Cellular mechanism of nutritionally induced insulin resistance: the desert rodent Psammomys obesus and other animals in which insulin resistance leads to detrimental outcome

J Basic Clin Physiol Pharmacol. 1998;9(2-4):347-85. doi: 10.1515/JBCPP.1998.9.2-4.347.

Abstract

Animal species with genetic or nutritionally induced insulin resistance, diabetes and obesity (diabesity) may be divided into two broad groups: those with resilient pancreatic beta-cells, e.g. ob/ob mice and fa/fa rats, capable of long-lasting compensatory insulin over-secretion, and those with labile beta-cells in which the secretion pressure leads to irreversible beta-cell degranulation, e.g. db/db mice, Macaca mulatta primates, ZDF diabetic rats. Prominent in this group is the Israeli desert gerbil Psammomys obesus (sand rat), which features low insulin receptor density in liver and muscle. On a diet of relatively high energy, the capacity of insulin to activate the receptor tyrosine kinase (TK) is reduced, in the face of hyperinsulinemia. With the following hyperglycemia, the rising insulin resistance imposes a vicious cycle of insulinemia and glycemia, accentuating the TK activation failure and the beta-cell failure. Among various factors affecting the insulin signaling pathway, multisite phosphorylation, including serine and threonine on the receptor beta-subunit, due to overexpression of certain protein kinase C isoforms, seems to be responsible for the inhibition of the critical step of TK phosphorylation activity. The compromised TK activation is reversible by diet restriction which restores to normal the glycemia and insulinemia. The beta-cell response to long-lasting stimulation and the receptor malfunction in diabesity have implications for a similar etiology in human insulin resistance syndrome and type 2 diabetes, particularly in populations emerging from a food scarce environment into nutritional affluence, inappropriate to the human metabolic capacity. It is suggested that the "thrifty gene" is characterized by a low threshold for insulin secretion and low capacity for insulin clearance. Thus, nutritionally-induced hyperinsulinemia is potentiated and becomes the primary phenotypic expression of the thrifty gene, linked to the insulin receptor signaling pathway malfunction.

MeSH terms

  • Animals
  • Blood Glucose / chemistry
  • Diabetes Mellitus, Experimental / diet therapy
  • Dietary Carbohydrates / administration & dosage
  • Dietary Carbohydrates / adverse effects
  • Disease Models, Animal
  • Gerbillinae* / genetics
  • Glucose Transporter Type 4
  • Humans
  • Hyperglycemia / etiology
  • Hyperinsulinism / etiology
  • Insulin / blood
  • Insulin / pharmacology
  • Insulin Resistance* / genetics
  • Islets of Langerhans / metabolism
  • Mice
  • Monosaccharide Transport Proteins / drug effects
  • Muscle Proteins*
  • Rats
  • Receptor, Insulin / drug effects
  • Signal Transduction / physiology

Substances

  • Blood Glucose
  • Dietary Carbohydrates
  • Glucose Transporter Type 4
  • Insulin
  • Monosaccharide Transport Proteins
  • Muscle Proteins
  • SLC2A4 protein, human
  • Slc2a4 protein, mouse
  • Slc2a4 protein, rat
  • Receptor, Insulin