Structure and function of chicken interleukin-1 beta mutants: uncoupling of receptor binding and in vivo biological activity

Sci Rep. 2016 Jun 9:6:27729. doi: 10.1038/srep27729.

Abstract

Receptor-binding and subsequent signal-activation of interleukin-1 beta (IL-1β) are essential to immune and proinflammatory responses. We mutated 12 residues to identify sites important for biological activity and/or receptor binding. Four of these mutants with mutations in loop 9 (T117A, E118K, E118A, E118R) displayed significantly reduced biological activity. Neither T117A nor E118K mutants substantially affected receptor binding, whereas both mutants lack the IL-1β signaling in vitro but can antagonize wild-type (WT) IL-1β. Crystal structures of T117A, E118A, and E118K revealed that the secondary structure or surface charge of loop 9 is dramatically altered compared with that of wild-type chicken IL-1β. Molecular dynamics simulations of IL-1β bound to its receptor (IL-1RI) and receptor accessory protein (IL-1RAcP) revealed that loop 9 lies in a pocket that is formed at the IL-1RI/IL-1RAcP interface. This pocket is also observed in the human ternary structure. The conformations of above mutants in loop 9 may disrupt structural packing and therefore the stability in a chicken IL-1β/IL-1RI/IL-1RAcP signaling complex. We identify the hot spots in IL-1β that are essential to immune responses and elucidate a mechanism by which IL-1β activity can be inhibited. These findings should aid in the development of new therapeutics that neutralize IL-1 activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Binding Sites
  • Cell Line
  • Chickens / genetics
  • Chickens / metabolism*
  • Crystallography, X-Ray
  • Gene Expression Regulation
  • Interleukin-1 Receptor Accessory Protein
  • Interleukin-1beta / chemistry*
  • Interleukin-1beta / genetics
  • Interleukin-1beta / metabolism*
  • Models, Molecular
  • Molecular Dynamics Simulation
  • Mutation*
  • Protein Binding
  • Protein Structure, Secondary
  • Receptors, Interleukin-1 / metabolism*

Substances

  • Interleukin-1 Receptor Accessory Protein
  • Interleukin-1beta
  • Receptors, Interleukin-1