Metabolically activated adipose tissue macrophages link obesity to triple-negative breast cancer

J Exp Med. 2019 Jun 3;216(6):1345-1358. doi: 10.1084/jem.20181616. Epub 2019 May 3.

Abstract

Obesity is associated with increased incidence and severity of triple-negative breast cancer (TNBC); however, mechanisms underlying this relationship are incompletely understood. Here, we show that obesity reprograms mammary adipose tissue macrophages to a pro-inflammatory metabolically activated phenotype (MMe) that alters the niche to support tumor formation. Unlike pro-inflammatory M1 macrophages that antagonize tumorigenesis, MMe macrophages are pro-tumorigenic and represent the dominant macrophage phenotype in mammary adipose tissue of obese humans and mice. MMe macrophages release IL-6 in an NADPH oxidase 2 (NOX2)-dependent manner, which signals through glycoprotein 130 (GP130) on TNBC cells to promote stem-like properties including tumor formation. Deleting Nox2 in myeloid cells or depleting GP130 in TNBC cells attenuates obesity-augmented TNBC stemness. Moreover, weight loss reverses the effects of obesity on MMe macrophage inflammation and TNBC tumor formation. Our studies implicate MMe macrophage accumulation in mammary adipose tissue as a mechanism for promoting TNBC stemness and tumorigenesis during obesity.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / pathology*
  • Animals
  • Carcinogenesis / metabolism
  • Carcinogenesis / pathology
  • Cell Line, Tumor
  • Cytokine Receptor gp130 / metabolism
  • Diet
  • Female
  • Humans
  • Interleukin-6 / metabolism
  • Macrophages / metabolism*
  • Mammary Glands, Animal / pathology
  • Mammary Glands, Human / pathology
  • Mice, Inbred C57BL
  • Neoplastic Stem Cells / pathology
  • Obesity / pathology*
  • Phenotype
  • Triple Negative Breast Neoplasms / pathology*
  • Weight Loss

Substances

  • Il6st protein, mouse
  • Interleukin-6
  • Cytokine Receptor gp130