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Homing in on a Moving Target: Androgen Receptor Cistromic Plasticity in Prostate Cancer

ENDOCRINOLOGY (2022)

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Article Oncology

Detecting Neuroendocrine Prostate Cancer Through Tissue-Informed Cell-Free DNA Methylation Analysis

Jacob E. Berchuck et al.

Summary: This study reports a novel tissue-informed epigenetic approach for noninvasive detection of neuroendocrine prostate cancer (NEPC) in men with advanced prostate cancer. The results demonstrate that the method can accurately discriminate between NEPC and CR-PRAD with high sensitivity and specificity.

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Article Biochemistry & Molecular Biology

RB1 loss in castration-resistant prostate cancer confers vulnerability to LSD1 inhibition

Wanting Han et al.

Summary: The genomic loss of RB1 is a common alteration in CRPC and is associated with poor patient outcomes. RB1 loss is also crucial for the neuroendocrine transdifferentiation of PCa induced by ARSi. Through cistromic and transcriptomic analysis, it has been found that RB1 has distinct binding sites and targets in CRPC with different genomic backgrounds. Furthermore, it has been discovered that the activity of E2F1 in Rb-deficient CRPC is highly dependent on LSD1/KDM1A, and that Rb inactivation sensitizes CRPC tumors to LSD1 inhibitor treatment.

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Article Oncology

Androgen receptor reprogramming demarcates prognostic, context-dependent gene sets in primary and metastatic prostate cancer

Tesa Severson et al.

Summary: The androgen receptor (AR) plays a fundamental role in prostate pathophysiology and its reprogrammed binding to DNA contributes to prostate tumorigenesis and disease progression. This study identifies genes regulated by AR in different histological contexts and demonstrates the clinical significance of their expression in prostate cancer patients. The research highlights the importance of integrating context-dependent epigenetic data into genetic analyses.

CLINICAL EPIGENETICS (2022)

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Review Cell Biology

Androgen Receptor-Mediated Transcription in Prostate Cancer

Dogancan Ozturan et al.

Summary: In this review, the authors discuss the mechanism of action of androgen receptor (AR) in prostate cancer (PCa), focusing on how cis-regulatory elements modulate gene expression. They explore emerging evidence of genetic variants that can impact AR regulatory regions and alter gene transcription in PCa. Several outstanding questions and potential mechanisms of this critical transcription factor are also highlighted.

CELLS (2022)

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Response to supraphysiological testosterone is predicted by a distinct androgen receptor cistrome

Xintao Qiu et al.

Summary: This study provides insight into the differences in the AR cistrome before treatment and identifies a signature that can distinguish between SPT-responding and -non responding tumors, offering the potential to identify patients who would benefit from SPT therapy.

JCI INSIGHT (2022)

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Article Oncology

The Prostate Cancer Androgen Receptor Cistrome in African American Men Associates with Upregulation of Lipid Metabolism and Immune Response

Jacob E. Berchuck et al.

Summary: The study reveals that African-American men have a higher probability and mortality rate of prostate cancer. Compared to European American men, African-American prostate cancer shows stronger binding of genes associated with lipid metabolism and immune response to the androgen receptor (AR). Furthermore, upregulated lipid metabolism gene expression and increased lipid levels are associated with worsened prognosis in African-American metastatic prostate cancer.

CANCER RESEARCH (2022)

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N/C Interactions Are Dispensable for Normal In Vivo Functioning of the Androgen Receptor in Male Mice

Sarah El Kharraz et al.

Summary: Research suggests that the N/C interactions in the androgen receptor (AR) are not essential for the development of male phenotype under normal physiological conditions.

ENDOCRINOLOGY (2022)

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Article Oncology

Drug-Induced Epigenomic Plasticity Reprograms Circadian Rhythm Regulation to Drive Prostate Cancer toward Androgen Independence

Simon Linder et al.

Summary: In this study, the researchers performed integrative multi-omics analyses on prostate cancer patients before and after AR-targeted therapy. They found that AR inhibition drives tumors towards a neuroendocrine-like disease state, and identified ARNTL as a potential therapeutic target associated with clinical outcomes.

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Targeting SWI/SNF ATPases in enhancer-addicted prostate cancer

Lanbo Xiao et al.

