-Dominguez, Shu Yang, Zachary M Connelly, Samantha StPierre, Bryce Rushing, Andy Watkins, Lawrence Shi, Meredith Lakey, Lyndsey Buckner Baiamonte, Tajammul Fazili, Aubrey Lurie, Eva Corey, Runhua Shi, Yunshin Yeh, Xiuping Yu,

BACKGROUND:After long-term androgen deprivation therapy, 25-30% prostate cancer (PCa) acquires an aggressive neuroendocrine (NE) phenotype. Dysregulation of YAP1, a key transcription coactivator of the Hippo pathway, has been related to cancer progression. However, its role in neuroendocrine prostate cancer (NEPC) has not been assessed. METHODS:Immunohistochemistry and bioinformatics analysis were conducted ... Read more >>

Prostate Cancer Prostatic Dis (Prostate cancer and prostatic diseases)
[2020, :]

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Targeting RET Kinase in Neuroendocrine Prostate Cancer.

Halena R VanDeusen, Johnny R Ramroop, Katherine L Morel, Song Yi Bae, Anjali V Sheahan, Zoi Sychev, Nathan A Lau, Larry C Cheng, Victor M Tan, Zhen Li, Ashley Petersen, John K Lee, Jung Wook Park, Rendong Yang, Justin H Hwang, Ilsa Coleman, Owen N Witte, Colm Morrissey, Eva Corey, Peter S Nelson, Leigh Ellis, Justin M Drake,

The increased treatment of metastatic castration-resistant prostate cancer (mCRPC) with second-generation antiandrogen therapies (ADT) has coincided with a greater incidence of lethal, aggressive variant prostate cancer (AVPC) tumors that have lost dependence on androgen receptor (AR) signaling. These AR-independent tumors may also transdifferentiate to express neuroendocrine lineage markers and are ... Read more >>

Mol Cancer Res (Molecular cancer research : MCR)
[2020, 18(8):1176-1188]

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Alternative splicing of LSD1+8a in neuroendocrine prostate cancer is mediated by SRRM4.

Daniel J Coleman, David A Sampson, Archana Sehrawat, Anbarasu Kumaraswamy, Duanchen Sun, Yuzhuo Wang, Jacob Schwartzman, Joshua Urrutia, Ahn R Lee, Ilsa M Coleman, Peter S Nelson, Xuesen Dong, Colm Morrissey, Eva Corey, Zheng Xia, Joel A Yates, Joshi J Alumkal,

Neuroendocrine prostate cancer (NEPC) is the most virulent form of prostate cancer. Importantly, our recent work examining metastatic biopsy samples demonstrates NEPC is increasing in frequency. In contrast to prostate adenocarcinomas that express a luminal gene expression program, NEPC tumors express a neuronal gene expression program. Despite this distinction, the ... Read more >>

Neoplasia (Neoplasia (New York, N.Y.))
[2020, 22(6):253-262]

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Combined TP53 and RB1 Loss Promotes Prostate Cancer Resistance to a Spectrum of Therapeutics and Confers Vulnerability to Replication Stress.

Michael D Nyquist, Alexandra Corella, Ilsa Coleman, Navonil De Sarkar, Arja Kaipainen, Gavin Ha, Roman Gulati, Lisa Ang, Payel Chatterjee, Jared Lucas, Colin Pritchard, Gail Risbridger, John Isaacs, Bruce Montgomery, Colm Morrissey, Eva Corey, Peter S Nelson,

Prostate cancers (PCs) with loss of the potent tumor suppressors TP53 and RB1 exhibit poor outcomes. TP53 and RB1 also influence cell plasticity and are frequently lost in PCs with neuroendocrine (NE) differentiation. Therapeutic strategies that address these aggressive variant PCs are urgently needed. Using deep genomic profiling of 410 ... Read more >>

Cell Rep (Cell reports)
[2020, 31(8):107669]

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Antitumor Activity of the IGF-1/IGF-2-Neutralizing Antibody Xentuzumab (BI 836845) in Combination with Enzalutamide in Prostate Cancer Models.

