Reducing affinity as a strategy to boost immunomodulatory antibody agonism

Nature. 2023 Feb;614(7948):539-547. doi: 10.1038/s41586-022-05673-2. Epub 2023 Feb 1.

Abstract

Antibody responses during infection and vaccination typically undergo affinity maturation to achieve high-affinity binding for efficient neutralization of pathogens1,2. Similarly, high affinity is routinely the goal for therapeutic antibody generation. However, in contrast to naturally occurring or direct-targeting therapeutic antibodies, immunomodulatory antibodies, which are designed to modulate receptor signalling, have not been widely examined for their affinity-function relationship. Here we examine three separate immunologically important receptors spanning two receptor superfamilies: CD40, 4-1BB and PD-1. We show that low rather than high affinity delivers greater activity through increased clustering. This approach delivered higher immune cell activation, in vivo T cell expansion and antitumour activity in the case of CD40. Moreover, an inert anti-4-1BB monoclonal antibody was transformed into an agonist. Low-affinity variants of the clinically important antagonistic anti-PD-1 monoclonal antibody nivolumab also mediated more potent signalling and affected T cell activation. These findings reveal a new paradigm for augmenting agonism across diverse receptor families and shed light on the mechanism of antibody-mediated receptor signalling. Such affinity engineering offers a rational, efficient and highly tuneable solution to deliver antibody-mediated receptor activity across a range of potencies suitable for translation to the treatment of human disease.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal* / immunology
  • Antibodies, Monoclonal* / pharmacology
  • Antibody Affinity*
  • CD40 Antigens / drug effects
  • CD40 Antigens / immunology
  • Humans
  • Immunomodulation* / drug effects
  • Immunomodulation* / immunology
  • Nivolumab / immunology
  • Nivolumab / pharmacology

Substances

  • Antibodies, Monoclonal
  • CD40 Antigens
  • TNFRSF9 protein, human
  • PDCD1 protein, human
  • Nivolumab