Aquaporin-4 orthogonal arrays of particles are the target for neuromyelitis optica autoantibodies

Glia. 2009 Oct;57(13):1363-73. doi: 10.1002/glia.20855.

Abstract

Neuromyelitis optica (NMO) is an inflammatory autoimmune demyelinating disease of the central nervous system (CNS) which in autoantibodies produced by patients with NMO (NMO-IgG) recognize a glial water channel protein, Aquaporin-4 (AQP4) expressed as two major isoforms, M1- and M23-AQP4, in which the plasma membrane form orthogonal arrays of particles (OAPs). AQP4-M23 is the OAP-forming isoform, whereas AQP4-M1 alone is unable to form OAPs. The function of AQP4 organization into OAPs in normal physiology is unknown; however, alteration in OAP assemblies is reported for several CNS pathological states. In this study, we demonstrate that in the CNS, NMO-IgG is able to pull down both M1- and M23-AQP4 but experiments performed using cells selectively transfected with M1- or M23-AQP4 and native tissues show NMO-IgG epitope to be intrinsic in AQP4 assemblies into OAPs. Other OAP-forming water-channel proteins, such as the lens Aquaporin-0 and the insect Aquaporin-cic, were not recognized by NMO-IgG, indicating an epitope characteristic of AQP4-OAPs. Finally, water transport measurements show that NMO-IgG treatment does not significantly affect AQP4 function. In conclusion, our results suggest for the first time that OAP assemblies are required for NMO-IgG to recognize AQP4.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aquaporin 4 / chemistry*
  • Aquaporin 4 / immunology*
  • Aquaporin 4 / metabolism
  • Aquaporins / chemistry
  • Aquaporins / immunology
  • Aquaporins / metabolism
  • Autoantibodies / immunology*
  • Autoantibodies / metabolism
  • Cell Line
  • Cell Membrane / immunology
  • Cell Membrane / metabolism
  • Cells, Cultured
  • Eye Proteins / chemistry
  • Eye Proteins / immunology
  • Eye Proteins / metabolism
  • HeLa Cells
  • Hemiptera
  • Humans
  • Immunoglobulin G / immunology
  • Immunoglobulin G / metabolism
  • Insect Proteins / chemistry
  • Insect Proteins / immunology
  • Insect Proteins / metabolism
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Neuromyelitis Optica / immunology*
  • Neuromyelitis Optica / metabolism
  • Protein Isoforms / immunology
  • Protein Isoforms / metabolism
  • Rats
  • Rats, Wistar

Substances

  • AQPcic protein, Cicadella viridis
  • Aqp4 protein, rat
  • Aquaporin 4
  • Aquaporins
  • Autoantibodies
  • Eye Proteins
  • Immunoglobulin G
  • Insect Proteins
  • Protein Isoforms
  • aquaporin 0