12/15-lipoxygenase products induce inflammation and impair insulin signaling in 3T3-L1 adipocytes

Obesity (Silver Spring). 2009 Sep;17(9):1657-63. doi: 10.1038/oby.2009.192. Epub 2009 Jun 11.

Abstract

Inflammation and insulin resistance associated with visceral obesity are important risk factors for the development of type 2 diabetes, atherosclerosis, and the metabolic syndrome. The 12/15-lipoxygenase (12/15-LO) enzyme has been linked to inflammatory changes in blood vessels that precede the development of atherosclerosis. The expression and role of 12/15-LO in adipocytes have not been evaluated. We found that 12/15-LO mRNA was dramatically upregulated in white epididymal adipocytes of high-fat fed mice. 12/15-LO was poorly expressed in 3T3-L1 fibroblasts and was upregulated during differentiation into adipocytes. Interestingly, the saturated fatty acid palmitate, a major component of high fat diets, augmented expression of 12/15-LO in vitro. When 3T3-L1 adipocytes were treated with the 12/15-LO products, 12-hydroxyeicosatetranoic acid (12(S)-HETE) and 12-hydroperoxyeicosatetraenoic acid (12(S)-HPETE), expression of proinflammatory cytokine genes, including tumor necrosis factor-alpha (TNF-alpha), monocyte chemoattractant protein 1 (MCP-1), interleukin 6 (IL-6), and IL-12p40, was upregulated whereas anti-inflammatory adiponectin gene expression was downregulated. 12/15-LO products also augmented c-Jun N-terminal kinase 1 (JNK-1) phosphorylation, a known negative regulator of insulin signaling. Consistent with impaired insulin signaling, we found that insulin-stimulated 3T3-L1 adipocytes exhibited decreased IRS-1(Tyr) phosphorylation, increased IRS-1(Ser) phosphorylation, and impaired Akt phosphorylation when treated with 12/15-LO product. Taken together, our data suggest that 12/15-LO products create a proinflammatory state and impair insulin signaling in 3T3-L1 adipocytes. Because 12/15-LO expression is upregulated in visceral adipocytes by high-fat feeding in vivo and also by addition of palmitic acid in vitro, we propose that 12/15-LO plays a role in promoting inflammation and insulin resistance associated with obesity.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • 12-Hydroxy-5,8,10,14-eicosatetraenoic Acid / metabolism
  • 3T3-L1 Cells
  • Adipocytes / enzymology*
  • Adiponectin / metabolism
  • Animals
  • Arachidonate 12-Lipoxygenase / genetics
  • Arachidonate 12-Lipoxygenase / metabolism*
  • Arachidonate 15-Lipoxygenase / genetics
  • Arachidonate 15-Lipoxygenase / metabolism*
  • Cell Differentiation
  • Cytokines / metabolism
  • Disease Models, Animal
  • Gene Expression Regulation, Enzymologic
  • Inflammation / enzymology*
  • Inflammation / physiopathology
  • Inflammation Mediators / metabolism*
  • Insulin / metabolism*
  • Insulin Receptor Substrate Proteins / metabolism
  • Insulin Resistance*
  • Leukotrienes / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mitogen-Activated Protein Kinase 8 / metabolism
  • Obesity / enzymology*
  • Obesity / physiopathology
  • Palmitic Acid / metabolism
  • Phosphorylation
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Messenger / metabolism
  • Signal Transduction*
  • Time Factors
  • Up-Regulation

Substances

  • 12-15-lipoxygenase
  • Adiponectin
  • Adipoq protein, mouse
  • Cytokines
  • Inflammation Mediators
  • Insulin
  • Insulin Receptor Substrate Proteins
  • Irs1 protein, mouse
  • Leukotrienes
  • RNA, Messenger
  • Palmitic Acid
  • 12-Hydroxy-5,8,10,14-eicosatetraenoic Acid
  • 12-HPETE
  • Arachidonate 12-Lipoxygenase
  • Arachidonate 15-Lipoxygenase
  • Proto-Oncogene Proteins c-akt
  • Mitogen-Activated Protein Kinase 8