Disruption of Lipid Raft Function Increases Expression and Secretion of Monocyte Chemoattractant Protein-1 in 3T3-L1 Adipocytes

PLoS One. 2016 Dec 28;11(12):e0169005. doi: 10.1371/journal.pone.0169005. eCollection 2016.

Abstract

The adipocyte is unique in its capacity to store lipids. In addition to triglycerides, the adipocyte stores a significant amount of cholesterol. Moreover, obese adipocytes are characterized by a redistribution of cholesterol with depleted cholesterol in the plasma membrane, suggesting that cholesterol perturbation may play a role in adipocyte dysfunction. We used methyl-β-cyclodextrin (MβCD), a molecule with high affinity for cholesterol, to rapidly deplete cholesterol level in differentiated 3T3-L1 adipocytes. We tested whether this perturbation altered adipocyte secretion of monocyte chemoattractant protein-1 (MCP-1), a chemokine that is elevated in obesity and is linked to obesity-associated chronic diseases. Depletion of cholesterol by MβCD increased MCP-1 secretion as well as the mRNA and protein levels, suggesting perturbation at biosynthesis and secretion. Pharmacological inhibition revealed that NF-κB, but not MEK, p38 and JNK, was involved in MβCD-stimulated MCP-1 biosynthesis and secretion in adipocytes. Finally, another cholesterol-binding drug, filipin, also induced MCP-1 secretion without altering membrane cholesterol level. Interestingly, both MβCD and filipin disturbed the integrity of lipid rafts, the membrane microdomains enriched in cholesterol. Thus, the depletion of membrane cholesterol in obese adipocytes may result in dysfunction of lipid rafts, leading to the elevation of proinflammatory signaling and MCP-1 secretion in adipocytes.

MeSH terms

  • 3T3-L1 Cells
  • Adipocytes / cytology
  • Adipocytes / metabolism*
  • Animals
  • Cell Differentiation
  • Chemokine CCL2 / metabolism*
  • Cholesterol / metabolism*
  • Gene Expression Regulation / drug effects
  • Membrane Microdomains / metabolism
  • Membrane Microdomains / pathology*
  • Mice
  • NF-kappa B / metabolism*
  • Signal Transduction
  • beta-Cyclodextrins / pharmacology

Substances

  • Ccl2 protein, mouse
  • Chemokine CCL2
  • NF-kappa B
  • beta-Cyclodextrins
  • methyl-beta-cyclodextrin
  • Cholesterol

Grants and funding

This study was supported by the Ministry of Science and Technology Grant NSC101-2320-B-182-007 and NSC102-2320-B-182-022-MY3, and Chang Gung Medical Research Project CMRPD1C0591~3, CMRPD180513, and BMRPC03. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.