The C-terminal fibrinogen-like domain of angiopoietin-like 4 stimulates adipose tissue lipolysis and promotes energy expenditure

J Biol Chem. 2017 Sep 29;292(39):16122-16134. doi: 10.1074/jbc.M117.803973. Epub 2017 Aug 24.

Abstract

Angptl4 (Angiopoietin-like 4) is a circulating protein secreted by white and brown adipose tissues and the liver. Structurally, Angptl4 contains an N-terminal coiled-coil domain (CCD) connected to a C-terminal fibrinogen-like domain (FLD) via a cleavable linker, and both full-length Angptl4 and its individual domains circulate in the bloodstream. Angptl4 inhibits extracellular lipoprotein lipase (LPL) activity and stimulates the lipolysis of triacylglycerol stored by adipocytes in the white adipose tissue (WAT). The former activity is furnished by the CCD, but the Angptl4 domain responsible for stimulating adipocyte lipolysis is unknown. We show here that the purified FLD of Angptl4 is sufficient to stimulate lipolysis in mouse primary adipocytes and that increasing circulating FLD levels in mice through adenovirus-mediated overexpression (Ad-FLD) not only induces WAT lipolysis in vivo but also reduces diet-induced obesity without affecting LPL activity. Intriguingly, reduced adiposity in Ad-FLD mice was associated with increased oxygen consumption, fat utilization, and the expression of thermogenic genes (Ucp1 and Ppargc1a) in subcutaneous WAT. Moreover, Ad-FLD mice exhibited increased glucose tolerance. Chronically enhancing WAT lipolysis could produce ectopic steatosis because of an overflow of lipids from the WAT to peripheral tissues; however, this did not occur when Ad-FLD mice were fed a high-fat diet. Rather, these mice had reductions in both circulating triacylglycerol levels and the mRNA levels of lipogenic genes in the liver and skeletal muscle. We conclude that separating the FLD from the CCD-mediated LPL-inhibitory activity of full-length Angptl4 reveals lipolytic and thermogenic properties with therapeutic relevance to obesity and diabetes.

Keywords: Energy expenditure; adipocyte; angiopoietin-like; metabolic disease; metabolism; obesity; type 2 diabetes.

MeSH terms

  • Abdominal Fat / cytology
  • Abdominal Fat / metabolism*
  • Abdominal Fat / pathology
  • Adipose Tissue, Beige / cytology
  • Adipose Tissue, Beige / metabolism
  • Adipose Tissue, Beige / pathology
  • Adiposity
  • Angiopoietin-Like Protein 4
  • Angiopoietins / blood
  • Angiopoietins / chemistry
  • Angiopoietins / genetics
  • Angiopoietins / metabolism*
  • Animals
  • Cells, Cultured
  • Energy Metabolism*
  • Lipolysis*
  • Liver / enzymology
  • Liver / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Models, Biological*
  • Muscle, Skeletal / enzymology
  • Muscle, Skeletal / metabolism
  • Mutation
  • Obesity / blood
  • Obesity / metabolism
  • Obesity / pathology
  • Obesity / prevention & control
  • Oligopeptides / genetics
  • Oligopeptides / metabolism
  • Peptide Fragments / blood
  • Peptide Fragments / chemistry
  • Peptide Fragments / genetics
  • Peptide Fragments / metabolism
  • Protein Interaction Domains and Motifs
  • Recombinant Fusion Proteins / blood
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / metabolism
  • Triglycerides / blood
  • Triglycerides / metabolism
  • Up-Regulation*

Substances

  • ANGPTL4 protein, human
  • Angiopoietin-Like Protein 4
  • Angiopoietins
  • Oligopeptides
  • Peptide Fragments
  • Recombinant Fusion Proteins
  • Triglycerides
  • FLAG peptide