Publication Date

7-22-2024

Journal

Nucleic Acids Research

DOI

10.1093/nar/gkae547

PMID

38932701

PMCID

PMC11260453

PubMedCentral® Posted Date

6-27-2024

PubMedCentral® Full Text Version

Post-print

Published Open-Access

yes

Keywords

Male, Humans, Receptors, Androgen, Adenocarcinoma, Receptors, Glucocorticoid, Prostatic Neoplasms, Drug Resistance, Neoplasm, Benzamides, Cell Line, Tumor, Nitriles, Gene Expression Regulation, Neoplastic, Phenylthiohydantoin, Nerve Tissue Proteins, Epigenesis, Genetic, RNA-Binding Proteins, Neuroendocrine Tumors, Animals, Cell Lineage, Mice

Abstract

Androgen receptor- (AR-) indifference is a mechanism of resistance to hormonal therapy in prostate cancer (PC). Here we demonstrate that ONECUT2 (OC2) activates resistance through multiple drivers associated with adenocarcinoma, stem-like and neuroendocrine (NE) variants. Direct OC2 gene targets include the glucocorticoid receptor (GR; NR3C1) and the NE splicing factor SRRM4, which are key drivers of lineage plasticity. Thus, OC2, despite its previously described NEPC driver function, can indirectly activate a portion of the AR cistrome through epigenetic activation of GR. Mechanisms by which OC2 regulates gene expression include promoter binding, enhancement of genome-wide chromatin accessibility, and super-enhancer reprogramming. Pharmacologic inhibition of OC2 suppresses lineage plasticity reprogramming induced by the AR signaling inhibitor enzalutamide. These results demonstrate that OC2 activation promotes a range of drug resistance mechanisms associated with treatment-emergent lineage variation in PC and support enhanced efforts to therapeutically target OC2 as a means of suppressing treatment-resistant disease.

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