Probing Receptor Specificity by Sampling the Conformational Space of the Insulin-like Growth Factor II C-domain

J Biol Chem. 2016 Sep 30;291(40):21234-21245. doi: 10.1074/jbc.M116.741041. Epub 2016 Aug 10.

Abstract

Insulin and insulin-like growth factors I and II are closely related protein hormones. Their distinct evolution has resulted in different yet overlapping biological functions with insulin becoming a key regulator of metabolism, whereas insulin-like growth factors (IGF)-I/II are major growth factors. Insulin and IGFs cross-bind with different affinities to closely related insulin receptor isoforms A and B (IR-A and IR-B) and insulin-like growth factor type I receptor (IGF-1R). Identification of structural determinants in IGFs and insulin that trigger their specific signaling pathways is of increasing importance in designing receptor-specific analogs with potential therapeutic applications. Here, we developed a straightforward protocol for production of recombinant IGF-II and prepared six IGF-II analogs with IGF-I-like mutations. All modified molecules exhibit significantly reduced affinity toward IR-A, particularly the analogs with a Pro-Gln insertion in the C-domain. Moreover, one of the analogs has enhanced binding affinity for IGF-1R due to a synergistic effect of the Pro-Gln insertion and S29N point mutation. Consequently, this analog has almost a 10-fold higher IGF-1R/IR-A binding specificity in comparison with native IGF-II. The established IGF-II purification protocol allowed for cost-effective isotope labeling required for a detailed NMR structural characterization of IGF-II analogs that revealed a link between the altered binding behavior of selected analogs and conformational rearrangement of their C-domains.

Keywords: insulin; insulin receptor; insulin-like growth factor (IGF); nuclear magnetic resonance (NMR); structural biology; structure-function.

MeSH terms

  • Amino Acid Substitution
  • Antigens, CD / chemistry*
  • Antigens, CD / genetics
  • Antigens, CD / metabolism
  • Humans
  • Insulin-Like Growth Factor II / chemistry*
  • Insulin-Like Growth Factor II / genetics
  • Insulin-Like Growth Factor II / metabolism
  • Mutation, Missense
  • Protein Domains
  • Protein Isoforms / chemistry
  • Protein Isoforms / genetics
  • Protein Isoforms / metabolism
  • Receptor, IGF Type 1 / chemistry*
  • Receptor, IGF Type 1 / genetics
  • Receptor, IGF Type 1 / metabolism
  • Receptor, Insulin / chemistry*
  • Receptor, Insulin / genetics
  • Receptor, Insulin / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism

Substances

  • Antigens, CD
  • IGF2 protein, human
  • Protein Isoforms
  • Recombinant Proteins
  • Insulin-Like Growth Factor II
  • INSR protein, human
  • Receptor, IGF Type 1
  • Receptor, Insulin

Associated data

  • PDB/1GZR
  • PDB/4XSS