The splicing machinery is dysregulated and represents a therapeutic vulnerability in breast cancer

Cell Mol Life Sci. 2024 Dec 27;82(1):18. doi: 10.1007/s00018-024-05515-6.

Abstract

Breast cancer (BCa) is a highly prevalent pathological condition (̴30% in women) with limited and subtype-dependent prognosis and therapeutic options. Therefore, BCa management might benefit from the identification of novel molecular elements with clinical potential. Since splicing process is gaining a great relevance in cancer, this work analysed the expression of multiple Spliceosome Components (SCs = 17) and Splicing Factors (SFs = 26) and found a drastic dysregulation in BCa (n = 69) vs. control (negative biopsies; n = 50) samples. Among all the components analysed, we highlight the upregulation of ESRP1 and down-regulation of PRPF8 and NOVA1 in BCa vs. control samples. Indeed, ESRP1 was specially overexpressed in triple-negative BCa (TNBCa) and associated with worse prognosis (i.e., higher BCa grade and lower overall survival), suggesting an association of ESRP1 with BCa aggressiveness. On the other hand, PRPF8 expression was generally downregulated in BCa with no associations to clinical characteristics, while NOVA1 expression was lower in TNBCa patients and highly aggressive tumours. Consistently, NOVA1 overexpression in vitro reduced functional parameters of aggressiveness in ER-/PR- cell lines (MDA-MB-231 and BT-549) but not in ER+/PR+ cells (MCF7), suggesting a critical role of NOVA1 in subtype-specific BCa. Finally, the in vitro pharmacological inhibition of splicing machinery using pladienolide B decreased aggressiveness features in all the BCa cell lines, showing a subtype-independent inhibitory potential, but being relatively innocuous in normal-like breast cells. These results demonstrate the profound dysregulation of the splicing machinery in BCa and their potential as source of promising diagnosis/prognosis markers, as well as valuable therapeutic targets for BCa.

Keywords: Breast cancer; Hormone receptor; NOVA1; Pharmacological inhibition; Pladienolide B; Splicing.

MeSH terms

  • Aged
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Epoxy Compounds
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Macrolides
  • Middle Aged
  • Neuro-Oncological Ventral Antigen*
  • Prognosis
  • Pyrans / pharmacology
  • RNA Splicing Factors / genetics
  • RNA Splicing Factors / metabolism
  • RNA Splicing* / genetics
  • RNA-Binding Proteins* / genetics
  • RNA-Binding Proteins* / metabolism
  • Spliceosomes / genetics
  • Spliceosomes / metabolism
  • Triple Negative Breast Neoplasms / genetics
  • Triple Negative Breast Neoplasms / metabolism
  • Triple Negative Breast Neoplasms / pathology

Substances

  • RNA-Binding Proteins
  • Neuro-Oncological Ventral Antigen
  • ESRP1 protein, human
  • NOVA1 protein, human
  • RNA Splicing Factors
  • pladienolide B
  • Pyrans
  • Epoxy Compounds
  • Macrolides