Ulrike Weyer-Czernilofsky, Marco H Hofmann, Katrin Friedbichler, Rosa Baumgartinger, Paul J Adam, Flavio Solca, Norbert Kraut, Holly M Nguyen, Eva Corey, Gang Liu, Cynthia C Sprenger, Stephen R Plymate, Thomas Bogenrieder,

Androgen deprivation therapy and second-generation androgen receptor signaling inhibitors such as enzalutamide are standard treatments for advanced/metastatic prostate cancer. Unfortunately, most men develop resistance and relapse; signaling via insulin-like growth factor (IGF) has been implicated in castration-resistant prostate cancer. We evaluated the antitumor activity of xentuzumab (IGF ligand-neutralizing antibody), alone ... Read more >>

Mol Cancer Ther (Molecular cancer therapeutics)
[2020, 19(4):1059-1069]

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Identification of Therapeutic Vulnerabilities in Small-cell Neuroendocrine Prostate Cancer.

Alexandra N Corella, Ma Victoria Andrea Cabiliza Ordonio, Ilsa Coleman, Jared M Lucas, Arja Kaipainen, Holly M Nguyen, Daniel Sondheim, Lisha G Brown, Lawrence D True, John K Lee, David MacPherson, Paul Nghiem, Roman Gulati, Colm Morrissey, Eva Corey, Peter S Nelson,

PURPOSE:Small-cell neuroendocrine prostate cancer (SCNPC) exhibits an aggressive clinical course and incidence rates seem to be increasing following resistance to potent androgen receptor (AR) antagonists. Currently, treatment options are limited and few model systems are available to identify new approaches for treatment. We sought to evaluate commonalities between SCNPC and ... Read more >>

Clin Cancer Res (Clinical cancer research : an official journal of the American Association for Cancer Research)
[2020, 26(7):1667-1677]

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The expression of YAP1 is increased in high-grade prostatic adenocarcinoma but is reduced in neuroendocrine prostate cancer

Siyuan Cheng, Nestor Prieto-Dominguez, Shu Yang, Zachary Connelly, Samantha StPierre, Bryce Rushing, Andy Watkins, Lawrence Shi, Meredith Lakey, Lyndsey Buckner Baiamonte, Tajammul Fazili, Aubrey Lurie, Eva Corey, Runhua Shi, Yunshin Yeh, Xiuping Yu,

ABSTRACT BACKGROUND After long-term androgen deprivation therapy, 25-30% prostate cancer (PCa) acquires an aggressive neuroendocrine (NE) phenotype. Dysregulation of YAP1, a key transcription coactivator of the Hippo pathway, has been related to cancer progression. However, its role in neuroendocrine prostate cancer (NEPC) has not been assessed. METHODS Immunohistochemistry was used ... Read more >>

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COMMD3:BMI1 Fusion and COMMD3 Protein Regulate C-MYC Transcription: Novel Therapeutic Target for Metastatic Prostate Cancer.

Syed Umbreen, Mudassir Meraj Banday, Anmbreen Jamroze, Adrian P Mansini, Arsheed A Ganaie, Marina G Ferrari, Raihana Maqbool, Firdous H Beigh, Paari Murugan, Colm Morrissey, Eva Corey, Badrinath R Konety, Mohammad Saleem,

Gene rearrangement is reported to be associated to the aggressive phenotype and poor prognosis in prostate cancer. We identified a gene fusion between a transcription repressor (BMI1) and transcriptional factor (COMMD3) in human prostate cancer. We show that COMMD3:BMI1 fusion expression is significantly increased in prostate cancer disease in an ... Read more >>

Mol. Cancer Ther. (Molecular cancer therapeutics)
[2019, 18(11):2111-2123]

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Hypoxia-Induced PIM Kinase and Laminin-Activated Integrin α6 Mediate Resistance to PI3K Inhibitors in Bone-Metastatic CRPC

Rachel Toth, Jack Tran, Michelle Muldong, Eric Nollet, Veronique Schulz, Corbin Jensen, Lori Hazelhurst, Eva Corey, Donald Durden, Christina Jamieson, Cindy Miranti, Noel Warfel,

ABSTRACT Bone-metastatic castration-resistant prostate cancer (CRPC) is lethal due to inherent resistance to androgen deprivation therapy, chemotherapy, and targeted therapies. Despite the fact that a majority of CRPC patients (approximately 70%) harbor a constitutively active PI3K survival pathway, targeting the PI3K/mTOR pathway has failed to increase overall survival in clinical ... Read more >>

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Hypoxia-induced PIM kinase and laminin-activated integrin α6 mediate resistance to PI3K inhibitors in bone-metastatic CRPC.

