Dysfunction of nodes of Ranvier: a mechanism for anti-ganglioside antibody-mediated neuropathies

Exp Neurol. 2012 Jan;233(1):534-42. doi: 10.1016/j.expneurol.2011.11.039. Epub 2011 Dec 8.

Abstract

Autoantibodies against gangliosides GM1 or GD1a are associated with acute motor axonal neuropathy (AMAN) and acute motor-sensory axonal neuropathy (AMSAN), whereas antibodies to GD1b ganglioside are detected in acute sensory ataxic neuropathy (ASAN). These neuropathies have been proposed to be closely related and comprise a continuous spectrum, although the underlying mechanisms, especially for sensory nerve involvement, are still unclear. Antibodies to GM1 and GD1a have been proposed to disrupt the nodes of Ranvier in motor nerves via complement pathway. We hypothesized that the disruption of nodes of Ranvier is a common mechanism whereby various anti-ganglioside antibodies found in these neuropathies lead to nervous system dysfunction. Here, we show that the IgG monoclonal anti-GD1a/GT1b antibody injected into rat sciatic nerves caused deposition of IgG and complement products on the nodal axolemma and disrupted clusters of nodal and paranodal molecules predominantly in motor nerves, and induced early reversible motor nerve conduction block. Injection of IgG monoclonal anti-GD1b antibody induced nodal disruption predominantly in sensory nerves. In an ASAN rabbit model associated with IgG anti-GD1b antibodies, complement-mediated nodal disruption was observed predominantly in sensory nerves. In an AMAN rabbit model associated with IgG anti-GM1 antibodies, complement attack of nodes was found primarily in motor nerves, but occasionally in sensory nerves as well. Periaxonal macrophages and axonal degeneration were observed in dorsal roots from ASAN rabbits and AMAN rabbits. Thus, nodal disruption may be a common mechanism in immune-mediated neuropathies associated with autoantibodies to gangliosides GM1, GD1a, or GD1b, providing an explanation for the continuous spectrum of AMAN, AMSAN, and ASAN.

Publication types

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

MeSH terms

  • Acute Disease
  • Animals
  • Antibodies / adverse effects*
  • Choline O-Acetyltransferase / metabolism
  • Complement C3 / metabolism
  • Disease Models, Animal
  • Ganglia, Spinal / drug effects
  • Ganglia, Spinal / metabolism
  • Ganglia, Spinal / ultrastructure
  • Gangliosides / immunology*
  • Gangliosidosis, GM1 / immunology
  • Injections, Subcutaneous
  • Microscopy, Electron, Transmission
  • Neural Conduction / drug effects
  • Neural Conduction / physiology
  • Polyneuropathies / chemically induced*
  • Polyneuropathies / physiopathology
  • Rabbits
  • Ranvier's Nodes / drug effects*
  • Ranvier's Nodes / metabolism
  • Ranvier's Nodes / ultrastructure
  • Rats
  • Rats, Sprague-Dawley
  • Sciatic Nerve / cytology
  • Sciatic Nerve / drug effects
  • Spectrin / metabolism
  • Spinal Cord / pathology
  • Statistics, Nonparametric
  • Time Factors

Substances

  • Antibodies
  • Complement C3
  • Gangliosides
  • Spectrin
  • ganglioside, GD1b
  • Choline O-Acetyltransferase