Summary: The SWI/SNF complex plays a crucial role in chromatin remodeling and is altered in over 20% of cancers. A newly developed proteolysis-targeting chimera (PROTAC) named AU-15330 can degrade the SWI/SNF ATPase subunits, SMARCA2 and SMARCA4, leading to inhibition of tumor growth in prostate cancer cells that are sensitive to this degradation. Impeding SWI/SNF-mediated enhancer accessibility could be a promising therapeutic approach for enhancer-addicted cancers.

NATURE (2022)

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The circadian cryptochrome, CRY1, is a pro-tumorigenic factor that rhythmically modulates DNA repair

Ayesha A. Shafi et al.

Summary: CRY1, a transcriptional coregulator associated with the circadian clock, is identified as a tumor specific regulator of DNA repair. It is androgen-responsive, stabilized by genomic insult, and promotes DNA repair and cell survival through temporal transcriptional regulation. These findings nominate CRY1 as a new therapeutic target for cancer treatment.

NATURE COMMUNICATIONS (2021)

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Article Oncology

Targeting the p300/CBP Axis in Lethal Prostate Cancer

Jonathan Welti et al.

Summary: The resistance to AR blockade in CRPC is associated with sustained AR signaling through alternative splicing of AR (AR-SV). Inhibitors of transcriptional coactivators like p300/CBP are attractive therapeutic targets for lethal prostate cancer. CCS1477, a novel small-molecule inhibitor of p300/CBP, shows promise in inhibiting cell proliferation in prostate cancer cell lines and regulating AR and C-MYC signaling.

CANCER DISCOVERY (2021)

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Article Cell Biology

Chromosome compartmentalization alterations in prostate cancer cell lines model disease progression

Rebeca San Martin et al.

Summary: The study reveals that changes in 3D genome structure play a detrimental role in the progression of prostate cancer, affecting spatial compartment identity, gene expression, and genomic aberrations.

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Proximity-dependent Mapping of the Androgen Receptor Identifies Kruppel-like Factor 4 as a Functional Partner

Lauriane Velot et al.

Summary: Prostate cancer is a frequently diagnosed cancer in men, driven by the androgen receptor (AR) which is activated by androgens. By utilizing proximity labeling proteomics, researchers identified an expanded AR signaling network with newly discovered AR-associated proteins involved in key biological processes like DNA metabolism and RNA processing.

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Epigenetic and transcriptional analysis reveals a core transcriptional program conserved in clonal prostate cancer metastases

Tesa M. Severson et al.

Summary: The study investigated the epigenomic landscape of prostate cancer drivers in four clonal metastatic tumors from a single patient, revealing a core transcriptional program in clonal metastatic prostate cancer despite differences in the AR cistrome. Shared AR binding sites among healthy prostate, primary prostate cancer, and metastatic tumors signify core AR-driven transcriptional regulation within the prostate cell lineage.

MOLECULAR ONCOLOGY (2021)

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A noncanonical AR addiction drives enzalutamide resistance in prostate cancer

Yundong He et al.

Summary: Resistance to next-generation anti-androgen enzalutamide in castration-resistant prostate cancer (CRPC) is a major challenge. Through genome-wide ChIP-seq profiling, it was found that AR-dependent transcription of noncanonical targets drives an ENZ-resistant mechanism, making resistant cells susceptible to dual inhibition of BET and CBP/p300 signaling.

NATURE COMMUNICATIONS (2021)

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MED19 alters AR occupancy and gene expression in prostate cancer cells, driving MAOA expression and growth under low androgen

Hannah Weber et al.

Summary: Androgen deprivation therapy (ADT) is crucial in prostate cancer treatment, but resistant tumors pose a challenge. MED19 upregulation promotes androgen-independent growth by altering AR occupancy, H3K27 acetylation, and gene expression, cooperating with ELK1 to regulate MAOA expression and driving androgen independence in prostate cancer cells.

PLOS GENETICS (2021)

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Opposing transcriptional programs of KLF5 and AR emerge during therapy for advanced prostate cancer

Meixia Che et al.

Summary: Endocrine therapies for prostate cancer often lead to the reactivation of the androgen receptor, promoting disease progression. This study shows that the transcription factor KLF5 is induced during treatment, promoting cellular migration and the development of a basal epithelial cell phenotype.