Rachel K Toth, Jack D Tran, Michelle T Muldong, Eric A Nollet, Veronique V Schulz, Corbin C Jensen, Lori A Hazlehurst, Eva Corey, Donald Durden, Christina Jamieson, Cindy K Miranti, Noel A Warfel,

Bone-metastatic castration-resistant prostate cancer (CRPC) is lethal due to inherent resistance to androgen deprivation therapy, chemotherapy, and targeted therapies. Despite the fact that a majority of CRPC patients (approximately 70%) harbor a constitutively active PI3K survival pathway, targeting the PI3K/mTOR pathway has failed to increase overall survival in clinical trials. ... Read more >>

(American journal of clinical and experimental urology)
[2019, 7(4):297-312]

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Durable Response of Enzalutamide-resistant Prostate Cancer to Supraphysiological Testosterone Is Associated with a Multifaceted Growth Suppression and Impaired DNA Damage Response Transcriptomic Program in Patient-derived Xenografts.

Hung-Ming Lam, Holly M Nguyen, Mark P Labrecque, Lisha G Brown, Ilsa M Coleman, Roman Gulati, Bryce Lakely, Daniel Sondheim, Payel Chatterjee, Brett T Marck, Alvin M Matsumoto, Elahe A Mostaghel, Michael T Schweizer, Peter S Nelson, Eva Corey,

BACKGROUND:Androgen deprivation therapy improves the survival of castration-resistant prostate cancer (CRPC) patients, yet ultimately fails with debilitating side effects. Supraphysiological testosterone (SPT)-based therapy produces clinical responses with improved quality of life in a subset of patients. Currently, no information defines a durable response to SPT. OBJECTIVE:To identify key molecular phenotypes ... Read more >>

Eur. Urol. (European urology)
[2020, 77(2):144-155]

Cited: 4 times

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Circular RNAs add diversity to androgen receptor isoform repertoire in castration-resistant prostate cancer.

Subing Cao, Tianfang Ma, Nathan Ungerleider, Claire Roberts, Margaret Kobelski, Lianjin Jin, Monica Concha, Xia Wang, Melody Baddoo, Holly M Nguyen, Eva Corey, Ladan Fazli, Elisa Ledet, Rubin Zhang, Jonathan L Silberstein, Wensheng Zhang, Kun Zhang, Oliver Sartor, Xuesen Dong, Erik K Flemington, Yan Dong,

Deregulated expression of circular RNAs (circRNAs) is associated with various human diseases, including many types of cancer. Despite their growing links to cancer, there has been limited characterization of circRNAs in metastatic castration-resistant prostate cancer, the major cause of prostate cancer mortality. Here, through the analysis of an exome-capture RNA-seq ... Read more >>

Oncogene (Oncogene)
[2019, 38(45):7060-7072]

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Molecular profiling stratifies diverse phenotypes of treatment-refractory metastatic castration-resistant prostate cancer.

Mark P Labrecque, Ilsa M Coleman, Lisha G Brown, Lawrence D True, Lori Kollath, Bryce Lakely, Holly M Nguyen, Yu C Yang, Rui M Gil da Costa, Arja Kaipainen, Roger Coleman, Celestia S Higano, Evan Y Yu, Heather H Cheng, Elahe A Mostaghel, Bruce Montgomery, Michael T Schweizer, Andrew C Hsieh, Daniel W Lin, Eva Corey, Peter S Nelson, Colm Morrissey,

Metastatic castration-resistant prostate cancer (mCRPC) is a heterogeneous disease with diverse drivers of disease progression and mechanisms of therapeutic resistance. We conducted deep phenotypic characterization of CRPC metastases and patient-derived xenograft (PDX) lines using whole genome RNA sequencing, gene set enrichment analysis and immunohistochemistry. Our analyses revealed five mCRPC phenotypes ... Read more >>

J. Clin. Invest. (The Journal of clinical investigation)
[2019, 129(10):4492-4505]

Cited: 4 times

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The androgen receptor regulates a druggable translational regulon in advanced prostate cancer.

