Poster Presentation The 47th Lorne Conference on Protein Structure and Function 2022

Molecular Basis of Chemokine Inhibition by Tick Evasins (#324)

Shankar Devkota 1 , Martin Stone 1 , Ram Bhusal 1 , Pramod Aryal 1
  1. Monash University, Clayton, VIC, Australia

Inflammation is a normal response to any injury or infection. However, sustained inflammation can cause numerous diseases. A hallmark of inflammation is leukocyte recruitment to the affected tissue, regulated by small secretory proteins called chemokines, which bind and activate chemokine receptors expressed on the leukocyte surface (1). As a strategy to suppress detection, and thereby prolong their feeding and residence time, “ticks”, hematophagous arachnids, produce chemokine-binding proteins called 'evasins', which bind to host chemokines and block chemokine receptor activation, preventing leukocyte migration. Several studies have shown that evasins are natural, selective chemokine-inhibitory proteins with excellent potential as therapeutics for inflammatory diseases (2,3). Using bioinformatics, we identified variants of previously characterised “class A” evasins with ten cysteine residues forming five-disulfide bonds. We expressed and purified EVA-ACA1001 using the E. coli expression system. Analysis of the purified protein confirmed the predicted five intramolecular disulfide bonds. Binding data, obtained using surface plasmon resonance (SPR), showed that EVA-ACA1001 binds to multiple CC chemokines with dissociation equilibrium constants (Kd) in the range (0.01-100 nM). Furthermore, a cAMP inhibition assay demonstrated the chemokine inhibitory function of EVA-ACA1001, with IC50 values of 1 nM to 100 nM. Truncation of the N- and C-terminus revealed that the core region confers the chemokine binding and selectivity of EVA-ACA1001, a distinct feature of C10 evasins. Moreover, several crystal structures of a C10 evasin in complex with chemokines showed extensive hydrogen bonding between the evasin and the CC motif of the chemokine, a common feature of class A evasins. However, in contrast to traditional class A evasins, the core region of C10 evasins includes a deep hydrophobic pocket that can accommodate the first amino residue from the N- loop of CC chemokines, making it a broad binder. Thus, this study elucidates the relationship between structure and function of novel C10 evasins and paves a pathway for the engineering of potent anti-inflammatory molecules.

  1. 1. Bhusal RP, Foster SR, Stone MJ. Structural basis of chemokine and receptor interactions: Key regulators of leukocyte recruitment in inflammatory responses. Protein Sci 2019.
  2. 2. Bhusal RP, Eaton JRO, Chowdhury ST, Power CA, Proudfoot AEI, Stone MJ, et al. Evasins: Tick Salivary Proteins that Inhibit Mammalian Chemokines. Trends Biochem Sci 2019.
  3. 3. Hayward J, Sanchez J, Perry A, Huang C, Rodriguez Valle M, Canals M, et al. Ticks from diverse genera encode chemokine-inhibitory evasin proteins. J Biol Chem. 2017;292(38):15670-80.