Dimerization interface of osteoprotegerin revealed by hydrogen-deuterium exchange mass spectrometry

J Biol Chem. 2018 Nov 9;293(45):17523-17535. doi: 10.1074/jbc.RA118.004489. Epub 2018 Sep 25.

Abstract

Previous structural studies of osteoprotegerin (OPG), a crucial negative regulator of bone remodeling and osteoclastogenesis, were mostly limited to the N-terminal ligand-binding domains. It is now known that the three C-terminal domains of OPG also play essential roles in its function by mediating OPG dimerization, OPG-heparan sulfate (HS) interactions, and formation of the OPG-HS-receptor activator of nuclear factor κB ligand (RANKL) ternary complex. Employing hydrogen-deuterium exchange MS methods, here we investigated the structure of full-length OPG in complex with HS or RANKL in solution. Our data revealed two noteworthy aspects of the OPG structure. First, we found that the interconnection between the N- and C-terminal domains is much more rigid than previously thought, possibly because of hydrophobic interactions between the fourth cysteine-rich domain and the first death domain. Second, we observed that two hydrophobic clusters located in two separate C-terminal domains directly contribute to OPG dimerization, likely by forming a hydrophobic dimerization interface. Aided by site-directed mutagenesis, we further demonstrated that an intact dimerization interface is essential for the biological activity of OPG. Our study represents an important step toward deciphering the structure-function relationship of the full-length OPG protein.

Keywords: RANKL; bone loss; dimerization; heparan sulfate; heparin-binding protein; hydrogen exchange mass spectrometry; hydrogen-deuterium exchange; osteoclastogenesis; osteoporosis; osteoprotegerin.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Deuterium Exchange Measurement*
  • Heparitin Sulfate / chemistry
  • Heparitin Sulfate / genetics
  • Heparitin Sulfate / metabolism
  • Mass Spectrometry*
  • Mice
  • Osteoprotegerin / chemistry*
  • Osteoprotegerin / genetics
  • Osteoprotegerin / metabolism
  • Protein Domains
  • Protein Multimerization*
  • RANK Ligand / chemistry
  • RANK Ligand / genetics
  • RANK Ligand / metabolism

Substances

  • Osteoprotegerin
  • RANK Ligand
  • Tnfrsf11b protein, mouse
  • Tnfsf11 protein, mouse
  • Heparitin Sulfate

Associated data

  • PDB/4E4D
  • PDB/3URF