GLUT4 defects in adipose tissue are early signs of metabolic alterations in Alms1GT/GT, a mouse model for obesity and insulin resistance

PLoS One. 2014 Oct 9;9(10):e109540. doi: 10.1371/journal.pone.0109540. eCollection 2014.

Abstract

Dysregulation of signaling pathways in adipose tissue leading to insulin resistance can contribute to the development of obesity-related metabolic disorders. Alström Syndrome, a recessive ciliopathy, caused by mutations in ALMS1, is characterized by progressive metabolic alterations such as childhood obesity, hyperinsulinemia, and type 2 diabetes. Here we investigated the role of Alms1 disruption in AT expansion and insulin responsiveness in a murine model for Alström Syndrome. A gene trap insertion in Alms1 on the insulin sensitive C57BL6/Ei genetic background leads to early hyperinsulinemia and a progressive increase in body weight. At 6 weeks of age, before the onset of the metabolic disease, the mutant mice had enlarged fat depots with hypertrophic adipocytes, but without signs of inflammation. Expression of lipogenic enzymes was increased. Pre-adipocytes isolated from mutant animals demonstrated normal adipogenic differentiation but gave rise to mature adipocytes with reduced insulin-stimulated glucose uptake. Assessment of whole body glucose homeostasis revealed glucose intolerance. Insulin stimulation resulted in proper AKT phosphorylation in adipose tissue. However, the total amount of glucose transporter 4 (SLC4A2) and its translocation to the plasma membrane were reduced in mutant adipose depots compared to wildtype littermates. Alterations in insulin stimulated trafficking of glucose transporter 4 are an early sign of metabolic dysfunction in Alström mutant mice, providing a possible explanation for the reduced glucose uptake and the compensatory hyperinsulinemia. The metabolic signaling deficits either reside downstream or are independent of AKT activation and suggest a role for ALMS1 in GLUT4 trafficking. Alström mutant mice represent an interesting model for the development of metabolic disease in which adipose tissue with a reduced glucose uptake can expand by de novo lipogenesis to an obese state.

Publication types

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

MeSH terms

  • Adipocytes / drug effects
  • Adipocytes / metabolism*
  • Adipocytes / pathology
  • Adipogenesis / genetics
  • Adipose Tissue / metabolism
  • Adipose Tissue / pathology
  • Alstrom Syndrome / genetics*
  • Alstrom Syndrome / metabolism
  • Alstrom Syndrome / pathology
  • Animals
  • Biological Transport
  • Body Weight
  • Cell Cycle Proteins
  • Chloride-Bicarbonate Antiporters / genetics
  • Chloride-Bicarbonate Antiporters / metabolism
  • DNA-Binding Proteins / deficiency
  • DNA-Binding Proteins / genetics*
  • Disease Models, Animal
  • Gene Expression Regulation
  • Glucose / metabolism
  • Glucose Intolerance
  • Humans
  • Hyperinsulinism / genetics*
  • Hyperinsulinism / metabolism
  • Hyperinsulinism / pathology
  • Insulin / metabolism
  • Insulin / pharmacology
  • Insulin Resistance
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Phosphorylation
  • Primary Cell Culture
  • Signal Transduction

Substances

  • Alms1 protein, mouse
  • Cell Cycle Proteins
  • Chloride-Bicarbonate Antiporters
  • DNA-Binding Proteins
  • Insulin
  • Slc4a2 protein, mouse
  • Glucose