Breast cancer cell-secreted miR-199b-5p hijacks neurometabolic coupling to promote brain metastasis

Nat Commun. 2024 May 29;15(1):4549. doi: 10.1038/s41467-024-48740-0.

Abstract

Breast cancer metastasis to the brain is a clinical challenge rising in prevalence. However, the underlying mechanisms, especially how cancer cells adapt a distant brain niche to facilitate colonization, remain poorly understood. A unique metabolic feature of the brain is the coupling between neurons and astrocytes through glutamate, glutamine, and lactate. Here we show that extracellular vesicles from breast cancer cells with a high potential to develop brain metastases carry high levels of miR-199b-5p, which shows higher levels in the blood of breast cancer patients with brain metastases comparing to those with metastatic cancer in other organs. miR-199b-5p targets solute carrier transporters (SLC1A2/EAAT2 in astrocytes and SLC38A2/SNAT2 and SLC16A7/MCT2 in neurons) to hijack the neuron-astrocyte metabolic coupling, leading to extracellular retention of these metabolites and promoting cancer cell growth. Our findings reveal a mechanism through which cancer cells of a non-brain origin reprogram neural metabolism to fuel brain metastases.

MeSH terms

  • Animals
  • Astrocytes* / metabolism
  • Astrocytes* / pathology
  • Brain / metabolism
  • Brain / pathology
  • Brain Neoplasms* / genetics
  • Brain Neoplasms* / metabolism
  • Brain Neoplasms* / pathology
  • Brain Neoplasms* / secondary
  • Breast Neoplasms* / genetics
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / pathology
  • Cell Line, Tumor
  • Cell Proliferation
  • Excitatory Amino Acid Transporter 2 / genetics
  • Excitatory Amino Acid Transporter 2 / metabolism
  • Extracellular Vesicles / metabolism
  • Female
  • Gene Expression Regulation, Neoplastic
  • Glutamic Acid / metabolism
  • Glutamine / metabolism
  • Humans
  • Lactic Acid / metabolism
  • Mice
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism
  • Monocarboxylic Acid Transporters / genetics
  • Monocarboxylic Acid Transporters / metabolism
  • Neurons* / metabolism
  • Neurons* / pathology

Substances

  • MicroRNAs
  • mirn199 microRNA, human
  • Excitatory Amino Acid Transporter 2
  • SLC1A2 protein, human
  • Monocarboxylic Acid Transporters
  • Glutamic Acid
  • Glutamine
  • Lactic Acid