Galectin-3 promotes the adipogenic differentiation of PDGFRα+ cells and ectopic fat formation in regenerating muscle

Development. 2022 Feb 1;149(3):dev199443. doi: 10.1242/dev.199443. Epub 2022 Feb 3.

Abstract

Worldwide prevalence of obesity is associated with the increase of lifestyle-related diseases. The accumulation of intermuscular adipose tissue (IMAT) is considered a major problem whereby obesity leads to sarcopenia and metabolic disorders and thus is a promising target for treating these pathological conditions. However, whereas obesity-associated IMAT is suggested to originate from PDGFRα+ mesenchymal progenitors, the processes underlying this adipogenesis remain largely unexplored. Here, we comprehensively investigated intra- and extracellular changes associated with these processes using single-cell RNA sequencing and mass spectrometry. Our single-cell RNA sequencing analysis identified a small PDGFRα+ cell population in obese mice directed strongly toward adipogenesis. Proteomic analysis showed that the appearance of this cell population is accompanied by an increase in galectin-3 in interstitial environments, which was found to activate adipogenic PPARγ signals in PDGFRα+ cells. Moreover, IMAT formation during muscle regeneration was significantly suppressed in galectin-3 knockout mice. Our findings, together with these multi-omics datasets, could unravel microenvironmental networks during muscle regeneration highlighting possible therapeutic targets against IMAT formation in obesity.

Keywords: Cellular senescence; Intermuscular adipose tissue; Mouse; PDGFRα+ mesenchymal progenitors; Sarcopenia; Single-cell RNA-Seq.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / genetics
  • Actins / metabolism
  • Adipogenesis
  • Adipose Tissue / cytology
  • Adipose Tissue / metabolism*
  • Animals
  • Cardiotoxins / pharmacology
  • Cell Differentiation
  • Cellular Senescence / genetics
  • Diet, High-Fat
  • Female
  • Galectin 3 / deficiency
  • Galectin 3 / genetics
  • Galectin 3 / metabolism*
  • Mesenchymal Stem Cells / cytology
  • Mesenchymal Stem Cells / metabolism
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Muscle, Skeletal / cytology
  • Muscle, Skeletal / drug effects
  • Muscle, Skeletal / physiology*
  • Obesity / metabolism
  • Obesity / pathology
  • PPAR gamma / metabolism
  • Receptor, Platelet-Derived Growth Factor alpha / deficiency
  • Receptor, Platelet-Derived Growth Factor alpha / genetics
  • Receptor, Platelet-Derived Growth Factor alpha / metabolism*
  • Regeneration
  • Signal Transduction / genetics

Substances

  • Acta2 protein, mouse
  • Actins
  • Cardiotoxins
  • Galectin 3
  • Lgals3 protein, mouse
  • PPAR gamma
  • Receptor, Platelet-Derived Growth Factor alpha