An engineered transforming growth factor β (TGF-β) monomer that functions as a dominant negative to block TGF-β signaling

J Biol Chem. 2017 Apr 28;292(17):7173-7188. doi: 10.1074/jbc.M116.768754. Epub 2017 Feb 22.

Abstract

The transforming growth factor β isoforms, TGF-β1, -β2, and -β3, are small secreted homodimeric signaling proteins with essential roles in regulating the adaptive immune system and maintaining the extracellular matrix. However, dysregulation of the TGF-β pathway is responsible for promoting the progression of several human diseases, including cancer and fibrosis. Despite the known importance of TGF-βs in promoting disease progression, no inhibitors have been approved for use in humans. Herein, we describe an engineered TGF-β monomer, lacking the heel helix, a structural motif essential for binding the TGF-β type I receptor (TβRI) but dispensable for binding the other receptor required for TGF-β signaling, the TGF-β type II receptor (TβRII), as an alternative therapeutic modality for blocking TGF-β signaling in humans. As shown through binding studies and crystallography, the engineered monomer retained the same overall structure of native TGF-β monomers and bound TβRII in an identical manner. Cell-based luciferase assays showed that the engineered monomer functioned as a dominant negative to inhibit TGF-β signaling with a Ki of 20-70 nm Investigation of the mechanism showed that the high affinity of the engineered monomer for TβRII, coupled with its reduced ability to non-covalently dimerize and its inability to bind and recruit TβRI, enabled it to bind endogenous TβRII but prevented it from binding and recruiting TβRI to form a signaling complex. Such engineered monomers provide a new avenue to probe and manipulate TGF-β signaling and may inform similar modifications of other TGF-β family members.

Keywords: cancer; cell signaling; dominant negative; fibrosis; inhibitor; protein engineering; transforming growth factor beta (TGF-B).

MeSH terms

  • Amino Acid Motifs
  • Animals
  • Disease Progression
  • Extracellular Matrix / metabolism
  • Fluorescence Resonance Energy Transfer
  • HEK293 Cells
  • Humans
  • Kinetics
  • Mice
  • Protein Binding
  • Protein Engineering / methods*
  • Protein Folding
  • Protein Isoforms
  • Protein Multimerization
  • Protein Serine-Threonine Kinases / antagonists & inhibitors*
  • Protein Serine-Threonine Kinases / metabolism
  • Receptor, Transforming Growth Factor-beta Type I
  • Receptors, Transforming Growth Factor beta / antagonists & inhibitors*
  • Receptors, Transforming Growth Factor beta / metabolism
  • Signal Transduction*
  • Solubility
  • Surface Plasmon Resonance
  • Transforming Growth Factor beta / chemistry*
  • Transforming Growth Factor beta / metabolism
  • Ultracentrifugation

Substances

  • Protein Isoforms
  • Receptors, Transforming Growth Factor beta
  • Transforming Growth Factor beta
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type I

Associated data

  • PDB/2PJY
  • PDB/2TGI
  • PDB/1M9Z