Roles of Alternative RNA Splicing of the Bif-1 Gene by SRRM4 During the Development of Treatment-induced Neuroendocrine Prostate Cancer

EBioMedicine. 2018 May:31:267-275. doi: 10.1016/j.ebiom.2018.05.002. Epub 2018 May 16.

Abstract

Treatment-induced neuroendocrine prostate cancer (t-NEPC) is an aggressive subtype of prostate cancer (PCa) that becomes more prevalent when hormonal therapy, chemotherapy, or radiation therapy is applied to patients with metastatic prostate adenocarcinoma (AdPC). How AdPC cells survive these anti-cancer therapies and progress into t-NEPC remains unclear. By comparing the whole transcriptomes between AdPC and t-NEPC, we identified Bif-1, an apoptosis-associated gene, which undergoes alternative RNA splicing in t-NEPC. We found that while Bif-1a is the predominant variant of the Bif-1 gene in AdPC, two neural-specific variants, Bif-1b and Bif-1c, are highly expressed in t-NEPC patients, patient derived xenografts, and cell models. The neural-specific RNA splicing factor, SRRM4, promotes Bif-1b and Bif-1c splicing, and the expression of SRRM4 in tumors is strongly associated with Bif-1b/-1c levels. Furthermore, we showed that Bif-1a is pro-apoptotic, while Bif-1b and Bif-1c are anti-apoptotic in PCa cells under camptothecin and UV light irritation treatments. Taken together, our data indicate that SRRM4 regulates alternative RNA splicing of the Bif-1 gene that enables PCa cells resistant to apoptotic stimuli under anti-cancer therapies, and may contribute to AdPC progression into t-NEPC.

Keywords: Alternative RNA splicing; Apoptosis; Bif-1; Neuroendocrine prostate cancer; SRRM4.

MeSH terms

  • Adaptor Proteins, Signal Transducing* / biosynthesis
  • Adaptor Proteins, Signal Transducing* / genetics
  • Alternative Splicing*
  • Animals
  • Apoptosis*
  • Carcinoma, Neuroendocrine* / genetics
  • Carcinoma, Neuroendocrine* / metabolism
  • Carcinoma, Neuroendocrine* / pathology
  • Cell Line, Tumor
  • Gene Expression Regulation, Neoplastic*
  • Humans
  • Male
  • Mice
  • Neoplasm Proteins* / genetics
  • Neoplasm Proteins* / metabolism
  • Nerve Tissue Proteins* / genetics
  • Nerve Tissue Proteins* / metabolism
  • Prostatic Neoplasms* / genetics
  • Prostatic Neoplasms* / metabolism
  • Prostatic Neoplasms* / pathology

Substances

  • Adaptor Proteins, Signal Transducing
  • Neoplasm Proteins
  • Nerve Tissue Proteins
  • SH3GLB1 protein, human
  • SRRM4 protein, human