Brain penetration, target engagement, and disposition of the blood-brain barrier-crossing bispecific antibody antagonist of metabotropic glutamate receptor type 1

FASEB J. 2016 May;30(5):1927-40. doi: 10.1096/fj.201500078. Epub 2016 Feb 2.

Abstract

Receptor mediated transcytosis harnessing the cellular uptake and transport of natural ligands across the blood-brain barrier (BBB) has been identified as a means for antibody delivery to the CNS. In this study, we characterized bispecific antibodies in which a BBB-crossing antibody fragment FC5 was used as a BBB carrier. Cargo antibodies were either a high-affinity, selective antibody antagonist of the metabotropic glutamate receptor-1 (BBB-mGluR1), a widely abundant CNS target, or an IgG that does not bind the CNS target (BBB-NiP). Both BBB-NiP and BBB-mGluR1 demonstrated a similar 20-fold enhanced rate of transcytosis across an in vitro BBB model compared with mGluR1 IgG fused to a control antibody fragment. All 3 bispecific antibodies exhibited identical pharmacokinetics in vivo Comparative assessment of BBB-NiP and BBB-mGluR1 revealed that, whereas their serum pharmacokinetics and BBB penetration were identical, their central disposition (brain levels) and elimination (cerebrospinal fluid levels) were widely different, due to central target-mediated removal of the mGluR1-engaging antibody. Central mGluR1 target engagement after systemic administration was demonstrated by a dose-dependent inhibition of mGluR-1-mediated thermal hyperalgesia and by colocalization of the antibody with thalamic neurons involved in mGluR1-mediated pain processing. We demonstrate the feasibility of targeting central G-protein-coupled receptors using a BBB-crossing bispecific antibody approach and emerging principles that govern brain distribution and disposition of these antibodies. These data will be important for designing safe and selective CNS antibody therapeutics.-Webster, C. I., Caram-Salas, N., Haqqani, A. S., Thom, G., Brown, L., Rennie, K., Yogi, A., Costain, W., Brunette, E., Stanimirovic, D. B. Brain penetration, target engagement, and disposition of the blood-brain barrier-crossing bispecific antibody antagonist of metabotropic glutamate receptor type 1.

Keywords: brain endothelial cells; mass spectrometry; pain; receptor-mediated transcytosis.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Analgesics
  • Animals
  • Antibodies, Bispecific / pharmacology*
  • Biological Products / metabolism
  • Biological Transport
  • Blood-Brain Barrier / metabolism
  • Brain / drug effects
  • Brain / metabolism*
  • Camelidae
  • Cell Membrane
  • HEK293 Cells
  • Hot Temperature / adverse effects
  • Humans
  • Immunoconjugates / metabolism
  • Immunoglobulin G / immunology
  • Pain / drug therapy*
  • Pain / etiology
  • Protein Engineering / methods
  • Rats
  • Receptors, Metabotropic Glutamate / antagonists & inhibitors*
  • Receptors, Metabotropic Glutamate / metabolism

Substances

  • Analgesics
  • Antibodies, Bispecific
  • Biological Products
  • Immunoconjugates
  • Immunoglobulin G
  • Receptors, Metabotropic Glutamate
  • metabotropic glutamate receptor type 1