NATURE COMMUNICATIONS (2021)

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Androgen receptor and MYC equilibration centralizes on developmental super-enhancer

Haiyang Guo et al.

Summary: The androgen receptor in prostate cancer can transcriptionally repress genes like MYC, potentially leading to resistance in response to androgen deprivation or enhanced response to supraphysiological androgen therapy. The interaction between AR and MYC involves coactivator redistribution and disrupts chromatin conformation, impacting gene expression. This intricate balance between AR and MYC highlights their suppressive effects and the potential implications for treatment responses in PCa.

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MAP3K7 Loss Drives Enhanced Androgen Signaling and Independently Confers Risk of Recurrence in Prostate Cancer with Joint Loss of CHD1

Lauren K. Jillson et al.

Summary: The text discusses the role of prostate cancer subtype with co-loss of MAP3K7 and CHD1 in AR signaling and highlights the importance of MAP3K7 loss as a significant factor challenging conventional therapeutic approaches in prostate cancer.

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

Sylvan C. Baca et al.

Summary: The study reveals that the transcription factor FOXA1 plays a crucial role in the development of neuroendocrine prostate cancer (NEPC) by regulating specific regulatory elements. Additionally, the expression of NE lineage TFs ASCL1 and NKX2-1 in PRAD cells can reprogram FOXA1 to bind to NE regulatory elements and induce enhancer activity.

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BET Bromodomain Inhibition Blocks an AR-Repressed, E2F1-Activated Treatment-Emergent Neuroendocrine Prostate Cancer Lineage Plasticity Program

Dae-Hwan Kim et al.

Summary: NEPC is the most aggressive lineage plasticity in prostate cancer, with limited treatment options. By inhibiting AR and using BET inhibitors, it is possible to block this lineage plasticity, showing promising potential for t-NEPC treatment.

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An androgen receptor switch underlies lineage infidelity in treatment-resistant prostate cancer

Alastair Davies et al.

Summary: The study demonstrates that prostate cancer can transition to a high-plasticity state in response to potent androgen receptor antagonism, maintaining AR activity and rerouting transcriptional activity through changes in chromatin architecture. This reprogramming is mediated by EZH2 and favors stem cell and neuronal gene networks, highlighting the potential for reversing treatment resistance in prostate cancer.

NATURE CELL BIOLOGY (2021)

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Review Urology & Nephrology

Molecular events in neuroendocrine prostate cancer development

Yong Wang et al.

Summary: Neuroendocrine prostate cancer mainly develops from adenocarcinoma following a period of androgen suppressive treatment, and patients have poor outcomes; understanding the molecular mechanisms behind its development will improve future targeted therapy options.

NATURE REVIEWS UROLOGY (2021)

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Article Biochemistry & Molecular Biology

Chromatin-directed proteomics-identified network of endogenous androgen receptor in prostate cancer cells

Kaisa-Mari Launonen et al.

Summary: The study used ChIP-SICAP to uncover the chromatome composition around endogenous AR in CRPC cells, revealing the roles of SMARCA4 and SIM2 in chromatin accessibility and AR target gene expression. Depletion of SMARCA4 impacted a restricted set of AR target genes involved in cell morphogenetic changes, while silencing of SIM2 affected a larger group of androgen-regulated genes related to cellular responses and proliferation in CRPC cells.

ONCOGENE (2021)

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Article Cell Biology

CRISPR screening identifies CDK12 as a conservative vulnerability of prostate cancer

Hanqi Lei et al.

Summary: The study identified CDK12 as a critical factor for PCa cell survival, and its inhibition by THZ531 led to anti-PCa effects. THZ531 downregulated AR signaling and selectively repressed a distinct class of transcripts, affecting cellular survival. CDK12 inhibition was also linked to the sensitivity of PCa cells to apoptosis pathways and potential oncogenes.

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Temporal evolution of cellular heterogeneity during the progression to advanced AR-negative prostate cancer

Nicholas J. Brady et al.

Summary: The study demonstrates the acceleration of progression from AR-positive prostate cancer to AR-negative NEPC through Rb1 loss and MYCN overexpression in a mouse model, as well as the emergence of distinct subpopulations of NEPC cells. Despite advancements in AR-directed therapies, a subset of patients still develop AR-negative tumors with neuroendocrine features.

