Single-Cell RNA Profiling Reveals Adipocyte to Macrophage Signaling Sufficient to Enhance Thermogenesis

Cell Rep. 2020 Aug 4;32(5):107998. doi: 10.1016/j.celrep.2020.107998.

Abstract

Adipocytes deficient in fatty acid synthase (iAdFASNKO) emit signals that mimic cold exposure to enhance the appearance of thermogenic beige adipocytes in mouse inguinal white adipose tissues (iWATs). Both cold exposure and iAdFASNKO upregulate the sympathetic nerve fiber (SNF) modulator Neuregulin 4 (Nrg4), activate SNFs, and require adipocyte cyclic AMP/protein kinase A (cAMP/PKA) signaling for beige adipocyte appearance, as it is blocked by adipocyte Gsα deficiency. Surprisingly, however, in contrast to cold-exposed mice, neither iWAT denervation nor Nrg4 loss attenuated adipocyte browning in iAdFASNKO mice. Single-cell transcriptomic analysis of iWAT stromal cells revealed increased macrophages displaying gene expression signatures of the alternately activated type in iAdFASNKO mice, and their depletion abrogated iWAT beiging. Altogether, these findings reveal that divergent cellular pathways are sufficient to cause adipocyte browning. Importantly, adipocyte signaling to enhance alternatively activated macrophages in iAdFASNKO mice is associated with enhanced adipose thermogenesis independent of the sympathetic neuron involvement this process requires in the cold.

Keywords: beige adipocytes; de novo lipogenesis; macrophage polarization; stromal vascular fraction; sympathetic nerve fibers.

Publication types

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

MeSH terms

  • Adipocytes, Beige / metabolism*
  • Adipose Tissue, Brown / metabolism
  • Adipose Tissue, White / metabolism
  • Animals
  • Cell Polarity
  • Cold Temperature
  • Cyclic AMP / metabolism
  • Denervation
  • Fatty Acid Synthases / metabolism
  • Macrophage Activation
  • Macrophages / metabolism*
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Neuregulins / deficiency
  • Neuregulins / metabolism
  • Phenotype
  • RNA / metabolism*
  • Signal Transduction*
  • Single-Cell Analysis*
  • Thermogenesis*
  • Uncoupling Protein 1 / genetics
  • Uncoupling Protein 1 / metabolism
  • Up-Regulation / genetics

Substances

  • Neuregulins
  • Uncoupling Protein 1
  • neuregulin-4
  • RNA
  • Cyclic AMP
  • Fatty Acid Synthases