Discoidin domain receptor 1-deletion ameliorates fibrosis and promotes adipose tissue beiging, brown fat activity, and increased metabolic rate in a mouse model of cardiometabolic disease

Mol Metab. 2020 Sep:39:101006. doi: 10.1016/j.molmet.2020.101006. Epub 2020 Apr 28.

Abstract

Objective: Discoidin domain receptor 1 (DDR1) is a collagen binding receptor tyrosine kinase implicated in atherosclerosis, fibrosis, and cancer. Our previous research showed that DDR1 could regulate smooth muscle cell trans-differentiation, fibrosis and calcification in the vascular system in cardiometabolic disease. This spectrum of activity led us to question whether DDR1 might also regulate adipose tissue fibrosis and remodeling.

Methods: We have used a diet-induced mouse model of cardiometabolic disease to determine whether DDR1 deletion impacts upon adipose tissue remodeling and metabolic dysfunction. Mice were fed a high fat diet (HFD) for 12 weeks, followed by assessment of glucose and insulin tolerance, respiration via indirect calorimetry, and brown fat activity by FDG-PET.

Results: Feeding HFD induced DDR1 expression in white adipose tissue, which correlated with adipose tissue expansion and fibrosis. Ddr1-/- mice fed an HFD had improved glucose tolerance, reduced body fat, and increased brown fat activity and energy expenditure compared to Ddr1+/+ littermate controls. HFD-fed DDR1-/- mice also had reduced fibrosis, smaller adipocytes with multilocular lipid droplets, and increased UCP-1 expression characteristic of beige fat formation in subcutaneous adipose tissue. In vitro, studying C3H10T1/2 cells stimulated to differentiate, DDR1 inhibition caused a shift from white to beige adipocyte differentiation, whereas DDR1 expression was increased with TGFβ-mediated pro-fibrotic differentiation.

Conclusion: This study is the first to identify a role for DDR1 as a driver of adipose tissue fibrosis and suppressor of beneficial beige fat formation.

Keywords: Collagen; Diabetes; Discoidin domain receptor 1; Fibrosis; Obesity; brown fat.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue, Beige / metabolism*
  • Adipose Tissue, Brown / metabolism*
  • Animals
  • Calorimetry
  • Diet, High-Fat / adverse effects
  • Discoidin Domain Receptor 1 / genetics*
  • Discoidin Domain Receptor 1 / metabolism
  • Disease Models, Animal
  • Disease Susceptibility
  • Energy Metabolism*
  • Fibrosis
  • Gene Deletion*
  • Immunohistochemistry
  • Metabolic Syndrome / diagnosis
  • Metabolic Syndrome / etiology*
  • Metabolic Syndrome / metabolism*
  • Mice
  • Mice, Knockout
  • Positron-Emission Tomography
  • RNA, Messenger / genetics
  • Subcutaneous Fat / metabolism
  • Tomography, X-Ray Computed

Substances

  • RNA, Messenger
  • Ddr1 protein, mouse
  • Discoidin Domain Receptor 1

Grants and funding