Consumption of the Fish Oil High-Fat Diet Uncouples Obesity and Mammary Tumor Growth through Induction of Reactive Oxygen Species in Protumor Macrophages

Cancer Res. 2020 Jun 15;80(12):2564-2574. doi: 10.1158/0008-5472.CAN-19-3184. Epub 2020 Mar 25.

Abstract

Obesity is associated with increased risk of many types of cancer and can be induced by various high-fat diets (HFD) from different fat sources. It remains unknown whether fatty acid composition in different HFD influences obesity-associated tumor development. Here we report that consumption of either a cocoa butter or fish oil HFD induced similar obesity in mouse models. While obesity induced by the cocoa butter HFD was associated with accelerated mammary tumor growth, consumption of the fish oil HFD uncoupled obesity from increased mammary tumor growth and exhibited a decrease in protumor macrophages. Compared with fatty acid (FA) components in both HFDs, n-3 FA rich in the fish oil HFD induced significant production of reactive oxygen species (ROS) and macrophage death. Moreover, A-FABP expression in the protumor macrophages facilitated intracellular transportation of n-3 FA and oxidation of mitochondrial FA. A-FABP deficiency diminished n-3 FA-mediated ROS production and macrophage death in vitro and in vivo. Together, our results demonstrate a novel mechanism by which n-3 FA induce ROS-mediated protumor macrophage death in an A-FABP-dependent manner. SIGNIFICANCE: This study provides mechanistic insight into dietary supplementation with fish oil for breast cancer prevention and advances a new concept that not all HFDs leading to obesity are tumorigenic. GRAPHICAL ABSTRACT: http://cancerres.aacrjournals.org/content/canres/80/12/2564/F1.large.jpg.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Carcinogenesis / immunology
  • Carcinogenesis / metabolism
  • Cell Line, Tumor / transplantation
  • Diet, High-Fat / adverse effects
  • Diet, High-Fat / methods*
  • Dietary Fats / adverse effects*
  • Fatty Acid-Binding Proteins / genetics
  • Fatty Acid-Binding Proteins / metabolism*
  • Female
  • Fish Oils / administration & dosage*
  • Humans
  • Macrophages / cytology
  • Macrophages / immunology*
  • Macrophages / metabolism
  • Mammary Glands, Animal / cytology
  • Mammary Glands, Animal / immunology
  • Mammary Glands, Animal / pathology
  • Mammary Neoplasms, Experimental / genetics
  • Mammary Neoplasms, Experimental / immunology*
  • Mammary Neoplasms, Experimental / metabolism
  • Mammary Neoplasms, Experimental / prevention & control
  • Mice
  • Mice, Knockout
  • Mitochondria / metabolism
  • Obesity / complications*
  • Obesity / immunology
  • Obesity / metabolism
  • Primary Cell Culture
  • Reactive Oxygen Species / metabolism

Substances

  • Dietary Fats
  • Fabp4 protein, mouse
  • Fatty Acid-Binding Proteins
  • Fish Oils
  • Reactive Oxygen Species
  • cocoa butter