Yuzhen Liu, Jessie L Horn, Kalyan Banda, Asha Z Goodman, Yiting Lim, Sujata Jana, Sonali Arora, Alexandre A Germanos, Lexiaochuan Wen, William R Hardin, Yu C Yang, Ilsa M Coleman, Robin G Tharakan, Elise Y Cai, Takuma Uo, Smitha P S Pillai, Eva Corey, Colm Morrissey, Yu Chen, Brett S Carver, Stephen R Plymate, Slobodan Beronja, Peter S Nelson, Andrew C Hsieh,

The androgen receptor (AR) is a driver of cellular differentiation and prostate cancer development. An extensive body of work has linked these normal and aberrant cellular processes to mRNA transcription; however, the extent to which AR regulates posttranscriptional gene regulation remains unknown. Here, we demonstrate that AR uses the translation ... Read more >>

Sci Transl Med (Science translational medicine)
[2019, 11(503):]

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Supraphysiological androgens suppress prostate cancer growth through androgen receptor-mediated DNA damage.

Payel Chatterjee, Michael T Schweizer, Jared M Lucas, Ilsa Coleman, Michael D Nyquist, Sander B Frank, Robin Tharakan, Elahe Mostaghel, Jun Luo, Colin C Pritchard, Hung-Ming Lam, Eva Corey, Emmanuel S Antonarakis, Samuel R Denmeade, Peter S Nelson,

Prostate cancer (PC) is initially dependent on androgen receptor (AR) signaling for survival and growth. Therapeutics designed to suppress AR activity serve as the primary intervention for advanced disease. However, supraphysiological androgen (SPA) concentrations can produce paradoxical responses leading to PC growth inhibition. We sought to discern the mechanisms by ... Read more >>

J. Clin. Invest. (The Journal of clinical investigation)
[2019, 129(10):4245-4260]

Cited: 5 times

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Targeting RET Kinase in Neuroendocrine Prostate Cancer

Halena VanDeusen, Johnny Ramroop, Katherine Morel, Anjali Sheahan, Zoi Sychev, Nathan Lau, Larry Cheng, Victor Tan, Zhen Li, Ashley Petersen, John Lee, Jung Wook Park, Rendong Yang, Ilsa Coleman, Owen Witte, Colm Morrissey, Eva Corey, Peter Nelson, Leigh Ellis, Justin Drake,

Abstract Increased treatment of metastatic castration resistant prostate cancer (mCRPC) with second-generation anti-androgen therapies (ADT) has coincided with a greater incidence of lethal, aggressive variant prostate cancer (AVPC) tumors that have lost androgen receptor (AR) signaling. AVPC tumors may also express neuroendocrine markers, termed neuroendocrine prostate cancer (NEPC). Recent evidence ... Read more >>

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Establishing a cryopreservation protocol for patient-derived xenografts of prostate cancer.

Laura H Porter, Mitchell G Lawrence, Hong Wang, Ashlee K Clark, Andrew Bakshi, Daisuke Obinata, David Goode, Melissa Papargiris, Mural, David Clouston, Andrew Ryan, Sam Norden, Eva Corey, Peter S Nelson, John T Isaacs, Jeremy Grummet, John Kourambas, Shahneen Sandhu, Declan G Murphy, David Pook, Mark Frydenberg, Renea A Taylor, Gail P Risbridger,

BACKGROUND:Serially transplantable patient-derived xenografts (PDXs) are invaluable preclinical models for studying tumor biology and evaluating therapeutic agents. As these models are challenging to establish from prostate cancer specimens, the ability to preserve them through cryopreservation has several advantages for ongoing research. Despite this, there is still uncertainty about the ability ... Read more >>

Prostate (The Prostate)
[2019, 79(11):1326-1337]

Cited: 1 time

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