Skeletal Muscle Insulin Resistance and Absence of Inflammation Characterize Insulin-Resistant Grade I Obese Women

PLoS One. 2016 Apr 25;11(4):e0154119. doi: 10.1371/journal.pone.0154119. eCollection 2016.

Abstract

Context: Obesity is associated with insulin-resistance (IR), the key feature of type 2 diabetes. Although chronic low-grade inflammation has been identified as a central effector of IR development, it has never been investigated simultaneously at systemic level and locally in skeletal muscle and adipose tissue in obese humans characterized for their insulin sensitivity.

Objectives: We compared metabolic parameters and inflammation at systemic and tissue levels in normal-weight and obese subjects with different insulin sensitivity to better understand the mechanisms involved in IR development.

Methods: 30 post-menopausal women were classified as normal-weight insulin-sensitive (controls, CT) and obese (grade I) insulin-sensitive (OIS) or insulin-resistant (OIR) according to their body mass index and homeostasis model assessment of IR index. They underwent a hyperinsulinemic-euglycemic clamp, blood sampling, skeletal muscle and subcutaneous adipose tissue biopsies, an activity questionnaire and a self-administrated dietary recall. We analyzed insulin sensitivity, inflammation and IR-related parameters at the systemic level. In tissues, insulin response was assessed by P-Akt/Akt expression and inflammation by macrophage infiltration as well as cytokines and IκBα expression.

Results: Systemic levels of lipids, adipokines, inflammatory cytokines, and lipopolysaccharides were equivalent between OIS and OIR subjects. In subcutaneous adipose tissue, the number of anti-inflammatory macrophages was higher in OIR than in CT and OIS and was associated with higher IL-6 level. Insulin induced Akt phosphorylation to the same extent in CT, OIS and OIR. In skeletal muscle, we could not detect any inflammation even though IκBα expression was lower in OIR compared to CT. However, while P-Akt/Akt level increased following insulin stimulation in CT and OIS, it remained unchanged in OIR.

Conclusion: Our results show that systemic IR occurs without any change in systemic and tissues inflammation. We identified a muscle defect in insulin response as an early mechanism of IR development in grade I obese post-menopausal women.

Publication types

  • Clinical Trial
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Blood Glucose / metabolism*
  • C-Reactive Protein
  • Case-Control Studies
  • Cell Movement / drug effects
  • Diabetes Mellitus, Type 2 / genetics
  • Diabetes Mellitus, Type 2 / metabolism*
  • Diabetes Mellitus, Type 2 / physiopathology
  • Diet
  • Female
  • Gene Expression Regulation
  • Glucose Clamp Technique
  • Humans
  • Inflammation
  • Insulin / administration & dosage
  • Insulin / metabolism*
  • Insulin Resistance*
  • Interleukin-6 / genetics
  • Interleukin-6 / metabolism
  • Lipopolysaccharides
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology
  • Middle Aged
  • Muscle, Skeletal / metabolism*
  • Muscle, Skeletal / physiopathology
  • NF-KappaB Inhibitor alpha / genetics
  • NF-KappaB Inhibitor alpha / metabolism
  • Phosphorylation
  • Postmenopause / metabolism
  • Proto-Oncogene Proteins c-akt / genetics
  • Proto-Oncogene Proteins c-akt / metabolism
  • Severity of Illness Index
  • Subcutaneous Fat / metabolism
  • Subcutaneous Fat / physiopathology
  • Surveys and Questionnaires

Substances

  • Blood Glucose
  • IL6 protein, human
  • Insulin
  • Interleukin-6
  • Lipopolysaccharides
  • NF-KappaB Inhibitor alpha
  • C-Reactive Protein
  • Proto-Oncogene Proteins c-akt

Grants and funding

This study was funded by the CHRU Montpellier PROM8685 and the French Society of Diabetes (http://www.sfdiabete.org/). OF and CA were recipient of a Ministère de l'Enseignement Supérieur et de la Recherche (www.enseignementsup-recherche.gouv.fr/) fellowship.