COX-2 promotes mammary adipose tissue inflammation, local estrogen biosynthesis, and carcinogenesis in high-sugar/fat diet treated mice

Cancer Lett. 2021 Apr 1:502:44-57. doi: 10.1016/j.canlet.2021.01.003. Epub 2021 Jan 9.

Abstract

Obesity is a major risk factor for breast cancer, especially in post-menopausal women. In the breast tissue of obese women, cyclooxygenase-2 (COX-2)-dependent prostaglandin E2 (PGE2) production has been correlated with inflammation and local estrogen biosynthesis via aromatase. Using a mouse model of 7,12-dimethylbenz[a]anthracene/medroxyprogesterone-acetate (DMBA/MPA)-induced carcinogenesis, we demonstrated that an obesogenic diet promotes mammary tissue inflammation and local estrogen production, and accelerates mammary tumor formation in a COX-2-dependent manner. High-sugar/fat (HSF) diet augmented the levels of the pro-inflammatory mediators MCP-1, IL-6, COX-2, and PGE2 in mammary tissue, and this was accompanied by crown-like structures of breast (CLS-B) formation and aromatase/estrogen upregulation. Treatment with a COX-2 selective inhibitor, etoricoxib, decreased PGE2, IL-6, MCP-1, and CLS-B formation as well as reduced aromatase protein and estrogen levels in the mammary tissue of mice fed a HSF diet. Etoricoxib-treated mice showed increased latency and decreased incidence of mammary tumors, which resulted in prolonged animal survival when compared to HSF diet alone. Inhibition of tumor angiogenesis also seemed to account for the prolonged survival of COX-2 inhibitor-treated animals. In conclusion, obesogenic diet-induced COX-2 is sufficient to trigger inflammation, local estrogen biosynthesis, and mammary tumorigenesis.

Keywords: Aromatase; Crown-like structures; Cyclooxygenase-2; Cytokines; Prostaglandin E2.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • 9,10-Dimethyl-1,2-benzanthracene / adverse effects
  • Animals
  • Aromatase / metabolism
  • Breast Neoplasms / chemically induced
  • Breast Neoplasms / drug therapy
  • Breast Neoplasms / metabolism*
  • Cell Line, Tumor
  • Chemokine CCL2 / metabolism
  • Cyclooxygenase 2 / metabolism*
  • Diet, High-Fat / adverse effects*
  • Dinoprostone / biosynthesis*
  • Disease Models, Animal
  • Etoricoxib / administration & dosage
  • Etoricoxib / pharmacology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Interleukin-6 / metabolism
  • MCF-7 Cells
  • Medroxyprogesterone Acetate / adverse effects
  • Mice
  • Sugars / adverse effects*
  • Up-Regulation*

Substances

  • CCL2 protein, human
  • Chemokine CCL2
  • IL6 protein, human
  • Interleukin-6
  • Sugars
  • 9,10-Dimethyl-1,2-benzanthracene
  • Medroxyprogesterone Acetate
  • Aromatase
  • Cyclooxygenase 2
  • PTGS2 protein, human
  • Dinoprostone
  • Etoricoxib