Meox2/Tcf15 heterodimers program the heart capillary endothelium for cardiac fatty acid uptake

Circulation. 2015 Mar 3;131(9):815-26. doi: 10.1161/CIRCULATIONAHA.114.013721. Epub 2015 Jan 5.

Abstract

Background: Microvascular endothelium in different organs is specialized to fulfill the particular needs of parenchymal cells. However, specific information about heart capillary endothelial cells (ECs) is lacking.

Methods and results: Using microarray profiling on freshly isolated ECs from heart, brain, and liver, we revealed a genetic signature for microvascular heart ECs and identified Meox2/Tcf15 heterodimers as novel transcriptional determinants. This signature was largely shared with skeletal muscle and adipose tissue endothelium and was enriched in genes encoding fatty acid (FA) transport-related proteins. Using gain- and loss-of-function approaches, we showed that Meox2/Tcf15 mediate FA uptake in heart ECs, in part, by driving endothelial CD36 and lipoprotein lipase expression and facilitate FA transport across heart ECs. Combined Meox2 and Tcf15 haplodeficiency impaired FA uptake in heart ECs and reduced FA transfer to cardiomyocytes. In the long term, this combined haplodeficiency resulted in impaired cardiac contractility.

Conclusions: Our findings highlight a regulatory role for ECs in FA transfer to the heart parenchyma and unveil 2 of its intrinsic regulators. Our insights could be used to develop new strategies based on endothelial Meox2/Tcf15 targeting to modulate FA transfer to the heart and remedy cardiac dysfunction resulting from altered energy substrate usage.

Keywords: endothelium; fatty acids; heart; metabolism; transcription factors.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipose Tissue / blood supply
  • Animals
  • Basic Helix-Loop-Helix Transcription Factors / chemistry
  • Basic Helix-Loop-Helix Transcription Factors / deficiency
  • Basic Helix-Loop-Helix Transcription Factors / genetics
  • Basic Helix-Loop-Helix Transcription Factors / physiology*
  • CD36 Antigens / biosynthesis
  • CD36 Antigens / genetics
  • Cardiac Output, Low / etiology
  • Cardiac Output, Low / genetics
  • Cardiac Output, Low / metabolism
  • Cells, Cultured
  • Coronary Vessels / cytology
  • Endothelial Cells / metabolism*
  • Fatty Acid-Binding Proteins / biosynthesis*
  • Fatty Acid-Binding Proteins / genetics
  • Fatty Acids / metabolism*
  • Glucose / metabolism
  • Heterozygote
  • Homeodomain Proteins / chemistry
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / physiology*
  • Humans
  • Lipoprotein Lipase / biosynthesis
  • Lipoprotein Lipase / genetics
  • Lipoproteins, VLDL / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Myocardium / metabolism*
  • Protein Interaction Mapping
  • RNA, Small Interfering / pharmacology
  • Tissue Array Analysis
  • Transcriptome

Substances

  • Basic Helix-Loop-Helix Transcription Factors
  • CD36 Antigens
  • Fatty Acid-Binding Proteins
  • Fatty Acids
  • Homeodomain Proteins
  • Lipoproteins, VLDL
  • Meox2 protein, mouse
  • RNA, Small Interfering
  • Tcf15 protein, mouse
  • LPL protein, human
  • Lipoprotein Lipase
  • Glucose