A high-fat diet promotes cancer progression by inducing gut microbiota-mediated leucine production and PMN-MDSC differentiation

Proc Natl Acad Sci U S A. 2024 May 14;121(20):e2306776121. doi: 10.1073/pnas.2306776121. Epub 2024 May 6.

Abstract

A high-fat diet (HFD) is a high-risk factor for the malignant progression of cancers through the disruption of the intestinal microbiota. However, the role of the HFD-related gut microbiota in cancer development remains unclear. This study found that obesity and obesity-related gut microbiota were associated with poor prognosis and advanced clinicopathological status in female patients with breast cancer. To investigate the impact of HFD-associated gut microbiota on cancer progression, we established various models, including HFD feeding, fecal microbiota transplantation, antibiotic feeding, and bacterial gavage, in tumor-bearing mice. HFD-related microbiota promotes cancer progression by generating polymorphonuclear myeloid-derived suppressor cells (PMN-MDSCs). Mechanistically, the HFD microbiota released abundant leucine, which activated the mTORC1 signaling pathway in myeloid progenitors for PMN-MDSC differentiation. Clinically, the elevated leucine level in the peripheral blood induced by the HFD microbiota was correlated with abundant tumoral PMN-MDSC infiltration and poor clinical outcomes in female patients with breast cancer. These findings revealed that the "gut-bone marrow-tumor" axis is involved in HFD-mediated cancer progression and opens a broad avenue for anticancer therapeutic strategies by targeting the aberrant metabolism of the gut microbiota.

Keywords: breast cancer; gut microbiota; high-fat diet; myeloid-derived suppressor cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Breast Neoplasms* / metabolism
  • Breast Neoplasms* / microbiology
  • Breast Neoplasms* / pathology
  • Cell Differentiation*
  • Cell Line, Tumor
  • Diet, High-Fat* / adverse effects
  • Disease Progression*
  • Female
  • Gastrointestinal Microbiome*
  • Humans
  • Leucine* / metabolism
  • Mice
  • Myeloid-Derived Suppressor Cells* / metabolism
  • Obesity / metabolism
  • Obesity / microbiology
  • Obesity / pathology

Substances

  • Leucine