Intravenous neuromyelitis optica autoantibody in mice targets aquaporin-4 in peripheral organs and area postrema

PLoS One. 2011;6(11):e27412. doi: 10.1371/journal.pone.0027412. Epub 2011 Nov 4.

Abstract

The pathogenesis of neuromyelitis optica (NMO) involves binding of IgG autoantibodies (NMO-IgG) to aquaporin-4 (AQP4) on astrocytes in the central nervous system (CNS). We studied the in vivo processing in mice of a recombinant monoclonal human NMO-IgG that binds strongly to mouse AQP4. Following intravenous administration, serum [NMO-IgG] decreased with t(½) ∼18 hours in wildtype mice and ∼41 hours in AQP4 knockout mice. NMO-IgG was localized to AQP4-expressing cell membranes in kidney (collecting duct), skeletal muscle, trachea (epithelial cells) and stomach (parietal cells). NMO-IgG was seen on astrocytes in the area postrema in brain, but not elsewhere in brain, spinal cord, optic nerve or retina. Intravenously administered NMO-IgG was also seen in brain following mechanical disruption of the blood-brain barrier. Selective cellular localization was not found for control (non-NMO) IgG, or for NMO-IgG in AQP4 knockout mice. NMO-IgG injected directly into brain parenchyma diffused over an area of ∼5 mm² over 24 hours and targeted astrocyte foot-processes. Our data establish NMO-IgG pharmacokinetics and tissue distribution in mice. The rapid access of serum NMO-IgG to AQP4 in peripheral organs but not the CNS indicates that restricted antibody access cannot account for the absence of NMO pathology in peripheral organs.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage
  • Antibodies, Monoclonal / pharmacokinetics*
  • Aquaporin 4 / physiology*
  • Area Postrema / immunology
  • Area Postrema / metabolism*
  • Autoantibodies / blood
  • Autoantibodies / immunology
  • Autoantibodies / metabolism*
  • Blood-Brain Barrier / metabolism
  • Cells, Cultured
  • Central Nervous System / immunology
  • Central Nervous System / metabolism*
  • Fluorescent Antibody Technique
  • Humans
  • Immunoenzyme Techniques
  • Immunoglobulin G / blood
  • Immunoglobulin G / immunology*
  • Injections, Intravenous
  • Mice
  • Mice, Knockout
  • Neuromyelitis Optica / blood
  • Neuromyelitis Optica / immunology*
  • Neuromyelitis Optica / metabolism
  • Tissue Distribution

Substances

  • Antibodies, Monoclonal
  • Aqp4 protein, mouse
  • Aquaporin 4
  • Autoantibodies
  • Immunoglobulin G