Biological and structural characterization of glycosylation on ephrin-A1, a preferred ligand for EphA2 receptor tyrosine kinase

J Biol Chem. 2013 Jun 21;288(25):18448-57. doi: 10.1074/jbc.M113.464008. Epub 2013 May 9.

Abstract

The EphA2 receptor tyrosine kinase is overexpressed in a number of malignancies and is activated by ephrin ligands, most commonly by ephrin-A1. The crystal structure of the ligand-receptor complex revealed a glycosylation on the Asn-26 of ephrin-A1. Here we report for the first time the significance of the glycosylation in the biology of EphA2 and ephrin-A1. Ephrin-A1 was enzymatically deglycosylated, and its activity was evaluated in several assays using glioblastoma (GBM) cells and recombinant EphA2. We found that deglycosylated ephrin-A1 does not efficiently induce EphA2 receptor internalization and degradation, and does not activate the downstream signaling pathways involved in cell migration and proliferation. Data obtained by surface plasmon resonance confirms that deglycosylated ephrin-A1 does not bind EphA2 with high affinity. Mutations in the glycosylation site on ephrin-A1 result in protein aggregation and mislocalization. Analysis of Eph/ephrin crystal structures reveals an interaction between the ligand's carbohydrates and two residues of EphA2: Asp-78 and Lys-136. These findings suggest that the glycosylation on ephrin-A1 plays a critical role in the binding and activation of the EphA2 receptor.

Keywords: Crystal Structure; EphA2; Glycosylation; Ligand-binding Protein; Receptor; Receptors; Signaling; ephrin-A1.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Amino Acid Sequence
  • Binding Sites / genetics
  • Binding, Competitive
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Movement
  • Cell Proliferation
  • Crystallography, X-Ray
  • Ephrin-A1 / chemistry
  • Ephrin-A1 / genetics
  • Ephrin-A1 / metabolism*
  • Ephrin-A2 / genetics
  • Ephrin-A2 / metabolism
  • Glycosylation
  • Humans
  • Ligands
  • Models, Molecular
  • Molecular Sequence Data
  • Mutation
  • Protein Binding
  • Protein Multimerization
  • Protein Structure, Tertiary
  • Receptor, EphA2 / chemistry
  • Receptor, EphA2 / genetics
  • Receptor, EphA2 / metabolism*
  • Sequence Homology, Amino Acid
  • Signal Transduction*
  • Surface Plasmon Resonance

Substances

  • Ephrin-A1
  • Ephrin-A2
  • Ligands
  • Receptor, EphA2