CCAAT/enhancer-binding protein β (C/EBPβ) expression regulates dietary-induced inflammation in macrophages and adipose tissue in mice

J Biol Chem. 2012 Oct 5;287(41):34349-60. doi: 10.1074/jbc.M112.410613. Epub 2012 Aug 19.

Abstract

Strong evidence exists for a link between chronic low level inflammation and dietary-induced insulin resistance; however, little is known about the transcriptional networks involved. Here we show that high fat diet (HFD) or saturated fatty acid exposure directly activates CCAAT/enhancer-binding protein β (C/EBPβ) protein expression in liver, adipocytes, and macrophages. Global C/EBPβ deletion prevented HFD-induced inflammation and surprisingly increased mitochondrial gene expression in white adipose tissue along with brown adipose tissue markers PRDM16, CIDEa, and UCP1, consistent with a resistance to HFD-induced obesity. In isolated peritoneal macrophages from C/EBPβ(-/-) mice, the anti-inflammatory gene LXRα and its targets SCD1 and DGAT2 were strikingly up-regulated along with IL-10, while NLRP3, a gene important for activating the inflammasome, was suppressed in response to palmitate. Using RAW 264.7 macrophage cells or 3T3-L1 adipocytes, C/EBPβ knockdown prevented palmitate-induced inflammation and p65-NFκB DNA binding activity, while C/EBPβ overexpression induced NFκB binding, JNK activation, and pro-inflammatory cytokine gene expression directly. Finally, chimeric bone marrow mice transplanted with bone marrow lacking C/EBPβ(-/-) demonstrated reduced systemic and adipose tissue inflammatory markers, macrophage content, and maintained insulin sensitivity on HFD. Taken together, these results demonstrate that HFD or palmitate exposure triggers C/EBPβ expression that controls expression of distinct aspects of alternative macrophage activation. Reducing C/EBPβ in macrophages confers protection from HFD-induced systemic inflammation and insulin resistance, suggesting it may be an attractive therapeutic target for ameliorating obesity-induced inflammatory responses.

Publication types

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

MeSH terms

  • 3T3-L1 Cells
  • Adipose Tissue, Brown / metabolism*
  • Adipose Tissue, Brown / pathology
  • Animals
  • Antigens, Differentiation / genetics
  • Antigens, Differentiation / metabolism
  • CCAAT-Enhancer-Binding Protein-beta / biosynthesis*
  • CCAAT-Enhancer-Binding Protein-beta / genetics
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Dietary Fats / adverse effects*
  • Dietary Fats / pharmacology
  • Enzyme Activation / drug effects
  • Enzyme Activation / genetics
  • Gene Expression Regulation / drug effects*
  • Inflammasomes / genetics
  • Inflammasomes / metabolism
  • Inflammation / genetics
  • Inflammation / metabolism
  • Inflammation / pathology
  • Interleukin-10 / genetics
  • Interleukin-10 / metabolism
  • MAP Kinase Kinase 4 / genetics
  • MAP Kinase Kinase 4 / metabolism
  • Macrophage Activation / drug effects*
  • Macrophage Activation / genetics
  • Macrophages / metabolism*
  • Macrophages / pathology
  • Mice
  • Mice, Knockout
  • Mitochondria / genetics
  • Mitochondria / metabolism
  • Mitochondria / pathology
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Obesity / chemically induced
  • Obesity / genetics
  • Obesity / metabolism*
  • Obesity / pathology
  • Transcription Factor RelA / genetics
  • Transcription Factor RelA / metabolism

Substances

  • Antigens, Differentiation
  • CCAAT-Enhancer-Binding Protein-beta
  • Carrier Proteins
  • Cebpb protein, mouse
  • Dietary Fats
  • IL10 protein, mouse
  • Inflammasomes
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • Nlrp3 protein, mouse
  • Rela protein, mouse
  • Transcription Factor RelA
  • Interleukin-10
  • MAP Kinase Kinase 4