Off-target binding of an anti-amyloid beta monoclonal antibody to platelet factor 4 causes acute and chronic toxicity in cynomolgus monkeys

MAbs. 2021 Jan-Dec;13(1):1887628. doi: 10.1080/19420862.2021.1887628.

Abstract

ABT-736 is a humanized monoclonal antibody generated to target a specific conformation of the amyloid-beta (Aβ) protein oligomer. Development of ABT-736 for Alzheimer's disease was discontinued due to severe adverse effects (AEs) observed in cynomolgus monkey toxicity studies. The acute nature of AEs observed only at the highest doses suggested potential binding of ABT-736 to an abundant plasma protein. Follow-up investigations indicated polyspecificity of ABT-736, including unintended high-affinity binding to monkey and human plasma protein platelet factor 4 (PF-4), known to be involved in heparin-induced thrombocytopenia (HIT) in humans. The chronic AEs observed at the lower doses after repeat administration in monkeys were consistent with HIT pathology. Screening for a backup antibody revealed that ABT-736 possessed additional unintended binding characteristics to other, unknown factors. A subsequently implemented screening funnel focused on nonspecific binding led to the identification of h4D10, a high-affinity Aβ oligomer binding antibody that did not bind PF-4 or other unintended targets and had no AEs in vivo. This strengthened the hypothesis that ABT-736 toxicity was not Aβ target-related, but instead was the consequence of polyspecificity including PF-4 binding, which likely mediated the acute and chronic AEs and the HIT-like pathology. In conclusion, thorough screening of antibody candidates for nonspecific interactions with unrelated molecules at early stages of discovery can eliminate candidates with polyspecificity and reduce potential for toxicity caused by off-target binding.

Keywords: Antibody biotherapeutic; a-beta oligomer; adverse effects; amyloid beta; cross-reactivity; heparin-induced thrombocytopenia; nonspecific binding; off-target binding; platelet factor 4; polyspecificity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alzheimer Vaccines / immunology*
  • Alzheimer Vaccines / pharmacokinetics
  • Alzheimer Vaccines / toxicity
  • Amyloid beta-Peptides / antagonists & inhibitors*
  • Amyloid beta-Peptides / immunology
  • Animals
  • Antibodies, Monoclonal, Humanized / immunology
  • Antibodies, Monoclonal, Humanized / pharmacokinetics
  • Antibodies, Monoclonal, Humanized / toxicity*
  • Antibody Specificity
  • Blood Platelets / drug effects*
  • Blood Platelets / immunology
  • Blood Platelets / metabolism
  • Female
  • Humans
  • Immunity, Heterologous*
  • Macaca fascicularis
  • Male
  • Mice
  • Mice, Inbred BALB C
  • No-Observed-Adverse-Effect Level
  • Platelet Activation / drug effects
  • Platelet Factor 4 / antagonists & inhibitors*
  • Platelet Factor 4 / immunology
  • Purpura, Thrombocytopenic, Idiopathic / blood
  • Purpura, Thrombocytopenic, Idiopathic / chemically induced*
  • Purpura, Thrombocytopenic, Idiopathic / immunology
  • Risk Assessment
  • Time Factors
  • Toxicity Tests, Acute
  • Toxicity Tests, Chronic

Substances

  • Alzheimer Vaccines
  • Amyloid beta-Peptides
  • Antibodies, Monoclonal, Humanized
  • Platelet Factor 4

Grants and funding

AbbVie sponsored and funded the studies described; contributed to the design; participated in collection, analysis, and interpretation of data; and in writing, reviewing, and approval of the final version. All authors are employees of AbbVie and own AbbVie stock.