The molecular mode of action and species specificity of canakinumab, a human monoclonal antibody neutralizing IL-1β

MAbs. 2015;7(6):1151-60. doi: 10.1080/19420862.2015.1081323. Epub 2015 Aug 18.

Abstract

Interleukin-1β (IL-1β) plays a key role in autoinflammatory diseases, such as systemic juvenile idiopathic arthritis (sJIA) or cryopyrin-associated periodic syndrome (CAPS). Canakinumab, a human monoclonal anti-IL-1β antibody, was recently approved for human use under the brand name Ilaris®. Canakinumab does not cross-react with IL-1β from mouse, rat, rabbit, or macaques. The crystal structure of the canakinumab Fab bound to human IL-1β was determined in an attempt to rationalize the species specificity. The X-ray analysis reveals a complex surface epitope with an intricate network of well-ordered water molecules at the antibody-antigen interface. The canakinumab paratope is largely pre-organized, as demonstrated by the structure determination of the free Fab. Glu 64 of human IL-1β is a pivotal epitope residue explaining the exquisite species specificity of canakinumab. We identified marmoset as the only non-human primate species that carries Glu 64 in its IL-1β and demonstrates full cross-reactivity of canakinumab, thereby enabling toxicological studies in this species. As demonstrated by the X-ray structure of the complex with IL-1β, canakinumab binds IL-1β on the opposite side with respect to the IL-1RAcP binding site, and in an approximately orthogonal orientation with respect to IL-1RI. However, the antibody and IL-1RI binding sites slightly overlap and the VH region of canakinumab would sterically interfere with the D1 domain of IL-1RI, as shown by a structural overlay with the IL-1β:IL-1RI complex. Therefore, direct competition with IL-1RI for IL-1β binding is the molecular mechanism of neutralization by canakinumab, which is also confirmed by competition assays with recombinant IL-1RI and IL-1RII.

Keywords: Interleukin-1β; canakinumab; cryopyrin-associated periodic syndrome; crystal structure; gouty arthritis; mode of action; species specificity; systemic juvenile idiopathic arthritis; therapeutic antibody.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / chemistry
  • Antibodies, Monoclonal / immunology*
  • Antibodies, Monoclonal / metabolism
  • Antibodies, Monoclonal, Humanized
  • Antibodies, Neutralizing / immunology*
  • Antibodies, Neutralizing / metabolism
  • Antibody Specificity / immunology*
  • Binding, Competitive / immunology
  • Callithrix
  • Cross Reactions / immunology
  • Crystallography, X-Ray
  • Epitopes / chemistry
  • Epitopes / immunology
  • Epitopes / metabolism
  • Glutamic Acid / chemistry
  • Glutamic Acid / immunology
  • Glutamic Acid / metabolism
  • Humans
  • Interleukin-1beta / chemistry
  • Interleukin-1beta / immunology*
  • Interleukin-1beta / metabolism
  • Macaca
  • Mice
  • Models, Molecular
  • Protein Binding / immunology
  • Protein Structure, Tertiary
  • Rabbits
  • Rats
  • Receptors, Interleukin-1 / immunology
  • Receptors, Interleukin-1 / metabolism
  • Species Specificity

Substances

  • Antibodies, Monoclonal
  • Antibodies, Monoclonal, Humanized
  • Antibodies, Neutralizing
  • Epitopes
  • Interleukin-1beta
  • Receptors, Interleukin-1
  • canakinumab
  • Glutamic Acid

Associated data

  • PDB/5BVJ
  • PDB/5BVP