Tick saliva protein Evasin-3 modulates chemotaxis by disrupting CXCL8 interactions with glycosaminoglycans and CXCR2

J Biol Chem. 2019 Aug 16;294(33):12370-12379. doi: 10.1074/jbc.RA119.008902. Epub 2019 Jun 24.

Abstract

Chemokines are a group of chemotaxis proteins that regulate cell trafficking and play important roles in immune responses and inflammation. Ticks are blood-sucking parasites that secrete numerous immune-modulatory agents in their saliva to evade host immune responses. Evasin-3 is a small salivary protein that belongs to a class of chemokine-binding proteins isolated from the brown dog tick, Rhipicephalus sanguineus Evasin-3 has been shown to have a high affinity for chemokines CXCL1 and CXCL8 and to diminish inflammation in mice. In the present study, solution NMR spectroscopy was used to investigate the structure of Evasin-3 and its CXCL8-Evasin-3 complex. Evasin-3 is found to disrupt the glycosaminoglycan-binding site of CXCL8 and inhibit the interaction of CXCL8 with CXCR2. Structural data were used to design two novel CXCL8-binding peptides. The linear tEv3 17-56 and cyclic tcEv3 16-56 dPG Evasin-3 variants were chemically synthesized by solid-phase peptide synthesis. The affinity of these newly synthesized variants to CXCL8 was measured by surface plasmon resonance biosensor analysis. The Kd values of tEv3 17-56 and tcEv3 16-56 dPG were 27 and 13 nm, respectively. Both compounds effectively inhibited CXCL8-induced migration of polymorphonuclear neutrophils. The present results suggest utility of synthetic Evasin-3 variants as scaffolds for designing and fine-tuning new chemokine-binding agents that suppress immune responses and inflammation.

Keywords: C-X-C motif chemokine ligand (CXCL); chemokine; nuclear magnetic resonance (NMR); peptide chemical synthesis; protein structure; protein-protein interaction.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Arthropod Proteins* / chemistry
  • Arthropod Proteins* / metabolism
  • Cell Movement
  • Dogs
  • Glycosaminoglycans* / chemistry
  • Glycosaminoglycans* / metabolism
  • Humans
  • Neutrophils / metabolism*
  • Protein Structure, Quaternary
  • Receptors, Interleukin-8B* / chemistry
  • Receptors, Interleukin-8B* / metabolism
  • Rhipicephalus sanguineus / chemistry*
  • Salivary Proteins and Peptides* / chemistry
  • Salivary Proteins and Peptides* / metabolism

Substances

  • Arthropod Proteins
  • CXCR2 protein, human
  • Glycosaminoglycans
  • Receptors, Interleukin-8B
  • Salivary Proteins and Peptides

Associated data

  • PDB/1IL8
  • PDB/6QJB