Uncoupling the Mitogenic and Metabolic Functions of FGF1 by Tuning FGF1-FGF Receptor Dimer Stability

Cell Rep. 2017 Aug 15;20(7):1717-1728. doi: 10.1016/j.celrep.2017.06.063.

Abstract

The recent discovery of metabolic roles for fibroblast growth factor 1 (FGF1) in glucose homeostasis has expanded the functions of this classically known mitogen. To dissect the molecular basis for this functional pleiotropy, we engineered an FGF1 partial agonist carrying triple mutations (FGF1ΔHBS) that diminished its ability to induce heparan sulfate (HS)-assisted FGF receptor (FGFR) dimerization and activation. FGF1ΔHBS exhibited a severely reduced proliferative potential, while preserving the full metabolic activity of wild-type FGF1 in vitro and in vivo. Hence, suboptimal FGFR activation by a weak FGF1-FGFR dimer is sufficient to evoke a metabolic response, whereas full FGFR activation by stable and sustained dimerization is required to elicit a mitogenic response. In addition to providing a physical basis for the diverse activities of FGF1, our findings will impact ongoing drug discoveries targeting FGF1 and related FGFs for the treatment of a variety of human diseases.

Keywords: FGF receptor; db/db mice; fibroblast growth factor 1; glucose uptake; heparin sulfate; metabolism; mitogenesis; receptor dimerization; signaling pathways; threshold.

MeSH terms

  • 3T3-L1 Cells
  • Animals
  • Binding Sites
  • Cell Line, Tumor
  • Cloning, Molecular
  • Escherichia coli / genetics
  • Escherichia coli / metabolism
  • Fibroblast Growth Factor 1 / chemistry*
  • Fibroblast Growth Factor 1 / genetics
  • Fibroblast Growth Factor 1 / metabolism
  • Fibroblast Growth Factor 1 / pharmacology
  • Gene Expression
  • Hepatocytes / cytology
  • Hepatocytes / drug effects*
  • Hepatocytes / metabolism
  • Humans
  • Mice
  • Mice, Inbred C57BL
  • Mitogens / chemistry*
  • Mitogens / genetics
  • Mitogens / metabolism
  • Mitogens / pharmacology
  • Models, Molecular
  • NIH 3T3 Cells
  • Protein Binding
  • Protein Conformation, alpha-Helical
  • Protein Conformation, beta-Strand
  • Protein Interaction Domains and Motifs
  • Protein Multimerization
  • Protein Stability
  • Rats
  • Receptors, Fibroblast Growth Factor / chemistry*
  • Receptors, Fibroblast Growth Factor / genetics
  • Receptors, Fibroblast Growth Factor / metabolism
  • Recombinant Proteins / chemistry
  • Recombinant Proteins / genetics
  • Recombinant Proteins / metabolism

Substances

  • Mitogens
  • Receptors, Fibroblast Growth Factor
  • Recombinant Proteins
  • Fibroblast Growth Factor 1