Low- and high-thermogenic brown adipocyte subpopulations coexist in murine adipose tissue

J Clin Invest. 2020 Jan 2;130(1):247-257. doi: 10.1172/JCI129167.

Abstract

Brown adipose tissue (BAT), as the main site of adaptive thermogenesis, exerts beneficial metabolic effects on obesity and insulin resistance. BAT has been previously assumed to contain a homogeneous population of brown adipocytes. Utilizing multiple mouse models capable of genetically labeling different cellular populations, as well as single-cell RNA sequencing and 3D tissue profiling, we discovered a brown adipocyte subpopulation with low thermogenic activity coexisting with the classical high-thermogenic brown adipocytes within the BAT. Compared with the high-thermogenic brown adipocytes, these low-thermogenic brown adipocytes had substantially lower Ucp1 and Adipoq expression, larger lipid droplets, and lower mitochondrial content. Functional analyses showed that, unlike the high-thermogenic brown adipocytes, the low-thermogenic brown adipocytes have markedly lower basal mitochondrial respiration, and they are specialized in fatty acid uptake. Upon changes in environmental temperature, the 2 brown adipocyte subpopulations underwent dynamic interconversions. Cold exposure converted low-thermogenic brown adipocytes into high-thermogenic cells. A thermoneutral environment had the opposite effect. The recruitment of high-thermogenic brown adipocytes by cold stimulation is not affected by high-fat diet feeding, but it does substantially decline with age. Our results revealed a high degree of functional heterogeneity of brown adipocytes.

Keywords: Adipose tissue; Metabolism.

Publication types

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

MeSH terms

  • Adipocytes, Brown / cytology
  • Adipocytes, Brown / metabolism*
  • Adiponectin / biosynthesis*
  • Adipose Tissue, Brown / cytology
  • Adipose Tissue, Brown / metabolism*
  • Animals
  • Gene Expression Regulation / physiology*
  • Mice
  • Thermogenesis / physiology*
  • Uncoupling Protein 1 / biosynthesis*

Substances

  • Adiponectin
  • Adipoq protein, mouse
  • Ucp1 protein, mouse
  • Uncoupling Protein 1