Structural basis for the dual recognition of IL-12 and IL-23 by ustekinumab

J Mol Biol. 2010 Oct 8;402(5):797-812. doi: 10.1016/j.jmb.2010.07.046. Epub 2010 Aug 4.

Abstract

Interleukin (IL)-12 and IL-23 are heterodimeric proinflammatory cytokines that share a common p40 subunit, paired with p35 and p19 subunits, respectively. They represent an attractive class of therapeutic targets for the treatment of psoriasis and other immune-mediated diseases. Ustekinumab is a fully human monoclonal antibody (mAb) that binds specifically to IL-12/IL-23p40 and neutralizes human IL-12 and IL-23 bioactivity. The crystal structure of ustekinumab Fab (antigen binding fragment of mAb), in complex with human IL-12, has been determined by X-ray crystallography at 3.0 Å resolution. Ustekinumab Fab binds the D1 domain of the p40 subunit in a 1:1 ratio in the crystal, consistent with a 2 cytokines:1 mAb stoichiometry, as measured by isothermal titration calorimetry. The structure indicates that ustekinumab binds to the same epitope on p40 in both IL-12 and IL-23 with identical interactions. Mutational analyses confirm that several residues identified in the IL-12/IL-23p40 epitope provide important molecular binding interactions with ustekinumab. The electrostatic complementarity between the mAb antigen binding site and the p40 D1 domain epitope appears to play a key role in antibody/antigen recognition specificity. Interestingly, this structure also reveals significant structural differences in the p35 subunit and p35/p40 interface, compared with the published crystal structure of human IL-12, suggesting unusual and potentially functionally relevant structural flexibility of p35, as well as p40/p35 recognition. Collectively, these data describe unique observations about IL-12p35 and ustekinumab interactions with p40 that account for its dual binding and neutralization of IL-12 and IL-23.

MeSH terms

  • Amino Acid Substitution / genetics
  • Antibodies, Monoclonal / chemistry*
  • Antibodies, Monoclonal / metabolism*
  • Antibodies, Monoclonal, Humanized
  • Calorimetry
  • Crystallography, X-Ray
  • Epitopes / genetics
  • Epitopes / immunology
  • Humans
  • Immunologic Factors / chemistry*
  • Immunologic Factors / metabolism*
  • Interleukin-12 / genetics
  • Interleukin-12 / metabolism*
  • Interleukin-23 / genetics
  • Interleukin-23 / metabolism*
  • Models, Molecular
  • Mutagenesis, Site-Directed
  • Protein Binding
  • Protein Structure, Quaternary
  • Ustekinumab

Substances

  • Antibodies, Monoclonal
  • Antibodies, Monoclonal, Humanized
  • Epitopes
  • Immunologic Factors
  • Interleukin-23
  • Interleukin-12
  • Ustekinumab

Associated data

  • PDB/3HMW
  • PDB/3HMX