Preventing BRCA1/ZBRK1 repressor complex binding to the GOT2 promoter results in accelerated aspartate biosynthesis and promotion of cell proliferation

Mol Oncol. 2019 Apr;13(4):959-977. doi: 10.1002/1878-0261.12466. Epub 2019 Mar 1.

Abstract

Breast cancer susceptibility gene 1 (BRCA1) has been implicated in modulating metabolism via transcriptional regulation. However, direct metabolic targets of BRCA1 and the underlying regulatory mechanisms are still unknown. Here, we identified several metabolic genes, including the gene which encodes glutamate-oxaloacetate transaminase 2 (GOT2), a key enzyme for aspartate biosynthesis, which are repressed by BRCA1. We report that BRCA1 forms a co-repressor complex with ZBRK1 that coordinately represses GOT2 expression via a ZBRK1 recognition element in the promoter of GOT2. Impairment of this complex results in upregulation of GOT2, which in turn increases aspartate and alpha ketoglutarate production, leading to rapid cell proliferation of breast cancer cells. Importantly, we found that GOT2 can serve as an independent prognostic factor for overall survival and disease-free survival of patients with breast cancer, especially triple-negative breast cancer. Interestingly, we also demonstrated that GOT2 overexpression sensitized breast cancer cells to methotrexate, suggesting a promising precision therapeutic strategy for breast cancer treatment. In summary, our findings reveal that BRCA1 modulates aspartate biosynthesis through transcriptional repression of GOT2, and provides a biological basis for treatment choices in breast cancer.

Keywords: BRCA1; GOT2; ZBRK1; aspartate; breast cancer; co-repressor.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aspartate Aminotransferase, Mitochondrial / genetics*
  • Aspartate Aminotransferase, Mitochondrial / metabolism
  • Aspartic Acid / biosynthesis*
  • BRCA1 Protein / metabolism*
  • Biomarkers, Tumor / metabolism
  • Breast Neoplasms / genetics
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Female
  • Gene Expression Regulation, Neoplastic / drug effects
  • HEK293 Cells
  • Humans
  • Ketoglutaric Acids / metabolism
  • Methotrexate / pharmacology
  • Mice
  • Middle Aged
  • Models, Biological
  • Phenotype
  • Promoter Regions, Genetic*
  • Protein Binding / drug effects
  • Repressor Proteins / metabolism*
  • Transcription, Genetic / drug effects

Substances

  • BRCA1 Protein
  • BRCA1 protein, human
  • Biomarkers, Tumor
  • Ketoglutaric Acids
  • Repressor Proteins
  • ZNF350 protein, human
  • Aspartic Acid
  • Aspartate Aminotransferase, Mitochondrial
  • Methotrexate