Activated Ask1-MKK4-p38MAPK/JNK stress signaling pathway in human omental fat tissue may link macrophage infiltration to whole-body Insulin sensitivity

J Clin Endocrinol Metab. 2009 Jul;94(7):2507-15. doi: 10.1210/jc.2009-0002. Epub 2009 Apr 7.

Abstract

Context: Adipose tissue in obesity is thought to be exposed to various stresses, predominantly in intraabdominal depots. We recently reported that p38MAPK and Jun N-terminal kinase (JNK), but not ERK and inhibitory-kappaB kinase beta, are more highly expressed and activated in human omental (OM) adipose tissue in obesity.

Objective: The aim was to investigate upstream components of the pathways that culminate in activation of p38MAPK and JNK.

Setting and patients: Phosphorylation and expression of kinases were studied in paired samples of OM and sc adipose tissue from lean and obese subjects of two different cohorts (n = 36 and n = 196) by Western and real-time PCR analyses. The association with fat distribution, macrophage infiltration, insulin sensitivity, and glucose metabolism was assessed by correlation analyses.

Results: The amount of phosphorylated forms of the kinases provided evidence for an activated stress-sensing pathway consisting of the MAP3K Ask1 (but not MLK3 or Tak1), and the MAP2Ks MKK4, 3/6, (but not MKK7), specifically in OM. OM Ask1-mRNA was more highly expressed in predominantly intraabdominally obese persons and most strongly correlated with estimated visceral fat. Diabetes was associated with higher OM Ask1-mRNA only in the lean group. In OM, macrophage infiltration strongly correlated with Ask1-mRNA, but the obesity-associated increase in Ask1-mRNA could largely be attributed to the adipocyte cell fraction. Finally, multivariate regression analyses revealed OM-Ask1 as an independent predictor of whole-body glucose uptake in euglycemic-hyperinsulinemic clamps.

Conclusions: An Ask1-MKK4-p38MAPK/JNK pathway reflects adipocyte stress associated with adipose tissue inflammation, linking visceral adiposity to whole-body insulin resistance in obesity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adult
  • Aged
  • Case-Control Studies
  • Chemotaxis / immunology
  • Enzyme Activation / physiology
  • Extracellular Signal-Regulated MAP Kinases / metabolism
  • Extracellular Signal-Regulated MAP Kinases / physiology
  • Female
  • Humans
  • Inflammation / immunology
  • Inflammation / metabolism
  • Insulin Resistance / physiology*
  • Intra-Abdominal Fat / enzymology
  • Intra-Abdominal Fat / immunology*
  • Intra-Abdominal Fat / metabolism
  • Intra-Abdominal Fat / pathology
  • JNK Mitogen-Activated Protein Kinases / metabolism
  • JNK Mitogen-Activated Protein Kinases / physiology*
  • MAP Kinase Kinase 4 / metabolism
  • MAP Kinase Kinase 4 / physiology*
  • MAP Kinase Kinase Kinase 5 / genetics
  • MAP Kinase Kinase Kinase 5 / metabolism
  • MAP Kinase Kinase Kinase 5 / physiology*
  • Macrophages / immunology
  • Macrophages / metabolism
  • Macrophages / physiology*
  • Male
  • Middle Aged
  • Obesity / immunology
  • Obesity / metabolism
  • Obesity / pathology
  • Omentum / metabolism
  • Omentum / pathology
  • Signal Transduction / physiology
  • Stress, Physiological / physiology
  • p38 Mitogen-Activated Protein Kinases / metabolism
  • p38 Mitogen-Activated Protein Kinases / physiology*

Substances

  • Extracellular Signal-Regulated MAP Kinases
  • JNK Mitogen-Activated Protein Kinases
  • p38 Mitogen-Activated Protein Kinases
  • MAP Kinase Kinase Kinase 5
  • MAP3K5 protein, human
  • MAP Kinase Kinase 4
  • MAP2K4 protein, human