NATURE COMMUNICATIONS (2021)

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Article Cell Biology

Reshaping of the androgen-driven chromatin landscape in normal prostate cells by early cancer drivers and effect on therapeutic sensitivity

Ivana Grbesa et al.

Summary: The study reveals the significant impact of SPOP mutations on the development of prostate cancer, highlighting the importance of conducting related experiments on mouse prostate organoids. The dependence on AR signaling is associated with the therapeutic effects of AR-targeted therapies in SPOP mutant prostate cancer.

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Selective androgen receptor modulators activate the canonical prostate cancer androgen receptor program and repress cancer growth

Michael D. Nyquist et al.

Summary: Prostate cancer is driven by androgen receptor activity, which can be targeted by selective androgen receptor modulators (SARMs) to inhibit tumor growth. SARMs have shown to activate AR program, repress MYC oncoprotein expression, and inhibit the growth of both castration-sensitive and castration-resistant prostate cancer. Further clinical investigation of SARMs for treating advanced prostate cancer is supported by these promising results.

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Article Biotechnology & Applied Microbiology

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Chia-Chi Flora Huang et al.

Summary: Using a functional map of AR enhancer activity, it was demonstrated that AR-regulated enhancers act as a regulatory hub that increases interactions with other AR binding sites and gene promoters. The study found that only 7% of AR binding sites display androgen-dependent enhancer activity, while the vast majority were either inactive or constitutively active enhancers. Somatic mutations of critical AR-regulated enhancers often impact enhancer activity.

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Tunc Morova et al.

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Small molecule JQ1 promotes prostate cancer invasion via BET-independent inactivation of FOXA1

Leiming Wang et al.

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Darolutamide antagonizes androgen signaling by blocking enhancer and super-enhancer activation

Simon J. Baumgart et al.

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ERG-Mediated Coregulator Complex Formation Maintains Androgen Receptor Signaling in Prostate Cancer

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

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CHD1 Loss Alters AR Binding at Lineage-Specific Enhancers and Modulates Distinct Transcriptional Programs to Drive Prostate Tumorigenesis

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Review Genetics & Heredity

ChIP-seq and beyond: new and improved methodologies to detect and characterize protein-DNA interactions

Terrence S. Furey

NATURE REVIEWS GENETICS (2012)

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Review Cell Biology

Pioneer transcription factors: establishing competence for gene expression

Kenneth S. Zaret et al.

GENES & DEVELOPMENT (2011)

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Article Oncology

An Integrated Network of Androgen Receptor, Polycomb, and TMPRSS2-ERG Gene Fusions in Prostate Cancer Progression

Jindan Yu et al.

CANCER CELL (2010)

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Review Biochemistry & Molecular Biology

Structure and function of SWI/SNF chromatin remodeling complexes and mechanistic implications for transcription

Liling Tang et al.

PROGRESS IN BIOPHYSICS & MOLECULAR BIOLOGY (2010)

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Article Biochemistry & Molecular Biology

Androgen Receptor Regulates a Distinct Transcription Program in Androgen-Independent Prostate Cancer

Qianben Wang et al.

CELL (2009)

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Article Biochemistry & Molecular Biology

A role for GATA-2 in transition to an aggressive phenotype in prostate cancer through modulation of key androgen-regulated genes

M. Boehm et al.

ONCOGENE (2009)

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Article Multidisciplinary Sciences

Nascent RNA Sequencing Reveals Widespread Pausing and Divergent Initiation at Human Promoters

Leighton J. Core et al.

SCIENCE (2008)

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Article Cell Biology

Compartmentalization of androgen receptor protein-protein interactions in living cells

Martin E. van Royen et al.

JOURNAL OF CELL BIOLOGY (2007)

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Review Pharmacology & Pharmacy

FOXA1 as a therapeutic target for breast cancer

Harikrishna Nakshatri et al.

EXPERT OPINION ON THERAPEUTIC TARGETS (2007)

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Article Multidisciplinary Sciences

Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer

SA Tomlins et al.

SCIENCE (2005)

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Article Oncology

Androgen-induced differentiation and tumorigenicity of human prostate epithelial cells

R Berger et al.

CANCER RESEARCH (2004)

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Article Biochemistry & Molecular Biology

Opening of compacted chromatin by early developmental transcription factors HNF3 (FoxA) and GATA-4

LA Cirillo et al.

MOLECULAR CELL (2002)

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