An arginine to cysteine(252) mutation in insulin receptors from a patient with severe insulin resistance inhibits receptor internalisation but preserves signalling events

Diabetologia. 2002 May;45(5):657-67. doi: 10.1007/s00125-002-0798-5. Epub 2002 Apr 5.

Abstract

Aims/hypothesis: We examined the properties of a mutant insulin receptor (IR) with an Arg(252) to Cys (IR(R252C)) substitution in the alpha-subunit originally identified in a patient with extreme insulin resistance and acanthosis nigricans.

Methods: We studied IR cell biology and signalling pathways in Chinese Hamster Ovary cells overexpressing this IR(R252C).

Results: Our investigation showed an impairment in insulin binding to IR(R252C) related mostly to a reduced affinity of the receptor for insulin and to a reduced rate of IR(R252C) maturation; an inhibition of IR(R252C)-mediated endocytosis resulting in a decreased insulin degradation and insulin-induced receptor down-regulation; a maintenance of IR(R252C) on microvilli even in the presence of insulin; a similar autophosphorylation of mutant IR(R252C) followed by IRS 1/IRS 2 phosphorylation, p85 association with IRS 1 and IRS 2 and Akt phosphorylation similar to those observed in cells expressing wild type IR (IRwt); and finally, a reduced insulin-induced Shc phosphorylation accompanied by decreased ERK1/2 phosphorylation and activity and of thymidine incorporation into DNA in cells expressing IR(R252C) as compared to cells expressing IRwt.

Conclusion/interpretation: These observations suggest that: parameters other than tyrosine kinase activation participate in or control the first steps of IR internalisation or both; IR-mediated IRS 1/2 phosphorylation can be achieved from the cell surface and microvilli in particular; Shc phosphorylation and its subsequent signalling pathway might require IR internalisation; defective IR endocytosis correlates with an enhancement of some biological responses to insulin and attenuation of others.

Publication types

  • Case Reports
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acanthosis Nigricans / genetics*
  • Adult
  • Amino Acid Substitution
  • Animals
  • Arginine*
  • CHO Cells
  • Cricetinae
  • Cysteine*
  • DNA / biosynthesis
  • Humans
  • Insulin / metabolism
  • Insulin Resistance / genetics*
  • Male
  • Mitogen-Activated Protein Kinase 1 / metabolism
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases / metabolism
  • Mutation*
  • Phosphorylation
  • Protein Subunits
  • Protein Transport
  • Receptor, Insulin / genetics*
  • Receptor, Insulin / metabolism*
  • Receptor, Insulin / physiology
  • Recombinant Proteins / metabolism
  • Signal Transduction / physiology*
  • Thymidine / metabolism
  • Transfection

Substances

  • Insulin
  • Protein Subunits
  • Recombinant Proteins
  • DNA
  • Arginine
  • Receptor, Insulin
  • Mitogen-Activated Protein Kinase 1
  • Mitogen-Activated Protein Kinase 3
  • Mitogen-Activated Protein Kinases
  • Cysteine
  • Thymidine